Richard dawkins the extended phenotype by Mariano R Cagnola

The Extended Phenotype The Gene as the Unit of Selection

Richard D a w k i n s University of Oxford

Oxford University Press

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Published in the United States by Oxford University P r e s s , New

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Acknowledgements pp.

141

142

'The

COLLECTED by

Donald

Watt.

Reproduced &

Windus

permission also

Inc.

hardcover Freeman

issued as

British

Laura

THE

HUXLEY Laura

edited

Huxley.

Huxley

of Harper

Rudyard

of Doubleday

Richard edition

and

Library

Dawkins,

1971

of Mrs.

Hymn'

1982

W. First

by permission

permission

Original H.

Song' from

ALDOUS

and &

Chatto

Row,

(USA)

'McAndrew's

reproduced

Philosopher's OF

Ltd,

Publishers, p.

Fifth

POETRY

published

Cataloguing

Extract

Company

Inc.

Dawkins

Company

Oxford

Kipling.

Limited

University in

Press paperback

Publication

1983

Data

Richard

The

extended

Evolution

Title

phenotype. 2.

575-12

Gene expression

QH.W

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Preface

T h e first c h a p t e r d o e s s o m e o f t h e w o r k o f a P r e f a c e , i n e x p l a i n i n g w h a t the b o o k d o e s a n d d o e s n o t set o u t t o a c c o m p l i s h , s o I c a n b e b r i e f h e r e . It is n o t a t e x t b o o k , n o r an i n t r o d u c t i o n to an e s t a b l i s h e d field.

It is a

p e r s o n a l l o o k a t t h e e v o l u t i o n o f life, a n d i n p a r t i c u l a r a t t h e l o g i c o f n a t u r a l s e l e c t i o n a n d t h e l e v e l i n t h e h i e r a r c h y o f life a t w h i c h n a t u r a l s e l e c t i o n c a n b e said t o a c t . I h a p p e n t o b e a n e t h o l o g i s t , b u t I h o p e p r e o c c u p a t i o n s w i t h a n i m a l b e h a v i o u r will not b e too n o t i c e a b l e . T h e i n t e n d e d scope o f the b o o k is w i d e r . T h e r e a d e r s for w h o m I a m m a i n l y w r i t i n g a r e m y p r o f e s s i o n a l c o l l e a g u e s , evolutionary

biologists,

ethologists

and

sociobiologists,

ecologists,

and

philosophers and humanists interested in e v o l u t i o n a r y science, including, of course,

graduate

and

undergraduate

students

all

these

disciplines.

T h e r e f o r e , a l t h o u g h this b o o k i s i n s o m e w a y s t h e s e q u e l t o m y p r e v i o u s b o o k , The Selfish Gene, it a s s u m e s t h a t t h e r e a d e r h a s p r o f e s s i o n a l k n o w l e d g e o f e v o l u t i o n a r y b i o l o g y a n d its t e c h n i c a l t e r m s . O n t h e o t h e r h a n d i t i s p o s s i b l e to e n j o y a p r o f e s s i o n a l b o o k as a s p e c t a t o r , e v e n if n o t a p a r t i c i p a n t i n the p r o f e s s i o n . S o m e l a y p e o p l e w h o r e a d this b o o k i n d r a f t h a v e b e e n k i n d e n o u g h , o r p o l i t e e n o u g h , t o c l a i m t o h a v e l i k e d it. I t w o u l d g i v e m e g r e a t satisfaction t o b e l i e v e t h e m , a n d I h a v e a d d e d a g l o s s a r y o f t e c h n i c a l t e r m s w h i c h I h o p e m a y h e l p . I h a v e also t r i e d t o m a k e t h e b o o k a s n e a r a s p o s s i b l e to being enjoyable to read. T h e resulting tone m a y possibly irritate some serious p r o f e s s i o n a l s . I v e r y m u c h h o p e n o t , b e c a u s e s e r i o u s p r o f e s s i o n a l s a r e the p r i m a r y a u d i e n c e t o w h o m I w i s h t o s p e a k . I t i s a s i m p o s s i b l e t o p l e a s e e v e r y b o d y i n l i t e r a r y s t y l e a s i t i s i n a n y o t h e r m a t t e r o f taste, a n d s t y l e s t h a t g i v e the most positive pleasure to s o m e p e o p l e are often the most a n n o y i n g to others. C e r t a i n l y the tone of the b o o k is not c o n c i l i a t o r y or a p o l o g e t i c â&#x20AC;&#x201D; s u c h is not the w a y o f a n a d v o c a t e t h a t s i n c e r e l y b e l i e v e s i n his c a s e â&#x20AC;&#x201D; a n d I m u s t p a c k all a p o l o g y i n t o t h e P r e f a c e . S o m e o f t h e e a r l i e r c h a p t e r s r e p l y t o criticisms of my previous book, w h i c h m i g h t recur in response to the present

Preface

o n e . I a m s o r r y t h a t this i s n e c e s s a r y , a n d I a m s o r r y i f a n o t e o f e x a s p e r a t i o n c r e e p s i n f r o m t i m e t o t i m e . I trust, a t l e a s t , t h a t m y e x a s p e r a t i o n r e m a i n s g o o d h u m o u r e d . I t i s n e c e s s a r y t o p o i n t t o p a s t m i s u n d e r s t a n d i n g s a n d try t o forestall

their

repetition,

but

would

not

wish

give

aggrieved

impression that m i s u n d e r s t a n d i n g has b e e n w i d e s p r e a d . It has been confined to n u m e r i c a l l y v e r y limited quarters, b u t in s o m e cases rather v o c a l ones. I a m g r a t e f u l t o m y c r i t i c s for f o r c i n g m e t o t h i n k a g a i n a b o u t h o w t o e x p r e s s difficult m a t t e r s m o r e c l e a r l y . I a p o l o g i z e to readers w h o m a y find a favourite and relevant w o r k missing from the b i b l i o g r a p h y . T h e r e are those c a p a b l e o f c o m p r e h e n s i v e l y and exhaustively s u r v e y i n g the literature of a large field, but I h a v e never been a b l e t o u n d e r s t a n d h o w t h e y m a n a g e it. I k n o w t h a t t h e e x a m p l e s I h a v e c i t e d are a small subset of those that could h a v e been cited, and are sometimes the w r i t i n g s or r e c o m m e n d a t i o n s of my friends. If the result a p p e a r s biased, w e l l , of course it is biased, a n d I am sorry. I think nearly e v e r y b o d y must be s o m e w h a t b i a s e d i n this k i n d o f w a y . A b o o k i n e v i t a b l y reflects the c u r r e n t p r e o c c u p a t i o n s of the author, and t h e s e p r e o c c u p a t i o n s a r e l i k e l y t o h a v e b e e n a m o n g the t o p i c s o f his m o s t r e c e n t p a p e r s . W h e n t h o s e p a p e r s a r e s o r e c e n t t h a t i t w o u l d b e a n artificial contrivance

change

the words,

h a v e not hesitated

to reproduce a

p a r a g r a p h almost v e r b a t i m here and there. T h e s e paragraphs, w h i c h will be f o u n d i n C h a p t e r s 4 , 5 , 6 a n d 1 4 , a r e a n i n t e g r a l p a r t o f t h e m e s s a g e o f this book, a n d to o m i t t h e m w o u l d be just as artificial as to m a k e gratuitous changes in their w o r d i n g . T h e o p e n i n g sentence of C h a p t e r

d e s c r i b e s the b o o k a s a w o r k o f

u n a b a s h e d a d v o c a c y b u t , w e l l , p e r h a p s I a m j u s t a little bit a b a s h e d ! W i l s o n ( 1 9 7 5 , p p . 28â&#x20AC;&#x201D;29) h a s r i g h t l y c a s t i g a t e d t h e ' a d v o c a c y m e t h o d ' i n a n y s e a r c h for s c i e n t i f i c t r u t h , a n d I h a v e t h e r e f o r e d e v o t e d s o m e o f m y f i r s t c h a p t e r t o a p l e a o f m i t i g a t i o n . I c e r t a i n l y w o u l d n o t w a n t s c i e n c e t o a d o p t the l e g a l s y s t e m i n w h i c h p r o f e s s i o n a l a d v o c a t e s m a k e t h e best c a s e t h e y c a n for a p o s i t i o n , e v e n i f t h e y b e l i e v e i t t o b e false. I b e l i e v e d e e p l y i n t h e v i e w o f life t h a t this b o o k a d v o c a t e s , a n d h a v e d o n e so, a t least i n p a r t , for a l o n g t i m e , c e r t a i n l y since the time of my first published paper, in w h i c h I c h a r a c t e r i z e d a d a p t a t i o n s a s f a v o u r i n g ' t h e s u r v i v a l o f the a n i m a l ' s g e n e s . . . '

(Dawkins

1 9 6 8 ) . T h i s b e l i e f â&#x20AC;&#x201D; t h a t i f a d a p t a t i o n s a r e t o b e t r e a t e d a s 'for t h e g o o d o f s o m e t h i n g , that s o m e t h i n g is the g e n e â&#x20AC;&#x201D; w a s the f u n d a m e n t a l assumption of m y p r e v i o u s b o o k . T h e present b o o k goes further. T o d r a m a t i z e i t a bit, i t a t t e m p t s t o free t h e selfish g e n e f r o m t h e i n d i v i d u a l o r g a n i s m w h i c h h a s b e e n its c o n c e p t u a l p r i s o n . T h e p h e n o t y p i c effects o f a g e n e a r e t h e tools b y w h i c h i t l e v e r s i t s e l f i n t o t h e n e x t g e n e r a t i o n , a n d these tools m a y ' e x t e n d ' far o u t s i d e t h e b o d y i n w h i c h t h e g e n e sits, e v e n r e a c h i n g d e e p i n t o t h e n e r v o u s systems of other organisms. S i n c e it is not a factual position I am a d v o c a t i n g , b u t a w a y of seeing facts,

wanted

to w a r n

the reader not to expect

Preface

vii

' e v i d e n c e ' i n the n o r m a l sense o f t h e w o r d . I a n n o u n c e d t h a t t h e b o o k w a s a work of a d v o c a c y , because I was anxious not to disappoint the reader, not to l e a d h e r o n u n d e r false p r e t e n c e s a n d w a s t e h e r t i m e . T h e l i n g u i s t i c e x p e r i m e n t o f t h e last s e n t e n c e r e m i n d s m e t h a t I w i s h I h a d h a d the c o u r a g e t o i n s t r u c t the c o m p u t e r t o f e m i n i z e p e r s o n a l p r o n o u n s at r a n d o m t h r o u g h o u t the text. T h i s is not o n l y b e c a u s e I a d m i r e the current awareness of the m a s c u l i n e bias in o u r l a n g u a g e . W h e n e v e r I w r i t e I h a v e a particular imaginary reader in mind

(different i m a g i n a r y r e a d e r s o v e r s e e

a n d 'filter' t h e s a m e p a s s a g e i n n u m e r o u s s u c c e s s i v e r e v i s i o n s ) a n d a t least half my

imaginary

readers

are,

least

half my

friends,

female.

U n f o r t u n a t e l y i t i s still t r u e i n E n g l i s h t h a t t h e u n e x p e c t e d n e s s o f a f e m i n i n e pronoun,

where

neutral

meaning

intended,

attention of most readers, of either sex.

p r e v i o u s p a r a g r a p h w i l l s u b s t a n t i a t e this.

seriously

distracts

the

b e l i e v e the e x p e r i m e n t of the W i t h regret,

therefore,

have

f o l l o w e d the s t a n d a r d c o n v e n t i o n i n this b o o k . F o r m e , w r i t i n g is almost a social activity, a n d I am grateful to the m a n y friends w h o h a v e , s o m e t i m e s u n w i t t i n g l y , p a r t i c i p a t e d t h r o u g h d i s c u s s i o n , argument and moral support.

I cannot thank them all by n a m e .

Marian

S t a m p D a w k i n s has not o n l y p r o v i d e d sensitive a n d k n o w l e d g e a b l e criticism o f the w h o l e b o o k i n several drafts. S h e has also k e p t m e g o i n g b y b e l i e v i n g i n the p r o j e c t e v e n t h r o u g h t h e t i m e s w h e n I lost m y o w n c o n f i d e n c e . A l a n Grafen a n d M a r k R i d l e y , officially m y g r a d u a t e students, r e a l l y , i n their different w a y s , m y m e n t o r s a n d g u i d e s t h r o u g h d i f f i c u l t t h e o r e t i c a l t e r r i t o r y , have

influenced

the

book

immeasurably.

the

first

draft

their

names

seemed to creep in on almost every p a g e , a n d it w a s only the p a r d o n a b l e g r u m b l i n g s of a referee that c o m p e l l e d me to banish to the P r e f a c e my a c k n o w l e d g m e n t o f debt t o t h e m . C a t h y K e n n e d y m a n a g e s t o c o m b i n e close f r i e n d s h i p for m e w i t h d e e p s y m p a t h y for m y b i t t e r e s t c r i t i c s . T h i s h a s p u t her in a u n i q u e position to advise m e , especially o v e r the earlier c h a p t e r s w h i c h a t t e m p t t o r e p l y t o c r i t i c i s m . I f e a r t h a t s h e w i l l still n o t l i k e t h e t o n e o f these c h a p t e r s , b u t s u c h i m p r o v e m e n t a s t h e r e m a y b e i s l a r g e l y d u e t o h e r influence and I am v e r y grateful to her. I w a s p r i v i l e g e d t o h a v e t h e first d r a f t c r i t i c i z e d i n its e n t i r e t y b y J o h n Maynard

Smith,

David

Smith, John

Krebs,

Paul

Harvey,

and

Ric

C h a r n o v , a n d the f i n a l d r a f t o w e s m u c h t o a l l o f t h e m . I n a l l c a s e s I a c t e d o n their a d v i c e , e v e n if I

d i d n o t a l w a y s t a k e it.

Others kindly criticized

chapters

special

Hansell

their

own

fields:

Michael

the

chapter

a r t e f a c t s , P a u l i n e L a w r e n c e t h a t o n p a r a s i t e s , E g b e r t L e i g h t h a t o n fitness, A n t h o n y H a l l a m the section o n p u n c t u a t e d e q u i l i b r i a , W . F o r d D o o l i t t l e that o n selfish D N A , a n d D i a n e D e S t e v e n b o t a n i c a l s e c t i o n s . T h e b o o k w a s f i n i s h e d a t O x f o r d , b u t b e g u n d u r i n g a visit t o t h e U n i v e r s i t y o f F l o r i d a a t Gainesville on a sabbatical leave kindly granted by the U n i v e r s i t y of O x f o r d a n d the W a r d e n a n d F e l l o w s o f N e w C o l l e g e . I a m g r a t e f u l t o m y m a n y

viii

Preface

F l o r i d a n friends for g i v i n g m e s u c h a p l e a s a n t a t m o s p h e r e i n w h i c h t o w o r k , especially

Jane

Brockmann,

who

also

provided

helpful

criticism

p r e l i m i n a r y d r a f t s , a n d D o n n a G i l l i s , w h o also d i d m u c h o f t h e t y p i n g . I b e n e f i t e d , t o o , f r o m a m o n t h ' s e x p o s u r e t o t r o p i c a l b i o l o g y a s the grateful guest of the S m i t h s o n i a n

I n s t i t u t i o n i n P a n a m a d u r i n g t h e w r i t i n g o f the

b o o k . F i n a l l y , it is a pleasure o n c e a g a i n to thank M i c h a e l R o d g e r s , formerly o f O x f o r d U n i v e r s i t y Press a n d n o w o f W . H . F r e e m a n a n d C o m p a n y , a 'Ks e l e c t e d ' e d i t o r w h o r e a l l y b e l i e v e s i n his b o o k s a n d i s t h e i r tireless a d v o c a t e . Oxford June

Richard Dawkins 1981

Contents

1 Necker

Cubes

2 Genetic

Determinism

3 Constraints

and

Buffaloes 1 and

Gene

Perfection

Selectionism 9

4 A r m s Races and Manipulation

5 The Active Germ-Line Replicator

6 Organisms, Groups and M e m e s : Replicators or Vehicles? 97 7 Selfish Wasp or Selfish Strategy? 8 Outlaws

and

Modifiers

118

133

9 Selfish DNA, Jumping Genes, and a Lamarckian Scare 10 An Agony in Five Fits 179 11 The Genetical Evolution of Animal Artefacts 195 12 Host Phenotypes of Parasite Genes 13 Action at a Distance

228

14 Rediscovering the O r g a n i s m Glossary

283

250

209

156

T h e Extended Phenotype

1 Necker C u b e s and Buffaloes

T h i s is a w o r k of u n a b a s h e d a d v o c a c y . I w a n t to a r g u e in favour of a particular w a y of looking at animals and plants, and a particular w a y of w o n d e r i n g w h y they do the things that they d o . W h a t I am a d v o c a t i n g is not a n e w t h e o r y , n o t a h y p o t h e s i s w h i c h c a n b e v e r i f i e d o r falsified, n o t a m o d e l w h i c h c a n b e j u d g e d b y its p r e d i c t i o n s . I f i t w e r e a n y o f t h o s e t h i n g s , I a g r e e with Wilson

(1975, p.

28)

that the ' a d v o c a c y m e t h o d ' w o u l d

be inap-

propriate a n d reprehensible. But it is not a n y of those things. W h a t I am a d v o c a t i n g i s a p o i n t o f v i e w , a w a y o f l o o k i n g a t f a m i l i a r facts a n d i d e a s , and a w a y of asking new questions about them. A n y reader w h o expects a c o n v i n c i n g n e w t h e o r y i n t h e c o n v e n t i o n a l sense o f t h e w o r d i s b o u n d t o b e left, t h e r e f o r e , w i t h a d i s a p p o i n t e d 'so w h a t ? ' f e e l i n g . B u t I a m n o t t r y i n g t o c o n v i n c e a n y o n e of the truth of any factual proposition. R a t h e r , I am t r y i n g to show the r e a d e r a w a y of seeing b i o l o g i c a l facts. T h e r e i s a w e l l - k n o w n v i s u a l i l l u s i o n c a l l e d the N e c k e r C u b e . I t c o n s i s t s o f a line d r a w i n g w h i c h t h e b r a i n i n t e r p r e t s a s a t h r e e - d i m e n s i o n a l c u b e . B u t there are t w o possible orientations of the p e r c e i v e d equally

compatible

with

the

two-dimensional

image

cube, on

and the

both are

paper.

u s u a l l y b e g i n b y s e e i n g o n e o f the t w o o r i e n t a t i o n s , b u t i f w e l o o k for s e v e r a l s e c o n d s t h e c u b e 'flips o v e r ' i n t h e m i n d , a n d w e see t h e o t h e r a p p a r e n t o r i e n t a t i o n . A f t e r a few m o r e s e c o n d s t h e m e n t a l i m a g e f l i p s b a c k a n d i t continues to alternate as l o n g as we look at the picture. T h e point is that neither of the t w o perceptions of the c u b e is the correct or 'true' o n e . T h e y a r e e q u a l l y c o r r e c t . S i m i l a r l y t h e v i s i o n o f life t h a t I a d v o c a t e , a n d l a b e l w i t h the n a m e o f t h e e x t e n d e d p h e n o t y p e , i s n o t p r o v a b l y m o r e c o r r e c t t h a n the o r t h o d o x v i e w . I t i s a different v i e w a n d I s u s p e c t t h a t , a t l e a s t i n s o m e r e s p e c t s , it p r o v i d e s a d e e p e r u n d e r s t a n d i n g . B u t I d o u b t t h a t t h e r e is a n y experiment that could be done to prove my claim. T h e p h e n o m e n a that I shall c o n s i d e r â&#x20AC;&#x201D; c o e v o l u t i o n , arms races, m a n i p u l a t i o n o f hosts b y p a r a s i t e s , m a n i p u l a t i o n o f t h e i n a n i m a t e w o r l d b y l i v i n g t h i n g s , e c o n o m i c ' s t r a t e g i e s ' for m i n i m i z i n g costs a n d m a x i m i z i n g b e n e f i t s â&#x20AC;&#x201D; 1

N e c k e r C u b e s and Buffaloes

are all familiar e n o u g h , a n d are a l r e a d y the subject of intensive study. W h y , then, should the busy reader bother to go o n ? It is tempting to borrow S t e p h e n G o u l d ' s w i n n i n g l y i n g e n u o u s a p p e a l at the b e g i n n i n g of a more substantial v o l u m e ( 1 9 7 7 a ) a n d simply say, 'Please read the b o o k ' a n d y o u w i l l f i n d o u t w h y i t w a s w o r t h b o t h e r i n g t o d o s o . U n f o r t u n a t e l y I d o not h a v e t h e s a m e g r o u n d s for c o n f i d e n c e . I c a n o n l y s a y t h a t , a s o n e o r d i n a r y biologist

studying

animal

behaviour,

have

found

that

the

viewpoint

r e p r e s e n t e d b y t h e l a b e l ' e x t e n d e d p h e n o t y p e ' h a s m a d e m e see a n i m a l s a n d t h e i r b e h a v i o u r d i f f e r e n t l y , a n d I t h i n k I u n d e r s t a n d t h e m b e t t e r for it. T h e e x t e n d e d p h e n o t y p e m a y n o t c o n s t i t u t e a t e s t a b l e h y p o t h e s i s i n itself, b u t i t s o far c h a n g e s t h e w a y w e see a n i m a l s a n d p l a n t s t h a t i t m a y c a u s e u s t o t h i n k o f t e s t a b l e h y p o t h e s e s t h a t w e w o u l d o t h e r w i s e n e v e r h a v e d r e a m e d of. L o r e n z ' s ( 1 9 3 7 ) d i s c o v e r y t h a t a b e h a v i o u r p a t t e r n c a n b e t r e a t e d like a n a n a t o m i c a l o r g a n w a s n o t a d i s c o v e r y i n t h e o r d i n a r y sense. N o e x p e r i m e n t a l results w e r e a d d u c e d i n its s u p p o r t . I t w a s s i m p l y a n e w w a y o f s e e i n g facts that

were

already

commonplace,

yet

dominates

modern

ethology

( T i n b e r g e n 1 9 6 3 ) , a n d it seems to us t o d a y so o b v i o u s that it is hard to understand that it ever needed 'discovering'. Similarly, D ' A r c y Thompson's ( 1 9 1 7 ) celebrated c h a p t e r ' O n the theory of t r a n s f o r m a t i o n s . . . ' is widely r e g a r d e d a s a w o r k o f i m p o r t a n c e a l t h o u g h i t d o e s n o t a d v a n c e o r test a h y p o t h e s i s . I n a sense i t i s o b v i o u s l y n e c e s s a r i l y t r u e t h a t a n y a n i m a l f o r m can

turned

into

form

mathematical

transformation,

a l t h o u g h it is not o b v i o u s that the transformation will be a simple one. In a c t u a l l y d o i n g i t for a n u m b e r o f s p e c i f i c e x a m p l e s , D ' A r c y T h o m p s o n i n v i t e d a 'so w h a t ? ' r e a c t i o n f r o m a n y o n e f a s t i d i o u s e n o u g h t o insist t h a t science p r o c e e d s o n l y b y the falsifying o f specific hypotheses. I f w e read D ' A r c y T h o m p s o n ' s c h a p t e r a n d t h e n ask o u r s e l v e s w h a t w e n o w k n o w t h a t we did

not k n o w

before,

the a n s w e r m a y w e l l b e not m u c h .

But our

i m a g i n a t i o n is fired. We go b a c k a n d look at animals in a n e w w a y ; and we think about

theoretical problems,

this c a s e t h o s e o f e m b r y o l o g y a n d

p h y l o g e n y and their interrelations, in a new w a y . I a m , of course, not so p r e s u m p t u o u s as to c o m p a r e the present modest w o r k w i t h the masterpiece of a g r e a t b i o l o g i s t . I u s e t h e e x a m p l e s i m p l y to d e m o n s t r a t e t h a t it is possible for a t h e o r e t i c a l b o o k t o b e w o r t h r e a d i n g e v e n i f i t d o e s n o t a d v a n c e t e s t a b l e h y p o t h e s e s b u t s e e k s , i n s t e a d , t o c h a n g e t h e w a y w e see. A n o t h e r g r e a t biologist o n c e r e c o m m e n d e d that to understand the actual we must c o n t e m p l a t e the possible: ' N o practical biologist interested in sexual reproduction

would

led

work

out

the

detailed

consequences ex-

p e r i e n c e d b y o r g a n i s m s h a v i n g t h r e e o r m o r e s e x e s ; y e t w h a t else s h o u l d h e d o i f h e w i s h e s t o u n d e r s t a n d w h y t h e sexes a r e , i n f a c t , a l w a y s t w o ? ' ( F i s h e r 1930a, p . i x ) . W i l l i a m s ( 1 9 7 5 ) , M a y n a r d S m i t h (1978a) and others h a v e t a u g h t u s t h a t o n e o f t h e c o m m o n e s t , m o s t u n i v e r s a l f e a t u r e s o f life o n E a r t h , sexuality

itself,

should

not

accepted

without

question.

Indeed,

its

N e c k e r C u b e s and Buffaloes

e x i s t e n c e turns o u t t o b e p o s i t i v e l y s u r p r i s i n g w h e n set a g a i n s t t h e i m a g i n e d possibility of asexual r e p r o d u c t i o n . To i m a g i n e a s e x u a l r e p r o d u c t i o n as a h y p o t h e t i c a l p o s s i b i l i t y i s n o t difficult, s i n c e w e k n o w i t i s a r e a l i t y i n s o m e animals and plants. B u t are there other cases w h e r e o u r i m a g i n a t i o n r e c e i v e s n o s u c h p r o m p t i n g ? A r e t h e r e i m p o r t a n t facts a b o u t life t h a t w e h a r d l y notice simply

because we

lack

the

imagination

visualise

alternatives

w h i c h , like Fisher's three sexes, m i g h t h a v e existed in some possible w o r l d ? I shall try t o s h o w t h a t t h e a n s w e r i s y e s . Playing with an imaginary world, in order to increase our understanding of the actual w o r l d , is the t e c h n i q u e of ' t h o u g h t e x p e r i m e n t ' . It is m u c h used by p h i l o s o p h e r s . F o r i n s t a n c e in a c o l l e c t i o n of essays on Mind (ed.

Glover

1976),

The Philosophy of

various authors i m a g i n e surgical operations in

which one person's brain is transplanted into another person's b o d y , and t h e y use t h e t h o u g h t e x p e r i m e n t t o c l a r i f y t h e m e a n i n g o f ' p e r s o n a l i d e n t i t y ' . A t times philosophers' t h o u g h t e x p e r i m e n t s are p u r e l y i m a g i n a r y a n d w i l d l y i m p r o b a b l e , b u t this d o e s n ' t m a t t e r g i v e n t h e p u r p o s e for w h i c h t h e y a r e m a d e . A t o t h e r t i m e s t h e y a r e i n f o r m e d , t o a g r e a t e r o r lesser e x t e n t , b y facts from t h e r e a l w o r l d , for i n s t a n c e t h e facts o f s p l i t - b r a i n e x p e r i m e n t s . Consider

another

thought

experiment,

this

time

from

evolutionary

b i o l o g y . W h e n I w a s a n u n d e r g r a d u a t e o b l i g e d t o w r i t e s p e c u l a t i v e essays o n 'the origin o f the C h o r d a t e s ' a n d other topics o f r e m o t e p h y l o g e n y , o n e o f m y tutors r i g h t l y tried t o s h a k e m y faith i n t h e v a l u e o f s u c h s p e c u l a t i o n s b y suggesting that a n y t h i n g c o u l d , in principle, e v o l v e into a n y t h i n g else. E v e n insects c o u l d e v o l v e i n t o m a m m a l s , i f o n l y t h e r i g h t s e q u e n c e o f s e l e c t i o n pressures w e r e p r o v i d e d i n the r i g h t o r d e r . A t t h e t i m e , a s m o s t z o o l o g i s t s w o u l d , I d i s m i s s e d t h e i d e a a s o b v i o u s n o n s e n s e , a n d I still, o f c o u r s e , d o n ' t b e l i e v e t h a t the r i g h t s e q u e n c e o f s e l e c t i o n p r e s s u r e s e v e r w o u l d b e p r o v i d e d . N o r d i d m y t u t o r . B u t a s far a s t h e p r i n c i p l e i s c o n c e r n e d , a s i m p l e t h o u g h t experiment shows it to be nearly incontrovertible. We need only prove that t h e r e exists a c o n t i n u o u s series of s m a l l steps l e a d i n g f r o m an i n s e c t , s a y a s t a g b e e t l e , t o a m a m m a l , s a y a s t a g . B y this I m e a n t h a t , s t a r t i n g w i t h t h e beetle, we could lay out a sequence of hypothetical animals, e a c h one as s i m i l a r t o t h e p r e v i o u s m e m b e r o f t h e series a s a p a i r o f b r o t h e r s m i g h t b e , a n d the s e q u e n c e w o u l d c u l m i n a t e i n a r e d d e e r s t a g . T h e proof is easy, p r o v i d e d only that we a c c e p t , as e v e r y o n e does, that b e e t l e a n d d e e r h a v e a c o m m o n a n c e s t o r , h o w e v e r far b a c k . E v e n i f t h e r e i s n o o t h e r s e q u e n c e o f steps f r o m b e e t l e t o d e e r , w e k n o w t h a t a t least o n e sequence must be obtained by simply tracing the beetle's ancestors b a c k to the c o m m o n a n c e s t o r , t h e n w o r k i n g f o r w a r d s d o w n t h e o t h e r l i n e t o t h e deer. We

have

proved

that

there

exists

trajectory

of stepwise

change

connecting beetle to deer and, by implication, a similar trajectory from a n y modern a n i m a l to any other m o d e r n animal. In principle, therefore, we m a y

N e c k e r C u b e s and Buffaloes

p r e s u m e t h a t a series o f s e l e c t i o n p r e s s u r e s c o u l d b e a r t i f i c i a l l y c o n t r i v e d t o p r o p e l a l i n e a g e a l o n g o n e of these trajectories.

It was a q u i c k thought

e x p e r i m e n t a l o n g t h e s e lines t h a t e n a b l e d m e t o s a y , w h e n d i s c u s s i n g D ' A r c y T h o m p s o n ' s t r a n s f o r m a t i o n s , t h a t ' I n a sense i t i s o b v i o u s l y n e c e s s a r i l y true that a n y a n i m a l form c a n be turned into a related form by a m a t h e m a t i c a l t r a n s f o r m a t i o n , a l t h o u g h it is n o t o b v i o u s t h a t t h e t r a n s f o r m a t i o n w i l l be a simple

one.'

this

book

shall

make

frequent

use

of the

thought-

e x p e r i m e n t t e c h n i q u e . I w a r n t h e r e a d e r o f this i n a d v a n c e , s i n c e scientists are s o m e t i m e s a n n o y e d by the lack of realism in such forms of reasoning. T h o u g h t e x p e r i m e n t s are not supposed to be realistic. T h e y are supposed to clarify our thinking a b o u t reality. O n e f e a t u r e o f life i n this w o r l d w h i c h , l i k e s e x , w e h a v e t a k e n for g r a n t e d and m a y b e should not, is that living matter comes in discrete p a c k a g e s called organisms.

particular,

biologists

interested

functional

explanation

u s u a l l y a s s u m e t h a t t h e a p p r o p r i a t e u n i t for d i s c u s s i o n i s t h e i n d i v i d u a l o r g a n i s m . T o us, ' c o n f l i c t ' u s u a l l y m e a n s c o n f l i c t b e t w e e n o r g a n i s m s , e a c h o n e s t r i v i n g t o m a x i m i z e its o w n i n d i v i d u a l 'fitness'. W e r e c o g n i z e s m a l l e r u n i t s s u c h a s c e l l s a n d g e n e s , a n d l a r g e r u n i t s s u c h a s p o p u l a t i o n s , societies a n d e c o s y s t e m s , b u t t h e r e i s n o d o u b t t h a t the i n d i v i d u a l b o d y , a s a discrete u n i t o f a c t i o n , e x e r t s a p o w e r f u l h o l d o v e r the m i n d s o f z o o l o g i s t s , e s p e c i a l l y those interested in the a d a p t i v e significance of a n i m a l b e h a v i o u r . O n e of my a i m s i n this b o o k i s t o b r e a k t h a t h o l d . I w a n t t o s w i t c h e m p h a s i s from the i n d i v i d u a l b o d y a s f o c a l u n i t o f f u n c t i o n a l d i s c u s s i o n . A t t h e v e r y least I w a n t t o m a k e u s a w a r e o f h o w m u c h w e t a k e for g r a n t e d w h e n w e l o o k a t life as a collection of discrete i n d i v i d u a l organisms. The

thesis

that

shall

s u p p o r t is

this.

legitimate

s p e a k of

a d a p t a t i o n s a s b e i n g 'for t h e b e n e f i t o f s o m e t h i n g , b u t t h a t s o m e t h i n g i s best n o t s e e n as t h e i n d i v i d u a l o r g a n i s m . It is a s m a l l e r u n i t w h i c h I c a l l the a c t i v e , g e r m - l i n e r e p l i c a t o r . T h e m o s t i m p o r t a n t k i n d o f r e p l i c a t o r i s the ' g e n e ' or small g e n e t i c f r a g m e n t . R e p l i c a t o r s are not, of course, selected d i r e c t l y , b u t b y p r o x y ; t h e y a r e j u d g e d b y t h e i r p h e n o t y p i c effects. A l t h o u g h for s o m e p u r p o s e s i t i s c o n v e n i e n t t o t h i n k o f t h e s e p h e n o t y p i c effects a s being p a c k a g e d together in discrete 'vehicles' such as individual organisms, this i s n o t f u n d a m e n t a l l y n e c e s s a r y . R a t h e r , t h e r e p l i c a t o r s h o u l d b e t h o u g h t o f a s h a v i n g extended p h e n o t y p i c effects, c o n s i s t i n g o f a l l its effects o n the w o r l d a t l a r g e , n o t j u s t its effects o n t h e i n d i v i d u a l b o d y i n w h i c h i t h a p p e n s to be sitting. To return to the a n a l o g y of the N e c k e r C u b e , the mental flip that I want t o e n c o u r a g e c a n b e c h a r a c t e r i z e d a s f o l l o w s . W e l o o k a t life a n d b e g i n b y seeing a collection of interacting individual organisms. We know that they c o n t a i n smaller units, a n d we k n o w that they are, in turn, parts of larger c o m p o s i t e units, but w e f i x our g a z e o n the w h o l e organisms. T h e n suddenly t h e i m a g e f l i p s . T h e i n d i v i d u a l b o d i e s a r e still t h e r e ; t h e y h a v e n o t m o v e d ,

Necker

but

they seem

have

gone

transparent.

Cubes

see

and

through

Buffaloes

them

the

r e p l i c a t i n g f r a g m e n t s o f D N A w i t h i n , a n d w e see t h e w i d e r w o r l d a s a n arena

which

these

genetic

fragments

play

out

their

tournaments

m a n i p u l a t i v e skill. G e n e s m a n i p u l a t e t h e w o r l d a n d s h a p e i t t o assist t h e i r replication. It happens that they h a v e 'chosen' to do so largely by m o u l d i n g m a t t e r i n t o l a r g e m u l t i c e l l u l a r c h u n k s w h i c h w e c a l l o r g a n i s m s , b u t this m i g h t n o t h a v e b e e n so. F u n d a m e n t a l l y , w h a t i s g o i n g o n i s t h a t r e p l i c a t i n g m o l e c u l e s e n s u r e t h e i r s u r v i v a l b y m e a n s o f p h e n o t y p i c effects o n t h e w o r l d . It is only incidentally

true

that

those p h e n o t y p i c

effects

happen

p a c k a g e d up into units c a l l e d i n d i v i d u a l o r g a n i s m s . We

not

phenomenon

at it

present

is.

appreciate

are

the

accustomed

organism to

for

asking,

the

remarkable

of any

widespread

b i o l o g i c a l p h e n o m e n o n , ' W h a t i s its s u r v i v a l v a l u e ? ' B u t w e d o n o t s a y , ' W h a t i s t h e s u r v i v a l v a l u e o f p a c k a g i n g life u p i n t o d i s c r e t e u n i t s c a l l e d o r g a n i s m s ? ' W e a c c e p t i t a s a g i v e n f e a t u r e o f t h e w a y life is. A s I h a v e already noted, the o r g a n i s m b e c o m e s the a u t o m a t i c subject of o u r questions a b o u t the s u r v i v a l v a l u e o f o t h e r t h i n g s : ' I n w h a t w a y d o e s this b e h a v i o u r p a t t e r n b e n e f i t the i n d i v i d u a l d o i n g i t ? I n w h a t w a y d o e s this m o r p h o l o g i c a l structure benefit the i n d i v i d u a l it is a t t a c h e d t o ? ' It has

become

a kind

of 'central

theorem'

(Barash

1977)

of m o d e r n

ethology that organisms are e x p e c t e d to b e h a v e in such a w a y as to benefit their

own

inclusive

fitness

(Hamilton

1964a,b),

rather

than

benefit

a n y o n e , o r a n y t h i n g , else. W e d o n o t ask i n w h a t w a y t h e b e h a v i o u r o f t h e left h i n d l e g b e n e f i t s t h e left h i n d l e g . N o r , n o w a d a y s , d o m o s t o f u s ask h o w the b e h a v i o u r o f a g r o u p o f o r g a n i s m s , o r t h e s t r u c t u r e o f a n e c o s y s t e m , benefits

that

group

ecosystem.

treat

groups

and

ecosystems

collections of warring, or uneasily cohabiting, organisms; a n d we treat legs, k i d n e y s , a n d cells a s c o o p e r a t i n g c o m p o n e n t s o f a s i n g l e o r g a n i s m . I a m n o t necessarily objecting to

this f o c u s o f a t t e n t i o n o n

individual

organisms,

m e r e l y c a l l i n g a t t e n t i o n t o i t a s s o m e t h i n g t h a t w e t a k e for g r a n t e d . P e r h a p s we

should

stop

taking

for

granted

and

start

wondering

about

the

i n d i v i d u a l o r g a n i s m , a s s o m e t h i n g t h a t n e e d s e x p l a i n i n g i n its o w n r i g h t , just a s w e f o u n d s e x u a l r e p r o d u c t i o n t o b e s o m e t h i n g t h a t n e e d s e x p l a i n i n g i n its o w n right. A t this p o i n t a n a c c i d e n t o f t h e h i s t o r y o f b i o l o g y n e c e s s i t a t e s a t i r e s o m e digression. T h e p r e v a i l i n g o r t h o d o x y o f m y p r e v i o u s p a r a g r a p h , the c e n t r a l d o g m a of individual organisms w o r k i n g to m a x i m i z e their o w n r e p r o d u c t i v e success, t h e p a r a d i g m o f ' t h e selfish o r g a n i s m ' , w a s D a r w i n ' s p a r a d i g m , a n d it is d o m i n a n t today. O n e m i g h t i m a g i n e , therefore, that it had h a d a g o o d run for its m o n e y a n d s h o u l d , b y n o w , b e r i p e for r e v o l u t i o n , o r a t l e a s t constitute a solid-enough bastion to withstand iconoclastic pinpricks such as a n y t h a t this b o o k m i g h t d e l i v e r . U n f o r t u n a t e l y , a n d this i s t h e h i s t o r i c a l accident I m e n t i o n e d , a l t h o u g h it is true that there has s e l d o m b e e n a n y

N e c k e r C u b e s a n d Buffaloes

t e m p t a t i o n t o t r e a t u n i t s s m a l l e r t h a n t h e o r g a n i s m a s a g e n t s w o r k i n g for their o w n benefit, the s a m e has not a l w a y s been true of larger units. T h e i n t e r v e n i n g y e a r s s i n c e D a r w i n h a v e s e e n a n a s t o n i s h i n g r e t r e a t from his individual-centred

stand,

lapse

into

sloppily

unconscious

group-

selectionism, ably d o c u m e n t e d by W i l l i a m s (1966), Ghiselin (1974a) and o t h e r s . A s H a m i l t o n ( 1 9 7 5 a ) p u t it, ' . . . a l m o s t t h e w h o l e field o f b i o l o g y s t a m p e d e d in the d i r e c t i o n w h e r e D a r w i n h a d g o n e c i r c u m s p e c t l y or not at a l l ' . I t i s o n l y i n r e c e n t y e a r s , r o u g h l y c o i n c i d i n g w i t h t h e b e l a t e d rise t o f a s h i o n o f H a m i l t o n ' s o w n i d e a s ( D a w k i n s 1 9 7 9 b ) , t h a t t h e s t a m p e d e has b e e n h a l t e d a n d t u r n e d . W e p a i n f u l l y s t r u g g l e d b a c k , h a r a s s e d b y s n i p i n g from a Jesuitically until

sophisticated finally

and

regained

dedicated Darwin's

neo-group-selectionist

ground,

the

position

rearguard, that

c h a r a c t e r i z i n g b y t h e l a b e l ' t h e selfish o r g a n i s m ' , t h e p o s i t i o n w h i c h , i n its m o d e r n f o r m , is d o m i n a t e d by t h e c o n c e p t of i n c l u s i v e fitness. Yet it is this h a r d - w o n fastness

that

m a y seem to

be a b a n d o n i n g here,

abandoning

a l m o s t b e f o r e i t i s p r o p e r l y s e c u r e d ; a n d for w h a t ? F o r a f l i c k e r i n g N e c k e r C u b e , a m e t a p h y s i c a l c h i m e r a called the e x t e n d e d p h e n o t y p e ? N o , t o r e n o u n c e t h o s e g a i n s i s far f r o m m y i n t e n t i o n . T h e p a r a d i g m o f the selfish o r g a n i s m i s v a s t l y p r e f e r a b l e t o w h a t H a m i l t o n ( 1 9 7 7 ) h a s c a l l e d 'the old,

departing

paradigm

of adaptation

for

the

benefit

of the

species'.

' E x t e n d e d p h e n o t y p e ' is misunderstood if it is taken to h a v e a n y connection w i t h a d a p t a t i o n a t t h e l e v e l o f t h e g r o u p . T h e selfish o r g a n i s m , a n d the selfish g e n e w i t h its e x t e n d e d p h e n o t y p e , a r e t w o v i e w s o f t h e s a m e N e c k e r C u b e . T h e r e a d e r w i l l n o t e x p e r i e n c e t h e c o n c e p t u a l f l i p - o v e r t h a t I seek t o assist u n l e s s h e b e g i n s b y l o o k i n g a t t h e r i g h t c u b e . T h i s b o o k i s a d d r e s s e d t o those that a l r e a d y a c c e p t the currently fashionable selfish-organism view of life, r a t h e r t h a n a n y f o r m o f ' g r o u p b e n e f i t ' v i e w . I a m n o t s a y i n g t h a t t h e selfish o r g a n i s m v i e w i s n e c e s s a r i l y w r o n g , b u t m y a r g u m e n t , i n its s t r o n g f o r m , i s t h a t i t i s l o o k i n g a t the m a t t e r t h e w r o n g w a y u p . I o n c e o v e r h e a r d an e m i n e n t C a m b r i d g e ethologist say to an eminent Austrian ethologist (they were a r g u i n g about behaviour d e v e l o p m e n t ) : ' Y o u k n o w , w e r e a l l y a g r e e . I t i s j u s t t h a t y o u say i t w r o n g . ' G e n t l e ' i n d i v i d u a l s e l e c t i o n i s t ' , w e r e a l l y d o a l m o s t a g r e e , a t least i n c o m p a r i s o n t o the g r o u p s e l e c t i o n i s t s . I t i s j u s t t h a t y o u see i t w r o n g ! B o n n e r ( 1 9 5 8 ) , discussing single-celled organisms, said ' . . . w h a t special u s e t o t h e s e o r g a n i s m s a r e n u c l e a r g e n e s ? H o w d i d t h e y arise b y s e l e c t i o n ? ' This is a g o o d e x a m p l e of the kind of i m a g i n a t i v e , r a d i c a l question that I t h i n k w e o u g h t t o a s k a b o u t life. B u t i f t h e thesis o f this b o o k i s a c c e p t e d , the particular question should be turned upside d o w n . Instead of asking of what use n u c l e a r g e n e s a r e t o organisms, w e s h o u l d ask w h y genes c h o s e t o g r o u p t h e m s e l v e s t o g e t h e r i n n u c l e i , a n d i n o r g a n i s m s . I n the o p e n i n g lines o f the same work, B o n n e r says: 'I do not propose to say a n y t h i n g new or original in these lectures. B u t I am a g r e a t b e l i e v e r in s a y i n g familiar, w e l l - k n o w n

N e c k e r C u b e s a n d Buffaloes

things b a c k w a r d s a n d inside out, h o p i n g that from s o m e n e w v a n t a g e p o i n t the o l d facts w i l l t a k e o n a d e e p e r s i g n i f i c a n c e . I t i s l i k e h o l d i n g a n a b s t r a c t painting upside d o w n ; I do not say that the m e a n i n g of the picture will suddenly be clear, but s o m e of the structure of the c o m p o s i t i o n that w a s hidden m a y show itself

(p.

I).

I c a m e a c r o s s this after w r i t i n g m y o w n

Necker C u b e passage, and was delighted to find the same v i e w s expressed by so respected an author. T h e trouble with my Necker Cubes, and with Bonner's abstract painting, is that, as analogies, they m a y be too timid a n d u n a m b i t i o u s . T h e a n a l o g y o f the N e c k e r C u b e e x p r e s s e s m y minimum h o p e for this b o o k . I a m p r e t t y confident that to look

a t life i n t e r m s o f g e n e t i c r e p l i c a t o r s p r e s e r v i n g

t h e m s e l v e s b y m e a n s o f t h e i r e x t e n d e d p h e n o t y p e s i s a t least a s s a t i s f a c t o r y a s t o l o o k a t i t i n t e r m s o f selfish o r g a n i s m s m a x i m i z i n g t h e i r i n c l u s i v e fitness. I n m a n y c a s e s t h e t w o w a y s o f l o o k i n g a t life w i l l , i n d e e d , b e e q u i v a l e n t . A s I shall s h o w , ' i n c l u s i v e f i t n e s s ' w a s d e f i n e d i n s u c h a w a y a s t o t e n d t o m a k e ' t h e i n d i v i d u a l m a x i m i z e s its i n c l u s i v e f i t n e s s ' e q u i v a l e n t t o ' t h e g e n e t i c replicators m a x i m i z e their s u r v i v a l ' . At least, therefore, the biologist s h o u l d try b o t h w a y s o f t h i n k i n g , a n d c h o o s e t h e o n e h e o r s h e p r e f e r s . B u t I s a i d this w a s a m i n i m u m h o p e . I s h a l l discuss p h e n o m e n a , ' m e i o t i c d r i v e ' for instance, w h o s e e x p l a n a t i o n is l u c i d l y written on the se c on d face of the c u b e , b u t w h i c h m a k e n o sense a t all i f w e k e e p o u r m e n t a l g a z e f i r m l y f i x e d o n t h e o t h e r f a c e , t h a t o f t h e selfish o r g a n i s m . M o v i n g f r o m m y m i n i m u m h o p e t o my wildest d a y d r e a m , it is that w h o l e areas of b i o l o g y , the s t u d y of a n i m a l communication, ecology,

indeed

animal all

artefacts,

interactions

parasitism between

and and

symbiosis, within

community

organisms,

will

eventually b e i l l u m i n a t e d i n n e w w a y s b y the d o c t r i n e o f the e x t e n d e d p h e n o t y p e . As is the w a y w i t h a d v o c a t e s , I shall try to m a k e the strongest c a s e I c a n , a n d this m e a n s t h e c a s e for t h e w i l d e r h o p e s r a t h e r t h a n t h e m o r e cautious m i n i m u m expectations. I f these g r a n d i o s e h o p e s a r e e v e n t u a l l y r e a l i z e d , p e r h a p s a less m o d e s t a n a l o g y t h a n the N e c k e r C u b e w i l l b e p a r d o n e d . C o l i n T u r n b u l l ( 1 9 6 1 ) t o o k a p y g m y friend, K e n g e , o u t o f t h e forest for t h e f i r s t t i m e i n his life, a n d t h e y climbed a m o u n t a i n together a n d looked out o v e r the plains. K e n g e s a w s o m e b u f f a l o ' g r a z i n g l a z i l y s e v e r a l m i l e s a w a y , far d o w n b e l o w . H e t u r n e d t o m e and said. " W h a t insects are t h o s e ? " . . . A t f i r s t I h a r d l y u n d e r s t o o d , t h e n I r e a l i z e d t h a t in t h e forest v i s i o n is so l i m i t e d t h a t t h e r e is no g r e a t n e e d t o m a k e a n a u t o m a t i c a l l o w a n c e for d i s t a n c e w h e n j u d g i n g s i z e . O u t h e r e i n t h e p l a i n s , K e n g e w a s l o o k i n g for t h e f i r s t t i m e o v e r a p p a r e n t l y u n e n d i n g miles of unfamiliar grasslands, w i t h not a tree w o r t h the n a m e to g i v e h i m a n y basis for c o m p a r i s o n . . . W h e n I t o l d K e n g e t h a t t h e i n s e c t s w e r e buffalo, he roared w i t h l a u g h t e r a n d told me not to tell s u c h stupid lies . . . ' ( p p . 2 2 7 - 2 2 8 ) . T h i s b o o k as a w h o l e , t h e n , is a w o r k of a d v o c a c y , b u t it is a p o o r a d v o c a t e

N e c k e r C u b e s a n d Buffaloes

t h a t l e a p s p r e c i p i t a t e l y t o his c o n c l u s i o n w h e n t h e j u r y a r e s c e p t i c a l . T h e second face of my N e c k e r C u b e is unlikely to click into clear focus until near t h e e n d o f t h e b o o k . E a r l i e r c h a p t e r s p r e p a r e t h e g r o u n d , a t t e m p t t o forestall c e r t a i n risks o f m i s u n d e r s t a n d i n g , d i s s e c t t h e first f a c e o f t h e N e c k e r C u b e i n v a r i o u s w a y s , p o i n t u p r e a s o n s w h y t h e p a r a d i g m o f t h e selfish i n d i v i d u a l , i f not a c t u a l l y i n c o r r e c t , c a n l e a d to difficulties. Parts of some early chapters are frankly retrospective and even defensive. R e a c t i o n t o a p r e v i o u s w o r k ( D a w k i n s 1 9 7 6 a ) s u g g e s t s t h a t this b o o k i s l i k e l y t o r a i s e n e e d l e s s fears t h a t i t p r o m u l g a t e s t w o u n p o p u l a r ' - i s m s ' â&#x20AC;&#x201D; ' g e n e t i c d e t e r m i n i s m ' a n d 'adaptationism'. I m y s e l f a d m i t to b e i n g irritated by a book that p r o v o k e s me into m u t t e r i n g ' Y e s b u t . . .' on e v e r y p a g e , w h e n the author c o u l d e a s i l y h a v e f o r e s t a l l e d m y w o r r y b y a little c o n s i d e r a t e e x p l a n a t i o n e a r l y o n . C h a p t e r s 2 a n d 3 t r y t o r e m o v e a t least t w o m a j o r s o u r c e s o f ' y e s buttery' at the outset. C h a p t e r 4 o p e n s t h e c a s e for t h e p r o s e c u t i o n a g a i n s t t h e selfish o r g a n i s m , a n d begins to hint at the s e c o n d aspect of the N e c k e r C u b e . C h a p t e r 5 opens t h e c a s e for t h e ' r e p l i c a t o r '

as the f u n d a m e n t a l unit of natural selection.

C h a p t e r 6 r e t u r n s t o t h e i n d i v i d u a l o r g a n i s m a n d s h o w s h o w n e i t h e r it, n o r a n y other m a j o r c a n d i d a t e e x c e p t the small genetic fragment, qualifies as a true replicator. R a t h e r , the individual organism should be thought of as a ' v e h i c l e ' for r e p l i c a t o r s . C h a p t e r 7 is a d i g r e s s i o n on r e s e a r c h m e t h o d o l o g y . C h a p t e r 8 raises s o m e a w k w a r d a n o m a l i e s for t h e selfish o r g a n i s m , a n d C h a p t e r 9 continues the theme.

Chapter

10 discusses v a r i o u s notions of

'individual fitness', and concludes that they are confusing, and probably dispensable. Chapters

11,

12 and

1 3 are the heart o f the book. T h e y d e v e l o p , b y

g r a d u a l d e g r e e s , t h e i d e a o f t h e e x t e n d e d p h e n o t y p e itself, t h e s e c o n d face o f the N e c k e r C u b e .

Finally, in Chapter

1 4 , w e t u r n b a c k w i t h refreshed

c u r i o s i t y t o t h e i n d i v i d u a l o r g a n i s m a n d ask w h y , after a l l , i t i s s u c h a salient l e v e l i n t h e h i e r a r c h y o f life.

â&#x20AC;˘

2 Genetic D e t e r m i n i s m and Gene Selectionism

L o n g after his d e a t h , t e n a c i o u s r u m o u r s p e r s i s t e d t h a t A d o l f H i t l e r h a d b e e n s e e n a l i v e a n d w e l l i n S o u t h A m e r i c a , o r i n D e n m a r k , a n d for y e a r s a s u r p r i s i n g n u m b e r o f p e o p l e w i t h n o l o v e for t h e m a n o n l y r e l u c t a n t l y accepted that he w a s d e a d ( T r e v o r - R o p e r 1 9 7 2 ) . In the First W o r l d W a r a story t h a t a h u n d r e d Scotland

thousand Russian troops had

'with snow on

their boots'

been seen l a n d i n g in

b e c a m e widely current,

apparently

because o f the m e m o r a b l e vividness o f that s n o w ( T a y l o r 1 9 6 3 ) . I n o u r o w n time

myths

such

that

of computers

persistently

sending

householders

e l e c t r i c i t y bills for a m i l l i o n p o u n d s ( E v a n s 1 9 7 9 ) , o r o f w e l l - h e e l e d w e l f a r e scroungers

with

two

expensive

cars

parked

outside

their

government-

subsidized council houses, are familiar to the point of cliche. T h e r e are some falsehoods, or half-truths, that seem to e n g e n d e r in us an a c t i v e desire to b e l i e v e t h e m a n d pass t h e m o n e v e n i f w e find t h e m u n p l e a s a n t , m a y b e i n p a r t , p e r v e r s e l y , because w e find t h e m u n p l e a s a n t . C o m p u t e r s a n d e l e c t r o n i c ' c h i p s ' p r o v o k e m o r e t h a n t h e i r fair s h a r e o f such m y t h - m a k i n g ,

perhaps because c o m p u t e r technology advances at a

speed w h i c h i s l i t e r a l l y f r i g h t e n i n g . I k n o w a n o l d p e r s o n w h o h a s i t o n g o o d authority that 'chips' are u s u r p i n g h u m a n functions to the extent not o n l y of 'driving tractors' but even of 'fertilizing w o m e n ' . G e n e s , as I shall show, are the s o u r c e o f w h a t m a y b e

even larger mythology

than computers.

I m a g i n e t h e result o f c o m b i n i n g t h e s e t w o p o w e r f u l m y t h s , t h e g e n e m y t h a n d the c o m p u t e r m y t h ! I b e l i e v e t h a t I m a y h a v e i n a d v e r t e n t l y a c h i e v e d some such unfortunate synthesis in the m i n d s of a few readers of my p r e v i o u s book,

and

the

result

was

comic

misunderstanding.

Happily,

such

mis-

understanding was not widespread, but it is w o r t h trying to a v o i d a repeat of it here, and that is o n e purpose of the present c h a p t e r . I shall e x p o s e the myth of genetic d e t e r m i n i s m , a n d e x p l a i n w h y it is necessary to use l a n g u a g e that c a n b e u n f o r t u n a t e l y m i s u n d e r s t o o d a s g e n e t i c d e t e r m i n i s m . A r e v i e w e r of W i l s o n ' s ( 1 9 7 8 )

On Human Nature, w r o t e :

' . . . a l t h o u g h he

does n o t go as far as R i c h a r d D a w k i n s (The Selfish Gene . . . ) in p r o p o s i n g s e x 9

G e n e t i c D e t e r m i n i s m and G e n e S e l e c t i o n i s m

l i n k e d g e n e s for " p h i l a n d e r i n g " , for W i l s o n h u m a n m a l e s h a v e a g e n e t i c tendency towards p o l y g y n y , females towards constancy (don't blame your m a t e s for s l e e p i n g a r o u n d , l a d i e s , it's n o t t h e i r f a u l t t h e y a r e g e n e t i c a l l y p r o g r a m m e d ) . G e n e t i c d e t e r m i n i s m c o n s t a n t l y c r e e p s i n a t the b a c k d o o r ' (Rose

1 9 7 8 ) . T h e r e v i e w e r ' s clear i m p l i c a t i o n is that the authors he is

c r i t i c i z i n g b e l i e v e in the existence of genes that force h u m a n males to be irremediable infidelity.

philanderers

The

who

cannot

r e a d e r i s left w i t h

therefore

the impression

blamed

that

for

marital

those authors are

protagonists in the 'nature or nurture' debate, and, moreover, died-in-thewool hereditarians with male chauvinist leanings. I n fact humans.

my original

passage about

'philanderer males'

w a s not about

It w a s a simple m a t h e m a t i c a l m o d e l of some unspecified animal

( n o t t h a t it m a t t e r s , I h a d a b i r d in m i n d ) . It w a s n o t e x p l i c i t l y (see b e l o w ) a m o d e l o f g e n e s , a n d i f i t h a d b e e n a b o u t g e n e s t h e y w o u l d h a v e b e e n sexl i m i t e d , n o t s e x - l i n k e d ! I t w a s a m o d e l o f ' s t r a t e g i e s ' i n t h e sense o f M a y n a r d Smith

( 1 9 7 4 ) . T h e ' p h i l a n d e r e r ' s t r a t e g y w a s p o s t u l a t e d , n o t a s the w a y

males b e h a v e , but as one of t w o hypothetical alternatives, the other being t h e ' f a i t h f u l ' s t r a t e g y . T h e p u r p o s e o f this v e r y s i m p l e m o d e l w a s t o illustrate the kinds of conditions under w h i c h philandering might be favoured by n a t u r a l s e l e c t i o n , a n d t h e k i n d s o f c o n d i t i o n s u n d e r w h i c h faithfulness m i g h t b e f a v o u r e d . T h e r e w a s n o p r e s u m p t i o n that p h i l a n d e r i n g w a s m o r e likely i n m a l e s t h a n f a i t h f u l n e s s . I n d e e d , t h e p a r t i c u l a r r u n o f t h e s i m u l a t i o n that I published

culminated

i n a m i x e d m a l e p o p u l a t i o n i n w h i c h faithfulness

slightly p r e d o m i n a t e d ( D a w k i n s 1976a, p.

1 6 5 , a l t h o u g h see S c h u s t e r &

S i g m u n d 1 9 8 1 ) . T h e r e is not just one misunderstanding in Rose's remarks, but multiple c o m p o u n d e d misunderstanding. T h e r e is a w a n t o n eagerness to misunderstand.

It bears the stamp of snow-covered Russian jackboots, of

little b l a c k m i c r o c h i p s m a r c h i n g to usurp the m a l e role and steal o u r tractord r i v e r s ' j o b s . It is a m a n i f e s t a t i o n of a p o w e r f u l m y t h , in this c a s e the g r e a t gene myth. T h e g e n e m y t h i s e p i t o m i z e d i n R o s e ' s p a r e n t h e t i c little j o k e a b o u t l a d i e s n o t b l a m i n g t h e i r m a t e s for s l e e p i n g a r o u n d .

It is the m y t h of 'genetic

d e t e r m i n i s m ' . E v i d e n t l y , for R o s e , g e n e t i c d e t e r m i n i s m i s d e t e r m i n i s m i n the full p h i l o s o p h i c a l s e n s e o f i r r e v e r s i b l e i n e v i t a b i l i t y .

H e a s s u m e s t h a t the

e x i s t e n c e o f a g e n e ' f o r ' X i m p l i e s t h a t X c a n n o t b e e s c a p e d . I n the w o r d s o f another critic of 'genetic determinism', G o u l d

( 1 9 7 8 , p . 238), ' I f w e are

p r o g r a m m e d t o b e w h a t w e a r e , t h e n these traits a r e i n e l u c t a b l e . W e m a y , a t best, c h a n n e l t h e m , but we c a n n o t c h a n g e t h e m either by will, e d u c a t i o n , or culture.' T h e v a l i d i t y o f t h e d e t e r m i n i s t p o i n t o f v i e w a n d , s e p a r a t e l y , its b e a r i n g o n a n i n d i v i d u a l ' s m o r a l r e s p o n s i b i l i t y for his a c t i o n s , h a s b e e n d e b a t e d b y p h i l o s o p h e r s a n d t h e o l o g i a n s for c e n t u r i e s p a s t , a n d n o d o u b t w i l l b e for centuries to c o m e . I suspect that both R o s e and G o u l d are determinists in

Genetic D e t e r m i n i s m and Gene Selectionism

that t h e y b e l i e v e i n a p h y s i c a l , m a t e r i a l i s t i c basis for a l l o u r a c t i o n s . S o a m I . We w o u l d also p r o b a b l y all three agree that h u m a n nervous systems are so c o m p l e x that in practice we c a n forget a b o u t d e t e r m i n i s m a n d b e h a v e as if w e h a d free w i l l . N e u r o n e s m a y b e a m p l i f i e r s o f f u n d a m e n t a l l y i n d e t e r m i n a t e physical events. T h e only point I wish to m a k e is that, w h a t e v e r v i e w one t a k e s o n the q u e s t i o n o f d e t e r m i n i s m , t h e i n s e r t i o n o f t h e w o r d ' g e n e t i c ' i s not g o i n g t o m a k e a n y d i f f e r e n c e . I f y o u a r e a f u l l - b l o o d e d d e t e r m i n i s t y o u w i l l b e l i e v e t h a t all y o u r a c t i o n s a r e p r e d e t e r m i n e d b y p h y s i c a l c a u s e s i n t h e past, a n d y o u m a y o r m a y n o t a l s o b e l i e v e t h a t y o u t h e r e f o r e c a n n o t b e h e l d responsible

for

your sexual

infidelities.

But,

that

may,

what

difference c a n it possibly m a k e w h e t h e r some of those p h y s i c a l causes are genetic? W h y a r e g e n e t i c d e t e r m i n a n t s t h o u g h t t o b e a n y m o r e i n e l u c t a b l e , o r blame-absolving, than 'environmental' ones? T h e belief that genes are s o m e h o w super-deterministic,

in comparison

with environmental causes, is a m y t h of extraordinary tenacity, and it c a n g i v e rise t o r e a l e m o t i o n a l distress. I w a s o n l y d i m l y a w a r e o f this u n t i l i t w a s m o v i n g l y b r o u g h t h o m e t o m e i n a q u e s t i o n session a t a m e e t i n g o f t h e A m e r i c a n A s s o c i a t i o n for t h e A d v a n c e m e n t o f S c i e n c e i n 1 9 7 8 . A y o u n g w o m a n asked the lecturer, a p r o m i n e n t 'sociobiologist', w h e t h e r there w a s a n y e v i d e n c e for g e n e t i c sex d i f f e r e n c e s i n h u m a n p s y c h o l o g y . I h a r d l y h e a r d the l e c t u r e r ' s a n s w e r , s o a s t o n i s h e d w a s I b y t h e e m o t i o n w i t h w h i c h t h e q u e s t i o n w a s p u t . T h e w o m a n s e e m e d t o set g r e a t s t o r e b y t h e a n s w e r a n d was almost in tears. A f t e r a m o m e n t of g e n u i n e a n d i n n o c e n t bafflement the explanation

hit m e .

Something or somebody,

certainly not

the eminent

s o c i o b i o l o g i s t himself, h a d m i s l e d h e r i n t o t h i n k i n g t h a t g e n e t i c d e t e r m i n a t i o n i s for k e e p s ; s h e s e r i o u s l y b e l i e v e d t h a t a ' y e s ' a n s w e r t o h e r q u e s t i o n w o u l d , i f c o r r e c t , c o n d e m n h e r a s a f e m a l e i n d i v i d u a l t o a life o f f e m i n i n e pursuits, c h a i n e d t o t h e n u r s e r y a n d t h e k i t c h e n sink. B u t if, u n l i k e m o s t o f us, she is a d e t e r m i n i s t in t h a t s t r o n g C a l v i n i s t i c sense, s h e s h o u l d be e q u a l l y upset w h e t h e r t h e c a u s a l f a c t o r s c o n c e r n e d a r e g e n e t i c o r ' e n v i r o n m e n t a l ' . W h a t does it ever m e a n to say that s o m e t h i n g d e t e r m i n e s s o m e t h i n g ? Philosophers, possibly w i t h justification, m a k e h e a v y w e a t h e r of the c o n c e p t of c a u s a t i o n , b u t to a w o r k i n g b i o l o g i s t c a u s a t i o n is a r a t h e r s i m p l e s t a t i s t i c a l concept. O p e r a t i o n a l l y we c a n never demonstrate that a particular observed e v e n t C c a u s e d a p a r t i c u l a r r e s u l t R , a l t h o u g h i t w i l l often b e j u d g e d h i g h l y likely. W h a t b i o l o g i s t s i n p r a c t i c e u s u a l l y d o i s t o e s t a b l i s h statistically t h a t events o f class R r e l i a b l y f o l l o w e v e n t s o f class C . T h e y n e e d a n u m b e r o f p a i r e d i n s t a n c e s o f t h e t w o classes o f e v e n t s i n o r d e r t o d o s o : o n e a n e c d o t e i s not e n o u g h . E v e n t h e o b s e r v a t i o n t h a t R e v e n t s r e l i a b l y t e n d to f o l l o w C e v e n t s after a relatively fixed time interval provides o n l y a w o r k i n g hypothesis that C events c a u s e R e v e n t s . T h e h y p o t h e s i s i s c o n f i r m e d , w i t h i n t h e l i m i t s o f t h e statistical m e t h o d , o n l y i f t h e C e v e n t s a r e d e l i v e r e d b y a n experimenter r a t h e r

G e n e t i c D e t e r m i n i s m and G e n e S e l e c t i o n i s m

t h a n s i m p l y n o t e d b y a n o b s e r v e r , a n d a r e still r e l i a b l y f o l l o w e d b y R e v e n t s . It is not necessary that e v e r y C should be followed by an R, nor that every R s h o u l d b e p r e c e d e d b y a C ( w h o has n o t h a d t o c o n t e n d w i t h a r g u m e n t s s u c h as 'smoking c a n n o t cause l u n g cancer, because I knew a non-smoker w h o d i e d o f it,

and

h e a v y s m o k e r w h o i s still g o i n g s t r o n g a t n i n e t y ' ? ) .

S t a t i s t i c a l m e t h o d s a r e d e s i g n e d t o h e l p u s assess, t o a n y s p e c i f i e d l e v e l o f probabilistic confidence,

w h e t h e r t h e results w e o b t a i n

really indicate a

causal relationship. If, t h e n , it w e r e t r u e t h a t t h e possession of a Y c h r o m o s o m e h a d a c a u s a l i n f l u e n c e o n , s a y , m u s i c a l a b i l i t y o r f o n d n e s s for k n i t t i n g , w h a t w o u l d this mean?

would

mean

that,

in s o m e specified

population

and

in some

s p e c i f i e d e n v i r o n m e n t , a n o b s e r v e r i n possession o f i n f o r m a t i o n a b o u t a n individual's

sex

would

able

make

statistically

accurate

p r e d i c t i o n a s t o t h e p e r s o n ' s m u s i c a l a b i l i t y t h a n a n o b s e r v e r i g n o r a n t o f the p e r s o n ' s s e x . T h e e m p h a s i s i s o n t h e w o r d ' s t a t i s t i c a l l y ' , a n d let u s t h r o w i n an

'other things being e q u a l '

for g o o d

measure. T h e observer might be

p r o v i d e d w i t h s o m e a d d i t i o n a l information, say on the person's e d u c a t i o n or u p b r i n g i n g , w h i c h w o u l d l e a d h i m t o r e v i s e , o r e v e n r e v e r s e , his p r e d i c t i o n based on sex.

I f f e m a l e s a r e s t a t i s t i c a l l y m o r e l i k e l y t h a n m a l e s t o enjoy

k n i t t i n g , this d o e s n o t m e a n t h a t a l l f e m a l e s e n j o y k n i t t i n g , n o r e v e n that a majority do. It is also fully c o m p a t i b l e w i t h the v i e w that the reason females enjoy knitting

that

society

brings

them

enjoy

knitting.

If society

s y s t e m a t i c a l l y t r a i n s c h i l d r e n w i t h o u t p e n i s e s t o k n i t a n d p l a y w i t h dolls, a n d t r a i n s c h i l d r e n w i t h p e n i s e s t o p l a y w i t h g u n s a n d t o y soldiers, a n y resulting differences in m a l e a n d female preferences are strictly speaking genetically

determined

differences!

They

are

determined,

through

the

m e d i u m o f s o c i e t a l c u s t o m , b y t h e fact o f possession o r n o n - p o s s e s s i o n o f a p e n i s , a n d t h a t i s d e t e r m i n e d (in a n o r m a l e n v i r o n m e n t a n d i n the a b s e n c e o f i n g e n i o u s p l a s t i c s u r g e r y o r h o r m o n e t h e r a p y ) b y sex c h r o m o s o m e s . O b v i o u s l y , o n this v i e w , i f w e e x p e r i m e n t a l l y b r o u g h t u p a s a m p l e o f b o y s to p l a y w i t h dolls a n d a s a m p l e of girls to p l a y w i t h guns, we w o u l d expect easily

reverse

the

normal

preferences.

This

might

interesting

e x p e r i m e n t t o d o , for t h e r e s u l t j u s t m i g h t t u r n o u t t o b e t h a t g i r l s still prefer d o l l s a n d b o y s still p r e f e r g u n s . I f so, this m i g h t tell u s s o m e t h i n g a b o u t the t e n a c i t y , in t h e f a c e of a particular e n v i r o n m e n t a l m a n i p u l a t i o n , of a g e n e t i c difference.

But

all

genetic

causes

have

work

the

context

of an

e n v i r o n m e n t o f s o m e k i n d . I f a g e n e t i c sex d i f f e r e n c e m a k e s i t s e l f felt t h r o u g h t h e m e d i u m o f a s e x - b i a s e d e d u c a t i o n s y s t e m , i t i s still a g e n e t i c d i f f e r e n c e . I f i t m a k e s i t s e l f felt t h r o u g h s o m e o t h e r m e d i u m , s u c h t h a t m a n i p u l a t i o n s o f t h e e d u c a t i o n s y s t e m d o n o t p e r t u r b it, i t is, i n p r i n c i p l e , n o m o r e a n d n o less a genetic difference than in the former, education-sensitive case: no doubt s o m e o t h e r e n v i r o n m e n t a l m a n i p u l a t i o n c o u l d b e f o u n d w h i c h did p e r t u r b it.

Genetic D e t e r m i n i s m and G e n e S e l e c t i o n i s m

H u m a n psychological attributes vary along almost as m a n y dimensions as p s y c h o l o g i s t s c a n m e a s u r e . I t i s difficult i n p r a c t i c e ( K e m p t h o r n e 1 9 7 8 ) , b u t i n p r i n c i p l e w e c o u l d p a r t i t i o n this v a r i a t i o n a m o n g s u c h p u t a t i v e c a u s a l factors a s a g e , h e i g h t , y e a r s o f e d u c a t i o n , t y p e o f e d u c a t i o n c l a s s i f i e d i n m a n y different w a y s , n u m b e r o f s i b l i n g s , b i r t h o r d e r , c o l o u r o f m o t h e r ' s e y e s , father's skill i n s h o e i n g h o r s e s , a n d , o f c o u r s e , s e x c h r o m o s o m e s . W e c o u l d also e x a m i n e t w o - w a y a n d m u l t i - w a y i n t e r a c t i o n s b e t w e e n s u c h f a c t o r s . F o r present purposes the i m p o r t a n t point is that the v a r i a n c e we seek to e x p l a i n will h a v e m a n y causes, w h i c h interact i n c o m p l e x w a y s . genetic

variance

a significant cause of m u c h

Undoubtedly

p h e n o t y p i c v a r i a n c e in

o b s e r v e d p o p u l a t i o n s , b u t its effects m a y b e o v e r r i d d e n , m o d i f i e d , e n h a n c e d o r r e v e r s e d b y o t h e r c a u s e s . G e n e s m a y m o d i f y t h e effects o f o t h e r g e n e s , a n d m a y modify

t h e effects o f t h e e n v i r o n m e n t .

Environmental

events,

both

i n t e r n a l a n d e x t e r n a l , m a y m o d i f y t h e effects o f g e n e s , a n d m a y m o d i f y t h e effects o f o t h e r e n v i r o n m e n t a l e v e n t s . P e o p l e s e e m t o h a v e little d i f f i c u l t y i n a c c e p t i n g t h e m o d i f i a b i l i t y o f 'environmental'

effects o n

human

development.

If a

child

has

had

bad

teaching in m a t h e m a t i c s , it is a c c e p t e d that the resulting d e f i c i e n c y c a n be r e m e d i e d b y e x t r a g o o d t e a c h i n g the f o l l o w i n g y e a r . B u t a n y s u g g e s t i o n t h a t the c h i l d ' s m a t h e m a t i c a l d e f i c i e n c y m i g h t h a v e a g e n e t i c o r i g i n i s l i k e l y t o b e greeted with something a p p r o a c h i n g despair:

i f i t i s i n t h e g e n e s 'it i s

written', it is 'determined' and nothing can be done a b o u t it; y o u m i g h t as well g i v e up a t t e m p t i n g to teach the child m a t h e m a t i c s . T h i s is p e r n i c i o u s rubbish on an almost astrological scale. G e n e t i c causes and e n v i r o n m e n t a l causes are in principle no different from e a c h other. S o m e influences of b o t h types m a y be hard to reverse; others m a y be easy to reverse. S o m e m a y be usually hard to reverse but easy if the right a g e n t is a p p l i e d . T h e i m p o r t a n t p o i n t i s t h a t t h e r e i s n o g e n e r a l r e a s o n for e x p e c t i n g g e n e t i c i n f l u e n c e s t o b e any more irreversible than environmental ones. W h a t d i d g e n e s d o t o d e s e r v e t h e i r sinister, j u g g e r n a u t - l i k e r e p u t a t i o n ? W h y d o w e n o t m a k e a s i m i l a r b o g e y o u t of, s a y , n u r s e r y e d u c a t i o n o r confirmation classes? W h y are genes t h o u g h t to be so m u c h m o r e fixed a n d i n e s c a p a b l e i n t h e i r effects t h a n t e l e v i s i o n , n u n s , o r b o o k s ? D o n ' t b l a m e y o u r m a t e s for s l e e p i n g a r o u n d , l a d i e s , it's n o t t h e i r f a u l t t h e y h a v e b e e n i n f l a m e d b y p o r n o g r a p h i c l i t e r a t u r e ! T h e a l l e g e d J e s u i t b o a s t , ' G i v e m e t h e c h i l d for his f i r s t s e v e n y e a r s , a n d I ' l l g i v e y o u t h e m a n ' , m a y h a v e s o m e t r u t h i n it. Educational, or other cultural influences m a y , in some circumstances, be just as unmodifiable a n d irreversible as genes a n d 'stars' are p o p u l a r l y t h o u g h t to be. I suppose part of the reason genes h a v e b e c o m e deterministic b o g e y s is a confusion

resulting

from

the

well-known

fact

of the

non-inheritance

a c q u i r e d c h a r a c t e r i s t i c s . B e f o r e this c e n t u r y i t w a s w i d e l y b e l i e v e d t h a t experience and other acquisitions of an individual's lifetime w e r e s o m e h o w

Genetic D e t e r m i n i s m and Gene Selectionism

i m p r i n t e d on the h e r e d i t a r y substance and transmitted to the children. T h e a b a n d o n i n g o f this belief, a n d its r e p l a c e m e n t b y W e i s m a n n ' s d o c t r i n e o f the c o n t i n u i t y o f t h e g e r m p l a s m , a n d its m o l e c u l a r c o u n t e r p a r t the ' c e n t r a l d o g m a ' , is o n e of the g r e a t a c h i e v e m e n t s of m o d e r n biology. If we steep ourselves in the implications of W e i s m a n n i a n o r t h o d o x y , there really does seem to be something j u g g e r n a u t - l i k e and inexorable about genes. T h e y march

through

generations,

influencing

the

form

and

behaviour

of a

s u c c e s s i o n o f m o r t a l b o d i e s , b u t , e x c e p t for r a r e a n d n o n - s p e c i f i c m u t a g e n i c effects, t h e y a r e n e v e r i n f l u e n c e d b y t h e e x p e r i e n c e o r e n v i r o n m e n t o f those bodies. T h e g e n e s i n m e c a m e from m y four g r a n d p a r e n t s ;

they flowed

straight t h r o u g h my parents to m e , and n o t h i n g that my parents achieved, acquired,

learned or experienced

h a d a n y effect o n those g e n e s a s t h e y

f l o w e d t h r o u g h . P e r h a p s t h e r e i s s o m e t h i n g a little sinister a b o u t that. B u t , h o w e v e r i n e x o r a b l e a n d u n d e v i a t i n g the g e n e s m a y b e a s t h e y m a r c h d o w n t h e g e n e r a t i o n s , t h e n a t u r e o f t h e i r p h e n o t y p i c effects o n t h e b o d i e s t h e y f l o w t h r o u g h i s b y n o m e a n s i n e x o r a b l e a n d u n d e v i a t i n g . I f I a m h o m o z y g o u s for a g e n e G , n o t h i n g s a v e m u t a t i o n c a n p r e v e n t m y p a s s i n g G o n t o all m y children. So m u c h is inexorable. But whether or not I, or my children, show t h e p h e n o t y p i c effect n o r m a l l y a s s o c i a t e d w i t h possession o f G m a y d e p e n d v e r y m u c h on h o w we are brought up, w h a t diet or education we experience, a n d w h a t o t h e r g e n e s w e h a p p e n t o possess. S o , o f t h e t w o effects t h a t g e n e s have on

the w o r l d â&#x20AC;&#x201D; m a n u f a c t u r i n g copies of themselves, and influencing

p h e n o t y p e s â&#x20AC;&#x201D; t h e first i s i n f l e x i b l e a p a r t f r o m t h e r a r e p o s s i b i l i t y o f m u t a t i o n ; the

second

evolution

may and

exceedingly

d e v e l o p m e n t is,

flexible.

then,

think

confusion

between

p a r t l y r e s p o n s i b l e for t h e m y t h o f

genetic determinism. But

there is another m y t h c o m p l i c a t i n g matters,

and

have already

m e n t i o n e d i t a t t h e b e g i n n i n g o f this c h a p t e r . T h e c o m p u t e r m y t h i s a l m o s t as d e e p - s e a t e d in the m o d e r n m i n d as the g e n e m y t h .

N o t i c e that both

passages I q u o t e d c o n t a i n the w o r d ' p r o g r a m m e d ' . T h u s R o s e sarcastically absolved

promiscuous

men

from

blame

because

they

are

genetically

programmed. G o u l d s a y s t h a t i f w e a r e programmed t o b e w h a t w e a r e t h e n these traits

are

ineluctable.

programmed of action.

And

to indicate

true

that

unthinking inflexibility,

Computers and

'robots'

are,

ordinarily

use

the

word

the antithesis o f f r e e d o m

by repute,

notoriously

inflexible,

c a r r y i n g out instructions to the letter, e v e n if the c o n s e q u e n c e s are obviously a b s u r d . W h y else w o u l d t h e y s e n d o u t t h o s e f a m o u s m i l l i o n p o u n d bills t h a t e v e r y b o d y ' s friend's friend's cousin's a c q u a i n t a n c e keeps r e c e i v i n g ? I had forgotten the great c o m p u t e r m y t h , as well as the great gene m y t h , or I w o u l d h a v e b e e n m o r e careful w h e n I m y s e l f w r o t e o f genes s w a r m i n g 'inside gigantic l u m b e r i n g robots . . . ' , and of ourselves as 'survival machinesâ&#x20AC;&#x201D;robot v e h i c l e s b l i n d l y p r o g r a m m e d t o p r e s e r v e t h e selfish m o l e c u l e s k n o w n a s genes'

(Dawkins

1 9 7 6 a ) . T h e s e passages h a v e been triumphantly quoted,

G e n e t i c D e t e r m i n i s m and G e n e S e l e c t i o n i s m

and

requoted

examples

apparently

of rabid

from

genetic

secondary

determinism

and

even

(e.g.

tertiary

'Nabi'

sources,

1981).

as not

a p o l o g i z i n g for u s i n g t h e l a n g u a g e o f r o b o t i c s . I w o u l d u s e i t a g a i n w i t h o u t hesitation. But I n o w realize that it is necessary to g i v e m o r e e x p l a n a t i o n . F r o m 1 3 y e a r s ' e x p e r i e n c e o f t e a c h i n g it, I k n o w t h a t a m a i n p r o b l e m w i t h the 'selfish-gene s u r v i v a l m a c h i n e ' w a y of l o o k i n g at n a t u r a l selection is a p a r t i c u l a r risk o f m i s u n d e r s t a n d i n g . T h e m e t a p h o r o f t h e i n t e l l i g e n t g e n e r e c k o n i n g u p h o w best t o e n s u r e its o w n s u r v i v a l

(Hamilton

1972)

is a

powerful and i l l u m i n a t i n g one. B u t it is all too easy to get carried a w a y , a n d allow hypothetical genes cognitive w i s d o m and foresight in p l a n n i n g their 'strategy'. A t least three out o f t w e l v e m i s u n d e r s t a n d i n g s o f kin selection (Dawkins

1979a)

a r e d i r e c t l y a t t r i b u t a b l e t o this b a s i c e r r o r . T i m e a n d

again, non-biologists h a v e tried to justify a form of g r o u p selection to me b y , i n effect, i m p u t i n g f o r e s i g h t t o g e n e s :

' T h e l o n g - t e r m interests of a g e n e

require the c o n t i n u e d existence of the species; therefore s h o u l d n ' t y o u e x p e c t adaptations to prevent species extinction, even at the expense of short-term individual r e p r o d u c t i v e success?' It w a s in an a t t e m p t to forestall errors like this t h a t I u s e d the l a n g u a g e o f a u t o m a t i o n a n d r o b o t i c s , a n d u s e d t h e w o r d ' b l i n d l y ' i n r e f e r r i n g t o g e n e t i c p r o g r a m m i n g . B u t i t is, o f c o u r s e , t h e g e n e s that are blind, not the a n i m a l s they p r o g r a m . N e r v o u s systems, like m a n made

computers,

can

sufficiently

complex

show

intelligence

and

foresight. S y m o n s (1979) m a k e s the c o m p u t e r m y t h e x p l i c i t : I wish to point out that D a w k i n s ' s i m p l i c a t i o n â&#x20AC;&#x201D; t h r o u g h the use of words

'robot'

and

'blindly'â&#x20AC;&#x201D;that

evolutionary

theory

favors

d e t e r m i n i s m is u t t e r l y w i t h o u t f o u n d a t i o n . . . A r o b o t is a m i n d l e s s automaton.

Perhaps some animals are robots

(we have no w a y of

k n o w i n g ) ; h o w e v e r , D a w k i n s i s n o t r e f e r r i n g t o some a n i m a l s , b u t t o a l l a n i m a l s a n d i n this c a s e s p e c i f i c a l l y t o h u m a n b e i n g s . N o w , t o paraphrase Stebbing, 'robot' can be opposed to 'thinking being' or it can

used

mechanically,

figuratively but

there

to indicate a person w h o seems is

common

usage

to act

of language

that

p r o v i d e s a m e a n i n g for t h e w o r d ' r o b o t ' i n w h i c h i t w o u l d m a k e sense to say that all l i v i n g things are robots [p. 4 1 ] .

T h e point o f the passage from S t e b b i n g w h i c h S y m o n s p a r a p h r a s e d i s the r e a s o n a b l e o n e t h a t X is a useless w o r d u n l e s s t h e r e a r e s o m e t h i n g s t h a t a r e n o t X . I f e v e r y t h i n g i s a r o b o t , t h e n the w o r d r o b o t d o e s n ' t m e a n a n y t h i n g useful. B u t the w o r d r o b o t h a s o t h e r a s s o c i a t i o n s , a n d r i g i d i n f l e x i b i l i t y w a s n o t t h e a s s o c i a t i o n I w a s t h i n k i n g of. A r o b o t is a p r o g r a m m e d m a c h i n e , a n d an important thing a b o u t p r o g r a m m i n g is that it is distinct from, and done in

advance

of,

performance

of the

behaviour

itself.

computer

Genetic D e t e r m i n i s m and Gene Selectionism

p r o g r a m m e d to p e r f o r m the b e h a v i o u r of c a l c u l a t i n g s q u a r e roots, or p l a y i n g c h e s s . T h e r e l a t i o n s h i p b e t w e e n a c h e s s - p l a y i n g c o m p u t e r a n d the person w h o p r o g r a m m e d it is not obvious, and is open to misunderstanding. It m i g h t be t h o u g h t that the p r o g r a m m e r w a t c h e s the progress of the g a m e and gives instructions to the c o m p u t e r m o v e by m o v e .

I n fact, h o w e v e r , the

p r o g r a m m i n g i s finished b e f o r e t h e g a m e b e g i n s . T h e p r o g r a m m e r tries t o anticipate

contingencies,

and

builds

conditional

instructions

of great

c o m p l e x i t y , b u t o n c e t h e g a m e b e g i n s h e h a s t o k e e p his h a n d s off. H e i s n o t a l l o w e d t o g i v e the c o m p u t e r a n y n e w hints d u r i n g the course o f the g a m e . I f h e d i d h e w o u l d n o t b e p r o g r a m m i n g b u t p e r f o r m i n g , a n d his e n t r y w o u l d be disqualified from the t o u r n a m e n t . In the w o r k criticized by S y m o n s , I m a d e e x t e n s i v e use o f t h e a n a l o g y o f c o m p u t e r chess i n o r d e r t o e x p l a i n the p o i n t t h a t g e n e s d o n o t c o n t r o l b e h a v i o u r d i r e c t l y i n t h e sense o f i n t e r f e r i n g i n its p e r f o r m a n c e . T h e y o n l y c o n t r o l b e h a v i o u r i n t h e sense o f p r o g r a m m i n g t h e m a c h i n e i n advance o f p e r f o r m a n c e . I t w a s this a s s o c i a t i o n w i t h the w o r d robot that I w a n t e d to i n v o k e , not the association w i t h mindless inflexibility. A s for t h e m i n d l e s s i n f l e x i b i l i t y a s s o c i a t i o n itself,

it could

have been

justified in the d a y s w h e n the a c m e of a u t o m a t i o n w a s the rod and c a m control system of a marine engine, and K i p l i n g wrote ' M c A n d r e w ' s H y m n ' :

F r o m c o u p l e r - f l a n g e t o s p i n d l e - g u i d e I see T h y H a n d , O G o d Predestination in the stride o' y o n c o n n e c t i n ' - r o d . J o h n C a l v i n m i g h t h a ' forged the s a m e â&#x20AC;&#x201D;

But that w a s 1893 a n d the h e y d a y o f steam. W e are n o w w e l l e m b a r k e d o n t h e g o l d e n a g e o f e l e c t r o n i c s . I f m a c h i n e s e v e r h a d a s s o c i a t i o n s w i t h rigid inflexibilityâ&#x20AC;&#x201D; and I a c c e p t that they h a d â&#x20AC;&#x201D; i t is high time they lived them down.

Computer

International

programs

have

Master standard

now

(Levy

been

written

that

play

chess

1978), that converse and reason in

correct and indefinitely c o m p l e x grammatical

English

(Winograd

1972),

that c r e a t e e l e g a n t a n d aesthetically satisfying n e w proofs o f m a t h e m a t i c a l theorems (Hofstadter 1 9 7 9 ) , that c o m p o s e music and diagnose illness; and t h e p a c e o f p r o g r e s s i n t h e f i e l d s h o w s n o sign o f s l o w i n g d o w n ( E v a n s 1 9 7 9 ) . T h e a d v a n c e d p r o g r a m m i n g field k n o w n as artificial intelligence is in a b u o y a n t , confident state ( B o d e n 1 9 7 7 ) . F e w w h o h a v e studied i t w o u l d n o w b e t a g a i n s t c o m p u t e r p r o g r a m s b e a t i n g t h e s t r o n g e s t G r a n d M a s t e r s a t chess w i t h i n the n e x t 10 years. F r o m b e i n g s y n o n y m o u s in the p o p u l a r mind with a

moronically

undeviating, jerky-limbed

zombie,

'robot'

will

one

day

b e c o m e a b y w o r d for f l e x i b i l i t y a n d r a p i d i n t e l l i g e n c e . U n f o r t u n a t e l y I j u m p e d t h e g u n a little i n t h e p a s s a g e q u o t e d . W h e n I wrote

had just

returned

from

eye-opening

and

mind-boggling

c o n f e r e n c e on the state of the art of artificial intelligence p r o g r a m m i n g , and

Genetic D e t e r m i n i s m and Gene Selectionism

genuinely

and

innocently

enthusiasm

forgot

that

robots

are

p o p u l a r l y s u p p o s e d t o b e i n f l e x i b l e i d i o t s . I a l s o h a v e t o a p o l o g i z e for t h e fact t h a t , w i t h o u t m y k n o w l e d g e , t h e c o v e r o f t h e G e r m a n e d i t i o n o f The Selfish Gene w a s g i v e n a p i c t u r e o f a h u m a n p u p p e t j e r k i n g o n t h e e n d o f strings d e s c e n d i n g f r o m t h e w o r d g e n e , a n d t h e F r e n c h e d i t i o n a p i c t u r e o f little b o w l e r - h a t t e d m e n w i t h c l o c k w o r k w i n d - u p k e y s s t i c k i n g o u t o f t h e i r b a c k s . I h a v e h a d slides o f b o t h c o v e r s m a d e u p a s i l l u s t r a t i o n s o f w h a t I w a s not t r y i n g to s a y . S o , the a n s w e r to S y m o n s is that of course he w a s right to criticize w h a t he thought I was saying, but of course I wasn't actually s a y i n g it ( R i d l e y 1 9 8 0 a ) . N o d o u b t I w a s p a r t l y t o b l a m e for t h e o r i g i n a l m i s u n d e r s t a n d i n g , but I c a n o n l y u r g e n o w that we put aside the p r e c o n c e p t i o n s d e r i v e d from common

usage

('...most

men

don't

understand

computers

even

the

slightest d e g r e e ' â&#x20AC;&#x201D; W e i z e n b a u m 1 9 7 6 , p . 9 ) , a n d a c t u a l l y g o a n d r e a d s o m e of the fascinating m o d e r n literature on robotics a n d c o m p u t e r intelligence (e.g. B o d e n 1 9 7 7 ; E v a n s 1 9 7 9 ; Hofstadter 1 9 7 9 ) . O n c e again, of course, philosophers m a y debate the ultimate d e t e r m i n a c y of computers p r o g r a m m e d to b e h a v e in artificially intelligent w a y s , but if we are g o i n g t o g e t i n t o t h a t l e v e l o f p h i l o s o p h y m a n y w o u l d a p p l y t h e s a m e arguments to h u m a n intelligence ( T u r i n g 1950). W h a t is a brain, they w o u l d ask, b u t a c o m p u t e r , a n d w h a t i s e d u c a t i o n b u t a f o r m o f p r o g r a m m i n g ? I t i s very

hard

give

a non-supernatural

account

of the

human

brain

and

h u m a n e m o t i o n s , f e e l i n g s a n d a p p a r e n t free w i l l , without r e g a r d i n g t h e b r a i n as, i n s o m e sense, t h e e q u i v a l e n t o f a p r o g r a m m e d , c y b e r n e t i c m a c h i n e . T h e astronomer Sir F r e d H o y l e (1964) expresses v e r y v i v i d l y w h a t , it seems to me, any evolutionist must think a b o u t nervous systems:

L o o k i n g b a c k [at e v o l u t i o n ] I a m o v e r w h e l m i n g l y i m p r e s s e d b y t h e w a y in w h i c h chemistry has g r a d u a l l y g i v e n w a y to electronics. It is not unreasonable

to describe the first l i v i n g creatures as entirely

chemical

character.

important

plants,

Although

organized

electrochemical

electronics,

the

processes sense

are

of data

processing, does not enter or operate in the plant w o r l d . But primitive electronics begins to assume i m p o r t a n c e as soon as we h a v e a creature that m o v e s a r o u n d primitive

animals

. . . T h e first electronic systems possessed by were

essentially

guidance

systems,

analogous

l o g i c a l l y t o s o n a r o r r a d a r . A s w e pass t o m o r e d e v e l o p e d a n i m a l s w e f i n d e l e c t r o n i c s y s t e m s b e i n g u s e d n o t m e r e l y for g u i d a n c e b u t for directing the a n i m a l t o w a r d food . . . T h e situation is a n a l o g o u s to a g u i d e d missile, the j o b of w h i c h is to intercept a n d destroy a n o t h e r missile. Just as in o u r m o d e r n w o r l d attack and defense b e c o m e m o r e and m o r e subtle in their m e t h o d s , so it was the case w i t h a n i m a l s . A n d w i t h i n c r e a s i n g subtlety, better a n d

Genetic D e t e r m i n i s m and Gene Selectionism

better systems of electronics b e c o m e necessary. W h a t happened in n a t u r e has a close parallel w i t h the d e v e l o p m e n t of electronics in m o d e r n m i l i t a r y a p p l i c a t i o n s . . . I find it a s o b e r i n g t h o u g h t that but for t h e t o o t h - a n d - c l a w e x i s t e n c e o f t h e j u n g l e w e s h o u l d n o t possess o u r i n t e l l e c t u a l c a p a b i l i t i e s , w e s h o u l d n o t b e a b l e t o i n q u i r e into the structure of the U n i v e r s e , or be able to a p p r e c i a t e a s y m p h o n y of B e e t h o v e n . . . V i e w e d i n this l i g h t , t h e q u e s t i o n t h a t i s s o m e t i m e s a s k e d â&#x20AC;&#x201D; c a n c o m p u t e r s think?â&#x20AC;&#x201D;is s o m e w h a t ironic. H e r e of course I mean

the

computers

that

ourselves

make

out

of inorganic

m a t e r i a l s . W h a t o n e a r t h d o those w h o ask s u c h a q u e s t i o n t h i n k they t h e m s e l v e s a r e ? S i m p l y c o m p u t e r s , b u t v a s t l y m o r e c o m p l i c a t e d ones than anything we have yet learned to make.

R e m e m b e r that our

m a n - m a d e c o m p u t e r industry is a mere t w o or three decades old, whereas

ourselves

are

the

products

of an

evolution

t h a t has

operated over hundreds of millions of years [pp. 24-26].

O t h e r s m a y d i s a g r e e w i t h this c o n c l u s i o n , a l t h o u g h I s u s p e c t t h a t the o n l y alternatives to it are religious ones. W h a t e v e r the o u t c o m e of that debate, to r e t u r n t o g e n e s a n d t h e m a i n p o i n t o f this c h a p t e r , t h e issue o f d e t e r m i n i s m v e r s u s free w i l l i s j u s t n o t a f f e c t e d o n e w a y o r t h e o t h e r b y w h e t h e r o r not y o u h a p p e n t o b e c o n s i d e r i n g genes a s c a u s a l a g e n t s r a t h e r t h a n e n v i r o n mental

determinants.

But, it will p a r d o n a b l y be said, there is no smoke without fire. Functional e t h o l o g i s t s a n d ' s o c i o b i o l o g i s t s ' m u s t h a v e said s o m e t h i n g t o d e s e r v e b e i n g tarred w i t h the brush of g e n e t i c d e t e r m i n i s m . Or if it is all a misunderstandi n g there must b e s o m e g o o d e x p l a n a t i o n , b e c a u s e m i s u n d e r s t a n d i n g s that a r e s o w i d e s p r e a d d o n o t c o m e a b o u t for n o r e a s o n , e v e n i f a b e t t e d b y c u l t u r a l m y t h s as p o w e r f u l as the g e n e m y t h and the c o m p u t e r m y t h in u n h o l y a l l i a n c e . S p e a k i n g for m y s e l f , I t h i n k I k n o w t h e r e a s o n . It is an interesting one,

and

will

occupy

the

rest

o f this c h a p t e r .

The

mis-

u n d e r s t a n d i n g arises f r o m t h e w a y w e t a l k a b o u t a q u i t e different s u b j e c t , n a m e l y natural selection. G e n e selectionism, w h i c h is a w a y of talking about e v o l u t i o n , i s m i s t a k e n for g e n e t i c d e t e r m i n i s m , w h i c h i s a p o i n t o f v i e w a b o u t d e v e l o p m e n t . P e o p l e l i k e m e a r e c o n t i n u a l l y p o s t u l a t i n g g e n e s ' f o r ' this a n d g e n e s for t h a t . W e g i v e t h e i m p r e s s i o n o f b e i n g o b s e s s e d w i t h g e n e s a n d w i t h 'genetically programmed'

behaviour.

T a k e this i n

conjunction

with

the

p o p u l a r m y t h s o f the C a l v i n i s t i c d e t e r m i n a c y o f genes, a n d o f ' p r o g r a m m e d ' b e h a v i o u r as the h a l l m a r k of j a c t i t a t i n g D i s n e y l a n d puppets, and is it any w o n d e r that we are accused of being genetic determinists? W h y , then, do functional ethologists talk about genes so m u c h ? Because w e a r e i n t e r e s t e d i n n a t u r a l s e l e c t i o n , a n d n a t u r a l s e l e c t i o n i s differential s u r v i v a l o f g e n e s . I f w e a r e t o s o m u c h a s d i s c u s s t h e possibility o f a b e h a v i o u r pattern's

evolving

natural

selection,

have

postulate

genetic

Genetic D e t e r m i n i s m and Gene Selectionism

variation with respect to the t e n d e n c y or c a p a c i t y to p e r f o r m that b e h a v i o u r p a t t e r n . T h i s i s n o t t o s a y t h a t t h e r e n e c e s s a r i l y i s s u c h g e n e t i c v a r i a t i o n for any particular b e h a v i o u r pattern, only that there must h a v e been genetic variation in the past if we are to treat the b e h a v i o u r p a t t e r n as a D a r w i n i a n adaptation.

Of course

the

behaviour

pattern

may

not

Darwinian

adaptation, in w h i c h case the a r g u m e n t will not a p p l y . Incidentally,

should

defend

my usage of ' D a r w i n i a n

adaptation'

s y n o n y m o u s w i t h ' a d a p t a t i o n p r o d u c e d b y n a t u r a l s e l e c t i o n ' , for G o u l d a n d L e w o n t i n (1979) h a v e recently emphasized, with a p p r o v a l , the 'pluralistic' character of D a r w i n ' s o w n thought. It is indeed true that, especially towards the e n d o f his life, D a r w i n w a s d r i v e n b y c r i t i c i s m s , w h i c h w e c a n n o w see t o be erroneous, to m a k e some concessions to 'pluralism': he did not regard natural selection as the o n l y i m p o r t a n t d r i v i n g force in e v o l u t i o n . As the historian R .

M. Y o u n g (1971)

h a s s a r d o n i c a l l y p u t it,

' . . . b y the sixth

e d i t i o n the b o o k w a s m i s t i t l e d a n d s h o u l d h a v e r e a d On the Origin of Species by Means

of Natural

arguably

Selection

incorrect

and use

All

Sorts

'Darwinian

of Other

Things'.

evolution'

is,

therefore,

synonymous

with

' e v o l u t i o n b y n a t u r a l s e l e c t i o n ' . B u t D a r w i n i a n adaptation i s a n o t h e r m a t t e r . A d a p t a t i o n c a n n o t b e p r o d u c e d b y r a n d o m drift, o r b y a n y o t h e r r e a l i s t i c evolutionary force that we k n o w of save natural selection. It is true that D a r w i n ' s p l u r a l i s m d i d f l e e t i n g l y a l l o w for o n e o t h e r d r i v i n g f o r c e t h a t might, in principle, lead to a d a p t a t i o n , but that d r i v i n g force is i n s e p a r a b l y linked with the n a m e o f L a m a r c k , not o f D a r w i n . ' D a r w i n i a n a d a p t a t i o n ' could

not

sensibly

mean

anything

other

than

adaptation

produced

n a t u r a l s e l e c t i o n , a n d I s h a l l use i t i n this sense. I n s e v e r a l o t h e r p l a c e s i n this b o o k ( e . g . i n C h a p t e r s 3 a n d 6 ) , w e s h a l l r e s o l v e a p p a r e n t d i s p u t e s b y drawing a distinction b e t w e e n evolution in general, and a d a p t i v e evolution in

particular.

regarded

The

fixation

as evolution,

of neutral

mutations,

for

instance,

but it is not a d a p t i v e e v o l u t i o n .

can

If a m o l e c u l a r

geneticist interested in g e n e substitutions, or a p a l a e o n t o l o g i s t interested in major trends, argues w i t h an ecologist interested in a d a p t a t i o n ,

they are

likely to find themselves at cross-purposes s i m p l y b e c a u s e e a c h of t h e m e m p h a s i z e s a different a s p e c t o f w h a t e v o l u t i o n m e a n s . 'Genes

for

conformity,

xenophobia,

and

aggressiveness

are

simply

p o s t u l a t e d for h u m a n s b e c a u s e t h e y a r e n e e d e d for t h e t h e o r y , n o t b e c a u s e a n y e v i d e n c e for t h e m e x i s t s ' ( L e w o n t i n 1 9 7 9 ) . T h i s i s a fair c r i t i c i s m o f E. O. Wilson, but not a v e r y d a m n i n g one. A p a r t from possible political repercussions w h i c h cautiously

might

speculating

about

unfortunate, a

possible

there is Darwinian

nothing wrong with survival

value

x e n o p h o b i a o r a n y other trait. A n d y o u c a n n o t b e g i n t o s p e c u l a t e , h o w e v e r cautiously,

about

the s u r v i v a l v a l u e of a n y t h i n g unless y o u

postulate a

g e n e t i c basis for v a r i a t i o n i n t h a t t h i n g . O f c o u r s e x e n o p h o b i a m a y n o t v a r y genetically, and of course x e n o p h o b i a m a y not be a D a r w i n i a n adaptation,

G e n e t i c D e t e r m i n i s m and G e n e S e l e c t i o n i s m

b u t w e c a n ' t e v e n d i s c u s s t h e p o s s i b i l i t y o f its b e i n g a D a r w i n i a n a d a p t a t i o n u n l e s s w e p o s t u l a t e a g e n e t i c b a s i s for it. L e w o n t i n h i m s e l f h a s e x p r e s s e d the p o i n t a s w e l l a s a n y b o d y : ' I n o r d e r for a trait t o e v o l v e b y n a t u r a l s e l e c t i o n i t i s n e c e s s a r y t h a t t h e r e b e g e n e t i c v a r i a t i o n i n the p o p u l a t i o n for s u c h a trait' ( L e w o n t i n 1 9 7 9 ) . A n d ' g e n e t i c v a r i a t i o n i n t h e p o p u l a t i o n for' a trait X i s e x a c t l y w h a t w e m e a n w h e n w e t a l k , for b r e v i t y , o f ' a g e n e for' X . X e n o p h o b i a is controversial, so consider a b e h a v i o u r pattern that n o b o d y w o u l d fear to r e g a r d as a D a r w i n i a n a d a p t a t i o n . P i t - d i g g i n g in antlions is o b v i o u s l y an a d a p t a t i o n to c a t c h prey. A n t l i o n s are insects, neuropteran l a r v a e w i t h t h e g e n e r a l a p p e a r a n c e a n d d e m e a n o u r o f m o n s t e r s from o u t e r s p a c e . T h e y a r e 'sit a n d w a i t ' p r e d a t o r s w h o d i g pits i n soft s a n d w h i c h t r a p ants a n d other small w a l k i n g insects. T h e pit is a nearly perfect c o n e , whose sides s l o p e s o s t e e p l y t h a t p r e y c a n n o t c l i m b o u t o n c e t h e y h a v e fallen in. T h e a n t l i o n sits j u s t u n d e r t h e s a n d a t the b o t t o m o f t h e pit, w h e r e i t l u n g e s w i t h its h o r r o r - f i l m j a w s a t a n y t h i n g t h a t falls in. P i t - d i g g i n g i s a c o m p l e x b e h a v i o u r p a t t e r n . I t costs t i m e a n d e n e r g y , a n d satisfies t h e m o s t e x a c t i n g c r i t e r i a for r e c o g n i t i o n a s a n a d a p t a t i o n ( W i l l i a m s 1966; C u r i o 1 9 7 3 ) . It must, then, h a v e evolved by natural selection. H o w m i g h t this h a v e h a p p e n e d ? T h e d e t a i l s d o n ' t m a t t e r for the m o r a l I w a n t t o d r a w . P r o b a b l y a n a n c e s t r a l a n t l i o n e x i s t e d w h i c h d i d not d i g a pit b u t s i m p l y l u r k e d j u s t b e n e a t h t h e s a n d s u r f a c e w a i t i n g for p r e y t o b l u n d e r o v e r it. I n d e e d s o m e s p e c i e s still d o this. L a t e r , b e h a v i o u r l e a d i n g t o t h e c r e a t i o n of a shallow depression in because

the

depression

the sand p r o b a b l y w a s favoured by selection

marginally

impeded

escaping

prey.

gradual

degrees o v e r m a n y generations the b e h a v i o u r c h a n g e d so that w h a t was a shallow

depression

became

deeper

and

wider.

This

not

only

hindered

e s c a p i n g p r e y but also increased the c a t c h m e n t area o v e r w h i c h prey might s t u m b l e i n t h e f i r s t p l a c e . L a t e r still t h e d i g g i n g b e h a v i o u r c h a n g e d a g a i n s o t h a t t h e r e s u l t i n g pit b e c a m e a s t e e p - s i d e d c o n e , l i n e d w i t h f i n e , s l i d i n g s a n d so that prey w e r e u n a b l e to c l i m b out. N o t h i n g in the previous p a r a g r a p h is contentious or controversial. It will be r e g a r d e d as l e g i t i m a t e s p e c u l a t i o n a b o u t historical events that we cannot see d i r e c t l y , a n d i t w i l l p r o b a b l y b e t h o u g h t p l a u s i b l e . O n e r e a s o n w h y i t will be a c c e p t e d as uncontroversial historical speculation is that it makes no mention

of genes.

But

point

that

none of that

history,

nor any

c o m p a r a b l e h i s t o r y , c o u l d p o s s i b l y h a v e b e e n t r u e unless t h e r e w a s g e n e t i c v a r i a t i o n in the b e h a v i o u r at e v e r y step of the e v o l u t i o n a r y w a y . P i t - d i g g i n g in antlions is o n l y o n e of the thousands of e x a m p l e s that I c o u l d h a v e chosen. U n l e s s n a t u r a l s e l e c t i o n h a s g e n e t i c v a r i a t i o n t o a c t u p o n , i t c a n n o t g i v e rise t o e v o l u t i o n a r y c h a n g e . I t f o l l o w s t h a t w h e r e y o u find D a r w i n i a n a d a p t a t i o n t h e r e m u s t h a v e b e e n g e n e t i c v a r i a t i o n i n the c h a r a c t e r c o n c e r n e d . N o b o d y has ever d o n e a genetic study of pit-digging b e h a v i o u r in antlions (J. L u c a s , p e r s o n a l c o m m u n i c a t i o n ) . T h e r e i s n o n e e d t o d o o n e , i f a l l w e

Genetic D e t e r m i n i s m and Gene Selectionism

w a n t t o d o i s satisfy o u r s e l v e s o f t h e s o m e t i m e e x i s t e n c e o f g e n e t i c v a r i a t i o n in the b e h a v i o u r p a t t e r n . It is sufficient t h a t we a r e c o n v i n c e d t h a t it is a D a r w i n i a n a d a p t a t i o n (if y o u a r e n o t c o n v i n c e d t h a t p i t - d i g g i n g i s s u c h a n adaptation, simply substitute a n y e x a m p l e o f w h i c h y o u are c o n v i n c e d ) . I s p o k e o f t h e sometime e x i s t e n c e o f g e n e t i c v a r i a t i o n . T h i s w a s b e c a u s e i t i s quite likely that, w e r e a genetic study to be m o u n t e d of antlions today, no genetic variation w o u l d be found. It is in general to be e x p e c t e d that, w h e r e t h e r e i s s t r o n g s e l e c t i o n i n f a v o u r o f s o m e trait, t h e o r i g i n a l v a r i a t i o n o n w h i c h selection a c t e d to g u i d e the e v o l u t i o n of the trait w i l l h a v e b e c o m e u s e d u p . T h i s i s t h e f a m i l i a r ' p a r a d o x ' (it i s n o t r e a l l y v e r y p a r a d o x i c a l w h e n w e t h i n k a b o u t i t c a r e f u l l y ) t h a t traits u n d e r s t r o n g s e l e c t i o n t e n d t o h a v e low heritability (Falconer 1960); ' . . .evolution by natural selection destroys the

genetic

variance

hypotheses

frequently

which

all

are

but

which

feeds'

concern phenotypic universal

the

(Lewontin traits,

1979).

Functional

like possession of eyes,

population,

and

therefore

without

contemporary genetic variation. W h e n we speculate about, or m a k e models of, the e v o l u t i o n a r y p r o d u c t i o n o f a n a d a p t a t i o n , w e a r e n e c e s s a r i l y t a l k i n g about a time w h e n there was appropriate genetic variation. We are b o u n d , in such discussions, to postulate, implicitly or explicitly, genes 'for' p r o p o s e d adaptations. Some m a y balk at treating 'a genetic contribution to variation in X' as e q u i v a l e n t t o ' a g e n e o r g e n e s for X ' . B u t this i s a r o u t i n e g e n e t i c p r a c t i c e , and one w h i c h close e x a m i n a t i o n shows to be almost i n e v i t a b l e . O t h e r than a t the m o l e c u l a r l e v e l , w h e r e o n e g e n e i s s e e n d i r e c t l y t o p r o d u c e o n e p r o t e i n chain, geneticists never deal w i t h units of p h e n o t y p e as such. R a t h e r , they a l w a y s d e a l w i t h differences. W h e n a g e n e t i c i s t s p e a k s o f a g e n e ' f o r ' r e d e y e s in

Drosophila,

h e i s n o t s p e a k i n g o f t h e c i s t r o n w h i c h a c t s a s t e m p l a t e for t h e

synthesis o f t h e r e d p i g m e n t m o l e c u l e .

He is implicitly s a y i n g :

there is

variation in e y e c o l o u r in the p o p u l a t i o n ; other things b e i n g e q u a l , a fly w i t h this g e n e i s m o r e l i k e l y t o h a v e r e d e y e s t h a n a f l y w i t h o u t t h e g e n e . T h a t i s all that we e v e r m e a n by a g e n e 'for' red eyes. T h i s h a p p e n s to be a morphological rather than a behavioural example,

but exactly the same

a p p l i e s to b e h a v i o u r . A g e n e ' f o r ' b e h a v i o u r X is a g e n e ' f o r ' w h a t e v e r m o r p h o l o g i c a l a n d p h y s i o l o g i c a l states t e n d t o p r o d u c e t h a t b e h a v i o u r . A r e l a t e d p o i n t is t h a t t h e use of s i n g l e - l o c u s m o d e l s is j u s t a c o n c e p t u a l c o n v e n i e n c e , a n d this i s t r u e o f a d a p t i v e h y p o t h e s e s i n e x a c t l y t h e s a m e w a y a s i t i s t r u e o f o r d i n a r y p o p u l a t i o n g e n e t i c m o d e l s . W h e n w e use s i n g l e - g e n e l a n g u a g e in our adaptive hypotheses, we do not intend to m a k e a point about single-gene models as against multi-gene models.

We are usually

m a k i n g a p o i n t a b o u t gene m o d e l s a s a g a i n s t n o n - g e n e m o d e l s , for e x a m p l e a s against ' g o o d of the species' m o d e l s . S i n c e it is difficult e n o u g h c o n v i n c i n g p e o p l e t h a t t h e y o u g h t to t h i n k in g e n e t i c t e r m s at all r a t h e r t h a n in t e r m s of, s a y , the g o o d o f t h e s p e c i e s , t h e r e i s n o sense i n m a k i n g t h i n g s e v e n m o r e

G e n e t i c D e t e r m i n i s m and G e n e S e l e c t i o n i s m

difficult b y t r y i n g t o h a n d l e t h e c o m p l e x i t i e s o f m a n y l o c i a t t h e o u t s e t . W h a t L l o y d ( 1 9 7 9 ) c a l l s t h e O G A M ( o n e g e n e a n a l y s i s m o d e l ) is, o f c o u r s e , not t h e last w o r d i n g e n e t i c a c c u r a c y . O f course w e s h a l l e v e n t u a l l y h a v e t o face u p t o multi-locus c o m p l e x i t y . But the O G A M i s vastly preferable t o modes o f a d a p t i v e r e a s o n i n g t h a t f o r g e t a b o u t g e n e s a l t o g e t h e r , a n d this i s the o n l y point I am trying to m a k e at present. S i m i l a r l y we m a y find ourselves aggressively challenged to substantiate o u r ' c l a i m s ' o f t h e e x i s t e n c e o f ' g e n e s for' s o m e a d a p t a t i o n i n w h i c h w e are i n t e r e s t e d . B u t this c h a l l e n g e , if it is a r e a l c h a l l e n g e at a l l , s h o u l d be d i r e c t e d a t t h e w h o l e o f t h e n e o - D a r w i n i a n ' m o d e r n s y n t h e s i s ' a n d the w h o l e of population genetics. To phrase a functional hypothesis in terms of genes is to m a k e no strong claims about genes at all: it is simply to m a k e explicit an a s s u m p t i o n w h i c h is i n s e p a r a b l y built into the m o d e r n synthesis, albeit it is sometimes implicit rather than explicit. A few w o r k e r s h a v e , indeed, flung just such a c h a l l e n g e at the w h o l e neoD a r w i n i a n m o d e r n synthesis, a n d h a v e c l a i m e d not to be n e o - D a r w i n i a n s . Goodwin

(1979)

in a published debate with D e b o r a h Charlesworth and

o t h e r s , s a i d , '. . . n e o - D a r w i n i s m h a s an i n c o h e r e n c e in it . . . we are not g i v e n a n y w a y o f g e n e r a t i n g p h e n o t y p e s from g e n o t y p e s i n n e o - D a r w i n i s m . T h e r e f o r e t h e t h e o r y i s i n this r e s p e c t d e f e c t i v e . ' G o o d w i n is, o f c o u r s e , q u i t e right that d e v e l o p m e n t is terribly complicated, and we don't yet understand m u c h a b o u t h o w p h e n o t y p e s a r e g e n e r a t e d . B u t that t h e y a r e g e n e r a t e d , a n d that g e n e s

contribute

facts, a n d

t h o s e facts a r e a l l w e n e e d i n o r d e r t o m a k e n e o - D a r w i n i s m

significantly

their variation

are

incontrovertible

c o h e r e n t . G o o d w i n m i g h t just a s w e l l s a y t h a t , b e f o r e H o d g k i n a n d H u x l e y w o r k e d out h o w the n e r v e impulse fired, we w e r e not entitled to believe t h a t n e r v e i m p u l s e s c o n t r o l l e d b e h a v i o u r . O f course i t w o u l d b e n i c e t o k n o w h o w p h e n o t y p e s a r e m a d e b u t , w h i l e e m b r y o l o g i s t s a r e b u s y f i n d i n g o u t , the rest o f u s a r e e n t i t l e d b y t h e k n o w n facts o f g e n e t i c s t o c a r r y o n b e i n g n e o D a r w i n i a n s , treating e m b r y o n i c d e v e l o p m e n t as a black box. T h e r e is no c o m p e t i n g theory that has even a remote claim to be called coherent. It

follows

from

the

fact

that

geneticists

are

always

concerned

with

p h e n o t y p i c differences t h a t w e n e e d n o t b e a f r a i d o f p o s t u l a t i n g g e n e s w i t h i n d e f i n i t e l y c o m p l e x p h e n o t y p i c effects, a n d w i t h p h e n o t y p i c effects t h a t show themselves only in highly complex developmental conditions. Together w i t h Professor J o h n M a y n a r d S m i t h , I recently took part in a public debate w i t h t w o radical critics of 'sociobiology', before an a u d i e n c e of students. At one time in the discussion we w e r e trying to establish that to talk of a gene 'for X ' i s t o m a k e n o o u t l a n d i s h c l a i m , e v e n w h e r e X i s a c o m p l e x , l e a r n e d b e h a v i o u r p a t t e r n . M a y n a r d S m i t h r e a c h e d for a h y p o t h e t i c a l e x a m p l e a n d c a m e u p w i t h a ' g e n e for skill i n t y i n g s h o e l a c e s ' . P a n d e m o n i u m b r o k e loose at

this

rampant

genetic

determinism!

The

air was

thick

with

the

un-

mistakable sound of worst suspicions being gleefully confirmed. Delightedly

G e n e t i c D e t e r m i n i s m and G e n e S e l e c t i o n i s m

s c e p t i c a l cries d r o w n e d t h e q u i e t a n d p a t i e n t e x p l a n a t i o n o f j u s t w h a t a modest c l a i m i s b e i n g m a d e w h e n e v e r o n e p o s t u l a t e s a g e n e for, s a y , skill in tying shoelaces.

Let me

explain

the point w i t h

the

aid

of an

more radical-sounding yet truly innocuous thought experiment

even

(Dawkins

1981). R e a d i n g i s a l e a r n e d skill o f p r o d i g i o u s c o m p l e x i t y , b u t this p r o v i d e s n o r e a s o n i n itself for s c e p t i c i s m a b o u t t h e p o s s i b l e e x i s t e n c e o f a g e n e for r e a d i n g . A l l w e w o u l d n e e d i n o r d e r t o e s t a b l i s h t h e e x i s t e n c e o f a g e n e for r e a d i n g is to d i s c o v e r a g e n e for n o t r e a d i n g , s a y a g e n e w h i c h i n d u c e d a brain lesion c a u s i n g specific d y s l e x i a .

S u c h a dyslexic person

might be

n o r m a l a n d intelligent i n all respects e x c e p t that h e c o u l d not r e a d . N o g e n e t i c i s t w o u l d b e p a r t i c u l a r l y s u r p r i s e d i f this t y p e o f d y s l e x i a t u r n e d o u t t o b r e e d t r u e i n s o m e M e n d e l i a n f a s h i o n . O b v i o u s l y , i n this e v e n t , t h e g e n e w o u l d o n l y e x h i b i t its effect i n a n e n v i r o n m e n t w h i c h i n c l u d e d n o r m a l education.

In a prehistoric environment it m i g h t h a v e h a d no detectable

effect, o r i t m i g h t h a v e h a d s o m e different effect a n d h a v e b e e n k n o w n t o cave-dwelling

geneticists

as,

say,

gene

for

inability

read

animal

footprints. In our e d u c a t e d e n v i r o n m e n t it w o u l d p r o p e r l y be c a l l e d a g e n e 'for' d y s l e x i a , s i n c e d y s l e x i a w o u l d b e its m o s t s a l i e n t c o n s e q u e n c e . S i m i l a r l y , a gene w h i c h caused total blindness w o u l d also p r e v e n t r e a d i n g , b u t it w o u l d n o t usefully b e r e g a r d e d a s a g e n e for n o t r e a d i n g . T h i s i s s i m p l y b e c a u s e p r e v e n t i n g r e a d i n g w o u l d n o t b e its m o s t o b v i o u s o r d e b i l i t a t i n g p h e n o t y p i c effect. R e t u r n i n g t o o u r g e n e for s p e c i f i c d y s l e x i a , i t f o l l o w s f r o m t h e o r d i n a r y conventions of genetic t e r m i n o l o g y that the w i l d - t y p e g e n e at the s a m e locus, the g e n e t h a t t h e rest o f t h e p o p u l a t i o n h a s i n d o u b l e d o s e , w o u l d p r o p e r l y b e c a l l e d a g e n e 'for r e a d i n g ' . I f y o u o b j e c t t o t h a t , y o u m u s t a l s o o b j e c t t o o u r s p e a k i n g o f a g e n e for t a l l n e s s i n M e n d e l ' s p e a s , b e c a u s e t h e l o g i c o f t h e t e r m i n o l o g y is identical in the t w o cases.

In b o t h cases the c h a r a c t e r of

interest is a difference, a n d in b o t h c a s e s t h e d i f f e r e n c e o n l y s h o w s i t s e l f in some specified e n v i r o n m e n t . T h e reason w h y s o m e t h i n g so simple as a o n e g e n e d i f f e r e n c e c a n h a v e s u c h a c o m p l e x effect a s t o d e t e r m i n e w h e t h e r o r not a person c a n learn to read, or h o w g o o d he is at t y i n g shoelaces, is basically as follows. H o w e v e r c o m p l e x a g i v e n state of the w o r l d m a y be, the difference b e t w e e n t h a t s t a t e o f t h e w o r l d a n d s o m e a l t e r n a t i v e s t a t e o f t h e world may be caused by something extremely simple. T h e point I m a d e using antlions is a g e n e r a l one. I c o u l d h a v e used a n y real o r p u r p o r t e d D a r w i n i a n a d a p t a t i o n w h a t s o e v e r . F o r f u r t h e r e m p h a s i s I shall

use

one

example.

Tinbergen

al.

(1962)

investigated

the

adaptive significance of a particular behaviour pattern in b l a c k - h e a d e d gulls (Larus

ridibundus),

eggshell

removal.

Shortly

after

chick

hatches,

the

parent bird grasps the e m p t y eggshell in the bill a n d r e m o v e s it from the v i c i n i t y o f t h e nest. T i n b e r g e n a n d his c o l l e a g u e s c o n s i d e r e d a n u m b e r o f

Genetic D e t e r m i n i s m and Gene Selectionism

p o s s i b l e h y p o t h e s e s a b o u t t h e s u r v i v a l v a l u e o f this b e h a v i o u r p a t t e r n . F o r instance t h e y suggested that the e m p t y eggshells m i g h t serve as breeding g r o u n d s for h a r m f u l b a c t e r i a , o r t h e s h a r p e d g e s m i g h t c u t t h e c h i c k s . B u t t h e h y p o t h e s i s for w h i c h t h e y e n d e d u p f i n d i n g e v i d e n c e w a s t h a t t h e e m p t y eggshell serves as a c o n s p i c u o u s visual b e a c o n s u m m o n i n g crows and other p r e d a t o r s o f c h i c k s o r e g g s t o t h e nest. T h e y d i d i n g e n i o u s e x p e r i m e n t s , l a y i n g o u t a r t i f i c i a l nests w i t h a n d w i t h o u t e m p t y e g g s h e l l s , a n d s h o w e d t h a t eggs a c c o m p a n i e d

by e m p t y eggshells were,

indeed,

m o r e likely to be

a t t a c k e d b y c r o w s t h a n eggs w i t h o u t e m p t y eggshells b y their side. T h e y c o n c l u d e d that natural selection had favoured eggshell r e m o v a l behaviour of adult gulls, b e c a u s e past adults w h o did not do it reared fewer children. As in the case of antlion d i g g i n g , n o b o d y has ever d o n e a genetic study of eggshell

removal

behaviour

black-headed

gulls.

There

direct

e v i d e n c e t h a t v a r i a t i o n i n t e n d e n c y t o r e m o v e e m p t y eggshells breeds true. Y e t c l e a r l y t h e a s s u m p t i o n t h a t i t d o e s , o r o n c e d i d , i s e s s e n t i a l for the T i n b e r g e n hypothesis. T h e T i n b e r g e n hypothesis, as normally phrased in g e n e - f r e e l a n g u a g e , i s n o t p a r t i c u l a r l y c o n t r o v e r s i a l . Y e t it, l i k e a l l t h e r i v a l f u n c t i o n a l h y p o t h e s e s t h a t T i n b e r g e n r e j e c t e d , rests f u n d a m e n t a l l y u p o n the assumption that o n c e u p o n a time there must h a v e been gulls with a genetic t e n d e n c y t o r e m o v e e g g s h e l l s , a n d o t h e r g u l l s w i t h a g e n e t i c t e n d e n c y not t o r e m o v e t h e m , o r t o b e less l i k e l y t o r e m o v e t h e m . T h e r e m u s t h a v e b e e n g e n e s for r e m o v i n g e g g s h e l l s . H e r e I m u s t e n t e r a n o t e o f c a u t i o n . S u p p o s e w e a c t u a l l y d i d a s t u d y o f the genetics of eggshell r e m o v a l b e h a v i o u r in modern gulls.

It w o u l d be a

behaviour-geneticist's d r e a m to find a simple M e n d e l i a n mutation which radically altered

the b e h a v i o u r pattern, p e r h a p s abolished the b e h a v i o u r

a l t o g e t h e r . B y t h e a r g u m e n t g i v e n a b o v e , this m u t a n t w o u l d t r u l y b e a g e n e ' f o r ' n o t r e m o v i n g e g g s h e l l s , a n d , b y d e f i n i t i o n , its w i l d - t y p e a l l e l e w o u l d h a v e t o b e c a l l e d a g e n e for e g g s h e l l r e m o v a l . B u t n o w c o m e s t h e n o t e o f caution.

I t m o s t d e f i n i t e l y d o e s n o t f o l l o w t h a t this p a r t i c u l a r l o c u s 'for'

eggshell r e m o v a l w a s one of the ones u p o n w h i c h natural selection worked d u r i n g the e v o l u t i o n o f the a d a p t a t i o n . O n the c o n t r a r y , i t seems m u c h more p r o b a b l e that a c o m p l e x b e h a v i o u r pattern like eggshell r e m o v a l must h a v e been built up by selection on a large n u m b e r of loci, e a c h h a v i n g a small effect i n i n t e r a c t i o n w i t h t h e o t h e r s . O n c e t h e b e h a v i o u r c o m p l e x h a d b e e n b u i l t u p , i t i s e a s y t o i m a g i n e a s i n g l e m a j o r m u t a t i o n a r i s i n g , w h o s e effect i s t o d e s t r o y it. G e n e t i c i s t s p e r f o r c e m u s t e x p l o i t t h e g e n e t i c v a r i a t i o n a v a i l a b l e for t h e m t o s t u d y . T h e y a l s o b e l i e v e t h a t n a t u r a l s e l e c t i o n m u s t h a v e w o r k e d on similar genetic variation in w r e a k i n g evolutionary c h a n g e . But there is no r e a s o n for t h e m t o b e l i e v e t h a t t h e l o c i c o n t r o l l i n g m o d e r n v a r i a t i o n i n a n a d a p t a t i o n w e r e the v e r y s a m e loci at w h i c h selection acted in b u i l d i n g up the a d a p t a t i o n in the first p l a c e . C o n s i d e r the most famous e x a m p l e of single gene control of c o m p l e x

Genetic D e t e r m i n i s m and Gene Selectionism

behaviour, the case of R o t h e n b u h l e r ' s (1964) h y g i e n i c bees. T h e point of u s i n g this e x a m p l e i s t h a t i t i l l u s t r a t e s w e l l h o w a h i g h l y c o m p l e x b e h a v i o u r difference c a n be d u e to a single g e n e difference. T h e h y g i e n i c b e h a v i o u r of the B r o w n strain o f h o n e y b e e s involves the w h o l e n e u r o m u s c u l a r system, but the fact t h a t t h e y p e r f o r m t h e b e h a v i o u r w h e r e a s V a n S c o y b e e s d o n o t is, a c c o r d i n g to R o t h e n b u h l e r ' s m o d e l , d u e to differences at t w o loci o n l y . O n e locus determines the u n c a p p i n g of cells c o n t a i n i n g diseased b r o o d , the o t h e r l o c u s d e t e r m i n e s t h e r e m o v i n g o f d i s e a s e d b r o o d after u n c a p p i n g . I t w o u l d be possible, therefore, to i m a g i n e a natural selection in f a v o u r of u n c a p p i n g behaviour and a natural selection in favour of r e m o v i n g behaviour, m e a n i n g selection of the t w o genes versus their respective alleles. B u t the p o i n t I am m a k i n g here is that, although that could h a p p e n , it is not likely to be very interesting evolutionarily.

The

modern uncapping gene

and

the modern

r e m o v i n g gene m a y very well not h a v e been i n v o l v e d in the original natural selection

process

that

steered

the

evolutionary

putting

together

of the

behaviour. Rothenbuhler observed

that

even

Van

Scoy

bees

sometimes

perform

h y g i e n i c b e h a v i o u r . T h e y a r e j u s t q u a n t i t a t i v e l y m u c h less l i k e l y t o d o s o than are B r o w n bees. It is likely, therefore, that b o t h B r o w n and V a n S c o y bees h a v e h y g i e n i c a n c e s t o r s , a n d b o t h h a v e i n t h e i r n e r v o u s s y s t e m s t h e machinery of u n c a p p i n g and removing b e h a v i o u r : it is just that V a n S c o y bees

have

genes

that

prevent

them

from

turning

the

machinery

on.

P r e s u m a b l y i f w e w e n t b a c k e v e n f u r t h e r i n t i m e w e s h o u l d find a n a n c e s t o r of all m o d e r n bees w h i c h not o n l y w a s not h y g i e n i c itself b u t h a d n e v e r h a d a hygienic

ancestor.

There

must

have

been

evolutionary

progression

b u i l d i n g u p t h e u n c a p p i n g a n d r e m o v i n g b e h a v i o u r f r o m n o t h i n g , a n d this evolutionary progression involved the selection of m a n y genes w h i c h are n o w fixed in

both

the

Brown

and

the

Van

Scoy

strains.

So,

although

the

u n c a p p i n g and the r e m o v i n g genes of the B r o w n strain really are rightly c a l l e d g e n e s for u n c a p p i n g a n d r e m o v i n g , t h e y a r e d e f i n e d a s s u c h o n l y b e c a u s e t h e y h a p p e n t o h a v e a l l e l e s w h o s e effect i s t o p r e v e n t t h e b e h a v i o u r from b e i n g p e r f o r m e d . T h e m o d e o f a c t i o n o f t h e s e a l l e l e s c o u l d b e b o r i n g l y destructive. T h e y m i g h t simply cut some vital link in the neural m a c h i n e r y . I am r e m i n d e d of G r e g o r y ' s ( 1 9 6 1 ) v i v i d illustration of the perils of m a k i n g inferences from a b l a t i o n e x p e r i m e n t s o n the b r a i n : ' . . . the r e m o v a l o f a n y o f s e v e r a l w i d e l y s p a c e d resistors m a y c a u s e a r a d i o set t o e m i t h o w l s , b u t i t d o e s n o t f o l l o w t h a t h o w l s a r e i m m e d i a t e l y a s s o c i a t e d w i t h t h e s e resistors, o r indeed that the causal relation is a n y t h i n g but the most indirect. In part i c u l a r , w e s h o u l d n o t s a y t h a t t h e f u n c t i o n o f t h e resistors i n t h e n o r m a l circuit is to inhibit h o w l i n g . Neurophysiologists, w h e n faced w i t h a c o m parable situation, have postulated "suppressor regions".' T h i s c o n s i d e r a t i o n s e e m s t o m e t o b e a r e a s o n for c a u t i o n , n o t a r e a s o n for rejecting the w h o l e genetic theory o f natural selection! N e v e r m i n d i f l i v i n g

Genetic D e t e r m i n i s m and Gene Selectionism

geneticists are d e b a r r e d from s t u d y i n g the p a r t i c u l a r loci at w h i c h selection i n t h e p a s t g a v e rise t o t h e o r i g i n a l e v o l u t i o n o f i n t e r e s t i n g a d a p t a t i o n s . I t i s t o o b a d i f g e n e t i c i s t s u s u a l l y a r e f o r c e d t o c o n c e n t r a t e o n loci t h a t a r e convenient rather than evolutionary

putting

evolutionarily important. together

complex

I t i s still t r u e t h a t the

and

interesting

adaptation

consisted in the r e p l a c e m e n t of genes by their alleles. This

argument

can

contribute

tangentially

the

resolution

of a

f a s h i o n a b l e c o n t e m p o r a r y d i s p u t e , b y h e l p i n g t o p u t t h e issue i n p e r s p e c t i v e . It

now

highly,

indeed

passionately,

controversial

whether

there

significant genetic variation in h u m a n mental abilities. A r e some of us g e n e t i c a l l y b r a i n i e r t h a n others? W h a t w e m e a n b y ' b r a i n y ' i s also highly c o n t e n t i o u s , a n d r i g h t l y so. B u t I suggest that, by a n y m e a n i n g of the term, the f o l l o w i n g propositions c a n n o t be d e n i e d , (1) T h e r e w a s a time w h e n our a n c e s t o r s w e r e less b r a i n y t h a n w e a r e .

(2) T h e r e f o r e t h e r e h a s b e e n a n

i n c r e a s e i n b r a i n i n e s s i n o u r a n c e s t r a l l i n e a g e . (3) T h a t i n c r e a s e c a m e a b o u t through evolution, p r o b a b l y propelled by natural selection.

(4)

Whether

p r o p e l l e d by selection or not, at least part of the e v o l u t i o n a r y c h a n g e in p h e n o t y p e r e f l e c t e d a n u n d e r l y i n g g e n e t i c c h a n g e : a l l e l e r e p l a c e m e n t took p l a c e a n d c o n s e q u e n t l y m e a n m e n t a l a b i l i t y i n c r e a s e d o v e r g e n e r a t i o n s . (5) By definition therefore, at least in the past, there must h a v e b e e n significant g e n e t i c v a r i a t i o n i n braininess w i t h i n the h u m a n p o p u l a t i o n . S o m e people w e r e g e n e t i c a l l y clever in c o m p a r i s o n w i t h their contemporaries, others were genetically relatively stupid. T h e last s e n t e n c e m a y e n g e n d e r a frisson o f i d e o l o g i c a l d i s q u i e t , y e t n o n e of my five propositions c o u l d be seriously d o u b t e d , nor could their logical s e q u e n c e . T h e a r g u m e n t w o r k s for b r a i n s i z e , b u t i t e q u a l l y w o r k s for a n y b e h a v i o u r a l measure of cleverness we care to d r e a m up. It does not depend on simplistic v i e w s of h u m a n intelligence as b e i n g a one-dimensional scalar quantity. T h e fact that intelligence is not a simple scalar quantity, important as

that

fact

intelligence

is, in

simply

practice.

inevitable,

provided

proposition

that

once

irrelevant.

The

only upon

that a

conclusion we time

are

the

difficulty

of measuring

of the

paragraph

evolutionists

our ancestors

who

were

agree

less

the

clever

(by

w h a t e v e r c r i t e r i o n ) t h e n w e a r e . Y e t i n s p i t e o f a l l t h a t , i t still d o e s n o t f o l l o w t h a t t h e r e i s a n y g e n e t i c v a r i a t i o n i n m e n t a l a b i l i t i e s left i n t h e h u m a n p o p u l a t i o n t o d a y : the g e n e t i c v a r i a n c e m i g h t all h a v e b e e n used u p b y selection. O n the o t h e r h a n d i t m i g h t not, a n d m y t h o u g h t e x p e r i m e n t shows a t l e a s t t h e i n a d v i s a b i l i t y o f d o g m a t i c a n d h y s t e r i c a l o p p o s i t i o n t o the v e r y possibility o f genetic variation i n h u m a n mental abilities. M y o w n opinion, for w h a t i t i s w o r t h , i s t h a t e v e n i f t h e r e i s s u c h g e n e t i c v a r i a t i o n i n m o d e r n h u m a n populations, to base any policy on it w o u l d be illogical and wicked. T h e existence of a D a r w i n i a n adaptation,

then,

implies the sometime

e x i s t e n c e o f g e n e s for p r o d u c i n g t h e a d a p t a t i o n . T h i s i s n o t a l w a y s m a d e

Genetic D e t e r m i n i s m and G e n e S e l e c t i o n i s m

explicit.

It is a l w a y s

possible

talk a b o u t the natural

selection of a

behaviour pattern in t w o w a y s . We can either talk a b o u t individuals with a tendency to perform the b e h a v i o u r pattern b e i n g 'fitter' t h a n i n d i v i d u a l s with

less s t r o n g l y

developed

tendency.

This

the

now

fashionable

p h r a s e o l o g y , w i t h i n t h e p a r a d i g m o f t h e 'selfish o r g a n i s m ' a n d t h e ' c e n t r a l theorem of sociobiology'.

Alternatively,

and

equivalently,

can

talk

d i r e c t l y o f g e n e s for p e r f o r m i n g t h e b e h a v i o u r p a t t e r n s u r v i v i n g b e t t e r t h a n their alleles. It is a l w a y s legitimate to postulate genes in a n y discussion of D a r w i n i a n a d a p t a t i o n , a n d i t w i l l b e o n e o f m y c e n t r a l p o i n t s i n this b o o k t h a t i t i s often p o s i t i v e l y b e n e f i c i a l t o d o s o . O b j e c t i o n s , s u c h a s I h a v e h e a r d made,

the

'unnecessary

geneticizing'

of the

language

of functional

ethology, betray a fundamental failure to face up to the reality of w h a t D a r w i n i a n selection is all a b o u t . L e t m e i l l u s t r a t e this f a i l u r e b y a n o t h e r a n e c d o t e . I r e c e n t l y a t t e n d e d a research seminar g i v e n by an anthropologist. He w a s t r y i n g to interpret the incidence a m o n g various h u m a n tribes of a p a r t i c u l a r m a t i n g system h a p p e n e d to be p o l y a n d r y )

(it

in terms of a theory of kin selection. A kin

selection theorist c a n m a k e m o d e l s t o predict the c o n d i t i o n s u n d e r w h i c h w e would expect to find polyandry. Thus, on one model applied to T a s m a n i a n native hens ( M a y n a r d S m i t h & R i d p a t h

1972), the p o p u l a t i o n sex ratio

w o u l d need to be male-biased, and partners w o u l d need to be close kin, before a biologist w o u l d predict p o l y a n d r y . T h e a n t h r o p o l o g i s t s o u g h t to s h o w t h a t his p o l y a n d r o u s h u m a n t r i b e s l i v e d u n d e r s u c h c o n d i t i o n s , a n d , b y implication,

that

other

tribes

showing

the

normal

patterns

m o n o g a m y o r p o l y g y n y lived u n d e r different conditions. T h o u g h fascinated by the information he presented, I tried to w a r n h i m of s o m e difficulties i n his h y p o t h e s i s .

pointed out that the t h e o r y of kin

selection is f u n d a m e n t a l l y a genetic theory, a n d that kin-selected a d a p t a t i o n s to local conditions h a d to c o m e a b o u t t h r o u g h the r e p l a c e m e n t of alleles by o t h e r a l l e l e s , o v e r g e n e r a t i o n s . H a d his p o l y a n d r o u s t r i b e s b e e n l i v i n g , I asked,

u n d e r t h e i r c u r r e n t p e c u l i a r c o n d i t i o n s for l o n g e n o u g h â&#x20AC;&#x201D; e n o u g h

generationsâ&#x20AC;&#x201D;for the necessary genetic r e p l a c e m e n t to h a v e t a k e n p l a c e ? W a s there, indeed, a n y reason to believe that variations in h u m a n m a t i n g systems are u n d e r g e n e t i c control at a l l ? T h e s p e a k e r , s u p p o r t e d b y m a n y o f his a n t h r o p o l o g i c a l c o l l e a g u e s i n t h e seminar, objected to my d r a g g i n g genes into the discussion. He w a s not talking a b o u t genes, he said, b u t a b o u t a social b e h a v i o u r pattern. S o m e of his c o l l e a g u e s s e e m e d u n c o m f o r t a b l e w i t h t h e v e r y m e n t i o n o f t h e f o u r - l e t t e r w o r d ' g e n e ' . I tried t o p e r s u a d e h i m t h a t i t w a s h e w h o h a d ' d r a g g e d g e n e s in' to the discussion a l t h o u g h , to be sure, he h a d not m e n t i o n e d the w o r d g e n e i n his t a l k . T h a t i s e x a c t l y t h e p o i n t I a m t r y i n g t o m a k e . Y o u c a n n o t t a l k a b o u t k i n s e l e c t i o n , o r a n y o t h e r f o r m o f D a r w i n i a n s e l e c t i o n , without d r a g g i n g g e n e s in, w h e t h e r y o u d o s o e x p l i c i t l y o r n o t . B y e v e n s p e c u l a t i n g

G e n e t i c D e t e r m i n i s m and G e n e S e l e c t i o n i s m

a b o u t k i n s e l e c t i o n a s a n e x p l a n a t i o n o f d i f f e r e n c e s i n t r i b a l m a t i n g systems, m y a n t h r o p o l o g i s t f r i e n d w a s i m p l i c i t l y d r a g g i n g g e n e s i n t o the d i s c u s s i o n . I t i s a p i t y h e d i d n o t m a k e i t explicit, b e c a u s e h e w o u l d t h e n h a v e r e a l i z e d w h a t f o r m i d a b l e d i f f i c u l t i e s l a y i n t h e p a t h o f his k i n s e l e c t i o n h y p o t h e s i s : e i t h e r his p o l y a n d r o u s t r i b e s h a d t o h a v e b e e n l i v i n g , i n p a r t i a l g e n e t i c i s o l a t i o n , u n d e r t h e i r p e c u l i a r c o n d i t i o n s for a l a r g e n u m b e r o f c e n t u r i e s , o r n a t u r a l selection h a d to h a v e f a v o u r e d the universal o c c u r r e n c e of genes p r o g r a m ming some complex

' c o n d i t i o n a l s t r a t e g y ' , t h e i r o n y i s t h a t , o f all the

p a r t i c i p a n t s i n t h a t s e m i n a r o n p o l y a n d r y , i t w a s I w h o w a s a d v a n c i n g the least ' g e n e t i c a l l y d e t e r m i n i s t i c ' v i e w o f the b e h a v i o u r u n d e r discussion. Y e t because

insisted

making

the

genetic

nature

of the

kin

selection

h y p o t h e s i s e x p l i c i t , I e x p e c t I a p p e a r e d t o b e c h a r a c t e r i s t i c a l l y obsessed w i t h g e n e s , a ' t y p i c a l g e n e t i c d e t e r m i n i s t ' . T h e s t o r y i l l u s t r a t e s w e l l the m a i n m e s s a g e o f this c h a p t e r , t h a t f r a n k l y f a c i n g u p t o t h e f u n d a m e n t a l g e n e t i c n a t u r e o f D a r w i n i a n selection i s a l l t o o e a s i l y m i s t a k e n

for a n

unhealthy

p r e o c c u p a t i o n w i t h h e r e d i t a r i a n i n t e r p r e t a t i o n s o f o n t o g e n e t i c development. T h e same prejudice against explicit mention of genes w h e r e one can get a w a y w i t h a n i n d i v i d u a l - l e v e l c i r c u m l o c u t i o n i s c o m m o n a m o n g biologists. T h e s t a t e m e n t , ' g e n e s for p e r f o r m i n g b e h a v i o u r X a r e f a v o u r e d o v e r g e n e s for n o t p e r f o r m i n g X ' h a s a v a g u e l y n a i v e a n d u n p r o f e s s i o n a l r i n g t o it. W h a t e v i d e n c e i s t h e r e for s u c h g e n e s ? H o w d a r e y o u c o n j u r e u p a d hoc g e n e s s i m p l y t o satisfy y o u r h y p o t h e t i c a l c o n v e n i e n c e ! T o s a y ' i n d i v i d u a l s t h a t p e r f o r m X a r e fitter t h a n i n d i v i d u a l s t h a t d o n o t p e r f o r m X ' s o u n d s m u c h m o r e respectable. E v e n if it is not k n o w n to be true, it will probably be a c c e p t e d as a permissible s p e c u l a t i o n . B u t the t w o sentences are exactly e q u i v a l e n t i n m e a n i n g . T h e s e c o n d o n e s a y s n o t h i n g t h a t the f i r s t d o e s n o t s a y m o r e c l e a r l y . Y e t i f w e r e c o g n i z e this e q u i v a l e n c e a n d t a l k e x p l i c i t l y a b o u t g e n e s ' f o r ' a d a p t a t i o n s , w e r u n t h e risk o f b e i n g a c c u s e d o f ' g e n e t i c d e t e r m i n i s m ' . I h o p e I h a v e s u c c e e d e d in s h o w i n g t h a t this risk results from n o t h i n g m o r e than misunderstanding. A sensible a n d u n e x c e p t i o n a b l e w a y o f t h i n k i n g a b o u t n a t u r a l s e l e c t i o n â&#x20AC;&#x201D; ' g e n e s e l e c t i o n i s m ' â&#x20AC;&#x201D; i s m i s t a k e n for a s t r o n g b e l i e f a b o u t d e v e l o p m e n t â&#x20AC;&#x201D; ' g e n e t i c d e t e r m i n i s m ' . A n y o n e w h o thinks clearly a b o u t the details of h o w adaptations c o m e into b e i n g is almost bound to

think,

implicitly

if not

explicitly,

about

genes,

albeit

they

may be

h y p o t h e t i c a l g e n e s . A s I s h a l l s h o w i n this b o o k , t h e r e i s m u c h t o b e said for m a k i n g t h e g e n e t i c basis o f D a r w i n i a n f u n c t i o n a l s p e c u l a t i o n s e x p l i c i t r a t h e r than

implicit.

is a good

w a y of avoiding certain

t e m p t i n g errors o f

r e a s o n i n g ( L l o y d 1 9 7 9 ) . I n d o i n g this w e m a y g i v e t h e i m p r e s s i o n , e n t i r e l y for t h e w r o n g r e a s o n ,

of b e i n g obsessed

with genes and

all the m y t h i c

b a g g a g e that genes c a r r y in the c o n t e m p o r a r y journalistic consciousness. But d e t e r m i n i s m , i n t h e sense o f a n i n f l e x i b l e , t r a m l i n e - f o l l o w i n g o n t o g e n y , is, o r should

be,

sociobiologists

thousand may

miles may

from not

our

thoughts.

genetic

Of course,

determinists.

individual

They may

Genetic D e t e r m i n i s m and G e n e S e l e c t i o n i s m

Rastafarians,

Shakers or Marxists. B u t their private opinions on genetic

determinism, like their p r i v a t e opinions on religion, h a v e n o t h i n g to do w i t h the fact t h a t t h e y use t h e l a n g u a g e o f ' g e n e s for b e h a v i o u r ' w h e n t a l k i n g about natural selection. A l a r g e p a r t o f this c h a p t e r h a s b e e n b a s e d o n t h e a s s u m p t i o n t h a t a biologist m i g h t wish to s p e c u l a t e on the D a r w i n i a n 'function' of b e h a v i o u r patterns. T h i s is not to say that all b e h a v i o u r patterns necessarily h a v e a D a r w i n i a n function.

It m a y be that there is a l a r g e class of b e h a v i o u r

patterns w h i c h are selectively neutral or deleterious to their performers, a n d c a n n o t u s e f u l l y b e r e g a r d e d a s t h e p r o d u c t s o f n a t u r a l s e l e c t i o n . I f so, t h e a r g u m e n t s o f this c h a p t e r d o n o t a p p l y t o t h e m . B u t i t i s l e g i t i m a t e t o s a y T am interested in a d a p t a t i o n . I d o n ' t necessarily think all b e h a v i o u r patterns are adaptations, adaptations.'

but

want

Similarly,

to study those

behaviour patterns

that are

e x p r e s s a p r e f e r e n c e for s t u d y i n g v e r t e b r a t e s

rather than invertebrates does not c o m m i t us to the belief that all animals a r e v e r t e b r a t e s . G i v e n t h a t o u r field o f i n t e r e s t i s a d a p t i v e b e h a v i o u r , w e c a n n o t talk a b o u t t h e D a r w i n i a n e v o l u t i o n o f t h e o b j e c t s o f i n t e r e s t w i t h o u t postulating a genetic

basis for t h e m .

And

to use

' a g e n e for X '

c o n v e n i e n t w a y o f t a l k i n g a b o u t ' t h e g e n e t i c basis o f X ' , h a s b e e n s t a n d a r d p r a c t i c e i n p o p u l a t i o n g e n e t i c s for o v e r h a l f a c e n t u r y . T h e q u e s t i o n o f h o w l a r g e i s t h e class o f b e h a v i o u r p a t t e r n s t h a t w e c a n consider to be adaptations is an entirely separate question. It is the subject of the n e x t c h a p t e r .

3 C o n s t r a i n t s on Perfection

I n o n e w a y o r a n o t h e r , this b o o k i s l a r g e l y p r e o c c u p i e d w i t h the l o g i c of D a r w i n i a n

explanations

of function.

Bitter

experience

warns

that

biologist w h o shows a strong interest in functional e x p l a n a t i o n is likely to be a c c u s e d , s o m e t i m e s w i t h a p a s s i o n t h a t startles t h o s e m o r e a c c u s t o m e d t o scientific than i d e o l o g i c a l d e b a t e animals

are

perfectly

(Lewontin

optimalâ&#x20AC;&#x201D;accused

1 9 7 7 ) , of believing that all of

being

'adaptationist'

( L e w o n t i n 1 9 7 8 a , b ; G o u l d & L e w o n t i n 1 9 7 9 ) . A d a p t a t i o n i s m is defined as ' t h a t a p p r o a c h t o e v o l u t i o n a r y s t u d i e s w h i c h a s s u m e s w i t h o u t further p r o o f that all aspects of the m o r p h o l o g y , p h y s i o l o g y and b e h a v i o r of organisms are a d a p t i v e o p t i m a l s o l u t i o n s t o p r o b l e m s ' ( L e w o n t i n 1 9 7 9 ) . I n the first d r a f t o f this c h a p t e r I e x p r e s s e d d o u b t s t h a t a n y o n e w a s t r u l y a n a d a p t a t i o n i s t in the e x t r e m e sense, b u t I h a v e r e c e n t l y found the f o l l o w i n g q u o t a t i o n from, i r o n i c a l l y e n o u g h , L e w o n t i n himself: ' T h a t is the one point w h i c h I think all evolutionists are a g r e e d u p o n , that it is virtually impossible to do a better j o b (Lewontin

1967).

than an organism Lewontin

i s d o i n g i n its o w n

has since,

seems,

environment'

travelled

his

road

D a m a s c u s , s o i t w o u l d b e u n f a i r t o use h i m a s m y a d a p t a t i o n i s t s p o k e s m a n . I n d e e d t o g e t h e r w i t h G o u l d h e h a s , i n r e c e n t y e a r s , b e e n o n e o f the m o s t articulate

and

forceful

critics

of adaptationism.

representative

adaptationist I take A. J. C a i n , w h o has r e m a i n e d ( C a i n 1979) consistently t r u e t o t h e v i e w s e x p r e s s e d i n his t r e n c h a n t a n d e l e g a n t p a p e r o n

'The

perfection of animals'. W r i t i n g as a t a x o n o m i s t , C a i n (1964) is c o n c e r n e d to attack the traditional d i c h o t o m y b e t w e e n 'functional' characters, w h i c h by implication are not reliable t a x o n o m i c indicators, a n d ' a n c e s t r a l ' c h a r a c t e r s w h i c h are. C a i n a r g u e s f o r c e f u l l y t h a t a n c i e n t ' g r o u n d p l a n ' c h a r a c t e r s , like t h e p e n t a d a c t y l l i m b of tetrapods a n d the a q u a t i c phase of a m p h i b i a n s , are there because they

are

functionally

useful,

rather

than

because

they

are

inescapable

h i s t o r i c a l l e g a c i e s a s i s often i m p l i e d . I f o n e o f t w o g r o u p s 'is i n a n y w a y m o r e p r i m i t i v e t h a n t h e o t h e r , t h e n its p r i m i t i v e n e s s m u s t i n itself b e a n 30

C o n s t r a i n t s on P e r f e c t i o n

adaptation

some

less

specialized

mode

o f life

which

can

pursue

successfully; it c a n n o t be m e r e l y a sign of inefficiency' (p. 5 7 ) . C a i n m a k e s a s i m i l a r p o i n t a b o u t s o - c a l l e d t r i v i a l c h a r a c t e r s , c r i t i c i z i n g D a r w i n for b e i n g t o o r e a d y , u n d e r t h e a t first s i g h t s u r p r i s i n g i n f l u e n c e o f R i c h a r d O w e n , t o c o n c e d e functionlessness: ' N o o n e will suppose that the stripes on the w h e l p o f a l i o n , o r the spots o n t h e y o u n g b l a c k b i r d , a r e o f a n y u s e t o t h e s e animals . . . ' D a r w i n ' s remark must sound foolhardy t o d a y e v e n to the most extreme critic of a d a p t a t i o n i s m . I n d e e d , history seems to be on the side of the

adaptationists,

the

sense

that

particular

instances

they

have

c o n f o u n d e d t h e scoffers a g a i n a n d a g a i n . C a i n ' s o w n c e l e b r a t e d w o r k , w i t h Sheppard

and

their

school,

the

selection

pressures

maintaining

the

b a n d i n g p o l y m o r p h i s m i n t h e s n a i l Cepaea nemoralis m a y h a v e b e e n p a r t l y p r o v o k e d b y t h e fact t h a t 'it h a d b e e n c o n f i d e n t l y a s s e r t e d t h a t i t c o u l d n o t m a t t e r t o a s n a i l w h e t h e r i t h a d o n e b a n d o n its s h e l l o r t w o ' ( C a i n , p . 4 8 ) . 'But perhaps the most r e m a r k a b l e functional interpretation of a " t r i v i a l " c h a r a c t e r i s g i v e n b y M a n t o n ' s w o r k o n t h e d i p l o p o d Polyxenus, i n w h i c h s h e has s h o w n that a c h a r a c t e r formerly d e s c r i b e d as an " o r n a m e n t " ( a n d w h a t c o u l d s o u n d m o r e useless?) i s a l m o s t l i t e r a l l y t h e p i v o t o f t h e a n i m a l ' s l i f e ' (Cain, p. 51). A d a p t a t i o n i s m as a w o r k i n g hypothesis, a l m o s t as a faith, has u n d o u b t e d l y b e e n t h e i n s p i r a t i o n for s o m e o u t s t a n d i n g d i s c o v e r i e s , v o n F r i s c h ( 1 9 6 7 ) , i n defiance of the prestigious o r t h o d o x y of v o n Hess, c o n c l u s i v e l y d e m o n s t r a t e d colour vision in fish and in honeybees by controlled experiments. He w a s d r i v e n t o u n d e r t a k e t h o s e e x p e r i m e n t s b y his refusal t o b e l i e v e t h a t , for e x a m p l e , t h e c o l o u r s o f f l o w e r s w e r e t h e r e for n o r e a s o n , o r s i m p l y t o d e l i g h t m e n ' s e y e s . T h i s is, o f c o u r s e , n o t e v i d e n c e for t h e v a l i d i t y o f a d a p t a t i o n i s t faith. E a c h q u e s t i o n m u s t b e t a c k l e d afresh, o n its m e r i t s . W e n n e r ( 1 9 7 1 ) performed a valuable service in questioning von Frisch's dance l a n g u a g e hypothesis, since he p r o v o k e d J. L. G o u l d ' s (1976) brilliant confirmation

of von

Frisch's

theory.

If Wenner

had

been

of an

adaptationist G o u l d ' s research might never h a v e been done, but W e n n e r would

also

not

have

allowed

himself to

blithely

wrong.

Any

adaptationist, while perhaps c o n c e d i n g that W e n n e r h a d usefully exposed lacunae in von Frisch's original experimental design, w o u l d instantly h a v e j u m p e d , with L i n d a u e r ( 1 9 7 1 ) , o n the f u n d a m e n t a l q u e s t i o n o f w h y bees dance at all. W e n n e r never denied

that they d a n c e , nor that the d a n c e

c o n t a i n e d all t h e i n f o r m a t i o n a b o u t t h e d i r e c t i o n a n d d i s t a n c e o f f o o d t h a t von Frisch c l a i m e d . A l l he denied w a s that other bees used

the d a n c e

information. A n adaptationist c o u l d not h a v e rested h a p p y w i t h the i d e a o f animals performing such a time-consuming, and a b o v e all c o m p l e x a n d s t a t i s t i c a l l y i m p r o b a b l e , a c t i v i t y for n o t h i n g . A d a p t a t i o n i s m c u t s b o t h w a y s , h o w e v e r . I a m n o w d e l i g h t e d t h a t G o u l d d i d his c l i n c h i n g e x p e r i m e n t s , a n d it is entirely to my discredit that, e v e n in the u n l i k e l y e v e n t of my h a v i n g

C o n s t r a i n t s on P e r f e c t i o n

been ingenious e n o u g h to think of them, I w o u l d have been too adaptationist t o h a v e b o t h e r e d . I j u s t knew W e n n e r w a s w r o n g ( D a w k i n s 1 9 6 9 ) ! Adaptationist

thinking,

if not

blind

conviction,

has

been

valuable

stimulator of testable hypotheses in physiology. Barlow's (1961) recognition of the

overwhelming

functional

need

sensory

systems

reduce

re-

d u n d a n c y in input led h i m to a u n i q u e l y coherent understanding of a variety o f facts a b o u t s e n s o r y p h y s i o l o g y . A n a l o g o u s f u n c t i o n a l r e a s o n i n g c a n b e applied to the m o t o r system, and to hierarchical systems of organization generally (Dawkins 1 9 7 6 b ; H a i l m a n 1977). Adaptationist conviction cannot tell u s a b o u t p h y s i o l o g i c a l m e c h a n i s m . O n l y p h y s i o l o g i c a l e x p e r i m e n t c a n do that. But cautious adaptationist reasoning can suggest w h i c h of m a n y p o s s i b l e p h y s i o l o g i c a l h y p o t h e s e s a r e m o s t p r o m i s i n g a n d s h o u l d b e tested first. I h a v e t r i e d t o s h o w t h a t a d a p t a t i o n i s m c a n h a v e v i r t u e s a s w e l l a s faults. But

this

chapter's

main

purpose

list

and

classify

constraints

p e r f e c t i o n , t o list t h e m a i n r e a s o n s w h y t h e s t u d e n t o f a d a p t a t i o n s h o u l d proceed

with

caution.

Before

coming

list

o f six

constraints

perfection, I should deal w i t h three others that h a v e been proposed, but w h i c h I f i n d less p e r s u a s i v e . T a k i n g , f i r s t , t h e m o d e r n c o n t r o v e r s y a m o n g biochemical critiques

geneticists

about

of adaptationism,

'neutral

simply

mutations', irrelevant.

repeatedly If there

cited

are

neutral

m u t a t i o n s i n t h e b i o c h e m i s t s ' sense, w h a t this m e a n s i s t h a t a n y c h a n g e i n p o l y p e p t i d e s t r u c t u r e w h i c h t h e y i n d u c e h a s n o effect o n t h e e n z y m a t i c a c t i v i t y of the protein. T h i s m e a n s that the neutral m u t a t i o n will not c h a n g e t h e c o u r s e o f e m b r y o n i c d e v e l o p m e n t , w i l l h a v e n o p h e n o t y p i c effect a t all, a s a

whole-organism

biologist

would

understand

phenotypic

effect.

The

b i o c h e m i c a l c o n t r o v e r s y o v e r n e u t r a l i s m i s c o n c e r n e d w i t h the i n t e r e s t i n g a n d i m p o r t a n t q u e s t i o n o f w h e t h e r all g e n e s u b s t i t u t i o n s h a v e p h e n o t y p i c effects. T h e a d a p t a t i o n i s m c o n t r o v e r s y i s q u i t e different. I t i s c o n c e r n e d w i t h w h e t h e r , given t h a t w e a r e d e a l i n g w i t h a p h e n o t y p i c effect b i g e n o u g h t o see a n d ask q u e s t i o n s a b o u t , w e s h o u l d a s s u m e t h a t i t i s t h e p r o d u c t o f n a t u r a l s e l e c t i o n . T h e b i o c h e m i s t ' s ' n e u t r a l m u t a t i o n s ' a r e m o r e t h a n n e u t r a l . A s far a s t h o s e o f u s w h o l o o k a t gross m o r p h o l o g y , p h y s i o l o g y a n d b e h a v i o u r a r e c o n c e r n e d , t h e y a r e n o t m u t a t i o n s a t a l l . I t w a s i n this spirit t h a t M a y n a r d S m i t h (1976b) w r o t e : 'I interpret "rate of e v o l u t i o n " as a rate of adaptive c h a n g e . I n this s e n s e , t h e s u b s t i t u t i o n o f a n e u t r a l a l l e l e w o u l d n o t c o n s t i t u t e e v o l u t i o n . . . ' I f a w h o l e - o r g a n i s m b i o l o g i s t sees a g e n e t i c a l l y d e t e r m i n e d difference a m o n g p h e n o t y p e s , he already knows he c a n n o t be dealing with neutrality

the

sense

of the

modern

controversy

among

biochemical

geneticists. H e m i g h t , n e v e r t h e l e s s , b e d e a l i n g w i t h a n e u t r a l c h a r a c t e r i n t h e sense o f an

earlier controversy

(Fisher &

Ford

1950;

Wright

1951).

A genetic

d i f f e r e n c e c o u l d s h o w i t s e l f a t t h e p h e n o t y p i c l e v e l , y e t still b e s e l e c t i v e l y

C o n s t r a i n t s on P e r f e c t i o n

neutral. But m a t h e m a t i c a l calculations such as those of Fisher (1930b) a n d Haldane (1932a) show how unreliable h u m a n subjective j u d g e m e n t can be o n the ' o b v i o u s l y t r i v i a l ' n a t u r e o f s o m e b i o l o g i c a l c h a r a c t e r s . H a l d a n e , for e x a m p l e , s h o w e d that, with plausible assumptions a b o u t a t y p i c a l p o p u l a t i o n , a s e l e c t i o n p r e s s u r e as w e a k as 1

1000 w o u l d t a k e o n l y a f e w

thousand generations to push an initially rare m u t a t i o n to fixation, a small time by g e o l o g i c a l standards. It a p p e a r s that, in the c o n t r o v e r s y referred to a b o v e , W r i g h t w a s m i s u n d e r s t o o d (see b e l o w ) . W r i g h t ( 1 9 8 0 ) w a s e m b a r rassed a t f i n d i n g t h e i d e a o f e v o l u t i o n o f n o n a d a p t i v e c h a r a c t e r s b y g e n e t i c drift

labelled

previously rejected

the

'Sewall

advanced

from

Wright

effect',

the s a m e idea,

the

first

(1929),

'not

only

but because stating

that

"inevitably to degeneration and extinction" '.

because

pure I

others

myself had random

drift

have attributed

had

strongly leads

apparent

n o n a d a p t i v e t a x o n o m i c differences to pleiotropy, w h e r e not m e r e l y ignorance of an a d a p t i v e significance.' W r i g h t was in fact s h o w i n g h o w a subtle mixture

o f drift

and

selection

can

produce

adaptations

superior

the

p r o d u c t s o f s e l e c t i o n a l o n e (see p p . 3 9 - 4 0 ) . A second suggested constraint on perfection concerns allometry ( H u x l e y 1 9 3 2 ) : 'In c e r v i n e deer, antler size increases m o r e t h a n p r o p o r t i o n a t e l y to body

s i z e . . . so

that

larger

deer

have

than

proportionately

large

a n t l e r s . It is t h e n u n n e c e s s a r y to g i v e a s p e c i f i c a l l y a d a p t i v e r e a s o n for t h e extremely large antlers of large deer' ( L e w o n t i n 1 9 7 9 ) . W e l l , L e w o n t i n has a p o i n t h e r e , b u t I w o u l d p r e f e r t o r e p h r a s e it. A s i t s t a n d s i t s u g g e s t s t h a t t h e allometric

constant

God-given

immutable

sense.

But

constants on one time scale c a n be variables on another. T h e allometric c o n s t a n t i s a p a r a m e t e r o f e m b r y o n i c d e v e l o p m e n t . Like; a n y o t h e r s u c h parameter it m a y be subject to genetic variation a n d therefore it m a y c h a n g e over evolutionary time (Clutton-Brock & H a r v e y 1979). L e w o n t i n ' s remark turns o u t t o b e a n a l o g o u s t o t h e f o l l o w i n g : a l l p r i m a t e s h a v e t e e t h ; this i s j u s t a

plain

fact

about

primates,

and

therefore

unnecessary

give

s p e c i f i c a l l y a d a p t i v e r e a s o n for t h e p r e s e n c e o f t e e t h i n p r i m a t e s . W h a t h e p r o b a b l y m e a n t to say is s o m e t h i n g like the f o l l o w i n g . Deer have

evolved

antlers r e l a t i v e t o allometry.

Very

development nothing

probably

occurred do

a developmental

mechanism

b o d y size is a l l o m e t r i c w i t h

with

the

under the

the

social

evolution

such

this

allometric

influence of selection function

that

growth

a p a r t i c u l a r constant of

of antlers:

system

pressures probably

having it

was

conveniently c o m p a t i b l e w i t h pre-existing d e v e l o p m e n t a l processes in a w a y w h i c h w e shall not understand until w e k n o w m o r e a b o u t the b i o c h e m i c a l and cellular details of e m b r y o l o g y . M a y b e ethological consequences of the e x t r a l a r g e a n t l e r s o f l a r g e d e e r e x e r t a s e l e c t i v e effect, b u t this s e l e c t i o n pressure i s l i k e l y t o b e s w a m p e d i n i m p o r t a n c e b y o t h e r s e l e c t i o n p r e s s u r e s concerned with concealed internal e m b r y o l o g i c a l details.

C o n s t r a i n t s on P e r f e c t i o n

W i l l i a m s ( 1 9 6 6 , p . 16) i n v o k e d a l l o m e t r y i n t h e s e r v i c e o f a s p e c u l a t i o n a b o u t t h e s e l e c t i o n p r e s s u r e s l e a d i n g t o i n c r e a s e d b r a i n size i n m a n . H e suggested that the p r i m e focus of selection w a s on early teachability, at an e l e m e n t a r y l e v e l , o f c h i l d r e n . ' T h e r e s u l t i n g s e l e c t i o n for a c q u i r i n g v e r b a l f a c i l i t y a s e a r l y a s p o s s i b l e m i g h t h a v e p r o d u c e d , a s a n a l l o m e t r i c effect o n cerebral development, populations in which an occasional Leonardo might a r i s e . ' W i l l i a m s , h o w e v e r , d i d n o t see a l l o m e t r y a s a w e a p o n a g a i n s t the use o f a d a p t i v e e x p l a n a t i o n s . O n e feels t h a t h e w a s r i g h t l y less l o y a l t o his particular

theory

of cerebral

hypertrophy

than

the

general

principle

e n u n c i a t e d i n his c o n c l u d i n g r h e t o r i c a l q u e s t i o n :

'Is it not reasonable to

anticipate

mind

that

our

understanding

o f the

human

would

aided

g r e a t l y b y k n o w i n g t h e p u r p o s e for w h i c h i t w a s d e s i g n e d ? ' W h a t h a s b e e n s a i d o f a l l o m e t r y a p p l i e s a l s o t o p l e i o t r o p y , t h e possession b y o n e g e n e o f m o r e t h a n o n e p h e n o t y p i c effect. T h i s i s t h e t h i r d o f t h e suggested constraints on perfection that I w a n t to get out of the w a y before e m b a r k i n g o n m y m a i n list. I t h a s a l r e a d y b e e n m e n t i o n e d i n m y q u o t a t i o n from W r i g h t . A possible source of confusion here is that p l e i o t r o p y has b e e n u s e d a s a w e a p o n b y b o t h sides i n this d e b a t e , i f i n d e e d i t i s a r e a l d e b a t e . Fisher

(1930b)

reasoned

that it was unlikely

that a n y one of a gene's

p h e n o t y p i c effects w a s n e u t r a l , s o h o w m u c h m o r e u n l i k e l y w a s i t t h a t all o f a g e n e ' s p l e i o t r o p i c effects c o u l d b e n e u t r a l . L e w o n t i n ( 1 9 7 9 ) , o n the o t h e r hand,

remarked

that

'many

changes

characters

are

the

result

p l e i o t r o p i c g e n e a c t i o n , r a t h e r t h a n the direct result of selection on the c h a r a c t e r itself. T h e y e l l o w c o l o r o f t h e M a l p i g h i a n t u b u l e s o f a n i n s e c t c a n n o t itself be the subject of n a t u r a l selection since that color c a n never be s e e n b y a n y o r g a n i s m . R a t h e r i t i s t h e p l e i o t r o p i c c o n s e q u e n c e o f red e y e p i g m e n t m e t a b o l i s m , w h i c h m a y be a d a p t i v e . ' T h e r e is no real disagreem e n t h e r e . F i s h e r w a s t a l k i n g o f t h e s e l e c t i v e effects o n a g e n e t i c m u t a t i o n , L e w o n t i n o f s e l e c t i v e effects o n a p h e n o t y p i c c h a r a c t e r ; distinction,

indeed,

was

making

discussing

i t i s the s a m e

neutrality

the

b i o c h e m i c a l geneticists' sense. L e w o n t i n ' s point a b o u t p l e i o t r o p y is related to a n o t h e r one w h i c h I shall c o m e o n t o b e l o w , a b o u t t h e p r o b l e m o f d e f i n i n g w h a t h e c a l l s the n a t u r a l ' s u t u r e l i n e s ' , t h e ' p h e n o t y p i c u n i t s ' o f e v o l u t i o n . S o m e t i m e s t h e d u a l effects o f a g e n e a r e i n p r i n c i p l e i n s e p a r a b l e ; t h e y a r e d i f f e r e n t v i e w s o f the s a m e t h i n g , j u s t a s E v e r e s t u s e d t o h a v e t w o n a m e s d e p e n d i n g o n w h i c h side i t w a s s e e n f r o m . W h a t a b i o c h e m i s t sees a s a n o x y g e n - c a r r y i n g m o l e c u l e m a y b e seen by an ethologist as red c o l o r a t i o n . B u t there is a m o r e interesting kind of p l e i o t r o p y i n w h i c h t h e t w o p h e n o t y p i c effects o f a m u t a t i o n a r e s e p a r a b l e . T h e p h e n o t y p i c effect o f a n y g e n e ( v e r s u s its a l l e l e s ) i s n o t a p r o p e r t y o f t h e g e n e alone, b u t also of the e m b r y o l o g i c a l context in w h i c h it acts. T h i s a l l o w s a b u n d a n t o p p o r t u n i t i e s for t h e p h e n o t y p i c effects o f o n e m u t a t i o n t o be modified by others, a n d is the basis of such respected ideas as Fisher's

C o n s t r a i n t s on P e r f e c t i o n

(1930a)

theory o f the e v o l u t i o n o f d o m i n a n c e ,

the M e d a w a r ( 1 9 5 2 )

and

Williams (1957) theories o f senescence, and H a m i l t o n ' s (1967) theory o f Y c h r o m o s o m e inertness.

In the present connection,

if a m u t a t i o n has one

b e n e f i c i a l effect a n d o n e h a r m f u l o n e , t h e r e i s n o r e a s o n w h y s e l e c t i o n s h o u l d not f a v o u r m o d i f i e r g e n e s t h a t d e t a c h t h e t w o p h e n o t y p i c effects, o r t h a t r e d u c e t h e h a r m f u l effect w h i l e e n h a n c i n g t h e b e n e f i c i a l o n e . A s i n t h e c a s e of allometry,

Lewontin

took

too static

a v i e w of gene

action,

treating

pleiotropy as if it w a s a p r o p e r t y of the g e n e rather than of the interaction b e t w e e n t h e g e n e a n d its ( m o d i f i a b l e ) e m b r y o l o g i c a l c o n t e x t . T h i s b r i n g s m e t o m y o w n c r i t i q u e o f n a i v e a d a p t a t i o n i s m , m y o w n list o f c o n s t r a i n t s o n p e r f e c t i o n , a list w h i c h h a s m u c h i n c o m m o n w i t h t h o s e o f L e w o n t i n a n d C a i n , a n d those o f M a y n a r d S m i t h ( 1 9 7 8 b ) , O s t e r a n d W i l s o n ( 1 9 7 8 ) , W i l l i a m s ( 1 9 6 6 ) , C u r i o ( 1 9 7 3 ) a n d o t h e r s . T h e r e is, i n d e e d , m u c h more a g r e e m e n t than the p o l e m i c a l tone of recent critiques w o u l d suggest. I shall n o t b e c o n c e r n e d w i t h p a r t i c u l a r c a s e s , e x c e p t a s e x a m p l e s . A s C a i n a n d L e w o n t i n b o t h stress,

it is not of general interest to c h a l l e n g e our

ingenuity in d r e a m i n g up possible a d v a n t a g e s of p a r t i c u l a r strange things that animals d o . H e r e w e are interested i n the m o r e g e n e r a l q u e s t i o n o f w h a t the t h e o r y o f n a t u r a l s e l e c t i o n e n t i t l e s u s t o e x p e c t . M y f i r s t c o n s t r a i n t o n perfection is an obvious one, mentioned by most writers on a d a p t a t i o n .

T i m e lags T h e animal we are looking at is v e r y p r o b a b l y out of date, built u n d e r the influence of genes that w e r e selected in some earlier era w h e n conditions w e r e different. M a y n a r d S m i t h ( 1 9 7 6 b ) g i v e s a q u a n t i t a t i v e m e a s u r e o f this effect, t h e ' l a g l o a d ' . H e ( M a y n a r d S m i t h

1978b)

cites N e l s o n ' s d e m o n -

stration that g a n n e t s , w h o n o r m a l l y lay o n l y o n e e g g , are q u i t e c a p a b l e o f successfully i n c u b a t i n g a n d r e a r i n g t w o i f a n e x t r a o n e i s e x p e r i m e n t a l l y a d d e d . O b v i o u s l y a n a w k w a r d c a s e for t h e L a c k h y p o t h e s i s o n o p t i m a l c l u t c h s i z e , a n d L a c k h i m s e l f ( 1 9 6 6 ) w a s n o t s l o w t o use t h e ' t i m e - l a g ' e s c a p e route. H e suggested, entirely plausibly, that the g a n n e t c l u t c h size o f o n e e g g e v o l v e d d u r i n g a t i m e w h e n food w a s less p l e n t i f u l , a n d t h a t t h e r e h a d n o t y e t b e e n t i m e for t h e m t o e v o l v e t o m e e t t h e c h a n g e d c o n d i t i o n s . S u c h post hoc

rescuing

of a

hypothesis

trouble

apt

provoke

a c c u s a t i o n s o f t h e sin o f u n f a l s i f i a b i l i t y , b u t I f i n d s u c h a c c u s a t i o n s r a t h e r unconstructive, almost nihilistic. We are not in P a r l i a m e n t or a c o u r t of l a w , with

advocates of D a r w i n i s m scoring d e b a t i n g points against

opponents,

and vice versa. W i t h the e x c e p t i o n of a few g e n u i n e o p p o n e n t s of D a r w i n i s m , who

are

unlikely

reading

this,

are

all

this

together,

all

D a r w i n i a n s w h o s u b s t a n t i a l l y a g r e e o n h o w w e i n t e r p r e t w h a t is, after a l l , the o n l y w o r k a b l e t h e o r y w e h a v e t o e x p l a i n t h e o r g a n i z e d c o m p l e x i t y o f life. W e s h o u l d a l l s i n c e r e l y w a n t t o know w h y g a n n e t s l a y o n l y o n e e g g w h e n t h e y c o u l d l a y t w o , r a t h e r t h a n t r e a t i n g t h e fact a s a d e b a t i n g p o i n t . L a c k ' s

C o n s t r a i n t s on Perfection

i n v o k i n g o f t h e ' t i m e - l a g ' h y p o t h e s i s m a y h a v e b e e n post hoc, b u t i t i s still t h o r o u g h l y p l a u s i b l e , a n d i t i s t e s t a b l e . N o d o u b t t h e r e a r e o t h e r possibilities w h i c h , w i t h luck, m a y also be testable. M a y n a r d S m i t h is surely right that we should

leave

aside

the

'defeatist'

(Tinbergen

1965)

and

untestable

' n a t u r a l s e l e c t i o n h a s b u n g l e d a g a i n ' e x p l a n a t i o n as a last resort, as a m a t t e r o f s i m p l e r e s e a r c h s t r a t e g y i f n o t h i n g else. L e w o n t i n ( 1 9 7 8 b ) says m u c h the s a m e : ' I n a sense, then, biologists are forced to the e x t r e m e adaptationist p r o g r a m b e c a u s e the alternatives, a l t h o u g h they are u n d o u b t e d l y operative in m a n y cases, are untestable in particular cases.' R e t u r n i n g t o t h e t i m e - l a g effect itself, s i n c e m o d e r n m a n h a s d r a s t i c a l l y c h a n g e d the e n v i r o n m e n t of m a n y a n i m a l s a n d plants o v e r a time-scale that i s n e g l i g i b l e b y o r d i n a r y e v o l u t i o n a r y s t a n d a r d s , w e c a n e x p e c t t o see a n a c h r o n i s t i c a d a p t a t i o n s rather often. T h e h e d g e h o g a n t i p r e d a t o r response of rolling up into a ball is sadly inadequate against motor cars. L a y critics frequently b r i n g u p some a p p a r e n t l y m a l a d a p t i v e feature o f modern down

human

behaviour—adoption,

a challenge to

'explain

say,

contraception—and fling

t h a t i f y o u c a n w i t h y o u r selfish g e n e s ' .

O b v i o u s l y , a s L e w o n t i n , G o u l d a n d o t h e r s h a v e r i g h t l y stressed, i t w o u l d b e possible, d e p e n d i n g on one's ingenuity, to pull a 'sociobiological' explan a t i o n o u t o f a h a t , a 'just-so s t o r y ' , b u t I a g r e e w i t h t h e m a n d C a i n t h a t t h e a n s w e r i n g of such c h a l l e n g e s is a trivial e x e r c i s e ; indeed it is likely to be p o s i t i v e l y h a r m f u l . A d o p t i o n a n d c o n t r a c e p t i o n , like r e a d i n g , m a t h e m a t i c s , a n d s t r e s s - i n d u c e d illness, a r e p r o d u c t s o f a n a n i m a l t h a t i s l i v i n g i n a n e n v i r o n m e n t r a d i c a l l y d i f f e r e n t f r o m t h e o n e i n w h i c h its g e n e s w e r e n a t u r a l l y selected. T h e question, about the a d a p t i v e significance of b e h a v i o u r in an a r t i f i c i a l w o r l d , s h o u l d n e v e r h a v e b e e n p u t ; a n d a l t h o u g h a silly q u e s t i o n m a y d e s e r v e a silly a n s w e r , it is wiser to g i v e no a n s w e r at all a n d to explain why. A useful a n a l o g y h e r e i s o n e t h a t I h e a r d f r o m R . D . A l e x a n d e r . M o t h s f l y i n t o c a n d l e f l a m e s , a n d this d o e s n o t h i n g t o h e l p t h e i r i n c l u s i v e f i t n e s s . I n the w o r l d before candles w e r e invented, small sources of bright light in darkness w o u l d either h a v e b e e n celestial b o d i e s at o p t i c a l infinity, or they m i g h t h a v e b e e n escape holes from c a v e s or other enclosed spaces. T h e latter case i m m e d i a t e l y s u g g e s t s a s u r v i v a l v a l u e for a p p r o a c h i n g l i g h t s o u r c e s . T h e f o r m e r c a s e a l s o s u g g e s t s o n e , b u t i n a m o r e i n d i r e c t sense ( F r a e n k e l & G u n n 1 9 4 0 ) . M a n y i n s e c t s use c e l e s t i a l b o d i e s a s c o m p a s s e s . S i n c e these a r e a t optical infinity, rays from them are parallel, and an insect that maintains a f i x e d o r i e n t a t i o n of, s a y , 3 0 ° t o t h e m w i l l g o i n a s t r a i g h t l i n e . B u t i f the r a y s d o n o t c o m e f r o m i n f i n i t y t h e y w i l l n o t b e p a r a l l e l , a n d a n insect t h a t b e h a v e s i n this w a y w i l l s p i r a l i n t o t h e l i g h t s o u r c e (if s t e e r i n g a n a c u t e a n g l e d c o u r s e ) o r s p i r a l a w a y (if s t e e r i n g a n o b t u s e - a n g l e d c o u r s e ) o r o r b i t t h e s o u r c e (if s t e e r i n g a c o u r s e o f e x a c t l y 9 0 ° t o t h e r a y s ) . S e l f - i m m o l a t i o n b y i n s e c t s i n c a n d l e f l a m e s , t h e n , h a s n o s u r v i v a l v a l u e i n itself: a c c o r d i n g t o

C o n s t r a i n t s on P e r f e c t i o n

this h y p o t h e s i s , i t i s a b y p r o d u c t o f t h e useful h a b i t o f s t e e r i n g b y m e a n s o f sources o f light w h i c h are ' a s s u m e d ' t o b e a t infinity. T h a t a s s u m p t i o n w a s o n c e safe. I t n o w i s safe n o l o n g e r , a n d i t m a y b e t h a t s e l e c t i o n i s e v e n n o w w o r k i n g t o modify the insects' b e h a v i o u r . ( N o t necessarily, h o w e v e r . T h e o v e r h e a d costs o f m a k i n g t h e n e c e s s a r y i m p r o v e m e n t s m a y o u t w e i g h t h e benefits t h e y m i g h t b r i n g : m o t h s t h a t p a y t h e costs o f d i s c r i m i n a t i n g c a n d l e s from stars m a y b e less s u c c e s s f u l , o n a v e r a g e , t h a n m o t h s t h a t d o n o t a t t e m p t the c o s t l y d i s c r i m i n a t i o n a n d a c c e p t t h e l o w risk o f s e l f - i m m o l a t i o n â&#x20AC;&#x201D; s e e n e x t chapter.) But now we h a v e reached a problem w h i c h is more subtle than the simple t i m e - l a g h y p o t h e s i s itself. T h i s i s t h e p r o b l e m , a l r e a d y m e n t i o n e d , a b o u t w h a t characteristics of animals we choose to r e c o g n i z e as units w h i c h require e x p l a n a t i o n . A s L e w o n t i n ( 1 9 7 9 ) p u t s it, ' W h a t a r e t h e " n a t u r a l " s u t u r e lines for e v o l u t i o n a r y d y n a m i c s ? W h a t i s t h e t o p o l o g y o f p h e n o t y p e i n e v o l u t i o n ? W h a t a r e t h e p h e n o t y p i c units o f e v o l u t i o n ? ' T h e c a n d l e f l a m e p a r a d o x arose o n l y because of the w a y in w h i c h we chose to c h a r a c t e r i z e the moth's behaviour. W e asked ' W h y d o moths f l y into c a n d l e f l a m e s ? ' and were puzzled. If we had characterized the b e h a v i o u r differently and asked 'Why

moths

maintain

fixed

angle

light

rays

habit

which

i n c i d e n t a l l y c a u s e s t h e m t o s p i r a l i n t o the l i g h t s o u r c e i f t h e r a y s h a p p e n n o t to be p a r a l l e l ) ? ' , we should not h a v e b e e n so p u z z l e d . Consider h u m a n m a l e h o m o s e x u a l i t y as a m o r e serious e x a m p l e . On the face o f it, t h e e x i s t e n c e o f a s u b s t a n t i a l m i n o r i t y o f m e n w h o p r e f e r s e x u a l r e l a t i o n s w i t h t h e i r o w n sex r a t h e r t h a n w i t h t h e o p p o s i t e s e x c o n s t i t u t e s a p r o b l e m for a n y s i m p l e D a r w i n i a n t h e o r y . T h e r a t h e r d i s c u r s i v e title o f a privately circulated homosexualist p a m p h l e t , w h i c h the author w a s kind e n o u g h t o send m e , s u m m a r i z e s the p r o b l e m : ' W h y are there " g a y s " a t a l l ? W h y hasn't evolution eliminated author,

incidentally,

thinks

the

" g a y n e s s " millions of years a g o ? ' T h e problem

important

that

seriously

u n d e r m i n e s t h e w h o l e D a r w i n i a n v i e w o f life. T r i v e r s ( 1 9 7 4 ) , W i l s o n ( 1 9 7 5 , 1978), and especially W e i n r i c h (1976) h a v e considered various versions of the p o s s i b i l i t y t h a t h o m o s e x u a l s m a y , a t s o m e t i m e i n h i s t o r y , h a v e b e e n f u n c t i o n a l l y e q u i v a l e n t t o sterile w o r k e r s , f o r e g o i n g p e r s o n a l r e p r o d u c t i o n the b e t t e r t o c a r e for o t h e r r e l a t i v e s . I d o n o t f i n d this i d e a p a r t i c u l a r l y plausible ( R i d l e y & D a w k i n s in press), certainly no m o r e so than a 'sneaky m a l e ' h y p o t h e s i s . A c c o r d i n g t o this l a t t e r i d e a , h o m o s e x u a l i t y r e p r e s e n t s a n ' a l t e r n a t i v e m a l e t a c t i c ' for o b t a i n i n g m a t i n g s w i t h f e m a l e s . I n a s o c i e t y w i t h harem defence by dominant males, a male w h o is k n o w n to be h o m o s e x u a l is more likely to be tolerated by a d o m i n a n t m a l e than a k n o w n heterosexual m a l e , a n d a n o t h e r w i s e s u b o r d i n a t e m a l e m a y b e a b l e , b y v i r t u e o f this, t o obtain clandestine copulations with females. B u t I raise t h e ' s n e a k y m a l e ' h y p o t h e s i s n o t as a p l a u s i b l e p o s s i b i l i t y so m u c h as a w a y of d r a m a t i z i n g h o w easy and inconclusive it is to d r e a m up

C o n s t r a i n t s on P e r f e c t i o n

e x p l a n a t i o n s o f this k i n d ( L e w o n t i n , 1 9 7 9 , u s e d t h e s a m e d i d a c t i c t r i c k i n d i s c u s s i n g a p p a r e n t h o m o s e x u a l i t y i n Drosophila). T h e m a i n p o i n t I w i s h t o m a k e is q u i t e different a n d m u c h m o r e i m p o r t a n t . It is a g a i n the point a b o u t h o w we c h a r a c t e r i z e the p h e n o t y p i c feature that we are trying to explain. H o m o s e x u a l i t y is, of c o u r s e , a p r o b l e m for D a r w i n i a n s o n l y if t h e r e is a genetic c o m p o n e n t to the difference b e t w e e n h o m o s e x u a l a n d heterosexual i n d i v i d u a l s . W h i l e the e v i d e n c e is controversial

(Weinrich

1 9 7 6 ) , let u s

a s s u m e for t h e s a k e o f a r g u m e n t t h a t this i s t h e c a s e . N o w the q u e s t i o n arises, w h a t d o e s it mean to s a y t h e r e is a g e n e t i c c o m p o n e n t to t h e d i f f e r e n c e , in c o m m o n p a r l a n c e t h a t t h e r e is a g e n e (or g e n e s ) ' f o r ' h o m o s e x u a l i t y ? It is a fundamental

truism,

of logic more than of genetics,

that the p h e n o t y p i c

'effect' of a g e n e is a c o n c e p t that has m e a n i n g o n l y if the context of environmental

influences

specified,

environment

being

understood

i n c l u d e a l l t h e o t h e r g e n e s in t h e g e n o m e . A g e n e ' f o r ' A in e n v i r o n m e n t X m a y w e l l t u r n o u t t o b e a g e n e for B i n e n v i r o n m e n t Y .

It is simply

m e a n i n g l e s s t o s p e a k o f a n a b s o l u t e , c o n t e x t - f r e e , p h e n o t y p i c effect o f a g i v e n gene. Even

if there

are

genes

which,

today's

environment,

produce

h o m o s e x u a l p h e n o t y p e , this d o e s n o t m e a n t h a t i n a n o t h e r e n v i r o n m e n t , s a y that of o u r Pleistocene ancestors, they w o u l d h a v e had the same p h e n o t y p i c effect. A g e n e for h o m o s e x u a l i t y i n o u r m o d e r n e n v i r o n m e n t m i g h t h a v e b e e n a g e n e for s o m e t h i n g u t t e r l y different i n t h e P l e i s t o c e n e . S o , w e h a v e the p o s s i b i l i t y o f a s p e c i a l k i n d o f ' t i m e - l a g effect' h e r e . I t m a y b e t h a t t h e p h e n o t y p e w h i c h w e a r e t r y i n g t o e x p l a i n d i d n o t e v e n exist i n s o m e e a r l i e r e n v i r o n m e n t , e v e n t h o u g h the g e n e did then exist. T h e o r d i n a r y time-lag effect w h i c h w e d i s c u s s e d a t t h e b e g i n n i n g o f this s e c t i o n w a s c o n c e r n e d w i t h c h a n g e s i n t h e e n v i r o n m e n t a s m a n i f e s t e d i n c h a n g e d s e l e c t i o n pressures. W e h a v e n o w a d d e d the more subtle point that changes in the environment m a y c h a n g e t h e v e r y n a t u r e o f t h e p h e n o t y p i c c h a r a c t e r w e set o u t t o e x p l a i n .

Historical constraints T h e j e t e n g i n e s u p e r s e d e d t h e p r o p e l l e r e n g i n e b e c a u s e , for m o s t p u r p o s e s , i t was superior.

T h e d e s i g n e r s o f t h e first j e t e n g i n e s t a r t e d

with a clean

d r a w i n g board. I m a g i n e w h a t they w o u l d h a v e produced if they had been constrained to ' e v o l v e ' the first j e t engine from an existing propeller engine, c h a n g i n g one c o m p o n e n t at a time, nut by nut, screw by screw, rivet by rivet. A j e t e n g i n e so assembled w o u l d be a w e i r d c o n t r a p t i o n indeed. It is hard to i m a g i n e that an a e r o p l a n e designed in that e v o l u t i o n a r y w a y w o u l d e v e r g e t off t h e g r o u n d . Y e t i n o r d e r t o c o m p l e t e t h e b i o l o g i c a l a n a l o g y w e h a v e t o a d d y e t a n o t h e r c o n s t r a i n t . N o t o n l y m u s t t h e e n d p r o d u c t g e t off the g r o u n d ; s o must e v e r y i n t e r m e d i a t e a l o n g the w a y , a n d e a c h intermediate m u s t b e s u p e r i o r t o its p r e d e c e s s o r . W h e n l o o k e d a t i n this l i g h t , far from

C o n s t r a i n t s on P e r f e c t i o n

expecting animals to be perfect we m a y w o n d e r that a n y t h i n g a b o u t them works at all. Examples character

o f the

Heath

of animals

are

Robinson harder

(or R u b e

Goldbergâ&#x20AC;&#x201D;Gould

confident

of than

the

1978)

paragraph might lead us to expect. A favourite e x a m p l e , suggested to me by Professor J . D . C u r r e y , i s t h e r e c u r r e n t l a r y n g e a l n e r v e . T h e s h o r t e s t d i s t a n c e from

the

brain

the

larynx

mammal,

especially

giraffe,

e m p h a t i c a l l y not v i a the posterior side of the aorta, y e t that is the route t a k e n by the recurrent l a r y n g e a l . P r e s u m a b l y there o n c e w a s a t i m e in the r e m o t e ancestry of the m a m m a l s w h e n the straight line from origin to e n d o r g a n of the n e r v e did run posterior to the aorta. W h e n , in d u e course, the n e c k b e g a n t o l e n g t h e n , t h e n e r v e l e n g t h e n e d its d e t o u r p o s t e r i o r t o t h e a o r t a , b u t the m a r g i n a l cost o f e a c h s t e p i n t h e l e n g t h e n i n g o f t h e d e t o u r w a s n o t g r e a t . A major mutation might h a v e re-routed the nerve c o m p l e t e l y , but only at a cost o f g r e a t u p h e a v a l i n e a r l y e m b r y o n i c p r o c e s s e s . P e r h a p s a p r o p h e t i c , G o d - l i k e designer b a c k i n the D e v o n i a n c o u l d h a v e foreseen the giraffe a n d d e s i g n e d the o r i g i n a l e m b r y o n i c r o u t i n g o f t h e n e r v e d i f f e r e n t l y , b u t n a t u r a l selection

has

foresight.

Sydney

Brenner

has

remarked,

natural

s e l e c t i o n c o u l d n o t b e e x p e c t e d t o h a v e f a v o u r e d s o m e useless m u t a t i o n i n the C a m b r i a n s i m p l y b e c a u s e 'it m i g h t c o m e i n h a n d y i n t h e C r e t a c e o u s ' . T h e P i c a s s o - l i k e f a c e o f a flatfish s u c h a s a s o l e , g r o t e s q u e l y t w i s t e d t o b r i n g b o t h e y e s r o u n d t o t h e s a m e side o f t h e h e a d , i s a n o t h e r s t r i k i n g demonstration

of a

historical

constraint on

perfection.

The

evolutionary

h i s t o r y o f these fish i s s o c l e a r l y w r i t t e n i n t o t h e i r a n a t o m y , t h a t t h e e x a m p l e is a g o o d one to thrust d o w n the throats of religious fundamentalists. M u c h the s a m e c o u l d b e s a i d o f t h e c u r i o u s f a c t t h a t t h e r e t i n a o f t h e v e r t e b r a t e e y e appears to be installed b a c k w a r d s . T h e light-sensitive 'photocells' are at the b a c k o f the r e t i n a , a n d l i g h t h a s t o pass t h r o u g h t h e c o n n e c t i n g c i r c u i t r y , with some inevitable attenuation,

before it reaches them.

P r e s u m a b l y it

w o u l d be possible to write d o w n a v e r y l o n g s e q u e n c e of mutations w h i c h would eventually lead to the production of an eye whose retina w a s 'the right w a y r o u n d ' a s i t i s i n c e p h a l o p o d s , a n d this m i g h t b e , i n t h e e n d , s l i g h t l y m o r e efficient. B u t t h e c o s t i n e m b r y o l o g i c a l u p h e a v a l w o u l d b e s o g r e a t t h a t the i n t e r m e d i a t e s t a g e s w o u l d b e h e a v i l y d i s f a v o u r e d b y n a t u r a l s e l e c t i o n i n c o m p a r i s o n w i t h t h e r i v a l , p a t c h e d - u p j o b w h i c h d o e s , after a l l , w o r k p r e t t y well. P i t t e n d r i g h (1958) has well said of a d a p t i v e o r g a n i z a t i o n that it is 'a p a t c h w o r k of makeshifts pieced together, as it w e r e , from w h a t w a s a v a i l a b l e w h e n o p p o r t u n i t y k n o c k e d , a n d a c c e p t e d in the hindsight, not the foresight, o f n a t u r a l s e l e c t i o n ' (see a l s o J a c o b , 1 9 7 7 , o n ' t i n k e r i n g ' ) . S e w a l l W r i g h t ' s (1932) m e t a p h o r , w h i c h has b e c o m e k n o w n u n d e r the n a m e of the ' a d a p t i v e l a n d s c a p e ' , c o n v e y s the s a m e i d e a that selection in favour of local o p t i m a prevents evolution in

the direction of ultimately

C o n s t r a i n t s on P e r f e c t i o n

s u p e r i o r , m o r e g l o b a l o p t i m a . H i s s o m e w h a t m i s u n d e r s t o o d ( W r i g h t 1980) e m p h a s i s o n t h e r o l e o f g e n e t i c drift i n a l l o w i n g l i n e a g e s t o e s c a p e from the pull of local o p t i m a , and thereby attain a closer a p p r o x i m a t i o n to w h a t a h u m a n m i g h t r e c o g n i z e as 'the' o p t i m a l solution, contrasts interestingly with L e w o n t i n ' s ( 1 9 7 9 ) i n v o k i n g o f drift a s a n ' a l t e r n a t i v e t o a d a p t a t i o n ' . A s i n the case of pleiotropy, there is no p a r a d o x here. L e w o n t i n is right that 'the finiteness o f r e a l p o p u l a t i o n s results i n r a n d o m c h a n g e s i n g e n e f r e q u e n c y s o that, with a certain probability, genetic combinations with lower reproduct i v e fitness w i l l b e f i x e d i n a p o p u l a t i o n ' . B u t o n t h e o t h e r h a n d i t i s also t r u e that, to the extent that l o c a l o p t i m a constitute a limitation on the attainment o f d e s i g n p e r f e c t i o n , drift w i l l t e n d t o p r o v i d e a n e s c a p e

(Lande

1976).

I r o n i c a l l y , t h e n , a weakness in n a t u r a l s e l e c t i o n c a n t h e o r e t i c a l l y enhance t h e l i k e l i h o o d o f a l i n e a g e a t t a i n i n g o p t i m a l d e s i g n ! B e c a u s e i t h a s n o foresight, unalloyed

natural

selection

i n a sense a n

anti-perfection

mechanism,

h u g g i n g , a s i t w i l l , t h e tops o f t h e l o w f o o t - h i l l s o f W r i g h t ' s l a n d s c a p e . A m i x t u r e of strong selection interspersed w i t h periods of relaxation of selection a n d drift m a y b e t h e f o r m u l a for c r o s s i n g t h e v a l l e y s t o t h e h i g h u p l a n d s . C l e a r l y i f ' a d a p t a t i o n i s m ' i s t o b e c o m e a n issue w h e r e d e b a t i n g p o i n t s a r e s c o r e d , t h e r e i s s c o p e for b o t h sides t o h a v e i t b o t h w a y s ! M y o w n f e e l i n g i s t h a t s o m e w h e r e h e r e m a y lie t h e s o l u t i o n t o the r e a l p a r a d o x o f this s e c t i o n o n h i s t o r i c a l c o n s t r a i n t s . T h e j e t e n g i n e a n a l o g y suggested

that

animals

improvisation,

ought

risible

monstrosities

of lashed-up

t o p - h e a v y w i t h g r o t e s q u e relics o f p a t c h e d - o v e r a n t i q u i t y .

H o w c a n w e r e c o n c i l e this r e a s o n a b l e e x p e c t a t i o n w i t h t h e f o r m i d a b l e g r a c e o f t h e h u n t i n g c h e e t a h , t h e a e r o d y n a m i c b e a u t y o f t h e swift, t h e s c r u p u l o u s attention to d e c e p t i v e detail of the l e a f insect? E v e n m o r e impressive is the detailed

agreement

between

different

convergent

solutions

common

p r o b l e m s , for i n s t a n c e t h e m u l t i p l e p a r a l l e l s t h a t exist b e t w e e n t h e m a m m a l radiations o f A u s t r a l i a , S o u t h A m e r i c a and the O l d W o r l d . C a i n (1964) remarks that,

' U p to n o w it has usually been assumed, by D a r w i n and

others, that c o n v e r g e n c e will n e v e r be so g o o d as to mislead us' but he goes on to g i v e e x a m p l e s w h e r e c o m p e t e n t taxonomists h a v e been fooled. M o r e and more groups w h i c h had hitherto been regarded as decently monophyletic, are n o w b e i n g suspected of p o l y p h y l e t i c origin. T h e citation of e x a m p l e a n d c o u n t e r - e x a m p l e is m e r e idle fact-dropping. W h a t w e n e e d i s c o n s t r u c t i v e w o r k o n the relation b e t w e e n local a n d g l o b a l o p t i m a i n a n e v o l u t i o n a r y context. O u r understanding o f natural selection itself needs to be s u p p l e m e n t e d by a study of 'escapes from specialization' to use H a r d y ' s

(1954)

phrase. H a r d y himself was suggesting neoteny as an

e s c a p e f r o m s p e c i a l i z a t i o n , w h i l e i n this c h a p t e r , f o l l o w i n g W r i g h t , I h a v e e m p h a s i z e d drift i n this r o l e . M u l l e r i a n m i m i c r y i n b u t t e r f l i e s m a y p r o v e t o b e a useful c a s e - s t u d y h e r e . Turner

(1977)

remarks

that

'among

the

long-winged

butterflies

o f the

C o n s t r a i n t s on P e r f e c t i o n

tropical

American

pericopids)

rainforests

(ithomiids,

heliconids,

danaids,

pierids,

t h e r e a r e six d i s t i n c t w a r n i n g p a t t e r n s , a n d a l t h o u g h a l l t h e

w a r n i n g l y c o l o r e d s p e c i e s b e l o n g t o o n e o f these m i m i c r y " r i n g s " t h e r i n g s t h e m s e l v e s c o e x i s t i n the s a m e h a b i t a t s t h r o u g h m o s t o f t h e A m e r i c a n t r o p i c s and remain v e r y distinct. . . . O n c e the difference b e t w e e n t w o patterns is too great to be j u m p e d by a single mutation, c o n v e r g e n c e b e c o m e s virtually i m p o s s i b l e , a n d the m i m i c r y r i n g s w i l l c o e x i s t i n d e f i n i t e l y . ' T h i s i s o n e o f t h e o n l y cases w h e r e ' h i s t o r i c a l c o n s t r a i n t s ' m a y b e c l o s e t o b e i n g u n d e r s t o o d i n full g e n e t i c d e t a i l . I t m a y p r o v i d e a w o r t h w h i l e o p p o r t u n i t y a l s o for t h e s t u d y o f the g e n e t i c d e t a i l s o f ' v a l l e y - c r o s s i n g ' , w h i c h i n t h e p r e s e n t c a s e w o u l d consist i n t h e d e t a c h m e n t o f a t y p e o f b u t t e r f l y f r o m t h e o r b i t o f o n e m i m i c r y r i n g , a n d its e v e n t u a l ' c a p t u r e ' b y t h e ' p u l l ' o f a n o t h e r m i m i c r y r i n g . T h o u g h h e d o e s n o t i n v o k e drift a s a n e x p l a n a t i o n i n this c a s e , T u r n e r t a n t a l i z i n g l y i n d i c a t e s t h a t ' I n s o u t h e r n E u r o p e Amata phegea . . . h a s . . . captured

Zygenea

ephialtes f r o m t h e M u l l e r i a n m i m i c r y r i n g o f z y g a e n i d s ,

h o m o p t e r a n s , e t c . t o w h i c h i t still b e l o n g s o u t s i d e t h e r a n g e o f A . phegea i n n o r t h e r n E u r o p e . . .' At a more general theoretical level, L e w o n t i n (1978b) notes that 'there m a y often b e s e v e r a l a l t e r n a t i v e s t a b l e e q u i l i b r i u m s o f g e n e t i c c o m p o s i t i o n even w h e n the force of n a t u r a l selection r e m a i n s the s a m e . W h i c h of these a d a p t i v e peaks in the space of genetic c o m p o s i t i o n is e v e n t u a l l y r e a c h e d by a population

depends

entirely

chance

events

the

b e g i n n i n g of the

selective process . . . F o r e x a m p l e , the I n d i a n rhinoceros has one h o r n a n d the A f r i c a n r h i n o c e r o s h a s t w o .

H o r n s a r e a n a d a p t a t i o n for p r o t e c t i o n

against predators b u t it is not true that one h o r n is specifically a d a p t i v e under Indian conditions as opposed to two horns on the A f r i c a n plains. Beginning with

t w o s o m e w h a t different d e v e l o p m e n t a l systems,

the t w o

species r e s p o n d e d t o t h e s a m e s e l e c t i v e forces i n s l i g h t l y d i f f e r e n t w a y s . ' T h e point is basically a g o o d one, a l t h o u g h it is w o r t h a d d i n g that L e w o n t i n ' s uncharacteristically 'adaptationist' b l u n d e r a b o u t the functional significance o f r h i n o c e r o s h o r n s i s n o t t r i v i a l . I f h o r n s r e a l l y were a n a d a p t a t i o n a g a i n s t predators it w o u l d indeed be hard to i m a g i n e h o w a single horn c o u l d be m o r e useful a g a i n s t A s i a n p r e d a t o r s w h i l e t w o h o r n s w e r e o f m o r e h e l p a g a i n s t A f r i c a n p r e d a t o r s . H o w e v e r if, a s s e e m s m u c h m o r e l i k e l y , r h i n o c e r o s horns a r e a n a d a p t a t i o n for i n t r a s p e c i f i c c o m b a t a n d i n t i m i d a t i o n , i t c o u l d well be the case that a o n e - h o r n e d rhino w o u l d be at a d i s a d v a n t a g e in o n e c o n t i n e n t w h i l e a t w o - h o r n e d r h i n o w o u l d suffer i n t h e o t h e r . W h e n e v e r t h e n a m e o f the g a m e i s i n t i m i d a t i o n (or s e x u a l a t t r a c t i o n a s F i s h e r t a u g h t u s long a g o ) , m e r e c o n f o r m i t y to the m a j o r i t y style, w h a t e v e r that m a j o r i t y style m a y h a p p e n t o b e , c a n h a v e a d v a n t a g e s . T h e d e t a i l s o f a t h r e a t d i s p l a y and its a s s o c i a t e d o r g a n s m a y b e a r b i t r a r y ,

but woe betide any mutant

individual that departs from established custom ( M a y n a r d S m i t h & P a r k e r I976).

C o n s t r a i n t s on P e r f e c t i o n

Available genetic variation No m a t t e r h o w strong a potential selection pressure m a y be, no evolution w i l l r e s u l t u n l e s s t h e r e i s g e n e t i c v a r i a t i o n for i t t o w o r k o n . ' T h u s , a l t h o u g h I m i g h t a r g u e that the possession of w i n g s in a d d i t i o n to arms a n d legs m i g h t be a d v a n t a g e o u s to some vertebrates, none has ever e v o l v e d a third pair of appendages,

presumably

because

the

genetic

variation

has

never

been

a v a i l a b l e ' ( L e w o n t i n 1 9 7 9 ) . O n e c o u l d r e a s o n a b l y d i s s e n t f r o m this o p i n i o n . It m a y be that the o n l y reason pigs h a v e no w i n g s is that selection has never favoured their e v o l u t i o n . C e r t a i n l y we must be careful before we assume, on h u m a n - c e n t r e d c o m m o n - s e n s e g r o u n d s , t h a t i t w o u l d o b v i o u s l y b e h a n d y for a n y a n i m a l t o h a v e a p a i r o f w i n g s e v e n i f i t d i d n ' t use t h e m v e r y o f t e n , a n d that therefore the absence of wings in a g i v e n lineage must be due to lack of available mutations.

F e m a l e ants c a n sprout w i n g s if they h a p p e n to be

n u r t u r e d as q u e e n s , b u t if nurtured as workers they do not express their c a p a c i t y t o d o s o . M o r e s t r i k i n g l y , t h e q u e e n s i n m a n y s p e c i e s use t h e i r w i n g s o n l y o n c e , for t h e i r n u p t i a l f l i g h t , a n d t h e n t a k e t h e d r a s t i c s t e p o f b i t i n g o r breaking

them

off at

the

roots

p r e p a r a t i o n for

the

rest o f t h e i r life

u n d e r g r o u n d . E v i d e n t l y w i n g s h a v e costs a s w e l l a s b e n e f i t s . One

of the

most impressive demonstrations of the subtlety of Charles

D a r w i n ' s m i n d i s g i v e n b y his d i s c u s s i o n o f w i n g l e s s n e s s a n d t h e costs o f h a v i n g w i n g s in the insects of o c e a n i c islands. F o r present purposes, the r e l e v a n t p o i n t i s t h a t w i n g e d i n s e c t s m a y risk b e i n g b l o w n o u t t o s e a , a n d D a r w i n ( 1 8 5 9 , p . 1 7 7 ) s u g g e s t e d t h a t this i s w h y m a n y i s l a n d i n s e c t s h a v e r e d u c e d w i n g s . B u t h e a l s o n o t e d t h a t s o m e i s l a n d insects a r e far from wingless; they have extra large wings. T h i s is quite c o m p a t i b l e with the action of natural selection. For w h e n a n e w insect first arrived on the island, the t e n d e n c y of natural selection to e n l a r g e or to r e d u c e the w i n g s , w o u l d d e p e n d on w h e t h e r a g r e a t e r n u m b e r of i n d i v i d u a l s w e r e saved by successfully battling w i t h the w i n d s , or by g i v i n g up the a t t e m p t a n d rarely or never flying. As with mariners ship-wrecked near a coast, it w o u l d have b e e n b e t t e r for t h e g o o d s w i m m e r s i f t h e y h a d b e e n a b l e t o s w i m still f u r t h e r , w h e r e a s i t w o u l d h a v e b e e n b e t t e r for the b a d s w i m m e r s i f t h e y h a d not b e e n a b l e to s w i m at all a n d h a d stuck to the w r e c k .

A neater piece of evolutionary reasoning w o u l d be hard to find, although one c a n almost h e a r the b a y i n g chorus o f 'Unfalsifiable! T a u t o l o g i c a l ! Just-so story!' R e t u r n i n g to the question of w h e t h e r pigs ever could d e v e l o p wings, L e w o n t i n is u n d o u b t e d l y right that biologists interested in adaptation cannot afford t o i g n o r e t h e q u e s t i o n o f t h e a v a i l a b i l i t y o f m u t a t i o n a l v a r i a t i o n . I t i s c e r t a i n l y t r u e t h a t m a n y o f us, w i t h M a y n a r d S m i t h ( 1 9 7 8 a ) t h o u g h w i t h o u t

C o n s t r a i n t s on P e r f e c t i o n

his a n d L e w o n t i n ' s a u t h o r i t a t i v e k n o w l e d g e o f g e n e t i c s , t e n d t o a s s u m e ' t h a t genetic variance of an appropriate kind will usually exist'. M a y n a r d Smith's grounds are that 'with rare exceptions, artificial selection has a l w a y s p r o v e d effective, w h a t e v e r t h e o r g a n i s m o r t h e s e l e c t e d c h a r a c t e r ' . A n o t o r i o u s c a s e , fully c o n c e d e d b y M a y n a r d S m i t h

( 1 9 7 8 b ) , w h e r e the genetic variation

necessary to an o p t i m a l i t y theory often seems to be l a c k i n g , is that of Fisher's ( 1 9 3 0 a ) sex r a t i o t h e o r y . C a t t l e b r e e d e r s h a v e h a d n o t r o u b l e i n b r e e d i n g for high milk yield, high b e e f production, large size, small size, hornlessness, resistance t o v a r i o u s d i s e a s e s , a n d f i e r c e n e s s i n

fighting

bulls.

It w o u l d

obviously be of i m m e n s e benefit to the d a i r y industry if cattle c o u l d be b r e d with a bias t o w a r d s p r o d u c i n g heifer c a l v e s rather t h a n b u l l c a l v e s . A l l a t t e m p t s t o d o this h a v e s i n g u l a r l y f a i l e d , a p p a r e n t l y b e c a u s e t h e n e c e s s a r y genetic variation does not exist. It m a y be the m e a s u r e of h o w misled is my o w n biological intuition

that

find

this f a c t r a t h e r a s t o n i s h i n g ,

indeed

w o r r y i n g . I w o u l d like t o t h i n k t h a t i t i s a n e x c e p t i o n a l c a s e , b u t L e w o n t i n i s certainly right that we need to p a y m o r e attention to the p r o b l e m of the limitations

of available

genetic

variation.

From

this

point

of view,

compilation of the a m e n a b i l i t y or resistance to artificial selection of a w i d e variety of characters w o u l d be of g r e a t interest. Meanwhile,

there

are

certain

common-sense

things

that

can

said.

F i r s t l y , i t m a y m a k e sense t o i n v o k e l a c k o f a v a i l a b l e m u t a t i o n t o e x p l a i n w h y animals do not h a v e some adaptation w h i c h we think reasonable, but it is harder to a p p l y the a r g u m e n t the other w a y r o u n d . F o r instance, we m i g h t i n d e e d t h i n k t h a t p i g s w o u l d b e b e t t e r off w i t h w i n g s a n d s u g g e s t t h a t t h e y lack

them

only

because

their

ancestors

never

produced

the

necessary

m u t a t i o n s . B u t i f w e see a n a n i m a l w i t h a c o m p l e x o r g a n , o r a c o m p l e x a n d time-consuming behaviour pattern, we w o u l d seem to be on strong grounds in guessing that it must h a v e been put together by natural selection. H a b i t s such as d a n c i n g in bees as a l r e a d y discussed, ' a n t i n g ' in birds, ' r o c k i n g ' in stick insects, a n d e g g - s h e l l r e m o v a l i n g u l l s a r e p o s i t i v e l y t i m e - c o n s u m i n g , energy-consuming and

complex.

T h e working hypothesis that they must

h a v e a D a r w i n i a n survival v a l u e is o v e r w h e l m i n g l y strong. In a few cases it has p r o v e d p o s s i b l e t o f i n d o u t w h a t t h a t s u r v i v a l v a l u e i s ( T i n b e r g e n 1 9 6 3 ) . T h e second c o m m o n - s e n s e point is that the hypothesis of 'no a v a i l a b l e m u t a t i o n s ' loses s o m e o f its f o r c e i f a r e l a t e d s p e c i e s , o r t h e s a m e s p e c i e s i n o t h e r c o n t e x t s , h a s s h o w n itself c a p a b l e o f p r o d u c i n g t h e n e c e s s a r y v a r i a t i o n . I shall m e n t i o n b e l o w a c a s e w h e r e t h e k n o w n c a p a b i l i t i e s o f t h e d i g g e r w a s p Ammophila campestris w e r e u s e d t o i l l u m i n a t e t h e l a c k o f s i m i l a r c a p a b i l i t i e s i n t h e r e l a t e d s p e c i e s Sphex ichneumoneus.

A more subtle version

of t h e s a m e

argument c a n be applied within any one species. F o r instance, M a y n a r d Smith

(1977,

see a l s o D a l y

1979)

concludes

a paper with

up-beat

question: W h y d o m a l e m a m m a l s not l a c t a t e ? W e need n o t g o into the d e t a i l s o f w h y h e t h o u g h t t h e y o u g h t t o ; h e m a y h a v e b e e n w r o n g , his m o d e l

C o n s t r a i n t s on P e r f e c t i o n

m a y h a v e b e e n w r o n g l y set u p , a n d t h e r e a l a n s w e r t o his q u e s t i o n m a y b e t h a t i t w o u l d n o t p a y m a l e m a m m a l s t o l a c t a t e . T h e p o i n t h e r e i s t h a t this i s a slightly different kind o f question from ' W h y d o n ' t pigs h a v e w i n g s ? ' . W e k n o w t h a t m a l e m a m m a l s c o n t a i n t h e g e n e s n e c e s s a r y for l a c t a t i o n , b e c a u s e all the g e n e s in a f e m a l e m a m m a l h a v e passed t h r o u g h m a l e ancestors and m a y be h a n d e d on to m a l e descendants. G e n e t i c m a l e m a m m a l s treated with h o r m o n e s , i n d e e d , c a n d e v e l o p a s l a c t a t i n g f e m a l e s . T h i s a l l m a k e s i t less plausible that the reason m a l e m a m m a l s d o n ' t lactate is simply that they h a v e n ' t ' t h o u g h t of it' m u t a t i o n a l l y speaking. (Indeed, I bet I c o u l d breed a r a c e o f s p o n t a n e o u s l y l a c t a t i n g m a l e s b y s e l e c t i n g for i n c r e a s e d s e n s i t i v i t y t o progressively reduced dosages of injected hormone, an interesting practical a p p l i c a t i o n o f the B a l d w i n / W a d d i n g t o n Effect.) The

third

common-sense

point

that if the v a r i a t i o n

that

being

p o s t u l a t e d consists in a s i m p l e q u a n t i t a t i v e extension of a l r e a d y existing variation it is m o r e plausible than a radical qualitative innovation. It m a y be i m p l a u s i b l e to postulate a m u t a n t pig w i t h w i n g rudiments, but it is not i m p l a u s i b l e t o p o s t u l a t e a m u t a n t p i g w i t h a c u r l i e r tail t h a n e x i s t i n g p i g s . I h a v e e l a b o r a t e d this p o i n t e l s e w h e r e ( D a w k i n s 1 9 8 0 ) . I n a n y c a s e , w e n e e d a m o r e s u b t l e a p p r o a c h t o t h e q u e s t i o n o f w h a t i s the e v o l u t i o n a r y i m p a c t of differing degrees of m u t a b i l i t y . It is not g o o d e n o u g h to ask, in an all or n o n e w a y , w h e t h e r there is or is not genetic variation a v a i l a b l e to respond to a g i v e n selection pressure. As L e w o n t i n

(1979)

rightly says, ' N o t only is the qualitative possibility of adaptive evolution c o n s t r a i n e d b y a v a i l a b l e g e n e t i c v a r i a t i o n , b u t the relative rates o f evolution o f d i f f e r e n t c h a r a c t e r s a r e p r o p o r t i o n a l t o t h e a m o u n t o f g e n e t i c v a r i a n c e for e a c h . ' I t h i n k this o p e n s u p a n i m p o r t a n t l i n e o f t h o u g h t w h e n c o m b i n e d w i t h the n o t i o n of historical constraints treated in the previous section. T h e point c a n be illustrated w i t h a fanciful e x a m p l e . Birds fly w i t h w i n g s m a d e of feathers, bats w i t h w i n g s consisting of flaps of skin. W h y d o they not b o t h h a v e w i n g s m a d e i n the s a m e w a y , w h i c h e v e r w a y is ' s u p e r i o r ' ? A c o n f i r m e d adaptationist m i g h t reply that birds must be better off w i t h feathers a n d bats better off w i t h skin f l a p s . A n e x t r e m e antiadaptationist m i g h t say that v e r y p r o b a b l y feathers w o u l d a c t u a l l y be better t h a n s k i n - f l a p s for b o t h b i r d s a n d b a t s , b u t b a t s n e v e r h a d t h e g o o d f o r t u n e to p r o d u c e the right m u t a t i o n s . B u t there is an intermediate position, one w h i c h I find m o r e p e r s u a s i v e t h a n e i t h e r e x t r e m e . L e t u s c o n c e d e t o t h e a d a p t a t i o n i s t that, g i v e n e n o u g h time, the ancestors of bats p r o b a b l y could have produced

t h e s e q u e n c e o f m u t a t i o n s n e c e s s a r y for t h e m

to sprout

feathers. T h e o p e r a t i v e phrase i s ' g i v e n e n o u g h t i m e ' . W e are not m a k i n g a n all-or-none distinction ation,

but

simply

between impossible and

stating

the

undeniable

fact

possible mutational that

some

mutations

variare

q u a n t i t a t i v e l y m o r e p r o b a b l e t h a n o t h e r s . I n this c a s e , a n c e s t r a l m a m m a l s

C o n s t r a i n t s on P e r f e c t i o n

might have p r o d u c e d both mutants with r u d i m e n t a r y feathers and mutants w i t h r u d i m e n t a r y skin f l a p s . B u t t h e p r o t o - f e a t h e r m u t a n t s ( t h e y m i g h t h a v e had to go through an intermediate stage of small scales) w e r e so slow in m a k i n g their a p p e a r a n c e in c o m p a r i s o n w i t h the skin-flap m u t a n t s ,

that

skin-flap w i n g s h a d l o n g a g o a p p e a r e d a n d l e d t o t h e e v o l u t i o n o f p a s s a b l y efficient w i n g s . The

general

point

akin

the

one

already

made

about

adaptive

landscapes. T h e r e we were concerned with selection preventing lineages from e s c a p i n g t h e c l u t c h e s o f l o c a l o p t i m a . H e r e w e h a v e a l i n e a g e f a c e d w i t h t w o a l t e r n a t i v e r o u t e s o f e v o l u t i o n , o n e l e a d i n g to, s a y , f e a t h e r e d w i n g s , the o t h e r t o s k i n - f l a p w i n g s . T h e f e a t h e r e d d e s i g n m a y b e n o t o n l y a g l o b a l o p t i m u m b u t the p r e s e n t l o c a l o p t i m u m a s w e l l . T h e l i n e a g e , i n o t h e r w o r d s , m a y b e s i t t i n g e x a c t l y a t t h e foot o f t h e s l o p e l e a d i n g t o t h e f e a t h e r e d p e a k o f the S e w a l l W r i g h t l a n d s c a p e . I f o n l y t h e n e c e s s a r y m u t a t i o n s w e r e a v a i l a b l e it w o u l d c l i m b easily up the hill.

E v e n t u a l l y , a c c o r d i n g t o this f a n c i f u l

p a r a b l e , those m u t a t i o n s m i g h t h a v e c o m e , b u t â&#x20AC;&#x201D; a n d this i s t h e i m p o r t a n t pointâ&#x20AC;&#x201D;they w e r e too late. Skin-flap mutations h a d c o m e before t h e m , a n d the l i n e a g e h a d

already

a d a p t i v e hill

turn back.

climbed

t o o far u p

the slopes of the

skin-flap

As a river takes the line of least resistance

d o w n h i l l , t h e r e b y m e a n d e r i n g i n a r o u t e t h a t i s far f r o m t h e m o s t d i r e c t o n e t o the sea, s o a l i n e a g e w i l l e v o l v e a c c o r d i n g t o t h e effects o f s e l e c t i o n o n t h e variation available at a n y g i v e n m o m e n t . O n c e a lineage has b e g u n to e v o l v e in a given direction,

this m a y i n i t s e l f c l o s e o p t i o n s t h a t w e r e f o r m e r l y

a v a i l a b l e , s e a l i n g off a c c e s s t o a g l o b a l o p t i m u m . M y p o i n t i s t h a t l a c k o f available variation does not h a v e to

be absolute in order to b e c o m e a

significant constraint on perfection. It need o n l y be a q u a n t i t a t i v e b r a k e to h a v e d r a m a t i c q u a l i t a t i v e effects. I n spirit, t h e n , I a g r e e w i t h G o u l d a n d C a l l o w a y (1980) w h e n t h e y s a y , c i t i n g V e r m e i j ' s ( 1 9 7 3 ) s t i m u l a t i n g p a p e r o n the m a t h e m a t i c s o f m o r p h o l o g i c a l v e r s a t i l i t y t h a t , ' S o m e m o r p h o l o g i e s can be twisted, bent and altered in a variety of w a y s , a n d others c a n n o t . ' B u t I w o u l d p r e f e r to soften ' c a n n o t ' , to m a k e it a q u a n t i t a t i v e c o n s t r a i n t , n o t an absolute

barrier.

M c C l e e r y ( 1 9 7 8 ) , in an a g r e e a b l y c o m p r e h e n s i b l e i n t r o d u c t i o n to the M c F a r l a n d school of ethological optimality theory, mentions H. A. Simon's concept of 'satisficing' as an alternative to o p t i m i z i n g . If o p t i m i z i n g systems are c o n c e r n e d w i t h m a x i m i z i n g s o m e t h i n g , s a t i s f i c i n g s y s t e m s g e t a w a y w i t h d o i n g j u s t e n o u g h . I n this c a s e , d o i n g e n o u g h m e a n s d o i n g e n o u g h t o s t a y alive. M c C l e e r y contents himself with c o m p l a i n i n g that such ' a d e q u a c y ' concepts h a v e not g e n e r a t e d m u c h e x p e r i m e n t a l w o r k . I think e v o l u t i o n a r y t h e o r y e n t i t l e s us to be a b i t m o r e n e g a t i v e a priori. L i v i n g t h i n g s a r e n o t s e l e c t e d for t h e i r c a p a c i t y s i m p l y t o s t a y a l i v e ; t h e y a r e s t a y i n g a l i v e i n competition with other such living things. T h e trouble w i t h satisficing as a

C o n s t r a i n t s on P e r f e c t i o n

c o n c e p t is that it c o m p l e t e l y leaves out the c o m p e t i t i v e element w h i c h is f u n d a m e n t a l t o a l l life. I n G o r e V i d a l ' s w o r d s : ' I t i s n o t e n o u g h t o s u c c e e d . O t h e r s must fail.' On the other h a n d ' o p t i m i z i n g ' is also an unfortunate w o r d because it s u g g e s t s t h e a t t a i n m e n t o f w h a t a n e n g i n e e r w o u l d r e c o g n i z e a s t h e best design in a g l o b a l sense. It tends to o v e r l o o k the constraints on perfection w h i c h a r e t h e s u b j e c t o f this c h a p t e r . I n m a n y w a y s t h e w o r d ' m e l i o r i z i n g ' expresses a sensible m i d d l e w a y b e t w e e n o p t i m i z i n g a n d satisficing. W h e r e optimus m e a n s b e s t , melior m e a n s b e t t e r . T h e p o i n t s w e h a v e b e e n c o n s i d e r i n g a b o u t historical constraints, about Wright's adaptive landscapes and about r i v e r s f o l l o w i n g t h e l i n e o f i m m e d i a t e least r e s i s t a n c e , a r e all r e l a t e d t o the fact that n a t u r a l selection chooses the better of present a v a i l a b l e alternatives. N a t u r e does not h a v e the foresight to put together a sequence of mutations w h i c h , for a l l t h a t t h e y m a y e n t a i l t e m p o r a r y d i s a d v a n t a g e , set a l i n e a g e o n the r o a d to u l t i m a t e g l o b a l superiority. slightly

It c a n n o t refrain from favouring

advantageous

available

mutations

a d v a n t a g e of superior

mutations

which

natural

selection

blindly

meliorizes

its

now,

may way

arrive down

as later.

take

successive

better

a river, lines

i m m e d i a t e l y a v a i l a b l e l e a s t r e s i s t a n c e . T h e a n i m a l t h a t results i s n o t the most perfect design c o n c e i v a b l e , nor is it merely good e n o u g h to scrape by. It is

the

product of a historical sequence of changes,

each

one of which

r e p r e s e n t e d , a t b e s t , t h e better o f t h e a l t e r n a t i v e s t h a t h a p p e n e d t o b e a r o u n d at the time.

Constraints of costs and materials ' I f t h e r e w e r e n o c o n s t r a i n t s o n w h a t i s p o s s i b l e , t h e best p h e n o t y p e w o u l d l i v e for e v e r , w o u l d b e i m p r e g n a b l e t o p r e d a t o r s , w o u l d l a y e g g s a t a n infinite r a t e , a n d s o o n ' ( M a y n a r d S m i t h 1 9 7 8 b ) . ' A n e n g i n e e r , g i v e n c a r t e b l a n c h e o n his d r a w i n g b o a r d c o u l d d e s i g n a n " i d e a l " w i n g for a b i r d , b u t he w o u l d d e m a n d to k n o w the constraints under w h i c h he must work. Is he constrained to use feathers a n d bones, or m a y he design the skeleton in titanium a l l o y ? H o w m u c h is he a l l o w e d to spend on the w i n g s , a n d h o w m u c h of the a v a i l a b l e e c o n o m i c investment must be diverted into, say, e g g p r o d u c t i o n ? ' ( D a w k i n s & B r o c k m a n n 1980). In practice, an engineer will normally be g i v e n a specification of m i n i m u m performance such as ' T h e b r i d g e m u s t b e a r a l o a d o f t e n tons . . . T h e a e r o p l a n e w i n g m u s t n o t b r e a k u n t i l i t r e c e i v e s a stress t h r e e t i m e s w h a t w o u l d b e e x p e c t e d i n w o r s t - c a s e turbulent conditions; n o w go ahead and build it as cheaply as you can.' T h e b e s t d e s i g n i s t h e o n e t h a t satisfies ('satisfices') t h e c r i t e r i o n s p e c i f i c a t i o n a t the least cost. A n y design that a c h i e v e s 'better' than the specified criterion performance is likely to be rejected, because p r e s u m a b l y the criterion could be achieved more cheaply. T h e particular criterion specification is an arbitrary w o r k i n g rule. T h e r e is

C o n s t r a i n t s on P e r f e c t i o n

n o t h i n g m a g i c a b o u t a safety m a r g i n o f t h r e e t i m e s t h e e x p e c t e d w o r s t - c a s e conditions. M i l i t a r y aircraft m a y be designed w i t h m o r e risky safety m a r g i n s t h a n c i v i l i a n o n e s . I n effect, t h e e n g i n e e r ' s o p t i m i z a t i o n i n s t r u c t i o n s a m o u n t to a m o n e t a r y e v a l u a t i o n of h u m a n safety, speed, c o n v e n i e n c e , p o l l u t i o n of the a t m o s p h e r e , e t c . T h e p r i c e p u t o n e a c h o f t h e s e i s a m a t t e r o f j u d g e m e n t , a n d is often a m a t t e r of c o n t r o v e r s y . I n the e v o l u t i o n a r y d e s i g n o f a n i m a l s a n d p l a n t s , j u d g e m e n t d o e s n o t e n t e r i n t o it, n o r d o e s c o n t r o v e r s y e x c e p t a m o n g t h e h u m a n s p e c t a t o r s o f t h e show. In some w a y , h o w e v e r , natural selection must p r o v i d e the e q u i v a l e n t of such j u d g e m e n t :

risks o f p r e d a t i o n m u s t b e e v a l u a t e d a g a i n s t risks o f

starving and benefits of m a t i n g w i t h an e x t r a f e m a l e . F o r a b i r d , resources s p e n t o n m a k i n g b r e a s t m u s c l e s for p o w e r i n g w i n g s a r e r e s o u r c e s t h a t c o u l d h a v e b e e n s p e n t o n m a k i n g e g g s . A n e n l a r g e d b r a i n w o u l d p e r m i t a finer tuning of b e h a v i o u r to e n v i r o n m e n t a l details, past a n d present, b u t at a cost of an enlarged h e a d , w h i c h m e a n s extra w e i g h t at the front e n d of the b o d y , w h i c h i n t u r n n e c e s s i t a t e s a l a r g e r tail for a e r o d y n a m i c s t a b i l i t y , w h i c h i n t u r n . . . W i n g e d a p h i d s a r e less f e c u n d t h a n w i n g l e s s o n e s o f t h e s a m e s p e c i e s (J.

Kennedy,

personal

communication).

That

every

evolutionary

a d a p t a t i o n m u s t c o s t s o m e t h i n g , costs b e i n g m e a s u r e d i n lost o p p o r t u n i t i e s to do other things, is as true as that g e m of traditional e c o n o m i c w i s d o m , ' T h e r e is no s u c h t h i n g as a free l u n c h ' . Of

course

the

mathematics

biological

currency-conversion,

e v a l u a t i n g t h e costs o f w i n g m u s c l e , s i n g i n g t i m e , p r e d a t o r - v i g i l a n c e t i m e , etc., i n s o m e c o m m o n c u r r e n c y s u c h a s ' g o n a d e q u i v a l e n t s ' , a r e l i k e l y t o b e v e r y c o m p l e x . W h e r e a s t h e e n g i n e e r i s a l l o w e d t o s i m p l i f y his m a t h e m a t i c s by working to an arbitrarily chosen m i n i m u m threshold of performance, the biologist is granted no such l u x u r y . O u r s y m p a t h y and a d m i r a t i o n must go out to

t h o s e few

biologists

who

have attempted

grapple

with

these

problems in detail (e.g. Oster & Wilson 1 9 7 8 ; M c F a r l a n d & H o u s t o n 1 9 8 1 ) . O n the o t h e r h a n d , a l t h o u g h t h e m a t h e m a t i c s m a y b e f o r m i d a b l e , w e d o n ' t need m a t h e m a t i c s to d e d u c e the most i m p o r t a n t point, w h i c h is that a n y v i e w o f b i o l o g i c a l o p t i m i z a t i o n that denies the existence o f costs a n d trade-offs i s d o o m e d . A n a d a p t a t i o n i s t w h o l o o k s a t o n e a s p e c t o f a n a n i m a l ' s b o d y o r b e h a v i o u r , s a y t h e a e r o d y n a m i c p e r f o r m a n c e o f its w i n g s , w h i l e forgetting that efficiency in the w i n g s c a n o n l y be b o u g h t at a cost w h i c h w i l l b e felt s o m e w h e r e else i n t h e a n i m a l ' s e c o n o m y , w o u l d d e s e r v e a l l t h e c r i t i c i s m h e g e t s . I t h a s t o b e a d m i t t e d t h a t t o o m a n y o f us, w h i l e n e v e r a c t u a l l y d e n y i n g t h e i m p o r t a n c e o f costs, f o r g e t t o m e n t i o n t h e m , p e r h a p s even forget to think a b o u t them, w h e n we discuss b i o l o g i c a l function. T h i s has p r o b a b l y p r o v o k e d s o m e o f t h e c r i t i c i s m t h a t h a s c o m e o u r w a y . I n a n earlier section I q u o t e d Pittendrigh's remark that a d a p t i v e o r g a n i z a t i o n w a s a ' p a t c h w o r k of makeshifts'. We must also not forget that it is a t a n g l e of compromises (Tinbergen 1965).

C o n s t r a i n t s on P e r f e c t i o n

I n p r i n c i p l e , i t w o u l d s e e m a v a l u a b l e h e u r i s t i c p r o c e d u r e t o assume t h a t a n a n i m a l i s o p t i m i z i n g s o m e t h i n g u n d e r a g i v e n set o f c o n s t r a i n t s , a n d t o try to w o r k out w h a t those constraints are. T h i s is a restricted version of w h a t M c F a r l a n d a n d his c o l l e a g u e s c a l l t h e ' r e v e r s e o p t i m a l i t y ' a p p r o a c h ( e . g . M c C l e e r y 1 9 7 8 ) . As a case study I shall take some w o r k with w h i c h I happen to be familiar. Dawkins

and

Brockmann

(1980)

found

that

the

digger

wasps

(Sphex

ichneumoneus) s t u d i e d b y B r o c k m a n n b e h a v e d i n a w a y t h a t a n a i v e h u m a n economist might have criticized as maladaptive. Individual wasps appeared to c o m m i t the ' C o n c o r d e F a l l a c y ' of v a l u i n g a resource a c c o r d i n g to how m u c h t h e y h a d a l r e a d y s p e n t o n it, r a t h e r t h a n a c c o r d i n g t o h o w m u c h t h e y c o u l d get out of it in the future. V e r y briefly, the e v i d e n c e is as follows. Solitary females provision burrows with stung and paralysed katydids which a r e t o s e r v e a s f o o d for t h e i r l a r v a e (see C h a p t e r 7 ) . O c c a s i o n a l l y t w o f e m a l e s find

themselves provisioning the same burrow,

and

they usually end

f i g h t i n g o v e r it. E a c h f i g h t g o e s o n u n t i l o n e w a s p , t h e r e b y d e f i n e d a s t h e loser, flees f r o m t h e a r e a , l e a v i n g t h e w i n n e r i n c o n t r o l o f t h e b u r r o w a n d a l l the k a t y d i d s c a u g h t by b o t h w a s p s . We m e a s u r e d the 'real v a l u e ' of a b u r r o w as the n u m b e r of katydids w h i c h it contained. T h e 'prior investment' by each w a s p i n t h e b u r r o w w a s m e a s u r e d a s t h e n u m b e r o f k a t y d i d s w h i c h she, a s a n i n d i v i d u a l , h a d p u t i n t o it. T h e e v i d e n c e s u g g e s t e d t h a t e a c h w a s p f o u g h t for a t i m e p r o p o r t i o n a l t o h e r o w n i n v e s t m e n t , r a t h e r t h a n p r o p o r t i o n a l t o the 'true v a l u e ' of the burrow. S u c h a p o l i c y has great h u m a n p s y c h o l o g i c a l a p p e a l . We too tend to fight t e n a c i o u s l y for p r o p e r t y w h i c h w e h a v e p u t g r e a t effort i n t o a c q u i r i n g . T h e f a l l a c y g e t s its n a m e f r o m t h e fact t h a t , a t a t i m e w h e n s o b e r e c o n o m i c j u d g e m e n t o f future prospects counselled a b a n d o n i n g the d e v e l o p i n g o f the C o n c o r d e a i r l i n e r , o n e o f t h e a r g u m e n t s i n f a v o u r o f c o n t i n u i n g w i t h the h a l f c o m p l e t e d project w a s retrospective: ' W e h a v e already spent so m u c h on it t h a t w e c a n n o t b a c k o u t n o w . ' A p o p u l a r a r g u m e n t for p r o l o n g i n g w a r s g a v e rise t o t h e o t h e r n a m e for t h e f a l l a c y , t h e ' O u r b o y s shall n o t h a v e d i e d i n vain' fallacy. W h e n D r B r o c k m a n n a n d I first r e a l i z e d t h a t d i g g e r w a s p s b e h a v e d i n like m a n n e r , I w a s , i t h a s t o b e c o n f e s s e d , a little d i s c o n c e r t e d , p o s s i b l y b e c a u s e o f m y o w n p a s t i n v e s t m e n t o f effort ( D a w k i n s & C a r l i s l e 1976a)

persuading

colleagues

that

1976; Dawkins

the p s y c h o l o g i c a l l y

appealing

C o n c o r d e F a l l a c y w a s , indeed, a fallacy! B u t then we started to think more seriously a b o u t cost constraints.

Could

it be

that w h a t appeared

to be

m a l a d a p t i v e w a s b e t t e r i n t e r p r e t e d as an o p t i m u m , given certain constraints? The

question

then

became:

there

constraint

such

that

the

wasps'

C o n c o r d i a n b e h a v i o u r is the best they c a n a c h i e v e u n d e r it? In fact the q u e s t i o n w a s m o r e c o m p l i c a t e d necessary to substitute

M a y n a r d Smith's

than

(1974)

that,

because it was

concept of evolutionary

C o n s t r a i n t s on P e r f e c t i o n

stability

('ESS'â&#x20AC;&#x201D;see Chapter

for t h a t o f s i m p l e o p t i m a l i t y ,

but the

principle remains that a reverse optimality a p p r o a c h m i g h t be heuristically valuable. If we c a n show that an animal's b e h a v i o u r is w h a t w o u l d be produced by an optimizing system w o r k i n g under constraint X, m a y b e we c a n use t h e a p p r o a c h t o l e a r n s o m e t h i n g o f t h e c o n s t r a i n t s u n d e r w h i c h animals actually do work. In the present case it s e e m e d that the r e l e v a n t constraint m i g h t be o n e of s e n s o r y c a p a c i t y . I f the w a s p s , for s o m e r e a s o n , c a n n o t c o u n t k a t y d i d s i n t h e b u r r o w , b u t c a n m e t r e s o m e a s p e c t o f t h e i r o w n h u n t i n g efforts, t h e r e i s a n asymmetry

of information

possessed

the

two

combatants.

Each

one

' k n o w s ' that the b u r r o w contains at least b k a t y d i d s , w h e r e b is the n u m b e r she h e r s e l f h a s c a u g h t .

She m a y 'estimate' that the true n u m b e r in the

b u r r o w is larger t h a n b, b u t she does not k n o w h o w m u c h l a r g e r . U n d e r s u c h conditions Grafen

(in p r e p a r a t i o n )

has shown that the expected

E S S is

a p p r o x i m a t e l y the one originally c a l c u l a t e d b y B i s h o p a n d C a n n i n g s (1978) for the s o - c a l l e d ' g e n e r a l i z e d w a r o f a t t r i t i o n ' . T h e m a t h e m a t i c a l d e t a i l s c a n be

left

aside;

for p r e s e n t

purposes w h a t

matters

that

the

behaviour

expected b y the e x t e n d e d w a r o f attrition m o d e l w o u l d look v e r y like the C o n c o r d i a n b e h a v i o u r actually s h o w n by the wasps. If we

were

interested

testing

the

general

hypothesis

that

animals

o p t i m i z e , this k i n d of post hoc r a t i o n a l i z a t i o n w o u l d be s u s p e c t . By post hoc m o d i f i c a t i o n o f t h e d e t a i l s o f t h e h y p o t h e s i s , o n e i s b o u n d t o find a v e r s i o n w h i c h fits t h e facts. M a y n a r d S m i t h ' s ( 1 9 7 8 b ) r e p l y t o this k i n d o f c r i t i c i s m i s very

relevant:

proposition

'...in

that

testing

nature

model

optimizes,

but

are

the

not

testing

specific

the

general

hypotheses

about

constraints, o p t i m i z a t i o n criteria, a n d heredity'. In the present case we are making a general assumption that nature does o p t i m i z e within constraints, and testing p a r t i c u l a r m o d e l s o f w h a t those constraints m i g h t b e . T h e particular constraint suggestedâ&#x20AC;&#x201D;inability of the w a s p ' s sensory system t o assess t h e

contents of a

b u r r o w â&#x20AC;&#x201D; i s in

accordance

with

independent

e v i d e n c e from the s a m e p o p u l a t i o n of w a s p s ( B r o c k m a n n , G r a f e n & D a w k i n s 1 9 7 9 ; B r o c k m a n n & D a w k i n s 1979). T h e r e is no reason to regard it as an i r r e v o c a b l y b i n d i n g l i m i t a t i o n for a l l t i m e . P r o b a b l y t h e w a s p s c o u l d e v o l v e the c a p a c i t y t o assess nest c o n t e n t s , b u t o n l y a t a c o s t . D i g g e r w a s p s o f t h e related

species

Ammophila

campestris

have

long

been

known

make

assessment o f t h e c o n t e n t s o f e a c h o f t h e i r nests e v e r y d a y ( B a e r e n d s 1 9 4 1 ) . U n l i k e Sphex, w h i c h p r o v i s i o n s o n e b u r r o w a t a t i m e , l a y s a n e g g , t h e n fills the b u r r o w i n w i t h soil a n d l e a v e s t h e l a r v a t o e a t t h e p r o v i s i o n o n its o w n , Ammophila

campestris

progressive

provisioner

several

burrows

concurrently. A female tends t w o or three g r o w i n g larvae, e a c h in a separate burrow, at the same time. T h e ages of her various l a r v a e are s t a g g e r e d , a n d t h e i r food

needs

are

different.

Every

m o r n i n g she

assesses

the

current

contents of each b u r r o w on a special early m o r n i n g 'inspection r o u n d ' . By

C o n s t r a i n t s on P e r f e c t i o n

e x p e r i m e n t a l l y c h a n g i n g t h e c o n t e n t s o f b u r r o w s , B a e r e n d s s h o w e d t h a t the female adjusts her w h o l e d a y ' s p r o v i s i o n i n g o f e a c h b u r r o w a c c o r d i n g t o w h a t i t c o n t a i n e d a t t h e t i m e o f h e r m o r n i n g i n s p e c t i o n . T h e c o n t e n t s o f the b u r r o w a t a n y o t h e r t i m e o f d a y h a v e n o effect o n h e r b e h a v i o u r , e v e n t h o u g h s h e i s p r o v i s i o n i n g i t a l l d a y . S h e a p p e a r s , t h e r e f o r e , t o use h e r a s s e s s m e n t f a c u l t y s p a r i n g l y , s w i t c h i n g i t off for t h e rest o f t h e d a y after the morning inspection, instrument.

almost as t h o u g h it w a s a costly,

power-consuming

F a n c i f u l a s t h a t a n a l o g y m a y b e , i t s u r e l y s u g g e s t s t h a t the

a s s e s s m e n t f a c u l t y , w h a t e v e r i t is, m a y h a v e o v e r h e a d r u n n i n g costs, e v e n i f ( G . P. B a e r e n d s , personal c o m m u n i c a t i o n ) these consist o n l y in the time consumed. Sphex ichneumoneus, n o t b e i n g a p r o g r e s s i v e p r o v i s i o n e r , a n d t e n d i n g o n l y o n e b u r r o w at a t i m e , p r e s u m a b l y h a s less n e e d t h a n Ammophila for a b u r r o w assessment faculty. By not a t t e m p t i n g to count prey in the b u r r o w , it c a n s a v e i t s e l f n o t o n l y t h e r u n n i n g e x p e n d i t u r e t h a t Ammophila s e e m s s o c a r e f u l to ration;

can

also

save

itself the

initial

m a n u f a c t u r i n g costs o f the

necessary neural a n d sensory a p p a r a t u s . P r o b a b l y it c o u l d benefit slightly from

having

ability

assess

burrow

contents,

but

only

the

c o m p a r a t i v e l y r a r e o c c a s i o n s w h e n i t f i n d s i t s e l f c o m p e t i n g for a b u r r o w w i t h a n o t h e r w a s p . I t i s e a s y t o b e l i e v e t h a t t h e costs o u t w e i g h t h e b e n e f i t s , a n d that

selection

has

therefore

never

favoured

the

evolution

o f assessment

a p p a r a t u s . I t h i n k this is a m o r e c o n s t r u c t i v e a n d i n t e r e s t i n g h y p o t h e s i s t h a n t h e a l t e r n a t i v e h y p o t h e s i s t h a t t h e n e c e s s a r y m u t a t i o n a l v a r i a t i o n has n e v e r a r i s e n . O f c o u r s e w e h a v e t o a d m i t t h a t the l a t t e r m i g h t b e r i g h t , b u t I w o u l d p r e f e r t o k e e p i t a s a h y p o t h e s i s o f last resort.

Imperfections at one level due to selection at another level O n e o f t h e m a i n t o p i c s t o b e t a c k l e d i n this b o o k i s t h a t o f t h e l e v e l a t w h i c h n a t u r a l s e l e c t i o n a c t s . T h e k i n d o f a d a p t a t i o n s w e s h o u l d see i f s e l e c t i o n a c t e d a t t h e l e v e l o f t h e g r o u p w o u l d b e q u i t e different f r o m t h e a d a p t a t i o n s w e s h o u l d e x p e c t i f s e l e c t i o n a c t s a t t h e l e v e l o f the i n d i v i d u a l . I t f o l l o w s t h a t a g r o u p s e l e c t i o n i s t m i g h t w e l l see a s i m p e r f e c t i o n s ,

features w h i c h

i n d i v i d u a l s e l e c t i o n i s t w o u l d see a s a d a p t a t i o n s . T h i s i s the m a i n r e a s o n w h y I

regard

adaptationism

unfair with

Gould the

and

naive

Lewontin's perfectionism

(1979) that

equating Haldane

of modern

named

after

V o l t a i r e ' s D r Pangloss. W i t h reservations d u e t o the various constraints o n p e r f e c t i o n , a n a d a p t a t i o n i s t m a y b e l i e v e t h a t all a s p e c t s o f o r g a n i s m s a r e ' a d a p t i v e o p t i m a l s o l u t i o n s t o p r o b l e m s ' , o r t h a t 'it i s v i r t u a l l y i m p o s s i b l e t o d o a b e t t e r j o b t h a n a n o r g a n i s m i s d o i n g i n its g i v e n e n v i r o n m e n t ' . Y e t the s a m e a d a p t a t i o n i s t m a y b e e x t r e m e l y fussy a b o u t t h e k i n d o f m e a n i n g h e allows

adaptive,

words indeed

'optimal'

Panglossian,

and

'better'.

explanations,

There for

are

many

example

most

kinds

group-

C o n s t r a i n t s on P e r f e c t i o n

selectionist

ones,

which

would

utterly

ruled

out

the

modern

adaptationist. F o r the Panglossian the d e m o n s t r a t i o n that s o m e t h i n g is ' b e n e f i c i a l '

(to

w h o m or to w h a t is often n o t s p e c i f i e d ) is a sufficient e x p l a n a t i o n for its e x i s t e n c e . T h e n e o - D a r w i n i a n a d a p t a t i o n i s t , o n t h e o t h e r h a n d , insists u p o n k n o w i n g the e x a c t nature of the selective process that has led to the e v o l u t i o n of the p u t a t i v e a d a p t a t i o n .

In particular,

h e insists o n p r e c i s e l a n g u a g e

a b o u t the l e v e l a t w h i c h n a t u r a l s e l e c t i o n i s s u p p o s e d t o h a v e a c t e d . T h e P a n g l o s s i a n l o o k s a t a o n e - t o - o n e s e x r a t i o a n d sees t h a t i t i s g o o d : d o e s i t n o t m i n i m i z e the w a s t a g e o f the p o p u l a t i o n ' s resources? T h e n e o - D a r w i n i a n a d a p t a t i o n i s t c o n s i d e r s i n d e t a i l t h e fates o f g e n e s a c t i n g o n p a r e n t s t o b i a s the sex r a t i o o f t h e i r o f f s p r i n g , a n d c a l c u l a t e s t h e e v o l u t i o n a r i l y s t a b l e s t a t e of the p o p u l a t i o n (Fisher 1 9 3 0 a ) . T h e Panglossian is d i s c o n c e r t e d by 1:1 sex ratios i n p o l y g y n o u s s p e c i e s , i n w h i c h a m i n o r i t y o f m a l e s h o l d h a r e m s a n d the rest sit a b o u t i n b a c h e l o r h e r d s c o n s u m i n g a l m o s t h a l f t h e p o p u l a t i o n ' s food r e s o u r c e s y e t c o n t r i b u t i n g n o t a t a l l t o t h e p o p u l a t i o n ' s r e p r o d u c t i o n . T h e n e o - D a r w i n i a n a d a p t a t i o n i s t t a k e s this i n his s t r i d e . T h e s y s t e m m a y b e hideously u n e c o n o m i c a l from the p o p u l a t i o n ' s point of v i e w , but, from the point of v i e w of the genes influencing the trait c o n c e r n e d , there is no m u t a n t that c o u l d do better. My point is that n e o - D a r w i n i a n a d a p t a t i o n i s m is not a c a t c h - a l l , b l a n k e t f a i t h i n a l l b e i n g for t h e b e s t . I t r u l e s o u t o f c o u r t m o s t o f the a d a p t i v e e x p l a n a t i o n s t h a t r e a d i l y o c c u r t o t h e P a n g l o s s i a n . S o m e years a g o , a c o l l e a g u e received an a p p l i c a t i o n from a p r o s p e c t i v e graduate student wishing to w o r k on adaptation, w h o was b r o u g h t up a religious fundamentalist a n d did not believe in e v o l u t i o n . He b e l i e v e d in adaptations,

but

thought

they were designed

by G o d ,

designed

for t h e

benefit o f . . . a h , b u t t h a t i s j u s t t h e p r o b l e m ! I t m i g h t b e t h o u g h t t h a t i t d i d not matter w h e t h e r the student

believed

adaptations

were

produced

natural selection or by G o d . A d a p t a t i o n s are 'beneficial' w h e t h e r because of natural

selection

because

beneficient

design,

and

could

not

fundamentalist student be usefully e m p l o y e d in u n c o v e r i n g the detailed w a y s i n w h i c h t h e y w e r e b e n e f i c i a l ? M y p o i n t i s t h a t this a r g u m e n t w i l l n o t d o , b e c a u s e w h a t i s b e n e f i c i a l t o o n e e n t i t y i n t h e h i e r a r c h y o f life i s h a r m f u l t o a n o t h e r , a n d c r e a t i o n i s m g i v e s u s n o g r o u n d s for s u p p o s i n g t h a t o n e e n t i t y ' s welfare will be preferred to another's. In passing, the fundamentalist student might pause to w o n d e r at a G o d w h o goes to great trouble to provide predators with beautiful adaptations to c a t c h prey, w h i l e w i t h the other hand g i v i n g prey beautiful adaptations to thwart them. P e r h a p s He enjoys the

spectator

sport.

Returning

the

main

point,

if adaptations

were

designed by G o d , He might h a v e designed them to benefit the i n d i v i d u a l a n i m a l (its s u r v i v a l o r â&#x20AC;&#x201D; n o t t h e s a m e t h i n g â&#x20AC;&#x201D; i t s i n c l u s i v e f i t n e s s ) , t h e s p e c i e s , some

other

species

such

mankind

(the

usual

view

religious

fundamentalists), the ' b a l a n c e of nature', or s o m e o t h e r i n s c r u t a b l e purpose

C o n s t r a i n t s on Perfection

k n o w n only to H i m . T h e s e are frequently incompatible alternatives. It really matters for w h o s e b e n e f i t a d a p t a t i o n s a r e d e s i g n e d . F a c t s s u c h a s t h e sex r a t i o in

harem-forming

mammals

are

inexplicable

certain

hypotheses

and

easily e x p l i c a b l e o n others. T h e adaptationist w o r k i n g w i t h i n the f r a m e w o r k of a

proper

understanding

of the

genetical

theory

of natural

selection

c o u n t e n a n c e s o n l y a v e r y r e s t r i c t e d set o f t h e p o s s i b l e f u n c t i o n a l h y p o t h e s e s w h i c h the Panglossian m i g h t admit. O n e o f t h e m a i n m e s s a g e s o f this b o o k i s t h a t , for m a n y p u r p o s e s , i t i s better to r e g a r d the level at w h i c h selection acts as neither the organism, nor the g r o u p or a n y larger unit, but the gene or small genetic fragment. T h i s difficult t o p i c w i l l b e d e b a t e d i n l a t e r c h a p t e r s . F o r the p r e s e n t , i t i s sufficient t o n o t e t h a t s e l e c t i o n a t t h e l e v e l o f t h e g e n e c a n g i v e rise t o a p p a r e n t i m p e r f e c t i o n s a t t h e l e v e l o f t h e i n d i v i d u a l . I s h a l l discuss ' m e i o t i c d r i v e ' a n d r e l a t e d p h e n o m e n a i n C h a p t e r 8 , b u t t h e classic e x a m p l e i s t h e c a s e o f h e t e r o z y g o u s a d v a n t a g e . A g e n e m a y b e p o s i t i v e l y s e l e c t e d b e c a u s e o f its b e n e f i c i a l effects w h e n h e t e r o z y g o u s , e v e n t h o u g h i t has h a r m f u l effects w h e n homozygous.

c o n s e q u e n c e o f this,

a predictable

p r o p o r t i o n o f the

individual organisms in the p o p u l a t i o n will h a v e defects. T h e general point i s this. T h e g e n o m e o f a n i n d i v i d u a l o r g a n i s m i n a s e x u a l p o p u l a t i o n i s t h e p r o d u c t o f a m o r e o r less r a n d o m s h u f f l i n g o f t h e g e n e s i n t h e p o p u l a t i o n . G e n e s a r e s e l e c t e d o v e r t h e i r a l l e l e s b e c a u s e o f t h e i r p h e n o t y p i c effects, a v e r a g e d o v e r all the i n d i v i d u a l bodies in w h i c h they are distributed, over the w h o l e population,

a n d t h r o u g h m a n y g e n e r a t i o n s . T h e effects t h a t a

g i v e n g e n e h a s w i l l u s u a l l y d e p e n d u p o n t h e o t h e r g e n e s w i t h w h i c h i t shares a body:

h e t e r o z y g o u s a d v a n t a g e is j u s t a s p e c i a l c a s e of this. A c e r t a i n

proportion of bad bodies seems an almost inevitable c o n s e q u e n c e of selection for g o o d g e n e s ,

w h e r e g o o d refers t o t h e a v e r a g e effects o f a g e n e o n a

s t a t i s t i c a l s a m p l e o f b o d i e s i n w h i c h i t f i n d s itself p e r m u t e d w i t h o t h e r g e n e s . I n e v i t a b l e , t h a t is, a s l o n g a s w e a c c e p t t h e M e n d e l i a n shuffle a s g i v e n a n d inescapable. adaptive

Williams

fine-adjustment

(1979),

disappointed

finding

evidence

for

of the sex ratio, m a k e s the p e r c e p t i v e point that

S e x is o n l y one of m a n y offspring characters that w o u l d seem a d a p t i v e for a p a r e n t t o c o n t r o l . F o r i n s t a n c e , i n h u m a n p o p u l a t i o n s affected b y s i c k l e - c e l l a n a e m i a , i t w o u l d b e a d v a n t a g e o u s for a h e t e r o z y g o u s w o m a n to h a v e her A eggs fertilized only by a-bearing sperm, and v i c e versa, or e v e n to a b o r t all h o m o z y g o u s e m b r y o s . Y e t if m a t e d to another

heterozygote

she

will

reliably

submit

the

Mendelian

l o t t e r y , e v e n t h o u g h this m e a n s m a r k e d l y l o w e r e d fitness for h a l f h e r children . .. T h e really fundamental questions in evolution m a y be a n s w e r a b l e only by r e g a r d i n g each gene as ultimately in conflict with e v e r y other g e n e , e v e n those at other loci in the s a m e cell. A really

C o n s t r a i n t s on P e r f e c t i o n

v a l i d t h e o r y o f n a t u r a l s e l e c t i o n m u s t b e b a s e d u l t i m a t e l y o n selfish replicators,

genes

and

all

other

entities

capable

the

biased

a c c u m u l a t i o n o f different v a r i a n t f o r m s . Amen!

Mistakes due to environmental unpredictability or 'malevolence' H o w e v e r well a d a p t e d a n a n i m a l m a y b e t o e n v i r o n m e n t a l c o n d i t i o n s , those conditions must be r e g a r d e d as a statistical a v e r a g e .

It will usually

i m p o s s i b l e t o c a t e r for e v e r y c o n c e i v a b l e c o n t i n g e n c y o f d e t a i l , a n d a n y given

animal

will therefore

frequently

be observed

to m a k e

'mistakes',

mistakes w h i c h c a n easily be fatal. T h i s is not the s a m e point as the t i m e - l a g p r o b l e m a l r e a d y m e n t i o n e d . T h e t i m e - l a g p r o b l e m arises b e c a u s e o f n o n stationarities

the

statistical

properties

of the

environment:

average

c o n d i t i o n s n o w a r e different f r o m t h e a v e r a g e c o n d i t i o n s e x p e r i e n c e d b y t h e animal's ancestors. T h e present point is m o r e inescapable. T h e m o d e r n a n i m a l m a y b e l i v i n g i n i d e n t i c a l average c o n d i t i o n s t o t h o s e o f a n a n c e s t o r , y e t the d e t a i l e d m o m e n t t o m o m e n t o c c u r r e n c e s f a c i n g e i t h e r o f t h e m a r e not the s a m e f r o m d a y t o d a y , a n d a r e t o o c o m p l e x for p r e c i s e p r e d i c t i o n t o be possible. It is particularly in b e h a v i o u r that such mistakes are seen. T h e m o r e static a t t r i b u t e s o f a n a n i m a l , its a n a t o m i c a l s t r u c t u r e for i n s t a n c e , a r e o b v i o u s l y adapted only to long-term average conditions. An individual is either big or s m a l l , i t c a n n o t c h a n g e s i z e f r o m m i n u t e t o m i n u t e a s t h e n e e d arises. Behaviour, rapid muscular m o v e m e n t , is that part of an animal's a d a p t i v e repertoire w h i c h is specifically concerned w i t h h i g h speed adjustment. T h e animal can be n o w here, n o w there, n o w up a tree, n o w u n d e r g r o u n d , rapidly a c c o m m o d a t i n g to environmental s u c h possible c o n t i n g e n c i e s ,

w h e n defined

contingencies. in

all

T h e number of

their detail,

the

n u m b e r of possible chess positions, v i r t u a l l y infinite. Just as c h e s s - p l a y i n g c o m p u t e r s ( a n d c h e s s - p l a y i n g p e o p l e ) l e a r n t o classify c h e s s p o s i t i o n s i n t o a m a n a g e a b l e n u m b e r o f g e n e r a l i z e d classes, s o t h e best t h a t a n a d a p t a t i o n i s t c a n h o p e for i s t h a t a n a n i m a l w i l l h a v e b e e n p r o g r a m m e d t o b e h a v e i n w a y s appropriate to a m a n a g e a b l e n u m b e r of g e n e r a l c o n t i n g e n c y classes. A c t u a l c o n t i n g e n c i e s w i l l f i t these g e n e r a l classes o n l y a p p r o x i m a t e l y , a n d a p p a r e n t mistakes are therefore b o u n d to be m a d e . T h e a n i m a l t h a t w e see u p a t r e e m a y c o m e f r o m a l o n g l i n e o f t r e e dwelling ancestors.

T h e trees i n w h i c h t h e a n c e s t o r s u n d e r w e n t n a t u r a l

s e l e c t i o n w e r e , i n g e n e r a l , m u c h t h e s a m e a s t h e trees o f t o d a y . G e n e r a l r u l e s of behaviour w h i c h w o r k e d then, such as ' N e v e r go out on a l i m b that is too t h i n ' , still w o r k . B u t t h e d e t a i l s o f a n y o n e t r e e a r e i n e v i t a b l y d i f f e r e n t from

C o n s t r a i n t s on P e r f e c t i o n

t h e d e t a i l s o f a n o t h e r . T h e l e a v e s a r e i n s l i g h t l y different p l a c e s , t h e b r e a k i n g strain of the b r a n c h e s is o n l y a p p r o x i m a t e l y p r e d i c t a b l e from their d i a m e t e r , a n d s o o n . H o w e v e r s t r o n g l y a d a p t a t i o n i s t o u r beliefs m a y b e , w e c a n o n l y e x p e c t animals to be a v e r a g e statistical optimizers, never perfect anticipators of every detail. S o far w e h a v e c o n s i d e r e d t h e e n v i r o n m e n t a s s t a t i s t i c a l l y c o m p l e x a n d therefore

hard

predict.

h a v e not

reckoned on

its

being actively

m a l e v o l e n t from o u r a n i m a l ' s point o f v i e w . T r e e b o u g h s surely d o not d e l i b e r a t e l y s n a p out of spite w h e n m o n k e y s v e n t u r e on to t h e m . B u t a 'tree b o u g h ' m a y t u r n o u t t o b e a c a m o u f l a g e d p y t h o n , a n d o u r m o n k e y ' s last m i s t a k e i s t h e n n o a c c i d e n t b u t is, i n a sense, d e l i b e r a t e l y e n g i n e e r e d . P a r t o f a m o n k e y ' s e n v i r o n m e n t i s n o n - l i v i n g o r a t least i n d i f f e r e n t t o t h e m o n k e y ' s existence,

and

the

unpredictability.

monkey's

mistakes

can

put

down

statistical

B u t o t h e r p a r t s o f t h e m o n k e y ' s e n v i r o n m e n t consist o f

l i v i n g t h i n g s t h a t a r e t h e m s e l v e s a d a p t e d t o profit a t the e x p e n s e o f m o n k e y s . T h i s portion o f the m o n k e y ' s e n v i r o n m e n t m a y b e called m a l e v o l e n t . M a l e v o l e n t e n v i r o n m e n t a l influences m a y themselves be hard to predict for t h e s a m e r e a s o n s a s i n d i f f e r e n t o n e s , b u t t h e y i n t r o d u c e a n a d d e d h a z a r d ; a n a d d e d o p p o r t u n i t y for t h e v i c t i m t o m a k e ' m i s t a k e s ' . T h e m i s t a k e m a d e by a r o b i n in f e e d i n g a c u c k o o in its nest is p r e s u m a b l y in s o m e sense a m a l a d a p t i v e blunder. T h i s is not an isolated, u n p r e d i c t a b l e o c c u r r e n c e such a s arises b e c a u s e o f t h e s t a t i s t i c a l u n p r e d i c t a b i l i t y o f t h e n o n - m a l e v o l e n t p a r t of the e n v i r o n m e n t .

It is a recurrent blunder,

a f f l i c t i n g g e n e r a t i o n after

g e n e r a t i o n o f r o b i n s , e v e n t h e s a m e r o b i n s e v e r a l t i m e s i n its life. E x a m p l e s o f this k i n d a l w a y s m a k e u s w o n d e r a t t h e c o m p l i a n c e , i n e v o l u t i o n a r y t i m e , of the organisms

that

are manipulated

against

t h e i r best

interests.

Why

doesn't selection s i m p l y e l i m i n a t e the susceptibility of robins to the deception of cuckoos? T h i s kind of problem is one of m a n y w h i c h I believe will one d a y b e c o m e the stock in trade of a n e w subdiscipline of b i o l o g y â&#x20AC;&#x201D; t h e study of m a n i p u l a t i o n , arms races a n d the extended p h e n o t y p e . M a n i p u l a t i o n and a r m s races form the subject of the next c h a p t e r , w h i c h in some w a y s can be r e g a r d e d a s a n e x p a n s i o n o f t h e t h e m e o f the final s e c t i o n o f this c h a p t e r .

4 A r m s Races and Manipulation

O n e o f m y p u r p o s e s i n this b o o k i s t o q u e s t i o n t h e ' c e n t r a l t h e o r e m ' t h a t i t i s useful t o e x p e c t i n d i v i d u a l o r g a n i s m s t o b e h a v e i n s u c h a w a y a s t o m a x i m i z e t h e i r o w n i n c l u s i v e fitness, o r i n o t h e r w o r d s t o m a x i m i z e t h e survival of copies of the genes inside them. T h e end of the p r e v i o u s c h a p t e r suggests one w a y i n w h i c h the c e n t r a l t h e o r e m m i g h t b e v i o l a t e d . O r g a n i s m s might consistently w o r k in the interests of other o r g a n i s m s r a t h e r t h a n of t h e m s e l v e s . T h a t is, t h e y m i g h t b e ' m a n i p u l a t e d ' . T h e fact that a n i m a l s frequently cause other a n i m a l s to p e r f o r m s o m e a c t i o n t h a t i s a g a i n s t t h e i r o w n b e s t i n t e r e s t s is, o f c o u r s e , w e l l k n o w n . O b v i o u s l y i t h a p p e n s e v e r y t i m e a n a n g l e r fish c a t c h e s p r e y , e v e r y t i m e a c u c k o o i s fed b y its foster m o t h e r . I s h a l l m a k e use o f b o t h t h e s e e x a m p l e s i n this c h a p t e r , b u t I s h a l l a l s o e m p h a s i z e t w o p o i n t s t h a t h a v e n o t a l w a y s b e e n stressed. F i r s t l y , i t i s n a t u r a l t o a s s u m e t h a t e v e n i f a m a n i p u l a t o r g e t s a w a y with it temporarily, it is o n l y a m a t t e r of e v o l u t i o n a r y time before the l i n e a g e of manipulated organisms comes up with a counter-adaptation.

In other

words, we tend to assume that m a n i p u l a t i o n o n l y w o r k s b e c a u s e of the 'timel a g ' c o n s t r a i n t o n p e r f e c t i o n . I n this c h a p t e r I s h a l l p o i n t o u t t h a t , o n t h e contrary, there are conditions under w h i c h we should e x p e c t m a n i p u l a t o r s to s u c c e e d c o n s i s t e n t l y a n d for i n d e f i n i t e l e n g t h s o f e v o l u t i o n a r y t i m e . I s h a l l discuss this l a t e r u n d e r t h e c a t c h - p h r a s e o f ' a r m s r a c e s ' . S e c o n d l y , u n t i l t h e last d e c a d e o r so, m o s t o f u s h a v e p a i d i n s u f f i c i e n t attention to the likelihood of intraspecific m a n i p u l a t i o n , especially e x p l o i t a t i v e m a n i p u l a t i o n w i t h i n t h e f a m i l y . I a t t r i b u t e this d e f i c i e n c y t o a r e s i d u u m of group-selectionist

intuition

which

often

lurks

the

depths

of the

b i o l o g i s t ' s m i n d e v e n after g r o u p s e l e c t i o n h a s b e e n r e j e c t e d a t t h e s u r f a c e level of reason. I think that a m i n o r revolution has taken p l a c e in the w a y we think a b o u t social relationships. ' G e n t e e l ' benevolent

mutual

cooperation

(Lloyd

are replaced

1979) ideas of v a g u e l y

by an

expectation

o f stark,

ruthless, o p p o r t u n i s t i c m u t u a l e x p l o i t a t i o n ( e . g . H a m i l t o n 1 9 6 4 a , b , 1 9 7 0 , 1971a; Williams

1966; Trivers 1972, 55

1974; Ghiselin

1974a; Alexander

A r m s Races and Manipulation

1 9 7 4 ) . T h i s r e v o l u t i o n is p o p u l a r l y associated w i t h the n a m e 'sociobiology', a l t h o u g h the association is s o m e w h a t ironic since, as I h a v e suggested before, Wilson's

(1975)

great

book

of that

name

many

respects

pre-

r e v o l u t i o n a r y i n a t t i t u d e : n o t t h e n e w s y n t h e s i s , b u t t h e last a n d g r e a t e s t s y n t h e s i s o f t h e o l d , b e n e v o l e n t r e g i m e ( e . g . his C h a p t e r 5 ) . I c a n e x e m p l i f y t h e c h a n g e d v i e w b y q u o t i n g from o n e r e c e n t p a p e r , L l o y d ' s ( 1 9 7 9 ) e n t e r t a i n i n g r e v i e w o f s e x u a l d i r t y tricks i n i n s e c t s . S e l e c t i o n for h a s t e i n m a l e s , a n d c o y n e s s i n f e m a l e s , results i n w h a t a m o u n t s t o c o m p e t i t i o n between t h e s e x e s . M a l e s m a y b e s e l e c t e d t o b y p a s s a n y c h o i c e that the females a t t e m p t to exercise, and then females selected to m a i n t a i n their options, to not be misled or to h a v e t h e i r c h o i c e s s u b v e r t e d . I f m a l e s s u b d u e a n d s e d u c e f e m a l e s w i t h true a p h r o d i s i a c s [ L l o y d g i v e s e v i d e n c e e l s e w h e r e i n the p a p e r ] , f e m a l e s m a y be expected to escape sooner or later in evolutionary time. A n d after s p e r m h a s b e e n p l a c e d i n a f e m a l e , s h e s h o u l d m a n i p u l a t e i t : s t o r e , t r a n s f e r (from c h a m b e r t o c h a m b e r ) , use, e a t , o r d i s s o l v e it, a s she m a k e s a d d i t i o n a l observations o n males. F e m a l e s m a y a c c e p t and s t o r e s p e r m f r o m a m a l e for i n s u r a n c e t h a t t h e y w i l l g e t a m a t e , a n d t h e n b e c o m e c h o o s y . . . I t i s p o s s i b l e for s p e r m t o b e m a n i p u l a t e d i n the female (e.g. sex d e t e r m i n a t i o n in H y m e n o p t e r a ) . F e m a l e reprod u c t i v e m o r p h o l o g y o f t e n i n c l u d e s sacs, v a l v e s , a n d t u b e s t h a t c o u l d h a v e e v o l v e d i n this c o n t e x t . I n f a c t , i t i s p o s s i b l e t h a t s o m e r e p o r t e d examples

sperm

competition

m a n i p u l a t i o n . .. G i v e n

that

are

females,

actually to

one

cases

extent

of or

sperm another,

s u b v e r t m a l e interests by the internal m a n i p u l a t i o n of ejaculate, it is not

inconceivable

that

males

will

have

evolved

little

openers,

snippers, levers a n d syringes that put sperm in the places females h a v e evolved

( ' i n t e n d e d ' ) for s p e r m w i t h p r i o r i t y u s a g e â&#x20AC;&#x201D; c o l l e c t i v e l y , a

veritable Swiss A r m y K n i f e of g a d g e t r y !

T h i s kind o f unsentimental, d o g eat d o g , l a n g u a g e w o u l d not h a v e c o m e e a s i l y t o b i o l o g i s t s a f e w y e a r s a g o , b u t n o w a d a y s I a m g l a d t o say i t dominates the textbooks (e.g. A l c o c k 1979). S u c h dirty tricks, as often as not, i n v o l v e direct a c t i o n , the muscles of one i n d i v i d u a l m o v i n g to molest the b o d y of another. T h e m a n i p u l a t i o n w h i c h is t h e s u b j e c t o f this c h a p t e r i s m o r e i n d i r e c t a n d m o r e s u b t l e . A n i n d i v i d u a l i n d u c e s t h e effectors o f a n o t h e r i n d i v i d u a l t o w o r k a g a i n s t its o w n best interests, a n d in f a v o u r of the interests of the m a n i p u l a t o r . A l e x a n d e r (1974) w a s o n e o f t h e first t o e m p h a s i z e t h e i m p o r t a n c e o f s u c h m a n i p u l a t i o n . H e g e n e r a l i z e d his c o n c e p t o f q u e e n d o m i n a t i o n i n t h e e v o l u t i o n o f s o c i a l insect worker behaviour, to produce a wide-ranging theory of 'parental manipul a t i o n ' (see a l s o G h i s e l i n

1 9 7 4 a ) . He suggested that parents are in such a

A r m s Races and Manipulation

c o m m a n d i n g position o v e r their offspring that offspring m a y be forced to w o r k i n t h e interests o f t h e i r p a r e n t s ' g e n e t i c f i t n e s s , e v e n w h e r e this c o n f l i c t s with their o w n .

West-Eberhard

(1975)

follows A l e x a n d e r in dignifying

parental manipulation as one of three general w a y s in w h i c h individual 'altruism' can e v o l v e , the others b e i n g kin selection a n d r e c i p r o c a l altruism. R i d l e y a n d I m a k e t h e s a m e p o i n t , b u t d o n o t r e s t r i c t o u r s e l v e s t o parental manipulation ( R i d l e y & D a w k i n s in press). T h e a r g u m e n t is as follows. Biologists define b e h a v i o u r as altruistic if it f a v o u r s o t h e r i n d i v i d u a l s a t the e x p e n s e o f t h e a l t r u i s t h i m s e l f . A p r o b l e m arises, i n c i d e n t a l l y , o v e r h o w b e n e f i t a n d e x p e n s e a r e t o b e d e f i n e d . I f t h e y are defined in terms of i n d i v i d u a l survival, acts of altruism are e x p e c t e d to be very c o m m o n , and will be taken to include parental care. If they are defined in terms of i n d i v i d u a l r e p r o d u c t i v e success, p a r e n t a l c a r e no l o n g e r c o u n t s as altruism, but altruistic acts towards other relatives are p r e d i c t e d by neoD a r w i n i a n theory. If benefit a n d expense are defined in terms of i n d i v i d u a l i n c l u s i v e f i t n e s s , n e i t h e r p a r e n t a l c a r e n o r c a r e for o t h e r g e n e t i c r e l a t i v e s counts as altruism, a n d indeed a n a i v e version of the t h e o r y e x p e c t s that altruism should not really exist. A n y of the three definitions c a n be justified, a l t h o u g h if we must talk of altruism at all I prefer the first definition, the o n e that allows parental care as altruistic. But my point here is that, w h i c h e v e r definition we favour, it is met if the 'altruist' is forcedâ&#x20AC;&#x201D; m a n i p u l a t e d â&#x20AC;&#x201D; b y the beneficiary into d o n a t i n g s o m e t h i n g to h i m . F o r instance, the definition (any o f the t h r e e ) a l l o w s u s n o c h o i c e b u t t o r e g a r d t h e f e e d i n g o f a c u c k o o n e s t l i n g b y its foster p a r e n t a s a l t r u i s t i c b e h a v i o u r . M a y b e this m e a n s w e n e e d a n e w k i n d o f d e f i n i t i o n , b u t t h a t i s a n o t h e r issue. K r e b s a n d I t a k e t h e a r g u m e n t t o its l o g i c a l c o n c l u s i o n , a n d i n t e r p r e t a l l o f a n i m a l c o m m u n i cation as manipulation of signal-receiver by signal-sender ( D a w k i n s & K r e b s 1978). M a n i p u l a t i o n is, i n d e e d , p i v o t a l t o t h e v i e w o f life e x p o u n d e d i n this b o o k , a n d i t i s a trifle i r o n i c t h a t I a m o n e o f those w h o h a s c r i t i c i z e d A l e x a n d e r ' s concept of parental manipulation (Dawkins 1976a, pp. 1 4 5 - 1 4 8 ; Blick 1 9 7 7 ; Parker & M a c n a i r 1 9 7 8 ; K r e b s & D a v i e s 1 9 7 8 ; S t a m p s & M e t c a l f 1980), a n d , i n t u r n , b e e n c r i t i c i z e d for d o i n g s o ( S h e r m a n 1 9 7 8 ; H a r p e n d i n g 1 9 7 9 ; D a l y 1 9 8 0 ) . N o t w i t h s t a n d i n g these d e f e n d e r s , A l e x a n d e r ( 1 9 8 0 , p p . 3 8 - 3 9 ) h i m s e l f h a s c o n c e d e d t h a t his c r i t i c s w e r e r i g h t . C l e a r l y some clarification is necessary. Neither I, nor a n y of the later critics

mentioned,

doubted

that

selection

would

favour

parents

who

s u c c e e d e d i n m a n i p u l a t i n g their offspring, o v e r parents w h o did not. N o r did we doubt that parents w o u l d indeed, in m a n y cases, ' w i n the a r m s r a c e ' a g a i n s t offspring. A l l w e w e r e o b j e c t i n g t o w a s t h e l o g i c o f s u g g e s t i n g t h a t parents enjoy a built-in a d v a n t a g e o v e r their children, simply b e c a u s e all children aspire to b e c o m e parents. T h a t is no m o r e true than that children enjoy a built-in a d v a n t a g e simply b e c a u s e all parents w e r e o n c e c h i l d r e n .

A r m s Races and Manipulation

A l e x a n d e r h a d s u g g e s t e d t h a t t e n d e n c i e s t o selfishness i n c h i l d r e n , t e n d e n c i e s to act a g a i n s t the interests of their parents, c o u l d not spread b e c a u s e , w h e n t h e c h i l d g r e w u p , its o w n c h i l d r e n ' s i n h e r i t e d selfishness a g a i n s t i t w o u l d d e t r a c t f r o m its o w n r e p r o d u c t i v e s u c c e s s . F o r A l e x a n d e r this s p r a n g from his c o n v i c t i o n that 'the entire parent-offspring interaction has evolved because it benefited one of the t w o individualsâ&#x20AC;&#x201D;the parent. No organism can evolve p a r e n t a l b e h a v i o u r , o r e x t e n d its p a r e n t a l c a r e , unless its o w n r e p r o d u c t i o n is t h e r e b y e n h a n c e d ' ( A l e x a n d e r 1 9 7 4 , p. 340). A l e x a n d e r was, therefore, t h i n k i n g f i r m l y w i t h i n t h e p a r a d i g m o f t h e selfish o r g a n i s m . H e u p h e l d the c e n t r a l t h e o r e m t h a t a n i m a l s a c t i n t h e interests o f t h e i r o w n i n c l u s i v e f i t n e s s , a n d h e u n d e r s t o o d this t o p r e c l u d e t h e p o s s i b i l i t y o f o f f s p r i n g a c t i n g a g a i n s t t h e i r p a r e n t ' s i n t e r e s t s . B u t t h e lesson I p r e f e r t o l e a r n f r o m A l e x a n d e r i s t h a t of t h e c e n t r a l i m p o r t a n c e of m a n i p u l a t i o n itself, w h i c h I r e g a r d as a violation of the central theorem. I

believe

animals

exert

strong

power

over

other

animals,

and

that

f r e q u e n t l y a n a n i m a l ' s a c t i o n s a r e m o s t u s e f u l l y i n t e r p r e t e d a s w o r k i n g i n the i n t e r e s t s of another i n d i v i d u a l ' s i n c l u s i v e fitness, r a t h e r t h a n its o w n . L a t e r in this b o o k w e s h a l l d i s p e n s e w i t h t h e use o f the c o n c e p t o f i n c l u s i v e f i t n e s s a l t o g e t h e r , a n d t h e p r i n c i p l e s o f m a n i p u l a t i o n w i l l b e s u b s u m e d u n d e r the u m b r e l l a o f the e x t e n d e d p h e n o t y p e . B u t for t h e rest o f this c h a p t e r i t w i l l b e c o n v e n i e n t t o d i s c u s s m a n i p u l a t i o n a t the l e v e l o f t h e i n d i v i d u a l o r g a n i s m . T h e r e is an inevitable o v e r l a p here with a paper w h i c h I wrote jointly with J.

R. K r e b s on a n i m a l signals as manipulation

(Dawkins & Krebs

1 9 7 8 ) . B e f o r e p r o c e e d i n g , I feel o b l i g e d t o a c k n o w l e d g e t h a t this p a p e r h a s b e e n s e v e r e l y c r i t i c i z e d b y H i n d e ( 1 9 8 1 ) . S o m e o f his c r i t i c i s m s , w h i c h d o n o t affect t h e p a r t s o f t h e p a p e r I w i s h t o use h e r e , a r e a n s w e r e d b y C a r y l (in p r e s s ) , w h o h a d a l s o b e e n c r i t i c i z e d b y H i n d e . H i n d e t o o k u s t o task for unfairness in q u o t i n g a p p a r e n t l y group-selectionist statements by T i n b e r g e n ( 1 9 6 4 ) a n d o t h e r s w h o m w e l a b e l l e d , for w a n t o f a b e t t e r title, c l a s s i c a l e t h o l o g i s t s . I h a v e s y m p a t h y w i t h this h i s t o r i c a l c r i t i c i s m . T h e ' g o o d o f the species' passage w h i c h we q u o t e d from T i n b e r g e n w a s a g e n u i n e quotation, b u t I a g r e e t h a t i t w a s n o t t y p i c a l o f T i n b e r g e n ' s ( e . g . 1 9 6 5 ) t h i n k i n g a t that t i m e . T h e f o l l o w i n g m u c h earlier q u o t a t i o n from T i n b e r g e n w o u l d , perhaps, h a v e b e e n a f a i r e r o n e for u s t o h a v e c h o s e n : ' . . . j u s t a s the f u n c t i o n i n g o f h o r m o n e s a n d the n e r v o u s system implies not o n l y the s e n d i n g out of signals b u t also a specific responsiveness in the r e a c t i n g o r g a n , so the releaser system i n v o l v e s a specific responsiveness to p a r t i c u l a r releasers in

the reacting

i n d i v i d u a l a s w e l l a s a s p e c i f i c t e n d e n c y t o s e n d o u t t h e s i g n a l s i n the i n i t i a t o r . T h e r e l e a s e r s y s t e m ties i n d i v i d u a l s i n t o u n i t s o f a s u p e r - i n d i v i d u a l order and renders t h e m h i g h e r units subject to natural selection' ( T i n b e r g e n 1954).

Even

if outright

group-selectionism

was

strongly

opposed

T i n b e r g e n a n d m o s t o f his p u p i l s i n t h e e a r l y 1960s, I still t h i n k t h a t n e a r l y all of us t h o u g h t of a n i m a l signals in terms of a v a g u e notion of 'mutual

A r m s Races and Manipulation

b e n e f i t ' : i f s i g n a l s w e r e n o t a c t u a l l y 'for t h e g o o d o f t h e s p e c i e s ' (as i n t h e unrepresentative

quotation

from

Tinbergen),

they

were

'for

the

mutual

benefit o f b o t h s i g n a l l e r a n d r e c e i v e r ' . T h e e v o l u t i o n o f r i t u a l i z e d s i g n a l s w a s regarded as m u t u a l e v o l u t i o n : e n h a n c e d signalling p o w e r on one side w a s a c c o m p a n i e d by increased sensitivity to the signals on the o t h e r side. T o d a y we w o u l d r e c o g n i z e that if receiver sensitivity increases, signal strength does not need to increase but, instead, is m o r e likely to d e c r e a s e o w i n g t o t h e a t t e n d a n t costs o f c o n s p i c u o u s o r l o u d s i g n a l s . T h i s m i g h t b e c a l l e d the S i r A d r i a n B o u l t p r i n c i p l e . O n c e , i n r e h e a r s a l , S i r A d r i a n t u r n e d t o the v i o l a s a n d told t h e m t o p l a y o u t m o r e . ' B u t S i r A d r i a n ' , p r o t e s t e d t h e p r i n c i p a l v i o l a , ' y o u w e r e i n d i c a t i n g less a n d less w i t h y o u r b a t o n . ' ' T h e i d e a ' , r e t o r t e d t h e m a e s t r o , 'is t h a t I s h o u l d d o less a n d less, a n d y o u s h o u l d d o m o r e a n d m o r e ! ' I n those cases w h e r e a n i m a l signals r e a l l y are o f m u t u a l b e n e f i t , t h e y w i l l t e n d t o sink t o the l e v e l o f a c o n s p i r a t o r i a l w h i s p e r : i n d e e d this m a y often h a v e h a p p e n e d , t h e r e s u l t i n g s i g n a l s b e i n g t o o i n c o n s p i c u o u s for u s t o h a v e n o t i c e d t h e m . I f s i g n a l s t r e n g t h i n c r e a s e s o v e r t h e g e n e r a t i o n s this

suggests,

the

other

hand,

that

there

has

been

increasing

sales

r e s i s t a n c e o n t h e side o f t h e r e c e i v e r ( W i l l i a m s 1 9 6 6 ) . As mentioned earlier, an a n i m a l will not necessarily submit passively to being manipulated, and an evolutionary 'arms race' is expected to develop. A r m s races w e r e the subject of a second j o i n t p a p e r ( D a w k i n s &

Krebs

1 9 7 9 ) . W e w e r e n o t , o f c o u r s e , t h e f i r s t t o m a k e t h e p o i n t s t h a t f o l l o w i n this chapter, but nevertheless it will be convenient to quote from our t w o joint papers. W i t h permission from Dr K r e b s , I shall do so w i t h o u t b r e a k i n g the flow with repeated bibliographic citations and quotation marks. A n a n i m a l often n e e d s t o m a n i p u l a t e o b j e c t s i n t h e w o r l d a r o u n d it. A p i g e o n c a r r i e s t w i g s t o its nest. A c u t t l e f i s h b l o w s s a n d f r o m t h e s e a b o t t o m t o e x p o s e p r e y . A b e a v e r fells trees a n d , b y m e a n s o f its d a m , m a n i p u l a t e s t h e e n t i r e l a n d s c a p e for m i l e s a r o u n d its l o d g e . W h e n t h e o b j e c t a n a n i m a l s e e k s t o m a n i p u l a t e i s n o n - l i v i n g , o r a t least w h e n i t i s n o t s e l f - m o b i l e , t h e a n i m a l has n o c h o i c e b u t t o shift i t b y b r u t e f o r c e . A d u n g b e e t l e c a n m o v e a b a l l o f d u n g o n l y b y f o r c i b l y p u s h i n g it. B u t s o m e t i m e s a n a n i m a l m a y b e n e f i t b y m o v i n g a n ' o b j e c t ' w h i c h h a p p e n s , itself, t o b e a n o t h e r l i v i n g a n i m a l . T h e o b j e c t has m u s c l e s a n d l i m b s o f its o w n , c o n t r o l l e d b y a n e r v o u s s y s t e m a n d sense o r g a n s . W h i l e i t m a y still b e p o s s i b l e t o shift s u c h a n ' o b j e c t ' b y b r u t e force, the g o a l m a y often b e m o r e e c o n o m i c a l l y e n g i n e e r e d b y s u b t l e r m e a n s . T h e object's musclesâ&#x20AC;&#x201D;may

internal be

chain

infiltrated

of commandâ&#x20AC;&#x201D;sense organs, and

subverted.

male

nervous system, cricket

does

not

p h y s i c a l l y roll a f e m a l e a l o n g t h e g r o u n d a n d i n t o his b u r r o w . H e sits a n d sings, a n d the f e m a l e c o m e s t o h i m u n d e r h e r o w n p o w e r . F r o m his p o i n t o f v i e w this communication i s e n e r g e t i c a l l y m o r e efficient t h a n t r y i n g t o t a k e h e r by force. A q u e s t i o n i m m e d i a t e l y arises. W h y s h o u l d t h e f e m a l e s t a n d for i t ? S i n c e

A r m s R a c e s and M a n i p u l a t i o n

s h e i s i n c o n t r o l o f h e r o w n m u s c l e s a n d l i m b s , w h y w o u l d she a p p r o a c h t h e male

unless

her

genetic

interests

so?

Surely

the

word

m a n i p u l a t i o n is a p p r o p r i a t e o n l y if the v i c t i m is u n w i l l i n g ? S u r e l y the m a l e c r i c k e t i s s i m p l y i n f o r m i n g t h e f e m a l e o f a f a c t t h a t i s useful t o h e r , t h a t o v e r h e r e i s a r e a d y a n d w i l l i n g m a l e o f h e r o w n s p e c i e s . H a v i n g g i v e n h e r this i n f o r m a t i o n , d o e s n ' t h e t h e n l e a v e i t u p t o h e r t o a p p r o a c h h i m o r n o t a s she pleases, or as natural selection has p r o g r a m m e d her? W e l l a n d g o o d w h e n m a l e s a n d f e m a l e s h a p p e n t o h a v e i d e n t i c a l interests, b u t e x a m i n e t h e p r e m i s e o f t h e last p a r a g r a p h . W h a t e n t i t l e s u s t o assert t h a t t h e f e m a l e i s ' i n c o n t r o l o f h e r o w n m u s c l e s a n d l i m b s ' ? D o e s n ' t this b e g the very question we are interested in? By a d v a n c i n g a manipulation hypothesis w e a r e , i n effect, s u g g e s t i n g t h a t t h e f e m a l e m a y not b e i n c o n t r o l o f h e r o w n muscles a n d limbs, a n d that the m a l e m a y be. T h i s e x a m p l e c o u l d , o f course, b e reversed, a n d the f e m a l e b e said t o m a n i p u l a t e the m a l e . T h e point b e i n g m a d e has no specific c o n n e c t i o n with sexuality.

could

h a v e u s e d the

e x a m p l e of plants, l a c k i n g muscles of their o w n , using insect muscles as e f f e c t o r o r g a n s t o t r a n s p o r t t h e i r p o l l e n , a n d f u e l l i n g those m u s c l e s w i t h nectar (Heinrich 1979). T h e general point is that an organism's limbs m a y be m a n i p u l a t e d

t o w o r k i n t h e i n t e r e s t s o f t h e g e n e t i c fitness o f a n o t h e r

o r g a n i s m . T h i s s t a t e m e n t c a n n o t be m a d e c o n v i n c i n g until later in the book when we have introduced

the i d e a o f the e x t e n d e d

phenotype.

F o r this

c h a p t e r w e a r e still w o r k i n g w i t h i n t h e p a r a d i g m o f the selfish o r g a n i s m , a l b e i t w e a r e s t a r t i n g t o s t r e t c h i t s o t h a t i t c r e a k s o m i n o u s l y a t the e d g e s . T h e e x a m p l e of male and female cricket m a y have been poorly chosen, b e c a u s e , a s I s a i d a b o v e , m a n y o f u s h a v e o n l y r e c e n t l y b e c o m e u s e d t o the i d e a of sexual relations as a battle. M a n y of us h a v e yet to absorb into our c o n s c i o u s n e s s t h e f a c t t h a t ' s e l e c t i o n c a n a c t i n o p p o s i t i o n o n t h e t w o sexes. C o m m o n l y , for a g i v e n t y p e o f e n c o u n t e r , m a l e s w i l l b e f a v o u r e d i f t h e y d o m a t e a n d f e m a l e s i f t h e y d o n ' t ' ( P a r k e r 1 9 7 9 ; see a l s o W e s t - E b e r h a r d 1 9 7 9 ) . I s h a l l r e t u r n t o this, b u t for t h e m o m e n t let u s use a s t a r k e r e x a m p l e o f m a n i p u l a t i o n . As starkly ruthless as a n y battle in n a t u r e is that b e t w e e n p r e d a t o r a n d p r e y . T h e r e a r e v a r i o u s t e c h n i q u e s a p r e d a t o r m a y use t o c a t c h his p r e y . H e m a y r u n after t h e m a n d a t t e m p t t o o u t p a c e , o u t s t a y , o r o u t f l a n k t h e m . H e m a y sit i n o n e p l a c e a n d a m b u s h o r t r a p t h e m . O r h e m a y d o a s angler fish and

'femmes

fatales' fireflies (Lloyd

1975,

1981)

do,

and

m a n i p u l a t e t h e p r e y ' s o w n n e r v o u s s y s t e m s o t h a t i t a c t i v e l y a p p r o a c h e s its o w n d o o m . A n a n g l e r f i s h sits o n t h e sea b o t t o m a n d i s h i g h l y c a m o u f l a g e d e x c e p t for a l o n g r o d p r o j e c t i n g f r o m t h e t o p o f t h e h e a d , o n t h e e n d o f w h i c h i s t h e ' l u r e ' , a f l e x i b l e p i e c e o f tissue w h i c h r e s e m b l e s s o m e a p p e t i z i n g m o r s e l s u c h as a w o r m . S m a l l fish, p r e y of the angler, are attracted by the lure w h i c h resembles their o w n prey. W h e n they a p p r o a c h it the a n g l e r ' p l a y s ' t h e m d o w n i n t o t h e v i c i n i t y o f his m o u t h , t h e n s u d d e n l y o p e n s his j a w s a n d

A r m s Races and Manipulation

the p r e y a r e e n g u l f e d i n t h e i n r u s h o f w a t e r . I n s t e a d o f u s i n g m a s s i v e b o d y and

tail

muscles

active

pursuit

of prey,

the

angler

uses

the

small

e c o n o m i c a l m u s c l e s c o n t r o l l i n g his r o d , t o t i t i l l a t e t h e p r e y ' s n e r v o u s s y s t e m v i a its e y e s . F i n a l l y i t i s t h e p r e y f i s h ' s o w n m u s c l e s t h a t t h e a n g l e r uses t o c l o s e the g a p b e t w e e n t h e m . K r e b s a n d I i n f o r m a l l y c h a r a c t e r i z e d a n i m a l ' c o m m u n i c a t i o n ' as a m e a n s by w h i c h one a n i m a l m a k e s use of a n o t h e r animal's muscle power. This is roughly synonymous with manipulation. T h e s a m e q u e s t i o n arises a s b e f o r e . W h y d o e s t h e v i c t i m o f m a n i p u l a t i o n s t a n d for i t ? W h y d o e s t h e p r e y f i s h r u s h l i t e r a l l y i n t o t h e j a w s o f d e a t h ? B e c a u s e i t ' t h i n k s ' i t i s r e a l l y r u s h i n g t o g e t a m e a l itself. M o r e f o r m a l l y , n a t u r a l s e l e c t i o n h a s a c t e d o n its a n c e s t o r s , f a v o u r i n g t e n d e n c i e s t o a p p r o a c h small w r i g g l i n g objects, because small w r i g g l i n g objects are usually w o r m s . Since they are not a l w a y s w o r m s but sometimes a n g l e r fish lures, there m a y well be some selection on prey fish to be cautious, or to sharpen up their powers of discrimination.

the

extent

that lures

are g o o d

mimics of

worms, we m a y surmise that selection has acted on the a n g l e r fishes' ancestors t o i m p r o v e t h e m , i n the f a c e o f i m p r o v e d d i s c r i m i n a t i o n b y t h e i r p r e y . S o m e prey are c a u g h t , and angler fish do m a k e a living, so some m a n i p u l a t i o n is g o i n g on successfully. I t i s c o n v e n i e n t t o use t h e m e t a p h o r o f a n a r m s r a c e w h e n e v e r w e h a v e progressive i m p r o v e m e n t s in adaptations in one lineage, as an e v o l u t i o n a r y response to progressive c o u n t e r - i m p r o v e m e n t s in an e n e m y l i n e a g e . important

realize

who

are

the

parties

that

are

'racing'

against

It is one

another. T h e y are not i n d i v i d u a l s but lineages. To be sure, it is i n d i v i d u a l s w h o a t t a c k a n d d e f e n d , i n d i v i d u a l s w h o k i l l o r resist b e i n g k i l l e d . B u t t h e arms race takes p l a c e on the e v o l u t i o n a r y time-scale, a n d i n d i v i d u a l s do not evolve. It is lineages that e v o l v e , and lineages that exhibit progressive trends i n r e s p o n s e t o t h e s e l e c t i o n p r e s s u r e s set u p b y t h e p r o g r e s s i v e i m p r o v e m e n t s in other lineages. O n e lineage will tend to e v o l v e a d a p t a t i o n s to m a n i p u l a t e the b e h a v i o u r o f a n o t h e r l i n e a g e , t h e n the s e c o n d l i n e a g e w i l l e v o l v e c o u n t e r - a d a p t a t i o n s . We must o b v i o u s l y be interested in a n y g e n e r a l rules g o v e r n i n g w h e t h e r o n e o r the o t h e r l i n e a g e c a n ' w i n ' , o r h a v e a b u i l t - i n a d v a n t a g e . I t w a s j u s t such a built-in a d v a n t a g e that A l e x a n d e r attributed to parents o v e r their c h i l d r e n . A p a r t f r o m his m a j o r t h e o r e t i c a l a r g u m e n t w h i c h , a s w e h a v e seen, is n o w not f a v o u r e d , he also p l a u s i b l y s u g g e s t e d v a r i o u s p r a c t i c a l a d v a n t a g e s of parents o v e r offspring: '. . . the p a r e n t is b i g g e r a n d stronger t h a n t h e o f f s p r i n g , h e n c e i n a b e t t e r p o s i t i o n t o i m p o s e its w i l l ' ( A l e x a n d e r 1974). T h i s is true, paragraph,

but we must not forget

t h e lesson o f t h e p r e v i o u s

that an arms race is run in e v o l u t i o n a r y

time.

In any one

g e n e r a t i o n the m u s c l e s o f a p a r e n t a r e s t r o n g e r t h a n t h o s e o f its o f f s p r i n g , and w h o e v e r controls those muscles must h a v e the u p p e r h a n d .

But the

A r m s R a c e s and M a n i p u l a t i o n

q u e s t i o n a t issue is, who c o n t r o l s t h e p a r e n t s ' m u s c l e s ? A s T r i v e r s ( 1 9 7 4 ) s a y s , A n o f f s p r i n g c a n n o t f l i n g its m o t h e r t o t h e g r o u n d a t w i l l a n d n u r s e . . . the offspring is e x p e c t e d to e m p l o y p s y c h o l o g i c a l rather than physical tactics.' Krebs

and

suggested

that

animal

signals

could

thought

of as

e m p l o y i n g p s y c h o l o g i c a l t a c t i c s i n r a t h e r the s a m e w a y a s h u m a n a d v e r t i s e m e n t s . A d v e r t i s e m e n t s a r e n o t t h e r e t o i n f o r m , o r t o m i s i n f o r m , t h e y are t h e r e t o persuade. T h e a d v e r t i s e r uses his k n o w l e d g e o f h u m a n p s y c h o l o g y , o f the

hopes,

fears

and

secret

motives

o f his

targets,

and

designs

a d v e r t i s e m e n t w h i c h is effective in m a n i p u l a t i n g their b e h a v i o u r . P a c k a r d ' s (1957) expose of the d e e p p s y c h o l o g i c a l techniques of c o m m e r c i a l advertisers m a k e s f a s c i n a t i n g r e a d i n g for t h e e t h o l o g i s t .

A s u p e r m a r k e t m a n a g e r is

q u o t e d a s s a y i n g ' P e o p l e like t o see a lot o f m e r c h a n d i s e . W h e n t h e r e a r e o n l y t h r e e o f f o u r c a n s o f a n i t e m o n a shelf, t h e y j u s t w o n ' t m o v e . ' T h e o b v i o u s a n a l o g y w i t h lek b i r d s d o e s n o t lose its v a l u e m e r e l y b e c a u s e the p h y s i o l o g i c a l m e c h a n i s m o f t h e effect w i l l p r o b a b l y p r o v e t o b e different i n the

t w o cases.

Hidden cine-cameras

r e c o r d i n g the e y e - b l i n k i n g rate of

h o u s e w i v e s i n a s u p e r m a r k e t i n d i c a t e d t h a t i n s o m e c a s e s t h e effect o f the multiplicity of bright-coloured packages was to induce a mild hypnoidal trance. K. N e l s o n o n c e g a v e a talk at a conference, entitled 'Is bird song music? W e l l , then, is it l a n g u a g e ? W e l l , then, w h a t is it?' Perhaps bird song is more akin to h y p n o t i c persuasion, or to a form of d r u g g i n g . T h e nightingale's song induced in J o h n K e a t s a drowsy numbness ' . . . drunk'.

as though of hemlock I had

M i g h t i t n o t h a v e a n e v e n m o r e p o w e r f u l effect o n t h e n e r v o u s

system of a n o t h e r n i g h t i n g a l e ? If nervous systems are susceptible to drug-like i n f l u e n c e s v i a t h e n o r m a l sense o r g a n s , s h o u l d w e n o t p o s i t i v e l y e x p e c t t h a t n a t u r a l s e l e c t i o n w o u l d h a v e f a v o u r e d t h e e x p l o i t a t i o n o f s u c h possibilities, would

have favoured

the d e v e l o p m e n t of visual,

olfactory,

or auditory

'drugs'? A neurophysiologist, presented w i t h an a n i m a l with a c o m p l e x nervous system

and

asked

manipulate

the

animal's

behaviour,

may

insert

electrodes in sensitive points of the brain a n d stimulate electrically, or m a k e p i n p o i n t l e s i o n s . A n a n i m a l n o r m a l l y d o e s n o t h a v e d i r e c t a c c e s s t o the b r a i n of a n o t h e r a n i m a l , a l t h o u g h I shall m e n t i o n o n e e x a m p l e , the so-called b r a i n w o r m , i n C h a p t e r 1 2 . B u t t h e e y e s a n d ears a r e a l s o e n t r y p o r t s t o the nervous system, a n d there m i g h t be patterns of light or sound w h i c h , if p r o p e r l y d e p l o y e d , c o u l d be as effective as direct electrical stimulation. G r e y W a l t e r ( 1 9 5 3 ) v i v i d l y i l l u s t r a t e s t h e p o w e r o f f l a s h i n g l i g h t s t u n e d t o the f r e q u e n c y o f h u m a n E E G r h y t h m s : i n o n e c a s e a m a n felt ' a n irresistible urge to strangle the person next to h i m ' . I f w e w e r e a s k e d t o i m a g i n e w h a t a n ' a u d i t o r y d r u g ' w o u l d s o u n d l i k e , say for m a k i n g t h e s o u n d t r a c k o f a s c i e n c e fiction f i l m , w h a t w o u l d w e s a y ? T h e i n c e s s a n t r h y t h m o f a n A f r i c a n d r u m ; t h e e e r i e t r i l l i n g o f t h e tree c r i c k e t

A r m s R a c e s and M a n i p u l a t i o n

Oecanthus, o f w h i c h i t h a s b e e n s a i d t h a t i f m o o n l i g h t c o u l d b e h e a r d t h a t i s how it would sound (quoted in Bennet-Clark

1 9 7 1 ) ; or the s o n g of the

n i g h t i n g a l e ? A l l three strike me as w o r t h y c a n d i d a t e s , a n d I b e l i e v e all three h a v e b e e n i n s o m e sense d e s i g n e d for t h e s a m e p u r p o s e : t h e m a n i p u l a t i o n o f one nervous system by another, in a w a y that is not in p r i n c i p l e different from manipulation of a nervous system by a neurophysiologist's electrodes. Of c o u r s e i f a n a n i m a l s o u n d p o w e r f u l l y affects a h u m a n n e r v o u s s y s t e m this i s probably incidental. T h e hypothesis being a d v a n c e d is that selection has shaped animal sounds to m a n i p u l a t e some nervous system, not necessarily a h u m a n o n e . T h e snort o f a p i g - f r o g Rana grylio m a y affect a n o t h e r p i g - f r o g a s the n i g h t i n g a l e a f f e c t e d K e a t s , o r t h e s k y l a r k S h e l l e y . T h e n i g h t i n g a l e h a p p e n e d t o b e a b e t t e r e x a m p l e for m e t o c h o o s e , b e c a u s e h u m a n n e r v o u s systems c a n b e m o v e d t o d e e p e m o t i o n b y n i g h t i n g a l e s o n g , w h e r e a s t h e y a r e u s u a l l y m o v e d t o l a u g h a t p i g - f r o g snorts. C o n s i d e r that other celebrated songster, the c a n a r y , since m u c h h a p p e n s t o b e k n o w n a b o u t t h e p h y s i o l o g y o f its r e p r o d u c t i v e b e h a v i o u r ( H i n d e & Steel

1978).

If a

physiologist

wants

bring

female

canary

into

r e p r o d u c t i v e c o n d i t i o n , i n c r e a s e t h e size o f h e r f u n c t i o n a l o v a r y a n d c a u s e h e r t o start n e s t - b u i l d i n g a n d o t h e r r e p r o d u c t i v e b e h a v i o u r p a t t e r n s , t h e r e are v a r i o u s t h i n g s h e c a n d o .

He c a n inject her w i t h g o n a d o t r o p i n s or

o e s t r o g e n s . H e c a n use e l e c t r i c l i g h t t o i n c r e a s e t h e d a y - l e n g t h

that she

experiences. O r , most interestingly from o u r point of v i e w , he c a n p l a y her a tape recording of m a l e c a n a r y song. It a p p a r e n t l y has to be c a n a r y s o n g ; b u d g e r i g a r s o n g w i l l n o t d o , a l t h o u g h b u d g e r i g a r s o n g h a s a s i m i l a r effect o n female budgerigars. N o w suppose a m a l e c a n a r y w a n t e d to bring a female into reproductive condition, w h a t could he d o ? He does not h a v e a syringe to inject h o r m o n e s . H e cannot switch o n artificial lights i n the female's e n v i r o n m e n t . O f course w h a t he does is sing. T h e particular pattern of sounds that he m a k e s enters the f e m a l e ' s h e a d t h r o u g h h e r e a r s , i s t r a n s l a t e d i n t o n e r v e i m p u l s e s , a n d bores i n s i d i o u s l y i n t o h e r p i t u i t a r y . T h e m a l e d o e s n o t h a v e t o s y n t h e s i z e a n d inject g o n a d o t r o p i n s ; h e m a k e s t h e f e m a l e ' s p i t u i t a r y w o r k t o s y n t h e s i z e t h e m for h i m . H e s t i m u l a t e s h e r p i t u i t a r y b y m e a n s o f n e r v e i m p u l s e s . T h e y a r e n o t ' h i s ' n e r v e i m p u l s e s , i n t h e sense t h a t t h e y a l l o c c u r w i t h i n t h e f e m a l e ' s o w n n e r v e c e l l s . B u t t h e y a r e his i n a n o t h e r s e n s e . I t i s his p a r t i c u l a r sounds w h i c h are subtly fashioned to m a k e the female's nerves w o r k on her pituitary. W h e r e a physiologist might p u m p g o n a d o t r o p i n s into the female's breast muscle, or electric c u r r e n t into her b r a i n , the m a l e c a n a r y p o u r s s o n g i n t o h e r e a r . A n d t h e effect i s t h e s a m e . S c h l e i d t ( 1 9 7 3 ) d i s c u s s e s o t h e r e x a m p l e s o f s u c h ' t o n i c ' effects o f s i g n a l s o n t h e p h y s i o l o g y o f t h e r e c e i v e r . ' B o r e s i n s i d i o u s l y i n t o h e r p i t u i t a r y ' m a y b e t o o m u c h for s o m e r e a d e r s . Certainly it begs important questions. T h e obvious point that will be m a d e is t h a t the f e m a l e m a y b e n e f i t f r o m t h e t r a n s a c t i o n a s m u c h a s t h e m a l e , i n

A r m s Races and Manipulation

which

case

'insidiously'

and

'manipulation'

are

inappropriate

words.

A l t e r n a t i v e l y , if there is a n y insidious m a n i p u l a t i o n it m a y be by the female o n t h e m a l e . M a y b e t h e f e m a l e 'insists' u p o n a n e x h a u s t i n g p e r f o r m a n c e o f s o n g b y h e r m a t e b e f o r e she w i l l c o m e i n t o r e p r o d u c t i v e c o n d i t i o n , t h e r e b y s e l e c t i n g o n l y t h e m o s t r o b u s t m a l e for a m a t e . I t h i n k s o m e t h i n g a l o n g those lines i s q u i t e p r o b a b l y t h e e x p l a n a t i o n o f t h e e x t r a o r d i n a r i l y h i g h r a t e o f c o p u l a t i o n o b s e r v e d in large cats ( E a t o n 1978). S c h a l l e r (1972) followed a s a m p l e m a l e l i o n for 5 5 h o u r s , d u r i n g w h i c h h e c o p u l a t e d 1 5 7 t i m e s , w i t h a n a v e r a g e inter-copulation interval of 21 minutes. O v u l a t i o n in cats is induced b y c o p u l a t i o n . I t s e e m s p l a u s i b l e t h a t t h e p r o d i g i o u s c o p u l a t i o n rates s h o w n by m a l e lions are the end p r o d u c t of a r u n a w a y arms race, in w h i c h females insisted o n p r o g r e s s i v e l y m o r e c o p u l a t i o n s b e f o r e o v u l a t i n g , a n d m a l e s w e r e s e l e c t e d for e v e r - i n c r e a s e d s e x u a l s t a m i n a . L i o n c o p u l a t i o n s t a m i n a m i g h t b e r e g a r d e d a s t h e b e h a v i o u r a l e q u i v a l e n t o f a p e a c o c k ' s t a i l . A v e r s i o n o f this hypothesis is c o m p a t i b l e with that of B e r t r a m

(1978), that females have

d e v a l u e d t h e c u r r e n c y o f c o p u l a t i o n a s a m e a n s o f r e d u c i n g the o c c u r r e n c e o f disruptive m a l e fights. T o c o n t i n u e the q u o t a t i o n from T r i v e r s o n p s y c h o l o g i c a l m a n i p u l a t i o n t a c t i c s t h a t c h i l d r e n m i g h t use a g a i n s t t h e i r p a r e n t s : S i n c e a n o f f s p r i n g w i l l often h a v e b e t t e r k n o w l e d g e o f its r e a l n e e d s t h a n w i l l its p a r e n t s , s e l e c t i o n s h o u l d f a v o u r p a r e n t a l a t t e n t i v e n e s s t o s i g n a l s f r o m its o f f s p r i n g t h a t a p p r i z e t h e p a r e n t o f t h e offspring's c o n d i t i o n . . . B u t o n c e s u c h a s y s t e m h a s e v o l v e d , t h e offspring c a n b e g i n t o e m p l o y i t o u t o f c o n t e x t . T h e o f f s p r i n g c a n c r y not o n l y w h e n i t i s f a m i s h e d b u t a l s o w h e n i t m e r e l y w a n t s m o r e f o o d t h a n the parent

selected

g i v e . .. Selection

will

then of course favor

p a r e n t a l a b i l i t y t o d i s c r i m i n a t e t h e t w o uses o f t h e s i g n a l s , b u t still subtler m i m i c r y a n d d e c e p t i o n by the offspring are a l w a y s possible [Trivers 1974]. W e h a v e a r r i v e d a g a i n a t the m a i n question raised b y arms races. A r e there a n y g e n e r a l i z a t i o n s w e c a n m a k e a b o u t w h i c h side i s l i k e l y t o ' w i n ' a n a r m s race? F i r s t , w h a t d o e s i t mean t o s p e a k o f o n e s i d e o r t h e o t h e r ' w i n n i n g ' ? D o e s the

'loser'

eventually go extinct? At

times

this m a y h a p p e n .

A bizarre

p o s s i b i l i t y i s s u g g e s t e d b y L l o y d a n d D y b a s ( 1 9 6 6 ) for p e r i o d i c a l c i c a d a s (Simon, 1979, gives an entertaining recent a c c o u n t ) . Periodical cicadas are t h r e e s p e c i e s o f t h e g e n u s Magicicada. A l l t h r e e s p e c i e s h a v e t w o v a r i e t i e s , a 17-year and a

1 3 - y e a r v a r i e t y . E a c h i n d i v i d u a l s p e n d s 1 7 (or 13) y e a r s

f e e d i n g a s a n u n d e r g r o u n d n y m p h , b e f o r e e m e r g i n g for a f e w w e e k s o f a d u l t r e p r o d u c t i v e life, after w h i c h i t d i e s . I n a n y p a r t i c u l a r a r e a a l l life c y c l e s a r e s y n c h r o n i z e d , w i t h the result that e a c h area experiences a c i c a d a p l a g u e

A r m s Races and Manipulation

e v e r y 1 7 (or 13) y e a r s . T h e f u n c t i o n a l s i g n i f i c a n c e o f this i s p r e s u m a b l y t h a t would-be predators or parasites are s w a m p e d in p l a g u e years and starved in i n t e r v e n i n g y e a r s . T h e risk t o a n i n d i v i d u a l w h o r e m a i n s s y n c h r o n i z e d i s t h e r e f o r e less t h a n t h e risk t o o n e w h o b r e a k s s y n c h r o n y a n d e m e r g e s , s a y , a y e a r early. But g i v e n the a d m i t t e d a d v a n t a g e o f s y n c h r o n y , w h y d i d n ' t the c i c a d a s settle o n a s h o r t e r life c y c l e t h a n 1 7 (or 13) y e a r s , t h e r e b y r e d u c i n g the u n f o r t u n a t e d e l a y b e f o r e r e p r o d u c t i o n ? L l o y d a n d D y b a s ' s s u g g e s t i o n i s t h a t the l o n g life c y c l e i s t h e e n d r e s u l t o f a n ' e v o l u t i o n a r y r a c e t h r o u g h time'

with

now

extinct

predator

(or

parasitoid).

'This

hypothetical

p a r a s i t o i d p r e s u m a b l y h a d a life c y c l e t h a t w a s a l m o s t s y n c h r o n i z e d w i t h , a n d n e a r l y e q u a l i n l e n g t h t o ( b u t a l w a y s s l i g h t l y less t h a n ) , t h e a n c e s t r a l protoperiodical c i c a d a . As the theory goes, the c i c a d a s finally o u t r a n their parasitoid

pursuer

and

the

poor specialized

beast

went extinct'

(Simon

1979). Ingeniously, L l o y d a n d D y b a s go further a n d suggest that the arms r a c e c u l m i n a t e d i n life c y c l e s l a s t i n g a p r i m e n u m b e r o f y e a r s ( 1 3 o r 1 7 ) b e c a u s e o t h e r w i s e a p r e d a t o r w i t h a s h o r t e r life c y c l e m i g h t s y n c h r o n i z e w i t h the c i c a d a s e v e r y s e c o n d o r e v e r y t h i r d t i m e a r o u n d ! T h e r e i s r e a l l y n o n e e d for t h e ' l o s e r ' l i n e a g e o f a n a r m s r a c e t o g o e x t i n c t , a s s u g g e s t e d for t h e c i c a d a p a r a s i t o i d . I t m a y b e t h a t t h e ' w i n n e r ' i s s u c h a r a r e s p e c i e s t h a t i t c o n s t i t u t e s a r e l a t i v e l y n e g l i g i b l e risk t o i n d i v i d u a l s o f t h e ' l o s e r ' s p e c i e s . T h e w i n n e r o n l y w i n s i n the sense t h a t its a d a p t a t i o n s a g a i n s t the loser a r e n o t e f f e c t i v e l y c o u n t e r e d . T h i s i s g o o d for i n d i v i d u a l s o f t h e w i n n e r l i n e a g e , b u t i t m a y n o t b e v e r y b a d for i n d i v i d u a l s o f t h e l o s e r l i n e a g e w h o , after a l l , a r e r u n n i n g o t h e r r a c e s s i m u l t a n e o u s l y a g a i n s t o t h e r l i n e a g e s , possibly v e r y successfully. This

' r a r e - e n e m y effect'

is an important e x a m p l e of an

asymmetry in

s e l e c t i o n p r e s s u r e s a c t i n g o n t h e t w o sides o f a n a r m s r a c e . A l t h o u g h w e g a v e no formal models, K r e b s and I considered one such a s y m m e t r y q u a l i t a t i v e l y u n d e r the c a t c h p h r a s e h e a d i n g o f t h e ' l i f e / d i n n e r p r i n c i p l e ' , n a m e d after a fable o f A e s o p w h i c h w a s c a l l e d t o o u r attention b y M . S l a t k i n : ' T h e r a b b i t runs faster t h a n t h e f o x , b e c a u s e t h e r a b b i t i s r u n n i n g for his life w h i l e t h e fox i s o n l y r u n n i n g for his d i n n e r . ' T h e g e n e r a l p o i n t h e r e i s t h a t for a n a n i m a l o n o n e side o f the a r m s r a c e t h e p e n a l t y o f f a i l u r e i s m o r e s e v e r e t h a n for a n a n i m a l o n the o t h e r side o f t h e a r m s r a c e . M u t a t i o n s t h a t m a k e f o x e s r u n m o r e s l o w l y t h a n r a b b i t s m i g h t t h e r e f o r e s u r v i v e i n t h e fox g e n e - p o o l l o n g e r than mutations that cause rabbits to run slowly c a n e x p e c t to survive in the r a b b i t g e n e - p o o l . A fox m a y r e p r o d u c e after b e i n g o u t r u n b y a r a b b i t . N o r a b b i t h a s e v e r r e p r o d u c e d after b e i n g o u t r u n b y a f o x . F o x e s m a y t h e r e f o r e b e b e t t e r a b l e t h a n r a b b i t s t o d i v e r t r e s o u r c e s a w a y f r o m a d a p t a t i o n s for r u n n i n g fast a n d i n t o o t h e r a d a p t a t i o n s ; r a b b i t s t h e r e f o r e a p p e a r t o ' w i n ' t h e a r m s r a c e a s far a s r u n n i n g s p e e d i s c o n c e r n e d . T h e p o i n t i s r e a l l y o n e a b o u t asymmetries in strengths of selection pressure. P r o b a b l y t h e s i m p l e s t a s y m m e t r y arises f r o m w h a t I h a v e j u s t c a l l e d t h e

A r m s Races and Manipulation

r a r e - e n e m y effect, w h e r e o n e side i n t h e a r m s r a c e i s r a r e e n o u g h t o e x e r t a r e l a t i v e l y n e g l i g i b l e influence on a n y g i v e n i n d i v i d u a l on the other side. T h i s c a n b e i l l u s t r a t e d b y t h e a n g l e r f i s h e x a m p l e a g a i n , a n d t h e e x a m p l e h a s the additional merit of s h o w i n g that there is no necessary reason w h y prey ('rabbits') should c o m e out ' a h e a d ' of predators ('foxes'). A s s u m e that angler f i s h a r e r a t h e r r a r e , s o h o w e v e r u n p l e a s a n t i t m a y b e for a n i n d i v i d u a l p r e y t o b e c a u g h t b y a n a n g l e r f i s h , t h e risk o f this h a p p e n i n g t o a r a n d o m l y d e s i g n a t e d i n d i v i d u a l i s n o t h i g h . A n y a d a p t a t i o n costs s o m e t h i n g . F o r a small

fish

discriminate

angler

fish

lures

from

real

worms

needs

s o p h i s t i c a t e d v i s u a l p r o c e s s i n g a p p a r a t u s . T o m a k e this a p p a r a t u s m a y cost i t r e s o u r c e s w h i c h c o u l d o t h e r w i s e h a v e b e e n p u t i n t o , s a y g o n a d s (see C h a p t e r 3). T h e n a g a i n , using the a p p a r a t u s takes time, w h i c h could h a v e b e e n spent on c o u r t i n g females or defending a territory, or indeed chasing the p r e y if it is j u d g e d to be a real w o r m . F i n a l l y , a fish that is v e r y c a u t i o u s a b o u t a p p r o a c h i n g w o r m - l i k e o b j e c t s m a y c u t its risk o f b e i n g e a t e n , b u t i t a l s o i n c r e a s e s its risk o f s t a r v i n g . T h i s i s b e c a u s e i t m a y a v o i d m a n y p e r f e c t l y g o o d w o r m s b e c a u s e t h e y might h a v e b e e n a n g l e r f i s h lures. I t may

well

that

the

balance

o f costs

and

benefits

favours

complete

r e c k l e s s n e s s o n t h e p a r t o f s o m e p r e y a n i m a l s . I n d i v i d u a l s t h a t always try t o e a t s m a l l w r i g g l i n g o b j e c t s , a n d d a m n the c o n s e q u e n c e s , m a y , o n a v e r a g e , d o b e t t e r t h a n i n d i v i d u a l s t h a t p a y t h e costs o f a t t e m p t i n g t o d i s c r i m i n a t e r e a l w o r m s f r o m a n g l e r f i s h l u r e s . W i l l i a m J a m e s m a d e m u c h the s a m e p o i n t in 1 9 1 0 : ' T h e r e are m o r e w o r m s unattached to hooks than impaled upon t h e m ; therefore, on the w h o l e , says N a t u r e to her fishy children, bite at every w o r m a n d take y o u r c h a n c e s ' (quoted by S t a d d o n in press). N o w l o o k a t i t f r o m t h e p o i n t o f v i e w o f the a n g l e r fish. It, t o o , n e e d s t o s p e n d r e s o u r c e s o n a p p a r a t u s t o o u t w i t its o p p o n e n t s i n t h e a r m s r a c e . T h e resources that go into m a k i n g a lure c o u l d h a v e been put into gonads. T h e t i m e s p e n t s i t t i n g m o t i o n l e s s w a i t i n g p a t i e n t l y for p r e y c o u l d h a v e b e e n spent

actively searching

for

mate.

But

the

angler fish absolutely

d e p e n d s o n t h e s u c c e s s o f its l u r e for s u r v i v a l . A n a n g l e r f i s h t h a t i s n o t w e l l e q u i p p e d to lure p r e y will starve. A prey fish that is not well e q u i p p e d to a v o i d b e i n g l u r e d m a y r u n o n l y a s m a l l risk o f b e i n g e a t e n , a n d m a y m o r e t h a n c o m p e n s a t e for t h e risk b y s a v i n g t h e c o s t o f m a k i n g a n d u s i n g the equipment. I n this e x a m p l e t h e a n g l e r w i n s t h e a r m s r a c e a g a i n s t its p r e y , s i m p l y b e c a u s e its s i d e o f t h e a r m s r a c e c o n s t i t u t e s a r e l a t i v e l y n e g l i g i b l e t h r e a t t o a n y g i v e n i n d i v i d u a l o f t h e o t h e r s i d e , t h r o u g h b e i n g r a r e . T h i s d o e s not, b y t h e w a y , m e a n t h a t s e l e c t i o n w i l l f a v o u r p r e d a t o r s t h a t t a k e steps t o b e r a r e , or

constitute

small

threat

their

prey!

Within

the

angler fish

p o p u l a t i o n s e l e c t i o n w i l l f a v o u r those i n d i v i d u a l s w h o a r e t h e m o s t efficient killers a n d the most prolific contributors to r e d u c i n g the rarity of their species. B u t t h e a n g l e r fish l i n e a g e m a y ' k e e p a h e a d ' i n t h e a r m s r a c e a g a i n s t t h e i r

A r m s Races and Manipulation

p r e y , s i m p l y a s a n i n c i d e n t a l c o n s e q u e n c e o f b e i n g r a r e for s o m e o t h e r r e a s o n , r a r e i n s p i t e o f a l l t h e i r efforts. I n a d d i t i o n , t h e r e a r e l i k e l y t o b e f r e q u e n c y - d e p e n d e n t effects for v a r i o u s reasons ( S l a t k i n & M a y n a r d S m i t h 1 9 7 9 ) . F o r i n s t a n c e , a s i n d i v i d u a l s o n o n e side i n a n a r m s r a c e , s a y a n g l e r fish, b e c o m e r a r e r , t h e y w i l l c o n s t i t u t e a steadily w e a k e r threat to i n d i v i d u a l s on the other side of the a r m s race. T h e r e f o r e i n d i v i d u a l s o n t h e o t h e r side w i l l b e s e l e c t e d t o shift p r e c i o u s r e s o u r c e s a w a y f r o m a d a p t a t i o n s c o n c e r n e d w i t h this p a r t i c u l a r a r m s r a c e . I n the p r e s e n t e x a m p l e , p r e y fish a r e s e l e c t e d t o shift r e s o u r c e s a w a y f r o m anti-angler adaptations and into other things such as g o n a d s , possibly to the e x t e n t o f t o t a l r e c k l e s s n e s s a s s u g g e s t e d a b o v e . T h i s w i l l m a k e life e a s i e r for individual anglers, w h o will therefore b e c o m e m o r e n u m e r o u s . A n g l e r s will t h e n c o m e t o c o n s t i t u t e a s e v e r e r t h r e a t t o t h e p r e y fish, w h o w i l l t h e n b e s e l e c t e d t o shift r e s o u r c e s b a c k i n t o a n t i - a n g l e r a d a p t a t i o n s . A s u s u a l i n s u c h arguments, we do not h a v e to imagine an oscillation. T h e r e m a y , instead, be a n e v o l u t i o n a r i l y s t a b l e e n d p o i n t t o t h e a r m s r a c e ; s t a b l e , t h a t is, u n t i l a n e n v i r o n m e n t a l c h a n g e shifts t h e r e l e v a n t costs a n d b e n e f i t s . O b v i o u s l y , u n t i l w e k n o w a g r e a t d e a l m o r e a b o u t costs a n d b e n e f i t s i n t h e field, w e c a n n o t p r e d i c t t h e o u t c o m e o f p a r t i c u l a r a r m s r a c e s . F o r p r e s e n t p u r p o s e s this d o e s n o t m a t t e r . A l l w e n e e d i s t o satisfy o u r s e l v e s t h a t i n a n y p a r t i c u l a r a r m s r a c e i n d i v i d u a l s o n o n e side m a y h a v e m o r e t o lose t h a n i n d i v i d u a l s o n t h e o t h e r s i d e . T h e r a b b i t h a s his life t o l o s e , t h e f o x o n l y h a s his d i n n e r . T h e i n c o m p e t e n t a n g l e r f i s h d i e s ; t h e i n c o m p e t e n t a v o i d e r o f a n g l e r f i s h o n l y r u n s a t i n y risk o f d y i n g , a n d m a y , b y s a v i n g c o s t s , e n d u p b e t t e r off t h a n t h e ' c o m p e t e n t ' p r e y f i s h . We only h a v e to accept the general plausibility of such asymmetries in order to a n s w e r the question raised by o u r discussion of m a n i p u l a t i o n . We agreed that if one o r g a n i s m c o u l d get a w a y w i t h m a n i p u l a t i n g the n e r v o u s s y s t e m o f a n o t h e r , a n d e x p l o i t i n g its m u s c l e p o w e r , s e l e c t i o n w o u l d f a v o u r such manipulation. But we w e r e b r o u g h t up short by the reflection that selection w o u l d also f a v o u r resistance t o b e i n g m a n i p u l a t e d . S h o u l d w e , t h e n , r e a l l y e x p e c t t o see e f f e c t i v e m a n i p u l a t i o n i n n a t u r e ? T h e l i f e / d i n n e r p r i n c i p l e , a n d o t h e r s u c h p r i n c i p l e s a s t h e r a r e - e n e m y effect, p r o v i d e u s w i t h an answer.

I f t h e i n d i v i d u a l m a n i p u l a t o r h a s m o r e t o lose b y f a i l i n g t o

manipulate

than

the

individual

victim

has

lose

failing

resist

m a n i p u l a t i o n , w e s h o u l d e x p e c t t o see successful m a n i p u l a t i o n i n n a t u r e . W e s h o u l d e x p e c t t o see a n i m a l s w o r k i n g i n t h e i n t e r e s t s o f o t h e r a n i m a l s ' g e n e s . Brood parasitism provides w h a t m a y be the most striking e x a m p l e . A p a r e n t b i r d s u c h as a r e e d w a r b l e r s w e e p s a c o p i o u s f l o w of f o o d f r o m a l a r g e c a t c h m e n t a r e a i n t o t h e n a r r o w f u n n e l o f its nest. T h e r e i s a l i v i n g t o b e m a d e by a n y c r e a t u r e that evolves the necessary a d a p t a t i o n s to insert itself in the f u n n e l a n d i n t e r c e p t t h e f l o w . T h a t i s w h a t c u c k o o s a n d o t h e r b r o o d parasites

have

done.

But

the

reed

warbler

not

uncomplaining

A r m s Races and Manipulation

c o r n u c o p i a o f free f o o d . I t i s a n a c t i v e , c o m p l e x m a c h i n e , w i t h sense o r g a n s , m u s c l e s a n d a b r a i n . T h e b r o o d p a r a s i t e m u s t n o t o n l y h a v e its b o d y inserted in the host's nest. It must also infiltrate the defences of the host's nervous s y s t e m , a n d its p o r t s o f e n t r y a r e t h e h o s t ' s sense o r g a n s . T h e c u c k o o uses k e y s t i m u l i t o u n l o c k t h e h o s t ' s m a c h i n e r y o f p a r e n t a l c a r e a n d s u b v e r t it. T h e a d v a n t a g e s o f t h e b r o o d - p a r a s i t e w a y o f life a r e s o m a n i f e s t t h a t t o d a y we are taken a b a c k to find H a m i l t o n and O r i a n s needing, in 1965, to defend the

proposition

theories

that

has

'degenerative

Hamilton and

been

favoured

breakdown'

O r i a n s went on

natural selection,

normal

breeding

against

behaviour.

t o p r o v i d e a s a t i s f y i n g d i s c u s s i o n o f the

p r o b a b l e e v o l u t i o n a r y origins o f b r o o d parasitism, the p r e a d a p t a t i o n s w h i c h p r e c e d e d its e v o l u t i o n , a n d t h e a d a p t a t i o n s w h i c h h a v e a c c o m p a n i e d its evolution. O n e o f these a d a p t a t i o n s i s e g g m i m i c r y . T h e perfection o f e g g m i m i c r y , i n a t least s o m e ' g e n t e s ' o f c u c k o o , s h o w s t h a t foster p a r e n t s a r e p o t e n t i a l l y c a p a b l e of keen-eyed discrimination against interlopers. T h i s only underlines t h e m y s t e r y o f w h y c u c k o o hosts s e e m t o b e s o p o o r a t d i s c r i m i n a t i n g a g a i n s t c u c k o o nestlings. H a m i l t o n and O r i a n s (1965) express the p r o b l e m v i v i d l y : ' Y o u n g b r o w n - h e a d e d c o w b i r d s a n d E u r o p e a n C u c k o o s , a s they reach their m a x i m u m d i m e n s i o n , d w a r f t h e i r foster p a r e n t s . C o n s i d e r t h e l u d i c r o u s s i g h t of a t i n y G a r d e n W a r b l e r . . . [ L a t i n n a m e l e a v e s e x a c t s p e c i e s i n t e n d e d u n clear] standing a t o p a c u c k o o to reach the m o u t h of the g a p i n g parasite. W h y d o e s n o t t h e G a r d e n W a r b l e r t a k e t h e a d a p t i v e m e a s u r e o f a b a n d o n i n g the n e s t l i n g p r e m a t u r e l y , e s p e c i a l l y w h e n to t h e h u m a n o b s e r v e r it is so c l e a r l y i d e n t i f i a b l e ? ' W h e n a p a r e n t is a s m a l l f r a c t i o n of the size of the n e s t l i n g it is f e e d i n g , the m o s t r u d i m e n t a r y e y e s i g h t s h o u l d suffice t o s h o w that s o m e t h i n g h a s g o n e s e r i o u s l y w r o n g w i t h t h e n o r m a l p a r e n t a l p r o c e s s . Y e t , a t the s a m e t i m e , the e x i s t e n c e o f e g g m i m i c r y s h o w s t h a t hosts a r e c a p a b l e o f fastidious d i s c r i m i n a t i o n , m a k i n g use o f k e e n e y e s i g h t . H o w a r e w e t o e x p l a i n this p a r a d o x (see a l s o Z a h a v i 1 9 7 9 ) ? O n e fact that helps to r e d u c e the m y s t e r y is that there must be stronger s e l e c t i o n p r e s s u r e o n hosts t o d i s c r i m i n a t e a g a i n s t c u c k o o s a t t h e e g g s t a g e than against c u c k o o s at the nestling stage, simply b e c a u s e eggs o c c u r earlier. T h e b e n e f i t o f d e t e c t i n g a c u c k o o e g g i s t h e p o t e n t i a l g a i n i n g o f a n entire b r e e d i n g c y c l e in the future. T h e benefit of d e t e c t i n g a nearly fledged c u c k o o is the s a v i n g of o n l y a few d a y s , at a time w h e n it m a y be too late to breed again

anyway.

Another

mitigating circumstance

the

c a s e o f Cuculus

canorus ( L a c k 1 9 6 8 ) i s t h a t t h e h o s t ' s o w n y o u n g i s u s u a l l y n o t t h e r e for s i m u l t a n e o u s c o m p a r i s o n , h a v i n g been tipped out by the b a b y c u c k o o . It is w e l l k n o w n t h a t d i s c r i m i n a t i o n i s e a s i e r i f t h e r e i s a m o d e l a c t u a l l y present for c o m p a r i s o n . V a r i o u s a u t h o r s h a v e i n v o k e d the ' s u p e r n o r m a l stimulus', in one form or a n o t h e r . T h u s L a c k r e m a r k s ( p . 88) t h a t ' t h e y o u n g c u c k o o , w i t h its h u g e

A r m s Races and Manipulation

g a p e and loud b e g g i n g call, has e v i d e n t l y e v o l v e d in e x a g g e r a t e d form the stimuli w h i c h elicit the feeding response of p a r e n t passerine birds. So m u c h is this s o t h a t t h e r e a r e m a n y r e c o r d s o f a d u l t p a s s e r i n e b i r d s f e e d i n g a f l e d g e d y o u n g C. canorus r a i s e d by a d i f f e r e n t host s p e c i e s ; this, l i k e l i p s t i c k in t h e courtship of m a n k i n d , d e m o n s t r a t e s successful e x p l o i t a t i o n by m e a n s of a "super-stimulus".' W i c k l e r (1968) makes a similar point, q u o t i n g Heinroth a s h a v i n g r e f e r r e d t o foster p a r e n t s a s b e h a v i n g l i k e ' a d d i c t s ' , a n d t o t h e c u c k o o n e s t l i n g a s a ' v i c e o f its foster p a r e n t s ' . A s i t s t a n d s , this k i n d o f suggestion will strike m a n y critics as unsatisfying, b e c a u s e it i m m e d i a t e l y p r o m p t s a q u e s t i o n a t least a s b i g a s t h e o n e i t a n s w e r s . W h y d o e s n ' t s e l e c t i o n e l i m i n a t e f r o m t h e host s p e c i e s t h e t e n d e n c y t o b e ' a d d i c t e d ' t o 'supernormal stimuli'? T h i s , of course, is w h e r e the arms race c o n c e p t c o m e s in a g a i n . W h e n a h u m a n b e h a v e s i n a w a y t h a t i s m a n i f e s t l y b a d for h i m , for i n s t a n c e w h e n h e c o n t i n u a l l y t a k e s p o i s o n , w e m a y e x p l a i n his b e h a v i o u r i n a t l e a s t t w o w a y s . He m a y not realize that the substance that he is d r i n k i n g is poison, so closely does it resemble a g e n u i n e l y nutritous s u b s t a n c e . T h i s c o r r e s p o n d s to the host b i r d ' s b e i n g f o o l e d b y the c u c k o o ' s e g g m i m i c r y . O r h e m a y b e u n a b l e to save himself because of some direct subverting influence of the poison on his n e r v o u s s y s t e m . S u c h i s t h e c a s e o f t h e h e r o i n a d d i c t w h o k n o w s t h e d r u g is killing him, but w h o c a n n o t stop taking it because the d r u g itself controls his n e r v o u s s y s t e m . W e h a v e a l r e a d y s e e n t h a t t h e c u c k o o n e s t l i n g ' s l i p s t i c k like g a p e i s r e g a r d e d a s a s u p e r n o r m a l s t i m u l u s , a n d t h a t foster p a r e n t s h a v e been described as a p p a r e n t l y ' a d d i c t e d ' to the s u p e r n o r m a l stimulus. C o u l d i t b e t h a t the host c a n n o m o r e resist t h e s u p e r n o r m a l m a n i p u l a t i v e p o w e r o f the c u c k o o n e s t l i n g t h a n t h e j u n k i e c a n resist his f i x , o r t h a n t h e b r a i n w a s h e d p r i s o n e r c a n resist t h e o r d e r s o f his c a p t o r , h o w e v e r m u c h i t w o u l d b e n e f i t him to do so? Perhaps c u c k o o s h a v e put their a d a p t i v e emphasis on m i m e t i c deception at the e g g stage, but on positive m a n i p u l a t i o n of the host's n e r v o u s s y s t e m a t the l a t e n e s t l i n g s t a g e . A n y nervous system c a n b e subverted i f treated i n the right w a y . A n y e v o l u t i o n a r y a d a p t a t i o n o f t h e host n e r v o u s s y s t e m t o resist m a n i p u l a t i o n b y c u c k o o nestlings lays itself o p e n to c o u n t e r - a d a p t a t i o n by the c u c k o o s . S e l e c t i o n a c t i n g o n c u c k o o s w i l l w o r k t o find w h a t e v e r c h i n k s t h e r e m a y b e i n the h o s t s ' n e w l y e v o l v e d p s y c h o l o g i c a l a r m o u r . H o s t b i r d s m a y b e v e r y g o o d a t resisting p s y c h o l o g i c a l m a n i p u l a t i o n , b u t c u c k o o s m i g h t b e c o m e e v e n b e t t e r a t m a n i p u l a t i n g . A l l w e n e e d t o p o s t u l a t e i s t h a t , for s o m e r e a s o n s u c h a s t h a t s u g g e s t e d b y t h e l i f e / d i n n e r p r i n c i p l e o r t h e r a r e - e n e m y effect, c u c k o o s h a v e w o n t h e a r m s r a c e : a c u c k o o i n t h e nest h a s got t o m a n i p u l a t e its host s u c c e s s f u l l y o r i t w i l l s u r e l y d i e ; its i n d i v i d u a l f o s t e r - p a r e n t w i l l benefit s o m e w h a t i f i t resists m a n i p u l a t i o n , b u t i t still h a s a g o o d c h a n c e o f future r e p r o d u c t i v e s u c c e s s i n o t h e r y e a r s e v e n i f i t

fails

t o resist this

p a r t i c u l a r c u c k o o . M o r e o v e r , c u c k o o s m i g h t b e s u f f i c i e n t l y r a r e t h a t t h e risk

7<>

A r m s R a c e s and M a n i p u l a t i o n

o f a n i n d i v i d u a l o f t h e foster s p e c i e s b e i n g p a r a s i t i z e d i s l o w ; c o n v e r s e l y the ' r i s k ' o f a n i n d i v i d u a l c u c k o o ' s b e i n g a p a r a s i t e i s 100 p e r c e n t , n o m a t t e r h o w c o m m o n or rare either party to the arms race m a y be. T h e c u c k o o is d e s c e n d e d f r o m a l i n e o f a n c e s t o r s , e v e r y s i n g l e o n e o f w h o m h a s successfully f o o l e d a host. T h e h o s t i s d e s c e n d e d f r o m a l i n e o f a n c e s t o r s , m a n y o f w h o m m a y n e v e r h a v e e n c o u n t e r e d a c u c k o o in their lives, or m a y h a v e reproduced s u c c e s s f u l l y after b e i n g p a r a s i t i z e d b y a c u c k o o . T h e a r m s r a c e c o n c e p t completes the classical supernormal stimulus explanation, by providing a functional a c c o u n t of the host's m a l a d a p t i v e b e h a v i o u r , instead of l e a v i n g it as an u n e x p l a i n e d limitation of the nervous system. I n o n e respect m y t r e a t m e n t o f c u c k o o s a s m a n i p u l a t o r s m a y b e found u n s a t i s f y i n g . T h e c u c k o o is, after a l l , o n l y d i v e r t i n g t h e n o r m a l p a r e n t a l b e h a v i o u r o f its h o s t .

It has not succeeded

b u i l d i n g i n t o t h e host's

b e h a v i o u r a l repertoire a w h o l e n e w b e h a v i o u r pattern that w a s not there, in s o m e f o r m , b e f o r e . S o m e m i g h t find a n a l o g i e s w i t h d r u g s , h y p n o t i s m a n d e l e c t r i c a l s t i m u l a t i o n o f t h e b r a i n m o r e p e r s u a s i v e i f a n e x a m p l e o f this m o r e extreme

kind

of m a n i p u l a t i o n

could

found.

possible

case

the

' p r e e n i n g i n v i t a t i o n ' display of a n o t h e r b r o o d parasite, the b r o w n - h e a d e d c o w b i r d Molothrus ater ( R o t h s t e i n

1980). A l l o p r e e n i n g , the p r e e n i n g of one

i n d i v i d u a l by another, is not u n c o m m o n within various species of birds. It is not

particularly

surprising,

therefore,

that

cowbirds

should

succeed

g e t t i n g o t h e r b i r d s o f s e v e r a l s p e c i e s t o p r e e n t h e m . A g a i n , this c a n b e seen a s a simple diversion of intraspecific a l l o p r e e n i n g , w i t h the c o w b i r d p r o v i d i n g a s u p e r n o r m a l e x a g g e r a t i o n o f t h e n o r m a l e l i c i t i n g s t i m u l i for a l l o p r e e n i n g . W h a t is rather surprising is that c o w b i r d s m a n a g e to get themselves preened by species that n e v e r e n g a g e in intraspecific allopreening. T h e d r u g a n a l o g y i s e s p e c i a l l y a p t for i n s e c t ' c u c k o o s ' t h a t use c h e m i c a l m e a n s t o c o e r c e t h e i r hosts i n t o a c t s t h a t a r e p r o f o u n d l y d a m a g i n g t o t h e i r o w n i n c l u s i v e f i t n e s s . S e v e r a l species o f ant h a v e n o w o r k e r s o f their o w n . T h e q u e e n s i n v a d e nests o f o t h e r s p e c i e s , d i s p o s e o f t h e host q u e e n , a n d use the host w o r k e r s t o b r i n g u p their o w n r e p r o d u c t i v e y o u n g . T h e m e t h o d o f d i s p o s i n g o f t h e host q u e e n v a r i e s . I n s o m e s p e c i e s , s u c h a s t h e d e s c r i p t i v e l y named

Bothriomyrmex

regicidus

and

decapitans,

the

parasite

queen

rides

a b o u t o n t h e b a c k o f t h e host q u e e n a n d t h e n , i n W i l s o n ' s ( 1 9 7 1 ) d e l i g h t f u l d e s c r i p t i o n , ' b e g i n s t h e o n e a c t for w h i c h s h e i s u n i q u e l y s p e c i a l i z e d : s l o w l y c u t t i n g off t h e h e a d o f h e r v i c t i m ' ( p . 3 6 3 ) . Monomorium santschii a c h i e v e s t h e s a m e result b y m o r e s u b t l e m e a n s . T h e host w o r k e r s h a v e w e a p o n s w i e l d e d b y strong muscles, a n d nerves attached t o t h e m u s c l e s ; w h y s h o u l d t h e p a r a s i t e q u e e n e x e r t h e r o w n j a w s i f she c a n subvert

the

nervous systems controlling

the

n u m e r o u s j a w s o f the

host

w o r k e r s ? I t d o e s n o t s e e m t o b e k n o w n h o w she a c h i e v e s it, b u t she d o e s : the h o s t w o r k e r s kill

their o w n m o t h e r and

a d o p t the usurper.

A chemical

A r m s Races and Manipulation

secreted by the parasite q u e e n seems the likely w e a p o n , in w h i c h case it m i g h t be labelled a p h e r o m o n e , but it is p r o b a b l y m o r e i l l u m i n a t i n g to think of it a s a f o r m i d a b l y p o w e r f u l d r u g . I n l i n e w i t h this i n t e r p r e t a t i o n , W i l s o n ( 1 9 7 1 , p. 413) writes of s y m p h y l i c substances as b e i n g 'more than just e l e m e n t a r y nutritive

substances

even

analogues

of the

natural

host

pheromones.

S e v e r a l a u t h o r s h a v e s p o k e n o f a n a r c o t i z i n g effect o f s y m p h y l i c s u b s t a n c e s . ' W i l s o n also uses t h e w o r d ' i n t o x i c a n t ' a n d q u o t e s a c a s e i n w h i c h w o r k e r a n t s under the influence of such a substance b e c a m e t e m p o r a r i l y disoriented a n d less sure o f t h e i r f o o t i n g . Those w h o have never been brainwashed or addicted to a d r u g find it hard to understand their fellow m e n w h o are d r i v e n by such c o m p u l s i o n s . In the s a m e n a i v e w a y w e c a n n o t u n d e r s t a n d a host b i r d ' s b e i n g c o m p e l l e d t o feed a n a b s u r d l y o v e r s i z e d c u c k o o , o r w o r k e r a n t s w a n t o n l y m u r d e r i n g t h e only b e i n g in the w h o l e w o r l d that is vital to their g e n e t i c success. B u t such subjective

feelings

are

misleading,

even

where

the

relatively

crude

achievements of h u m a n p h a r m a c o l o g y are concerned. W i t h natural selection w o r k i n g o n the p r o b l e m , w h o w o u l d b e s o p r e s u m p t u o u s a s t o g u e s s w h a t feats o f m i n d c o n t r o l m i g h t n o t b e a c h i e v e d ? D o n o t e x p e c t t o see a n i m a l s always b e h a v i n g in such a w a y as to m a x i m i z e their o w n inclusive fitness. Losers in an arms race m a y b e h a v e in some v e r y odd w a y s i n d e e d . If they appear

disoriented

and

unsure

of their

footing,

this

may

only

the

beginning. L e t me stress a g a i n w h a t a feat of m i n d - c o n t r o l t h e Monomorium santschii q u e e n a c h i e v e s . T o a sterile w o r k e r a n t , h e r m o t h e r i s a k i n d o f g e n e t i c g o l d m i n e . F o r a w o r k e r a n t t o kill h e r o w n m o t h e r i s a n a c t o f g e n e t i c m a d n e s s . W h y d o the w o r k e r s d o i t ? I a m s o r r y I c a n d o n o m o r e t h a n , o n c e a g a i n , vaguely

talk

about

arms

races.

Any

nervous

system

vulnerable

manipulation by a c l e v e r - e n o u g h p h a r m a c o l o g i s t . T h e r e is no difficulty in b e l i e v i n g t h a t n a t u r a l s e l e c t i o n a c t i n g o n M . santschii w o u l d s e e k o u t t h e w e a k p o i n t s i n t h e host w o r k e r s ' n e r v o u s s y s t e m , a n d i n s e r t a p h a r m a c o logical key in the lock. S e l e c t i o n on the host species w o u l d soon h a v e plugged

those

improve

the d r u g ,

weak

points,

and

the

whereupon

selection

arms race was

the

under way.

parasite If M.

would

santschii i s

sufficiently r a r e , i t i s e a s y t o see t h a t i t m i g h t ' w i n ' t h e a r m s r a c e , e v e n t h o u g h r e g i c i d e i s s u c h a d i s a s t r o u s a c t for e a c h host c o l o n y w h o s e w o r k e r s s u c c u m b t o it. T h e o v e r a l l risk o f p a r a s i t i z a t i o n b y M . santschii c o u l d b e v e r y l o w e v e n t h o u g h t h e m a r g i n a l cost o f r e g i c i d e , g i v e n t h a t a n M . santschii q u e e n has e n t e r e d , is d i s a s t r o u s l y h i g h . E a c h i n d i v i d u a l M. santschii q u e e n is descended from a line of ancestors e v e r y o n e of w h o m has s u c c e e d e d in m a n i p u l a t i n g host w o r k e r s i n t o r e g i c i d e . E a c h host w o r k e r i s d e s c e n d e d from a line o f a n c e s t o r s w h o s e c o l o n i e s m a y s e l d o m h a v e b e e n w i t h i n 1 0 m i l e s o f a n M . santschii q u e e n . T h e costs o f ' b o t h e r i n g ' t o b e e q u i p p e d t o

A r m s R a c e s and M a n i p u l a t i o n

resist m a n i p u l a t i o n b y a n o c c a s i o n a l M . santschii q u e e n m a y o u t w e i g h the b e n e f i t s . R e f l e c t i o n s s u c h a s this l e a d m e t o b e l i e v e t h a t t h e hosts m i g h t w e l l lose t h e a r m s r a c e . O t h e r s p e c i e s o f p a r a s i t i c a n t s use a d i f f e r e n t s y s t e m . I n s t e a d o f s e n d i n g o u t q u e e n s t o i m p l a n t t h e i r e g g s i n host nests a n d u s i n g host l a b o u r t h e r e , t h e y t r a n s p o r t h o s t l a b o u r b a c k t o t h e i r o w n nests. T h e s e a r e t h e s o - c a l l e d s l a v e m a k i n g ants.

S l a v e m a k i n g species h a v e workers,

b u t these w o r k e r s

d e v o t e part, or in some cases all, of their energy to g o i n g on slaving e x p e d i t i o n s . T h e y r a i d nests o f o t h e r s p e c i e s a n d c a r r y off l a r v a e a n d p u p a e . T h e s e s u b s e q u e n t l y h a t c h i n t h e s l a v e r s ' nest, w h e r e t h e y w o r k n o r m a l l y , f o r a g i n g a n d t e n d i n g b r o o d , n o t ' r e a l i z i n g ' t h a t t h e y a r e , i n effect, s l a v e s . T h e a d v a n t a g e o f t h e s l a v e m a k i n g w a y o f life i s p r e s u m a b l y t h a t m o s t o f the c o s t o f f e e d i n g t h e w o r k f o r c e i n t h e l a r v a l s t a g e i s s a v e d . T h a t cost i s b o r n e b y the h o m e c o l o n y from w h i c h the slave p u p a e w e r e taken. T h e s l a v e m a k i n g h a b i t is interesting from

the

present point

of view,

b e c a u s e i t raises a n u n u s u a l a r m s r a c e a s y m m e t r y . P r e s u m a b l y t h e r e i s a n arms race b e t w e e n s l a v e m a k i n g species and slave species. A d a p t a t i o n s to c o u n t e r s l a v e r y , for i n s t a n c e e n l a r g e d s o l d i e r j a w s for d r i v i n g off s l a v e raiders, should be e x p e c t e d in species that are victims of slave raids. But surely the m o r e o b v i o u s c o u n t e r m e a s u r e the slaves c o u l d take w o u l d simply b e t o w i t h h o l d t h e i r l a b o u r i n t h e s l a v e r s ' nest, o r t o kill s l a v e m a k e r b r o o d i n s t e a d o f f e e d i n g t h e m ? I t seems t h e o b v i o u s c o u n t e r m e a s u r e , b u t t h e r e a r e f o r m i d a b l e o b s t a c l e s t o its e v o l u t i o n .

Consider an adaptation to 'go on

s t r i k e ' , t o refuse t o w o r k i n t h e s l a v e m a k e r s ' nest. T h e s l a v e w o r k e r s w o u l d o f course h a v e to h a v e some m e a n s of r e c o g n i z i n g that they had hatched in a f o r e i g n nest, b u t t h a t s h o u l d n o t b e difficult i n p r i n c i p l e . T h e p r o b l e m arises w h e n we think in detail of h o w the a d a p t a t i o n s w o u l d be passed on. S i n c e w o r k e r s d o n ' t r e p r o d u c e , a l l w o r k e r a d a p t a t i o n s , i n a n y s o c i a l insect species, h a v e to be passed on by r e p r o d u c t i v e relatives of the workers. T h i s n o r m a l l y p r e s e n t s n o i n s u p e r a b l e p r o b l e m s , b e c a u s e w o r k e r s d i r e c t l y assist t h e i r o w n r e p r o d u c t i v e r e l a t i v e s , s o g e n e s g i v i n g rise t o w o r k e r a d a p t a t i o n s d i r e c t l y assist c o p i e s o f t h e m s e l v e s i n r e p r o d u c t i v e s . B u t t a k e t h e e x a m p l e o f a m u t a n t g e n e c a u s i n g slave workers to go on strike. It m a y v e r y effectively s a b o t a g e t h e s l a v e m a k e r s ' nest, p o s s i b l y w i p e i t o u t a l t o g e t h e r . A n d t o w h a t e f f e c t ? T h e a r e a n o w c o n t a i n s o n e less s l a v e m a k i n g nest, p r e s u m a b l y a g o o d t h i n g for all p o t e n t i a l v i c t i m nests i n t h e a r e a , n o t j u s t t h e nest f r o m w h i c h t h e r e b e l s l a v e s c a m e , b u t nests c o n t a i n i n g n o n - s t r i k i n g g e n e s a s w e l l . T h e s a m e k i n d o f p r o b l e m arises i n the g e n e r a l c a s e o f t h e s p r e a d o f ' s p i t e f u l ' behaviour (Hamilton 1970; K n o w l t o n & Parker 1979). T h e o n l y e a s y w a y t h e g e n e s for s t r i k i n g c a n b e p r e f e r e n t i a l l y p a s s e d o n i s for s t r i k i n g t o b e n e f i t , s e l e c t i v e l y , t h e s t r i k e r s ' o w n h o m e nest, t h e nest t h e y left b e h i n d a n d i n w h i c h t h e i r o w n r e p r o d u c t i v e r e l a t i v e s a r e b e i n g r e a r e d . T h i s c o u l d h a p p e n i f s l a v e m a k e r s h a b i t u a l l y returned t o m a k e repeat raids

A r m s Races and Manipulation

the

same

nest,

but

otherwise

must

conclude

that

anti-slavery

a d a p t a t i o n s m u s t b e c o n f i n e d t o t h e p e r i o d before t h e s l a v e p u p a e h a v e left t h e i r h o m e nest. O n c e t h e s l a v e s h a v e a r r i v e d i n t h e s l a v e m a k e r s ' nest t h e y effectively d r o p out of the arms race since they no l o n g e r h a v e a n y p o w e r to influence the success o f their r e p r o d u c t i v e relatives. T h e s l a v e m a k e r s c a n develop manipulative adaptations of any degree of sophistication, physical or chemical,

pheromones or powerful drugs,

and

the slaves c a n n o t e v o l v e

countermeasures. A c t u a l l y , t h e v e r y fact t h a t t h e s l a v e s c a n n o t e v o l v e c o u n t e r m e a s u r e s w i l l tend to r e d u c e the likelihood that the m a n i p u l a t i v e t e c h n i q u e s e v o l v e d by the s l a v e m a k e r s w i l l b e v e r y s o p h i s t i c a t e d : t h e f a c t t h a t t h e s l a v e s c a n n o t r e t a l i a t e , i n a n e v o l u t i o n a r y sense, m e a n s t h a t t h e s l a v e m a k e r s d o n o t n e e d to

spend

costly

resources

elaborate

and

sophisticated

manipulation

adaptations, because simple a n d c h e a p ones will d o . T h e e x a m p l e of slavery in a n t s is r a t h e r a s p e c i a l o n e , b u t it i l l u s t r a t e s a p a r t i c u l a r l y i n t e r e s t i n g sense i n w h i c h o n e s i d e i n a n a r m s r a c e c a n b e s a i d t o lose c o m p l e t e l y . A c a s e c o u l d b e m a d e for d r a w i n g a n a n a l o g y h e r e w i t h t h e h y b r i d f r o g Rana esculenta ( W h i t e 1 9 7 8 ) . T h i s c o m m o n E u r o p e a n f r o g , t h e e d i b l e frog o f French

restaurants,

not

a species

the

normal

sense

of the

word.

Individuals o f the 'species' are really v a r i o u s kinds o f h y b r i d s b e t w e e n t w o o t h e r species, Rana ridibunda a n d R. lessonae. T h e r e a r e t w o different d i p l o i d forms a n d t w o different t r i p l o i d f o r m s of R. esculenta. F o r s i m p l i c i t y I s h a l l c o n s i d e r o n l y o n e o f t h e d i p l o i d f o r m s , b u t t h e a r g u m e n t h o l d s for a l l t h e varieties. consists

These of one

frogs set

coexist of

with

lessonae

lessonae.

chromosomes

Their diploid and

one

set

karyotype of

ridibunda

c h r o m o s o m e s . A t m e i o s i s t h e y d i s c a r d the lessonae c h r o m o s o m e s a n d p r o d u c e pure

ridibunda

gametes.

They

mate

with

lessonae

individuals,

thereby

r e s t o r i n g the h y b r i d g e n o t y p e i n the n e x t g e n e r a t i o n . I n this r a c e o f Rana esculenta b o d i e s , t h e r e f o r e , ridibunda g e n e s a r e g e r m - l i n e r e p l i c a t o r s , lessonae g e n e s d e a d - e n d o n e s . D e a d - e n d r e p l i c a t o r s c a n e x e r t p h e n o t y p i c effects. T h e y c a n even b e n a t u r a l l y selected. B u t the c o n s e q u e n c e s o f that n a t u r a l selection are irrelevant to evolution paragraph

e a s i e r to f o l l o w ,

ridibunda G

(for g e r m - l i n e )

(see C h a p t e r 5 ) . T o m a k e t h e n e x t

s h a l l c a l l R.

a n d R.

lessonae D

esculenta

(for h y b r i d ) , R.

(for d e a d - e n d ,

a l t h o u g h it

should be r e m e m b e r e d that ' D ' genes are d e a d - e n d replicators o n l y w h e n in H f r o g s ; w h e n i n ' D ' frogs t h e y a r e n o r m a l g e r m - l i n e r e p l i c a t o r s ) . N o w , c o n s i d e r a g e n e in t h e D g e n e - p o o l w h i c h e x e r t s an effect on D b o d i e s t o m a k e t h e m refuse t o m a t e w i t h H . S u c h a g e n e s h o u l d b e f a v o u r e d b y n a t u r a l s e l e c t i o n o v e r its H - t o l e r a t i n g a l l e l e , s i n c e t h e l a t t e r w i l l t e n d t o end up in H bodies of the next generation, a n d will be d i s c a r d e d at meiosis. G genes are not discarded at meiosis, a n d they w i l l tend to be selected if they influence H bodies so that they o v e r c o m e the r e l u c t a n c e of D i n d i v i d u a l s to m a t e w i t h t h e m . W e s h o u l d t h e r e f o r e see a n a r m s r a c e b e t w e e n G g e n e s

A r m s Races and Manipulation

a c t i n g o n H b o d i e s , a n d D g e n e s a c t i n g o n D b o d i e s . I n those r e s p e c t i v e b o d i e s , b o t h sets o f g e n e s a r e g e r m - l i n e r e p l i c a t o r s . B u t w h a t a b o u t D g e n e s acting on H bodies? T h e y should h a v e just as powerful an influence over H p h e n o t y p e s as G genes, since they constitute e x a c t l y h a l f of the H g e n o m e . N a i v e l y , we m i g h t e x p e c t them to carry their arms race against G genes over i n t o t h e H b o d i e s w h i c h t h e y s h a r e . B u t in H b o d i e s , those D g e n e s a r e in the s a m e position as ants that h a v e been taken as slaves. A n y adaptation that t h e y m e d i a t e i n t h e H b o d y c a n n o t b e p a s s e d o n t o t h e n e x t g e n e r a t i o n ; for t h e g a m e t e s p r o d u c e d b y t h e H i n d i v i d u a l , r e g a r d l e s s o f h o w his d e v e l o p i n g p h e n o t y p e , a n d i n d e e d his s u r v i v a l , m a y h a v e b e e n i n f l u e n c e d b y D g e n e s , a r e s t r i c t l y G g a m e t e s . J u s t a s w o u l d - b e s l a v e a n t s c a n b e s e l e c t e d t o resist b e i n g t a k e n i n t o c a p t i v i t y w h i l e t h e y a r e still i n t h e i r h o m e nest, b u t c a n n o t b e s e l e c t e d t o s u b v e r t t h e s l a v e m a k i n g nest o n c e t h e y a r e i n it, s o D g e n e s c a n b e s e l e c t e d t o i n f l u e n c e D b o d i e s s o t h a t t h e y resist b e i n g i n c o r p o r a t e d i n H g e n o m e s i n t h e first p l a c e , b u t o n c e s o i n c o r p o r a t e d t h e y a r e n o l o n g e r u n d e r s e l e c t i o n , e v e n t h o u g h t h e y c a n still h a v e p h e n o t y p i c effects. T h e y lose the a r m s r a c e b e c a u s e they are a d e a d - e n d . A similar a r g u m e n t could be m a d e for fish o f t h e h y b r i d ' s p e c i e s ' Poeciliopsis monacha-occidentalis ( M a y n a r d Smith 1978a). T h e inability of slaves to e v o l v e counter-adaptations w a s originally invoked by T r i v e r s a n d H a r e ( 1 9 7 6 ) , in their theory of the sex-ratio arms race in s o c i a l H y m e n o p t e r a . T h i s i s o n e o f t h e best k n o w n o f r e c e n t d i s c u s s i o n s o f a p a r t i c u l a r a r m s r a c e , a n d i t i s w o r t h c o n s i d e r i n g further. E l a b o r a t i n g o n ideas of Fisher (1930a) and H a m i l t o n ( 1 9 7 2 ) , T r i v e r s and H a r e reasoned that the e v o l u t i o n a r i l y stable sex ratio in ant species w i t h one singly mated q u e e n per nest c a n n o t be s i m p l y p r e d i c t e d . If the q u e e n is assumed to h a v e all p o w e r o v e r the sex o f r e p r o d u c t i v e offspring ( y o u n g q u e e n s and males), the stable ratio of e c o n o m i c investment in m a l e and female reproductives is 1 : 1 . If, o n t h e o t h e r h a n d , n o n - l a y i n g w o r k e r s a r e a s s u m e d t o h o l d all p o w e r o v e r i n v e s t m e n t in y o u n g , the stable ratio will be 3 : 1 in favour of females, u l t i m a t e l y b e c a u s e o f t h e h a p l o d i p l o i d g e n e t i c s y s t e m . T h e r e is, t h e r e f o r e , a potential conflict b e t w e e n q u e e n and workers. Trivers and H a r e reviewed t h e , a d m i t t e d l y i m p e r f e c t , a v a i l a b l e d a t a , a n d r e p o r t e d a g o o d a v e r a g e fit t o the 3 : 1 p r e d i c t i o n , from w h i c h they c o n c l u d e d that they h a d found e v i d e n c e for w o r k e r p o w e r w i n n i n g t h e b a t t l e a g a i n s t q u e e n p o w e r . I t w a s a c l e v e r a t t e m p t to u s e r e a l d a t a to test a h y p o t h e s i s of a k i n d t h a t is often c r i t i c i z e d as u n t e s t a b l e , b u t l i k e o t h e r i n n o v a t i v e first a t t e m p t s it is e a s y to find fault with

it.

Alexander and

Sherman

(1977)

complained

about Trivers and

H a r e ' s h a n d l i n g o f t h e d a t a , a n d also s u g g e s t e d a n a l t e r n a t i v e e x p l a n a t i o n for t h e f e m a l e - b i a s e d s e x r a t i o c o m m o n i n a n t s . T h e i r e x p l a n a t i o n ( ' l o c a l m a t e c o m p e t i t i o n ' ) , like that of T r i v e r s and H a r e , was originally derived f r o m H a m i l t o n , i n this c a s e his p a p e r o n e x t r a o r d i n a r y s e x r a t i o s ( 1 9 6 7 ) . T h i s controversy has had

the g o o d

effect o f s t i m u l a t i n g f u r t h e r w o r k .

A r m s R a c e s and M a n i p u l a t i o n

Especially i l l u m i n a t i n g in the c o n t e x t of arms races a n d m a n i p u l a t i o n is the paper by C h a r n o v ( 1 9 7 8 ) , w h i c h is c o n c e r n e d w i t h the origins of eusociality, and

which

introduces

potentially

important

version

of the

life/dinner

p r i n c i p l e . H i s a r g u m e n t w o r k s for d i p l o i d a s w e l l a s h a p l o d i p l o i d o r g a n i s m s , a n d I s h a l l c o n s i d e r t h e d i p l o i d c a s e first. C o n s i d e r a m o t h e r w h o s e e l d e r c h i l d r e n h a v e still n o t left t h e nest w h e n t h e n e x t b r o o d h a t c h e s . W h e n t h e t i m e c o m e s for t h e m t o l e a v e t h e nest a n d b e g i n t h e i r o w n r e p r o d u c t i o n , t h e y o u n g h a v e the option, instead, of s t a y i n g b e h i n d a n d h e l p i n g to rear their y o u n g siblings. As is n o w w e l l k n o w n , all other things b e i n g e q u a l such a fledgling should

be g e n e t i c a l l y indifferent b e t w e e n

rearing offspring and

r e a r i n g full s i b l i n g s ( H a m i l t o n 1 9 6 4 a , b ) . B u t s u p p o s e t h e o l d m o t h e r c o u l d exert any m a n i p u l a t i v e p o w e r o v e r the decision of her elder c h i l d r e n : w o u l d she ' p r e f e r ' t h a t t h e y l e a v e a n d r e a r f a m i l i e s o f t h e i r o w n , o r s t a y a n d r e a r her next b r o o d ? O b v i o u s l y that they should stay and rear her next brood, since g r a n d c h i l d r e n a r e h a l f a s v a l u a b l e t o h e r a s c h i l d r e n . ( T h e a r g u m e n t a s i t s t a n d s i s i n c o m p l e t e . I f she m a n i p u l a t e d all h e r c h i l d r e n for t h e w h o l e o f h e r life i n t o r e a r i n g y e t m o r e n o n - p r o d u c i n g c h i l d l a b o u r e r s , h e r g e r m - l i n e w o u l d p e t e r o u t . W e m u s t a s s u m e t h a t she m a n i p u l a t e s s o m e o f f s p r i n g o f t h e same

genetic

type

developing as

into

developing

workers.)

Selection

into

reproductives

will,

then,

selection

and

favour such

others

into

manipulative

tendencies in parents. Normally, dutifully

pay

when lip

postulate

service

favour

counter-selection

of manipulation we the

victim

resist

m a n i p u l a t i o n . T h e b e a u t y o f C h a r n o v ' s p o i n t i s t h a t i n this c a s e t h e r e w i l l b e no counter-selection. T h e 'arms race' is a w a l k - o v e r b e c a u s e one side, so to speak, doesn't e v e n try. T h e offspring b e i n g m a n i p u l a t e d are, a s w e h a v e a l r e a d y seen, indifferent to w h e t h e r t h e y rear y o u n g siblings or offspring of their o w n ( a g a i n a s s u m i n g all other things e q u a l ) . T h e r e f o r e , a l t h o u g h w e m a y postulate r e v e r s e m a n i p u l a t i o n b y o f f s p r i n g o f p a r e n t s , this i s b o u n d , a t least i n t h e s i m p l e e x a m p l e v i s u a l i z e d b y C h a r n o v , t o b e o u t w e i g h e d b y parental m a n i p u l a t i o n of offspring. T h i s is an a s y m m e t r y to be a d d e d to the list o f p a r e n t a l a d v a n t a g e s offered b y A l e x a n d e r ( 1 9 7 4 ) , b u t I find i t m o r e g e n e r a l l y c o n v i n c i n g t h a n a n y o t h e r s o n t h e list. A t first s i g h t i t m i g h t a p p e a r t h a t C h a r n o v ' s a r g u m e n t d o e s n o t a p p l y t o haplodiploid animals, a n d that w o u l d be a pity since most social insects are h a p l o d i p l o i d . B u t this v i e w i s m i s t a k e n . C h a r n o v h i m s e l f s h o w s this for t h e special assumption that the p o p u l a t i o n has an u n b i a s e d sex ratio, in w h i c h case e v e n in h a p l o d i p l o i d species females are indifferent b e t w e e n r e a r i n g siblings ( r = t h e a v e r a g e o f Âž a n d Âź ) a n d r e a r i n g o f f s p r i n g ( r = Â˝ ) . B u t C r a i g (1980) a n d G r a f e n (in p r e p a r a t i o n ) i n d e p e n d e n t l y s h o w t h a t C h a r n o v d i d n o t e v e n n e e d t o a s s u m e a n u n b i a s e d sex r a t i o . T h e p o t e n t i a l w o r k e r i s still indifferent b e t w e e n r e a r i n g s i b l i n g s a n d r e a r i n g o f f s p r i n g a t a n y c o n c e i v a b l e p o p u l a t i o n sex r a t i o . T h u s s u p p o s e t h e p o p u l a t i o n sex r a t i o i s f e m a l e - b i a s e d ,

A r m s Races and Manipulation

e v e n s u p p o s e i t c o n f o r m s t o T r i v e r s a n d H a r e ' s p r e d i c t e d 3 : 1 . S i n c e the w o r k e r is

closely

t o h e r sister t h a n

her

brother or her

o f f s p r i n g o f e i t h e r s e x , i t m i g h t s e e m t h a t she w o u l d ' p r e f e r ' t o r e a r s i b l i n g s o v e r o f f s p r i n g g i v e n s u c h a f e m a l e - b i a s e d sex r a t i o : i s she n o t g a i n i n g m o s t l y v a l u a b l e sisters ( p l u s o n l y a f e w r e l a t i v e l y w o r t h l e s s b r o t h e r s ) w h e n she o p t s for s i b l i n g s ? B u t this r e a s o n i n g n e g l e c t s t h e r e l a t i v e l y g r e a t r e p r o d u c t i v e v a l u e of m a l e s in such a p o p u l a t i o n as a c o n s e q u e n c e of their rarity. T h e w o r k e r m a y not be closely related to e a c h of her brothers, but if males are r a r e i n t h e p o p u l a t i o n a s a w h o l e e a c h o n e o f those b r o t h e r s i s c o r r e s p o n d i n g l y h i g h l y likely t o b e a n a n c e s t o r o f future g e n e r a t i o n s . T h e m a t h e m a t i c s confirm that C h a r n o v ' s conclusion is even more general than

suggested.

both

diploid

and

haplodiploid

species,

any

p o p u l a t i o n sex r a t i o , a n i n d i v i d u a l f e m a l e i s t h e o r e t i c a l l y i n d i f f e r e n t w h e t h e r she h e r s e l f r e a r s o f f s p r i n g o r y o u n g e r s i b l i n g s . S h e i s n o t , h o w e v e r , indifferent w h e t h e r h e r o f f s p r i n g r e a r t h e i r o w n c h i l d r e n o r t h e i r s i b l i n g s : she prefers t h e m to rear their siblings

( h e r offspring)

o v e r their offspring (her g r a n d -

c h i l d r e n ) . T h e r e f o r e i f t h e r e i s a n y q u e s t i o n o f m a n i p u l a t i o n i n this s i t u a t i o n , p a r e n t a l m a n i p u l a t i o n of offspring is m o r e likely t h a n offspring m a n i p u l a tion o f parents. It

might

radically

appear

contradict

that

Charnov's,

Craig's

those

of Trivers

and

Hare

Grafen's

sex

conclusions

ratios

social

H y m e n o p t e r a . T h e s t a t e m e n t t h a t , a t a n y sex r a t i o , a f e m a l e h y m e n o p t e r a n is

indifferent

between

rearing

siblings

and

rearing

offspring,

sounds

t a n t a m o u n t t o s a y i n g t h a t s h e i s a l s o i n d i f f e r e n t t o w h a t t h e sex r a t i o i n h e r nest is. B u t this i s n o t s o . I t i s still t r u e t h a t , g i v e n t h e a s s u m p t i o n o f w o r k e r control over investment evolutionarily

stable

sex

male

ratio

and

will

female

not

reproductives, necessarily

the

resulting

same

the

e v o l u t i o n a r i l y s t a b l e sex r a t i o g i v e n q u e e n c o n t r o l . I n this sense a w o r k e r i s n o t i n d i f f e r e n t t o t h e s e x r a t i o : she m a y w e l l w o r k t o shift the sex r a t i o a w a y from w h a t the q u e e n is ' t r y i n g ' to a c h i e v e . T r i v e r s a n d H a r e ' s analysis of the e x a c t nature of the conflict b e t w e e n q u e e n a n d w o r k e r s o v e r t h e sex r a t i o c a n b e e x t e n d e d i n w a y s t h a t further illuminate the c o n c e p t of m a n i p u l a t i o n (e.g. O s t e r & W i l s o n

1978). T h e

following account

is d e r i v e d

from

Grafen

(in p r e p a r a t i o n ) .

shall

not

a n t i c i p a t e his c o n c l u s i o n s i n d e t a i l , b u t w i s h t o e m p h a s i z e o n e p r i n c i p l e w h i c h i s e x p l i c i t i n his a n a l y s i s a s w e l l a s i m p l i c i t i n t h a t o f T r i v e r s a n d Hare.

The

question

not

'Has

the

"best"

sex

ratio

been

successfully

a c h i e v e d ? ' On the contrary, we m a k e a w o r k i n g assumption that natural s e l e c t i o n h a s p r o d u c e d a r e s u l t , g i v e n s o m e c o n s t r a i n t s , a n d t h e n ask w h a t t h o s e c o n s t r a i n t s a r e (see C h a p t e r 3 ) . I n t h e p r e s e n t c a s e w e f o l l o w T r i v e r s and

H a r e in r e c o g n i z i n g that

the evolutionarily stable sex ratio d e p e n d s

crucially u p o n w h i c h parties to the arms race h a v e practical power, but we r e c o g n i z e a w i d e r range of possible dispositions of p o w e r than they did. In

A r m s Races and Manipulation

effect,

Trivers

and

Hare

deduced

the

consequences

of two

alternative

a s s u m p t i o n s a b o u t p r a c t i c a l p o w e r ; firstly t h e a s s u m p t i o n t h a t t h e q u e e n e x e r t s all t h e p o w e r , a n d s e c o n d l y t h e a s s u m p t i o n t h a t t h e w o r k e r s e x e r t a l l the p o w e r . B u t m a n y o t h e r p o s s i b l e a s s u m p t i o n s c o u l d b e m a d e , a n d e a c h g i v e s rise t o a different p r e d i c t i o n o f t h e e v o l u t i o n a r i l y s t a b l e s e x r a t i o . I n other parts o f their p a p e r , i n d e e d , T r i v e r s a n d H a r e c o n s i d e r s o m e o f these, for i n s t a n c e t h e a s s u m p t i o n t h a t w o r k e r s a r e a b l e t o l a y t h e i r o w n m a l e e g g s . Grafen,

Bulmer

and

Taylor

(in

preparation),

has

explored

the

c o n s e q u e n c e s o f a s s u m i n g t h a t p o w e r i s divided a s f o l l o w s : t h e q u e e n h a s a b s o l u t e p o w e r o v e r t h e sex o f t h e e g g s t h a t s h e l a y s ; t h e w o r k e r s h a v e absolute p o w e r o v e r feeding the l a r v a e . T h e w o r k e r s c a n thus d e t e r m i n e h o w m a n y o f the a v a i l a b l e female eggs shall d e v e l o p into q u e e n s a n d h o w m a n y into workers. T h e y h a v e the p o w e r to starve the y o u n g of o n e sex or the other, but they h a v e to w o r k w i t h i n the constraint of w h a t the q u e e n g i v e s them in the w a y of eggs. Q u e e n s h a v e the p o w e r to l a y eggs in a n y sex ratio they choose, i n c l u d i n g w i t h h o l d i n g , totally, eggs of o n e sex or the other. B u t , o n c e l a i d , t h o s e e g g s a r e a t t h e m e r c y o f t h e w o r k e r s . A q u e e n m i g h t , for i n s t a n c e , p l a y t h e s t r a t e g y (in t h e g a m e t h e o r y sense) o f l a y i n g o n l y m a l e eggs in a given year. R e l u c t a n t as we m i g h t e x p e c t them to be, the workers h a v e n o o p t i o n b u t t o r e a r t h e i r b r o t h e r s . T h e q u e e n , i n this c a s e , c a n p r e e m p t c e r t a i n w o r k e r s t r a t e g i e s , s u c h a s ' p r e f e r e n t i a l l y feed sisters', s i m p l y b e c a u s e she ' p l a y s ' first. B u t t h e r e a r e o t h e r t h i n g s w o r k e r s c a n d o . Using g a m e theory, Grafen shows that only certain q u e e n strategies are evolutionarily stable replies to p a r t i c u l a r w o r k e r strategies, a n d o n l y certain worker

strategies

are

evolutionarily

stable

replies

particular

queen

s t r a t e g i e s . T h e i n t e r e s t i n g q u e s t i o n is, W h a t a r e t h e e v o l u t i o n a r i l y s t a b l e combinations of w o r k e r and q u e e n strategies? It turns out that there is m o r e than one answer, and there can be as m a n y as three e v o l u t i o n a r i l y stable states for a g i v e n set o f p a r a m e t e r s . G r a f e n ' s p a r t i c u l a r c o n c l u s i o n s a r e n o t my concern here, although I will remark that they are interestingly 'counterintuitive'. W h a t is my c o n c e r n is that the e v o l u t i o n a r i l y stable state of the model

population

depends

upon

the

assumptions we

make

a b o u t power.

Trivers and H a r e contrasted two possible absolute assumptions worker

power

versus

absolute

queen

power).

Grafen

(absolute

investigated

one

p l a u s i b l e division o f p o w e r ( q u e e n s h a v e p o w e r o v e r e g g s , w o r k e r s o v e r l a r v a l feeding). But, as I h a v e already noted, numerous other assumptions a b o u t p o w e r could b e m a d e . E a c h assumption generates different predictions a b o u t e v o l u t i o n a r i l y s t a b l e sex r a t i o s , a n d tests o f t h e p r e d i c t i o n s c a n t h e r e f o r e be regarded as p r o v i d i n g e v i d e n c e a b o u t the disposition of p o w e r in the nest. For instance, we m i g h t focus o u r research attention on the e x a c t m o m e n t w h e n a q u e e n ' d e c i d e s ' w h e t h e r to fertilize a g i v e n e g g or not. It is p l a u s i b l e to assume that, since the e v e n t takes p l a c e w i t h i n the q u e e n ' s o w n b o d y , that

A r m s R a c e s and M a n i p u l a t i o n

p a r t i c u l a r decision is likely to h a v e b e e n selected to benefit the queen's g e n e s . P l a u s i b l e i t m a y b e , b u t i t i s p r e c i s e l y this k i n d o f a s s u m p t i o n t h a t t h e d o c t r i n e of the e x t e n d e d p h e n o t y p e is g o i n g to call in question. F o r the m o m e n t , w e s i m p l y note the possibility that workers m i g h t m a n i p u l a t e the q u e e n ' s n e r v o u s system, by p h e r o m o n a l or other m e a n s , so as to subvert her b e h a v i o u r in

their g e n e t i c interests.

Similarly,

it is w o r k e r nerves and

m u s c l e s t h a t a r e i m m e d i a t e l y r e s p o n s i b l e for f e e d i n g t h e l a r v a e , b u t w e a r e not, therefore, necessarily entitled to assume that w o r k e r limbs m o v e only in the interests of w o r k e r genes. As is w e l l k n o w n , there is massive p h e r o m o n a l traffic f l o w f r o m q u e e n t o w o r k e r s , a n d i t i s e a s y t o i m a g i n e p o w e r f u l manipulation

of worker

behaviour

queens.

The

point

that

each

assumption a b o u t p o w e r w h i c h we m i g h t m a k e yields a testable prediction a b o u t sex r a t i o s , a n d i t i s for this i n s i g h t t h a t w e h a v e t o t h a n k T r i v e r s a n d H a r e , n o t for t h e p a r t i c u l a r m o d e l w h o s e p r e d i c t i o n s t h e y h a p p e n e d t o test. It is e v e n c o n c e i v a b l e , in some H y m e n o p t e r a , that males might exert p o w e r . B r o c k m a n n (1980) is m a k i n g an intensive study of m u d - d a u b i n g wasps Trypoxylon politum. T h e s e a r e ' s o l i t a r y ' (as o p p o s e d to t r u l y s o c i a l ) w a s p s , b u t they are not a l w a y s totally alone. As in other sphecids, e a c h female builds h e r o w n n e s t (in this c a s e o u t o f m u d ) , p r o v i s i o n s i t w i t h p a r a l y s e d p r e y ( s p i d e r s ) , l a y s o n e e g g o n t h e p r e y , t h e n seals u p t h e nest a n d b e g i n s the c y c l e a g a i n . In m a n y H y m e n o p t e r a , the female carries a lifetime's supply of s p e r m f r o m o n e b r i e f p e r i o d o f i n s e m i n a t i o n e a r l y i n life. however,

copulate frequently

t h r o u g h o u t a d u l t life.

T . politum f e m a l e s ,

M a l e s haunt female

nests, l o s i n g n o o p p o r t u n i t y t o c o p u l a t e w i t h t h e f e m a l e o n e a c h o f h e r returns to the nest. A m a l e m a y spend hours at a time sitting passively in the nest, p r o b a b l y h e l p i n g t o g u a r d i t a g a i n s t p a r a s i t e s , a n d f i g h t i n g w i t h o t h e r males w h o a t t e m p t t o enter. U n l i k e most m a l e H y m e n o p t e r a then, the m a l e T . politum i s p r e s e n t a t t h e s c e n e o f t h e a c t i o n . M i g h t h e n o t , t h e r e f o r e , b e potentially in a position to influence the sex ratio, in the same kind of w a y as h a s b e e n p o s t u l a t e d for w o r k e r a n t s ? I f m a l e s did exert p o w e r , w h a t w o u l d w e e x p e c t the c o n s e q u e n c e s t o b e ? S i n c e a m a l e p a s s e s a l l his g e n e s o n t o his d a u g h t e r s , a n d n o n e t o his m a t e ' s sons, g e n e s t e n d i n g t o m a k e m a l e s f a v o u r d a u g h t e r s o v e r sons w o u l d b e f a v o u r e d . If m a l e s exerted total p o w e r , c o m p l e t e l y d e t e r m i n i n g the sex ratio o f their m a t e s ' offspring, the c o n s e q u e n c e w o u l d b e o d d . N o males w o u l d b e b o r n in the first g e n e r a t i o n of m a l e p o w e r . As a result, in the f o l l o w i n g y e a r all eggs laid w o u l d be unfertilized and therefore m a l e . T h e population w o u l d therefore oscillate violently and then go extinct ( H a m i l t o n 1967). If males e x e r t e d a l i m i t e d a m o u n t o f p o w e r , less d r a s t i c c o n s e q u e n c e s w o u l d f o l l o w , the situation b e i n g f o r m a ll y a n a l o g o u s to that of the ' d r i v i n g X c h r o m o s o m e ' in

the n o r m a l d i p l o i d g e n e t i c system

(Chapter 8).

In any case a male

h y m e n o p t e r a n , i f h e f o u n d h i m s e l f i n a p o s i t i o n t o i n f l u e n c e t h e sex r a t i o o f his m a t e ' s c h i l d r e n , w o u l d b e e x p e c t e d t o t r y t o d o s o i n a f e m a l e d i r e c t i o n .

A r m s Races and Manipulation

H e m i g h t d o this b y t r y i n g t o i n f l u e n c e his m a t e ' s d e c i s i o n w h e t h e r t o r e l e a s e s p e r m f r o m h e r s p e r m a t h e c a . I t i s n o t o b v i o u s h o w h e m i g h t a c t u a l l y d o this, but it is k n o w n that h o n e y b e e queens take longer o v e r l a y i n g a female e g g than a m a l e one, p e r h a p s using the e x t r a time to a c h i e v e fertilization. It would

interesting

try

experimentally

interrupting

queen

the

m i d d l e o f e g g - l a y i n g , t o see i f t h e d e l a y i n c r e a s e d t h e c h a n c e o f a f e m a l e e g g emerging. D o m a l e T . politum s h o w a n y b e h a v i o u r t h a t w e m i g h t s u s p e c t o f b e i n g a n a t t e m p t a t s u c h m a n i p u l a t i o n , for e x a m p l e d o t h e y b e h a v e a s i f t r y i n g t o prolong egg-laying? B r o c k m a n n describes a curious b e h a v i o u r pattern called ' h o l d i n g ' . T h i s i s seen a l t e r n a t i n g w i t h c o p u l a t i o n d u r i n g t h e f i n a l m i n u t e s before t h e f e m a l e l a y s h e r e g g . I n a d d i t i o n t o b r i e f c o p u l a t i o n s t h r o u g h o u t the p r o v i s i o n i n g p h a s e o f t h e nest, t h e f i n a l e g g - l a y i n g a n d s e a l i n g u p o f t h e nest i s h e r a l d e d b y a p r o l o n g e d b o u t o f r e p e a t e d c o p u l a t i o n s , w h i c h lasts m a n y m i n u t e s . T h e f e m a l e g o e s h e a d first i n t o t h e v e r t i c a l , o r g a n p i p e shaped

mud

nest,

and

pushes her head up

into

the cluster of p a r a l y s e d

spiders l o d g e d i n the t o p o f t h e nest. H e r a b d o m e n i s f a c i n g t h e e n t r a n c e a t t h e b o t t o m o f t h e nest, a n d i n this p o s i t i o n t h e m a l e c o p u l a t e s w i t h h e r . T h e f e m a l e t h e n t u r n s r o u n d s o t h a t she i s h e a d d o w n w a r d s f a c i n g o u t o f t h e nest, a n d p r o b e s t h e s p i d e r s w i t h t h e tip o f h e r a b d o m e n , a s i f a b o u t t o l a y a n e g g . T h e m a l e m e a n w h i l e ' h o l d s ' h e r h e a d i n his f o r e l e g s for a b o u t h a l f a m i n u t e , grabs her a n t e n n a e a n d pulls her d o w n w a r d s a w a y from the spiders. S h e t h e n turns a r o u n d a n d t h e y c o p u l a t e a g a i n . S h e a g a i n t u r n s t o p r o b e t h e spiders w i t h h e r a b d o m e n , t h e m a l e a g a i n h o l d s h e r h e a d a n d d r a g s h e r d o w n . T h e w h o l e c y c l e r e p e a t s s o m e h a l f d o z e n t i m e s . F i n a l l y , after o n e especially long bout of h e a d - h o l d i n g , the female lays her e g g . O n c e the e g g i s l a i d , its sex i s d e t e r m i n e d . W e h a v e a l r e a d y c o n s i d e r e d t h e hypothetical possibility of w o r k e r ants m a n i p u l a t i n g their m o t h e r ' s nervous system, forcing her to c h a n g e her fertilizing decision in their g e n e t i c interest. Brockmann's

suggestion

that

male

politum

might

attempt

similar

subversion, and that the h e a d - h o l d i n g a n d d r a g g i n g b e h a v i o u r m a y be a manifestation o f their m a n i p u l a t i o n t e c h n i q u e . W h e n the m a l e seizes the female's a n t e n n a e a n d drags her a w a y from the spiders w h i c h she is p r o b i n g with her a b d o m e n , is he forcing a p o s t p o n e m e n t of e g g - l a y i n g as a m e a n s of increasing the c h a n c e of the e g g ' s b e i n g fertilized

the o v i d u c t ? T h e

p l a u s i b i l i t y o f this s u g g e s t i o n m i g h t d e p e n d o n e x a c t l y w h e r e t h e e g g i s i n t h e female's b o d y d u r i n g the time o f h o l d i n g . O r i s he, a s D r W . D . H a m i l t o n has s u g g e s t e d t o us, b l a c k m a i l i n g t h e f e m a l e b y , i n effect, t h r e a t e n i n g t o b i t e h e r h e a d off unless she p o s t p o n e s e g g - l a y i n g u n t i l after f u r t h e r c o p u l a t i o n ? Perhaps he gains by repeated copulations, simply by flooding the female's i n t e r n a l p a s s a g e s w i t h his s p e r m , t h e r e b y r a i s i n g t h e c h a n c e t h a t t h e e g g w i l l encounter

sperm

without

s p e r m a t h e c a by the female.

one

being

deliberately

released

from

the

C l e a r l y these a r e j u s t s u g g e s t i o n s for f u r t h e r

A r m s Races and Manipulation

research, and B r o c k m a n n , together with Grafen and others, is following them u p . P r e l i m i n a r y i n d i c a t i o n s , I u n d e r s t a n d , d o n o t s u p p o r t the h y p o t h e s i s t h a t m a l e s a c t u a l l y s u c c e e d i n e x e r t i n g p o w e r o v e r t h e sex r a t i o . T h i s c h a p t e r is i n t e n d e d to b e g i n the process of u n d e r m i n i n g the reader's c o n f i d e n c e i n t h e c e n t r a l t h e o r e m o f t h e selfish o r g a n i s m . T h a t t h e o r e m states t h a t i n d i v i d u a l a n i m a l s a r e e x p e c t e d t o w o r k for t h e g o o d o f t h e i r o w n i n c l u s i v e f i t n e s s , for t h e g o o d o f c o p i e s o f t h e i r o w n g e n e s . T h e c h a p t e r has s h o w n t h a t a n i m a l s a r e q u i t e l i k e l y t o w o r k h a r d a n d v i g o r o u s l y for t h e g o o d o f s o m e o t h e r i n d i v i d u a l ' s g e n e s , a n d t o the d e t r i m e n t o f t h e i r o w n . T h i s i s not necessarily j u s t a t e m p o r a r y d e p a r t u r e from the central t h e o r e m , a brief i n t e r l u d e o f m a n i p u l a t i v e e x p l o i t a t i o n b e f o r e c o u n t e r s e l e c t i o n o n the v i c t i m lineage

redresses

the balance.

h a v e suggested

that fundamental asym-

m e t r i e s s u c h a s t h e l i f e / d i n n e r p r i n c i p l e , a n d t h e r a r e - e n e m y effect, w i l l see t o i t t h a t m a n y a r m s r a c e s r e a c h a s t a b l e s t a t e i n w h i c h a n i m a l s o n o n e side p e r m a n e n t l y w o r k for t h e b e n e f i t o f a n i m a l s o n t h e o t h e r s i d e , a n d t o t h e i r o w n d e t r i m e n t ; w o r k hard, energetically, w a n t o n l y against their o w n genetic i n t e r e s t s . W h e n w e see t h e m e m b e r s o f a s p e c i e s c o n s i s t e n t l y b e h a v i n g i n a c e r t a i n w a y , ' a n t i n g ' i n b i r d s o r w h a t e v e r i t is, w e a r e a p t t o s c r a t c h o u r h e a d s a n d w o n d e r h o w t h e b e h a v i o u r benefits the a n i m a l s ' i n c l u s i v e f i t n e s s . H o w d o e s i t b e n e f i t a b i r d t o a l l o w a n t s t o r u n a l l t h r o u g h its f e a t h e r s ? I s i t u s i n g t h e a n t s t o c l e a n i t o f p a r a s i t e s , o r w h a t ? T h e c o n c l u s i o n o f this c h a p t e r is

that

might

instead

ask

whose

inclusive

fitness

the

behaviour

benefiting!

Is it the a n i m a l ' s o w n , or that of some m a n i p u l a t o r lurking

behind

scenes?

the

case

of 'anting'

it does

seem

reasonable

s p e c u l a t e a b o u t a d v a n t a g e s t o t h e b i r d , b u t p e r h a p s w e s h o u l d g i v e a t least a s i d e w a y s g l a n c e a t t h e p o s s i b i l i t y t h a t i t i s a n a d a p t a t i o n for t h e g o o d o f the ants!

5 T h e Active Germ-line Replicator

In 1957, B e n z e r argued that 'the g e n e ' could no longer continue as a s i n g l e , u n i t a r y c o n c e p t . H e split i t i n t o t h r e e : t h e m u t o n w a s t h e m i n i m u m unit o f m u t a t i o n a l c h a n g e ; the recon w a s the m i n i m u m unit o f r e c o m b i nation; a n d the cistron w a s defined in a w a y that w a s directly a p p l i c a b l e only

microorganisms,

but

was

effectively

equivalent

the

unit

r e s p o n s i b l e for s y n t h e s i z i n g o n e p o l y p e p t i d e c h a i n . I h a v e s u g g e s t e d a d d i n g a fourth u n i t , t h e optimon, t h e u n i t o f n a t u r a l s e l e c t i o n

(Dawkins

Independently,

coined

'selecton'

Mayr

(personal

to serve the same purpose.

communication) T h e optimon

1978b). the

(or s e l e c t o n )

term is

the

' s o m e t h i n g ' t o w h i c h w e refer w h e n w e s p e a k o f a n a d a p t a t i o n a s b e i n g 'for the g o o d o f ' s o m e t h i n g . T h e q u e s t i o n is, w h a t i s t h a t s o m e t h i n g ; w h a t i s t h e optimon? T h e question of w h a t is the 'unit of selection' has b e e n d e b a t e d from t i m e t o t i m e i n the l i t e r a t u r e b o t h o f b i o l o g y ( W y n n e - E d w a r d s 1 9 6 2 ; W i l l i a m s 1966; Lewontin 1970a; Leigh 1977; D a w k i n s 1978a; A l e x a n d e r & Borgia 1 9 7 8 ; W r i g h t 1980) a n d o f p h i l o s o p h y ( H u l l 1 9 8 0 a , b ; W i m s a t t i n p r e p a r a t i o n ) . A t f i r s t s i g h t i t s e e m s a r a t h e r uselessly t h e o l o g i c a l a r g u m e n t . H u l l , indeed,

explicitly

for t h a t ) .

regards

'metaphysical'

m u s t j u s t i f y m y i n t e r e s t i n it.

(though

none

the

worse

W h y does it matter w h a t we

consider to be the unit of selection? T h e r e are v a r i o u s reasons, b u t I shall give only one. I agree with W i l l i a m s (1966), C u r i o (1973) and others that t h e r e is a n e e d to d e v e l o p a s e r i o u s s c i e n c e of a d a p t a t i o n â&#x20AC;&#x201D; t e l e o n o m y as P i t t e n d r i g h ( 1 9 5 8 ) c a l l e d it. T h e c e n t r a l t h e o r e t i c a l p r o b l e m o f t e l e o n o m y w i l l b e that o f t h e n a t u r e o f t h e e n t i t y for w h o s e b e n e f i t a d a p t a t i o n s m a y b e said t o exist. A r e t h e y for t h e b e n e f i t o f t h e i n d i v i d u a l o r g a n i s m , for t h e benefit o f the g r o u p o r s p e c i e s o f w h i c h i t i s a m e m b e r , o r for t h e b e n e f i t o f some smaller unit inside the i n d i v i d u a l o r g a n i s m ? As a l r e a d y e m p h a s i z e d in C h a p t e r 3 , this r e a l l y m a t t e r s . A d a p t a t i o n s for t h e g o o d o f a g r o u p w i l l l o o k q u i t e different f r o m a d a p t a t i o n s for the g o o d o f a n i n d i v i d u a l . 81

The Active Germ-line Replicator

G o u l d ( 1 9 7 7 b ) sets o u t w h a t , a t f i r s t s i g h t , a p p e a r s t o b e the i s s u e : T h e identification of i n d i v i d u a l s as the unit of selection is a central t h e m e in D a r w i n ' s t h o u g h t . . . I n d i v i d u a l s are the unit of selection; t h e ' s t r u g g l e for e x i s t e n c e ' i s a m a t t e r a m o n g i n d i v i d u a l s . . . I n the last fifteen y e a r s c h a l l e n g e s t o D a r w i n ' s f o c u s o n i n d i v i d u a l s h a v e c o m e from a b o v e and from b e l o w . F r o m a b o v e , Scottish biologist V . C . W y n n e - E d w a r d s raised o r t h o d o x hackles f i f t e e n years a g o b y a r g u i n g t h a t g r o u p s , n o t i n d i v i d u a l s , a r e u n i t s o f s e l e c t i o n , a t least for the

evolution

of social behaviour.

From below,

English

biologist

R i c h a r d D a w k i n s h a s r e c e n t l y r a i s e d m y h a c k l e s w i t h his c l a i m t h a t genes t h e m s e l v e s are units of selection, a n d i n d i v i d u a l s m e r e l y their temporary receptacles.

G o u l d is i n v o k i n g the i d e a of a h i e r a r c h y of levels in the o r g a n i z a t i o n of life. H e sees h i m s e l f a s p e r c h e d o n a n i n t e r m e d i a t e r u n g o f a l a d d e r , w i t h g r o u p selectionists a b o v e a n d g e n e selectionists b e l o w . T h e present chapter a n d t h e n e x t w i l l s h o w t h a t this k i n d o f a n a l y s i s i s false. T h e r e is, o f c o u r s e , a h i e r a r c h y o f l e v e l s o f b i o l o g i c a l o r g a n i z a t i o n (see n e x t c h a p t e r ) , b u t G o u l d i s a p p l y i n g it incorrectly. T h e c o n v e n t i o n a l dispute b e t w e e n g r o u p selection a n d i n d i v i d u a l selection is different in c a t e g o r y from the a p p a r e n t dispute b e t w e e n i n d i v i d u a l s e l e c t i o n a n d g e n e s e l e c t i o n . I t i s w r o n g t o t h i n k o f the three

arranged

a single-dimensional

ladder,

such

that

words

' a b o v e ' a n d ' b e l o w ' h a v e transitive m e a n i n g . I shall s h o w that the well-aired dispute b e t w e e n g r o u p a n d i n d i v i d u a l is c o n c e r n e d w i t h w h a t I shall call 'vehicle selection' and can be regarded as a factual biological dispute about units of n a t u r a l selection. T h e a t t a c k 'from b e l o w ' , on the other hand, is r e a l l y a n a r g u m e n t a b o u t w h a t w e o u g h t t o mean w h e n w e t a l k a b o u t a u n i t of natural selection. T o a n t i c i p a t e t h e c o n c l u s i o n o f these t w o c h a p t e r s , t h e r e a r e t w o w a y s i n w h i c h we c a n c h a r a c t e r i z e natural selection. B o t h are c o r r e c t ; they simply focus on different aspects of the same process. E v o l u t i o n is the external and visible

manifestation

of the

differential

survival

of alternative

replicators

( D a w k i n s 1978a). G e n e s are replicators; organisms and groups of organisms a r e b e s t n o t r e g a r d e d a s r e p l i c a t o r s ; t h e y a r e vehicles i n w h i c h r e p l i c a t o r s travel a b o u t . R e p l i c a t o r selection is the process by w h i c h some replicators s u r v i v e at the e x p e n s e of other replicators. V e h i c l e selection is the process by w h i c h s o m e v e h i c l e s a r e m o r e successful t h a n o t h e r v e h i c l e s i n e n s u r i n g the s u r v i v a l o f their replicators. T h e c o n t r o v e r s y a b o u t g r o u p selection versus i n d i v i d u a l selection is a c o n t r o v e r s y a b o u t the rival claims of t w o suggested k i n d s o f v e h i c l e . T h e c o n t r o v e r s y a b o u t g e n e s e l e c t i o n v e r s u s i n d i v i d u a l (or g r o u p ) s e l e c t i o n i s a c o n t r o v e r s y a b o u t w h e t h e r , w h e n w e t a l k a b o u t a unit o f selection, we o u g h t to m e a n a v e h i c l e at all, or a replicator. M u c h the same

The Active Germ-line Replicator

point has b e e n r e a l i z e d b y the p h i l o s o p h e r D . L . H u l l

(1980a,b),

b u t after

s o m e t h o u g h t I p r e f e r t o persist w i t h m y o w n t e r m i n o l o g y r a t h e r t h a n a d o p t his ' i n t e r a c t o r s ' a n d ' e v o l v o r s ' . I d e f i n e a replicator a s a n y t h i n g i n t h e u n i v e r s e o f w h i c h c o p i e s a r e m a d e . Examples are a D N A molecule,

a n d a sheet of p a p e r that is x e r o x e d .

R e p l i c a t o r s m a y b e classified i n t w o w a y s . T h e y m a y b e ' a c t i v e ' o r ' p a s s i v e ' , a n d , c u t t i n g a c r o s s this c l a s s i f i c a t i o n , t h e y m a y b e ' g e r m - l i n e ' o r ' d e a d - e n d ' replicators. A n active replicator i s a n y r e p l i c a t o r w h o s e n a t u r e h a s s o m e i n f l u e n c e o v e r its p r o b a b i l i t y o f b e i n g c o p i e d . F o r e x a m p l e a D N A m o l e c u l e , v i a p r o t e i n s y n t h e s i s , e x e r t s p h e n o t y p i c effects w h i c h i n f l u e n c e w h e t h e r i t i s c o p i e d : this is w h a t n a t u r a l s e l e c t i o n is a l l a b o u t . A passive replicator is a r e p l i c a t o r w h o s e n a t u r e h a s n o i n f l u e n c e o v e r its p r o b a b i l i t y o f b e i n g c o p i e d . A x e r o x e d s h e e t o f p a p e r a t f i r s t s i g h t s e e m s t o b e a n e x a m p l e , b u t s o m e m i g h t a r g u e t h a t its n a t u r e does i n f l u e n c e w h e t h e r i t i s c o p i e d , a n d t h e r e f o r e t h a t i t i s a c t i v e : h u m a n s are m o r e likely to x e r o x s o m e sheets of p a p e r t h a n others, b e c a u s e of w h a t is written on t h e m , a n d these copies are, in their turn, r e l a t i v e l y likely to be copied again. A section of D N A that is never transcribed m i g h t be a g e n u i n e e x a m p l e o f a p a s s i v e r e p l i c a t o r ( b u t see C h a p t e r 9 o n 'selfish D N A ' ) . A germ-line replicator ( w h i c h m a y be a c t i v e or p a s s i v e ) is a r e p l i c a t o r t h a t is potentially the ancestor of an indefinitely long line of d e s c e n d a n t replicators. A g e n e in a g a m e t e is a g e r m - l i n e r e p l i c a t o r . So is a g e n e in o n e of t h e g e r m line cells of a b o d y , a direct mitotic ancestor of a g a m e t e . So is a n y g e n e in Amoeba proteus. S o i s a n R N A m o l e c u l e i n o n e o f O r g e l ' s ( 1 9 7 9 ) t e s t - t u b e s . A dead-end replicator ( w h i c h a l s o m a y be a c t i v e or p a s s i v e ) is a r e p l i c a t o r w h i c h m a y b e c o p i e d a f i n i t e n u m b e r o f t i m e s , g i v i n g rise t o a s h o r t c h a i n o f descendants,

but

which

definitely

not

the

potential

ancestor

of an

indefinitely long line o f descendants. M o s t o f the D N A m o l e c u l e s i n o u r bodies are d e a d - e n d replicators. T h e y m a y be the ancestors of a few d o z e n generations of mitotic replication, but they will definitely not be long-term ancestors. A D N A m o l e c u l e in the g e r m - l i n e of an i n d i v i d u a l w h o h a p p e n s to die y o u n g , o r w h o o t h e r w i s e fails t o r e p r o d u c e , s h o u l d n o t b e c a l l e d a d e a d - e n d r e p l i c a t o r . S u c h g e r m - l i n e s a r e , a s i t t u r n s o u t , t e r m i n a l . T h e y fail i n w h a t m a y m e t a p h o r i c a l l y be c a l l e d their aspiration to i m m o r t a l i t y . Differential failure o f this k i n d i s w h a t w e m e a n b y n a t u r a l s e l e c t i o n . B u t w h e t h e r i t s u c c e e d s i n p r a c t i c e o r n o t , a n y g e r m - l i n e r e p l i c a t o r i s potentially i m m o r t a l . I t 'aspires' to i m m o r t a l i t y but in practice is in d a n g e r of failing. A l l the D N A m o l e c u l e s i n fully sterile s o c i a l i n s e c t w o r k e r s , h o w e v e r , a r e t r u e d e a d - e n d replicators. T h e y do not even aspire to replicate indefinitely. W o r k e r s lack a g e r m - l i n e , n o t a s a m a t t e r o f m i s f o r t u n e b u t a s a m a t t e r o f d e s i g n . I n this respect they resemble h u m a n liver cells rather than the s p e r m a t o g o n i a of a human who happens to be celibate. T h e r e m a y be a w k w a r d intermediate

The Active Germ-line Replicator

c a s e s , for i n s t a n c e t h e ' s t e r i l e ' w o r k e r w h o b e c o m e s f a c u l t a t i v e l y fertile i f h e r m o t h e r d i e s , a n d t h e Streptocarpus l e a f w h i c h i s not e x p e c t e d t o p r o p a g a t e a n e w p l a n t b u t w h i c h c a n d o s o i f p l a n t e d a s a c u t t i n g . B u t this i s g e t t i n g t h e o l o g i c a l : l e t u s n o t w o r r y precisely h o w m a n y a n g e l s c a n d a n c e o n a p i n ' s head. As I said, the a c t i v e / p a s s i v e distinction cuts across the g e r m - l i n e / d e a d - e n d distinction.

All

four

combinations

are

conceivable.

Particular

interest

a t t a c h e s t o o n e o f t h e four, t h e a c t i v e g e r m - l i n e r e p l i c a t o r , for i t is, I s u g g e s t , t h e ' o p t i m o n ' , t h e u n i t for w h o s e b e n e f i t a d a p t a t i o n s e x i s t . T h e r e a s o n a c t i v e g e r m - l i n e r e p l i c a t o r s a r e i m p o r t a n t u n i t s i s t h a t , w h e r e v e r i n the u n i v e r s e t h e y m a y b e f o u n d , t h e y a r e l i k e l y t o b e c o m e t h e basis for n a t u r a l s e l e c t i o n a n d h e n c e e v o l u t i o n . I f r e p l i c a t o r s exist t h a t a r e a c t i v e , v a r i a n t s o f t h e m with

certain

phenotypic

effects

tend

out-replicate

those

with

other

p h e n o t y p i c effects. I f t h e y a r e a l s o g e r m - l i n e r e p l i c a t o r s , these c h a n g e s i n relative frequency can

have long-term, evolutionary impact. T h e world

tends a u t o m a t i c a l l y to b e c o m e populated by germ-line replicators whose a c t i v e p h e n o t y p i c effects a r e s u c h a s t o e n s u r e t h e i r successful r e p l i c a t i o n . I t i s t h e s e p h e n o t y p i c effects t h a t w e see a s a d a p t a t i o n s t o s u r v i v a l . W h e n w e ask whose s u r v i v a l t h e y a r e a d a p t e d t o e n s u r e , t h e f u n d a m e n t a l a n s w e r h a s t o be not the g r o u p , nor the i n d i v i d u a l o r g a n i s m , but the relevant replicators themselves. I h a v e p r e v i o u s l y s u m m e d u p t h e q u a l i t i e s o f a successful r e p l i c a t o r ' i n a slogan

reminiscent

the

French

Revolution:

Longevity,

Fecundity,

F i d e l i t y ' ( D a w k i n s 1 9 7 8 a ) . H u l l (1980b) explains the point clearly. R e p l i c a t o r s n e e d n o t last f o r e v e r . T h e y n e e d o n l y last l o n g e n o u g h t o p r o d u c e a d d i t i o n a l replicators [fecundity] that retain their structure largely intact [fidelity]. T h e relevant l o n g e v i t y concerns the retention of structure

through

descent.

Some

entities,

though

structurally

similar, are not copies b e c a u s e they are not related by descent. For e x a m p l e , a l t h o u g h a t o m s of gold are structurally similar, they are not c o p i e s o f o n e a n o t h e r b e c a u s e a t o m s o f g o l d d o n o t g i v e rise t o o t h e r a t o m s of g o l d . C o n v e r s e l y , a large m o l e c u l e c a n break d o w n into successively secondary

smaller

bonds

molecules

are severed.

its

quaternary,

A l t h o u g h descent

tertiary, present,

and these

successively smaller molecules cannot count as copies because they l a c k the requisite structural similarity. A r e p l i c a t o r m a y b e s a i d t o ' b e n e f i t ' f r o m a n y t h i n g t h a t i n c r e a s e s the n u m b e r o f its d e s c e n d a n t

('germ-line')

copies.

T o the e x t e n t t h a t a c t i v e

g e r m - l i n e r e p l i c a t o r s b e n e f i t f r o m t h e s u r v i v a l o f t h e b o d i e s i n w h i c h t h e y sit, w e m a y e x p e c t t o see a d a p t a t i o n s t h a t c a n b e i n t e r p r e t e d a s for b o d i l y s u r v i v a l . A l a r g e n u m b e r o f a d a p t a t i o n s a r e o f this t y p e . T o t h e e x t e n t t h a t

The Active Germ-line Replicator

a c t i v e g e r m - l i n e r e p l i c a t o r s b e n e f i t f r o m t h e s u r v i v a l o f b o d i e s other t h a n those i n w h i c h t h e y sit, w e m a y e x p e c t t o see ' a l t r u i s m ' , p a r e n t a l c a r e , e t c . T o the extent that a c t i v e g e r m - l i n e replicators benefit from the s u r v i v a l o f the g r o u p o f i n d i v i d u a l s i n w h i c h t h e y sit, o v e r a n d a b o v e t h e t w o effects j u s t m e n t i o n e d , w e m a y e x p e c t t o see a d a p t a t i o n s for t h e p r e s e r v a t i o n o f t h e group.

But

all

these

adaptations

will

exist,

fundamentally,

through

differential r e p l i c a t o r s u r v i v a l . T h e b a s i c b e n e f i c i a r y o f a n y a d a p t a t i o n i s t h e active g e r m - l i n e replicator, the o p t i m o n . It is i m p o r t a n t not to forget the ' g e r m - l i n e ' proviso in the specification of the o p t i m o n . T h i s i s t h e p o i n t o f H u l l ' s g o l d a t o m a n a l o g y . K r e b s ( 1 9 7 7 ) a n d I ( D a w k i n s 1 9 7 9 a ) h a v e p r e v i o u s l y c r i t i c i z e d B a r a s h ( 1 9 7 7 ) for s u g g e s t i n g t h a t sterile w o r k e r i n s e c t s c a r e for other workers b e c a u s e t h e y s h a r e g e n e s w i t h t h e m . I w o u l d n o t h a r p o n this a g a i n , h a d t h e e r r o r n o t b e e n r e p e a t e d t w i c e recently in print (Barash 1 9 7 8 ; K i r k 1980). It w o u l d be m o r e correct to say t h a t w o r k e r s c a r e for t h e i r reproductive s i b l i n g s w h o c a r r y g e r m - l i n e c o p i e s o f the c a r i n g g e n e s . I f t h e y c a r e for o t h e r w o r k e r s , i t i s b e c a u s e t h o s e o t h e r w o r k e r s a r e l i k e l y t o w o r k o n b e h a l f o f t h e s a m e r e p r o d u c t i v e s (to w h o m t h e y also a r e k i n ) , not b e c a u s e t h e w o r k e r s a r e k i n t o e a c h o t h e r . W o r k e r g e n e s m a y be active, but they are dead-end, not germ-line replicators. No c o p y i n g process

is infallible.

It is no part of the definition of a

r e p l i c a t o r t h a t its c o p i e s m u s t a l l b e p e r f e c t . I t i s f u n d a m e n t a l t o t h e i d e a o f a replicator that w h e n a mistake or ' m u t a t i o n ' does o c c u r it is passed on to future c o p i e s : t h e m u t a t i o n b r i n g s i n t o e x i s t e n c e a n e w k i n d o f r e p l i c a t o r w h i c h 'breeds true' until there is a further m u t a t i o n . W h e n a sheet of p a p e r is x e r o x e d , a blemish m a y a p p e a r on the c o p y w h i c h w a s not present on the o r i g i n a l . I f the x e r o x c o p y itself i s n o w c o p i e d , the b l e m i s h i s i n c o r p o r a t e d i n t o t h e s e c o n d c o p y ( w h i c h m a y a l s o i n t r o d u c e a n e w b l e m i s h o f its o w n ) . The

important

principle

that

chain

of replicators

errors

are

cumulative. I h a v e p r e v i o u s l y u s e d t h e w o r d ' g e n e ' i n t h e s a m e sense a s I w o u l d n o w use ' g e n e t i c r e p l i c a t o r ' , t o refer t o a g e n e t i c f r a g m e n t w h i c h , for a l l t h a t i t serves a s a u n i t o f s e l e c t i o n , d o e s n o t h a v e r i g i d l y f i x e d b o u n d a r i e s . T h i s h a s not m e t w i t h uniform a p p r o v a l . T h e e m i n e n t m o l e c u l a r biologist G u n t h e r Stent ( 1 9 7 7 ) w r o t e that ' O n e o f the great t r i u m p h s o f 20th c e n t u r y b i o l o g y was the e v e n t u a l u n a m b i g u o u s identification o f the M e n d e l i a n h e r e d i t a r y factor, o r g e n e . . . a s that unit o f genetic m a t e r i a l . . . i n w h i c h the a m i n o a c i d sequence

of a

particular

protein

encoded.'

Stent

therefore

violently

objected to my a d o p t i n g the e q u i v a l e n t of W i l l i a m s ' s (1966) definition of a gene as 'that w h i c h segregates and recombines with a p p r e c i a b l e frequency', d e s c r i b i n g it as a ' h e i n o u s t e r m i n o l o g i c a l s i n ' . Such motherly protectiveness towards a rather recently usurped technical t e r m i s n o t u n i v e r s a l a m o n g m o l e c u l a r b i o l o g i s t s , for o n e o f t h e g r e a t e s t o f them has r e c e n t l y w r i t t e n that 'the t h e o r y o f the "selfish g e n e " w i l l h a v e t o

T h e Active Germ-line Replicator

b e e x t e n d e d t o a n y stretch o f D N A ' ( C r i c k 1 9 7 9 ) . A n d , a s w e saw a t the beginning

o f this

chapter,

another

molecular

biologist

of the

first

rank,

S e y m o u r B e n z e r ( 1 9 5 7 ) , r e c o g n i z e d the shortcomings of the traditional gene concept,

but

rather

than

grab

the

traditional

word

gene

itself for

one

p a r t i c u l a r m o l e c u l a r usage, he chose the m o r e modest course of coining a useful set o f n e w t e r m s â&#x20AC;&#x201D; m u t o n , r e c o n a n d c i s t r o n , t o w h i c h w e m a y a d d the optimon.

Benzer recognized

t h a t a l l t h r e e o f his u n i t s h a d

regarded

the

equivalent

gene

the

earlier

claims to be

literature.

Stent's

u n c o m p r o m i s i n g elevation of the cistron to the h o n o u r is arbitrary, though a d m i t t e d l y it is q u i t e c o m m o n . A m o r e b a l a n c e d v i e w w a s g i v e n by the lamented

Keeton

(1980):

'It

may

seem

strange

that

geneticists

c o n t i n u e t o e m p l o y d i f f e r e n t d e f i n i t i o n s o f t h e g e n e for different p u r p o s e s . T h e fact is that, at the present stage of k n o w l e d g e , o n e definition is more useful i n o n e c o n t e x t a n d a n o t h e r i n a n o t h e r c o n t e x t ; a r i g i d t e r m i n o l o g y w o u l d only h a m p e r the formulation of current ideas and

research

Lewontin

'it i s o n l y t h e

(1970b),

too,

gets

right

when

he says

that

aims.'

chromosomes that obey M e n d e l ' s L a w of Independent Assortment, and only t h e n u c l e o t i d e b a s e t h a t i s i n d i v i s i b l e . T h e c o d o n s a n d t h e g e n e s [ c i s t r o n s ] lie in

between,

being

neither unitary nor independent

their

behavior at

meiosis.' B u t let u s n o t b e c o m e w o r k e d u p o v e r t e r m i n o l o g y . M e a n i n g s o f w o r d s a r e i m p o r t a n t , b u t not i m p o r t a n t e n o u g h to justify the ill-feeling they sometimes p r o v o k e , as in the present case of Stent (and also as in Stent's passionate and apparently

sincere

denunciation

of my

following

the

standard

modern

f a s h i o n o f r e d e f i n i n g 'selfishness' a n d ' a l t r u i s m ' i n n o n - s u b j e c t i v e s e n s e s â&#x20AC;&#x201D; s e e Dawkins,

1 9 8 1 , for a r e p l y t o a s i m i l a r c r i t i c i s m ) . I a m h a p p y t o r e p l a c e

'gene' with 'genetic replicator' where there is any doubt. H e i n o u s t e r m i n o l o g i c a l sins a s i d e , S t e n t m a k e s t h e m o r e i m p o r t a n t p o i n t t h a t m y u n i t i s n o t p r e c i s e l y d e l i m i t e d i n t h e w a y t h a t t h e c i s t r o n is. W e l l , p e r h a p s I s h o u l d s a y ' i n t h e w a y t h a t t h e c i s t r o n o n c e s e e m e d t o b e ' , for the recent

discovery

of 'embedded'

cistrons

virus

ÎŚXi74,

and

of 'exons'

s u r r o u n d i n g ' i n t r o n s ' m u s t b e c a u s i n g a little d i s c o m f o r t t o a n y o n e w h o likes his u n i t s r i g i d . C r i c k ( 1 9 7 9 ) e x p r e s s e s t h e sense o f n o v e l t y w e l l : ' I n t h e last 2 years there has b e e n a mini-revolution in m o l e c u l a r genetics. W h e n I c a m e to California, in S e p t e m b e r 1976, I h a d no idea that a typical gene might be s p l i t i n t o s e v e r a l p i e c e s a n d I d o u b t i f a n y o n e else h a d . ' C r i c k s i g n i f i c a n t l y adds

footnote

the

word

gene:

'Throughout

this

article

have

d e l i b e r a t e l y u s e d t h e w o r d " g e n e " i n a l o o s e sense s i n c e a t this t i m e a n y precise definition called

gene

would

(Dawkins

be premature.' 1976a)

My unit of selection,

replicator

(1978a)

never

whether had

any

p r e t e n s i o n s t o u n i t a r i n e s s a n y w a y . F o r t h e p u r p o s e s for w h i c h i t w a s d e f i n e d , u n i t a r i n e s s i s n o t a n i m p o r t a n t c o n s i d e r a t i o n , a l t h o u g h I r e a d i l y see t h a t i t m i g h t b e i m p o r t a n t for o t h e r p u r p o s e s .

The Active Germ-line Replicator

T h e w o r d replicator is purposely defined in a g e n e r a l w a y , so that it does n o t e v e n h a v e t o refer t o D N A . I a m , i n d e e d , q u i t e s y m p a t h e t i c t o w a r d s t h e idea that h u m a n c u l t u r e p r o v i d e s a n e w m i l i e u in w h i c h an entirely different kind of replicator selection c a n go on. In the next c h a p t e r we shall look briefly a t this m a t t e r , a n d a l s o a t t h e c l a i m s o f s p e c i e s g e n e - p o o l s t o b e regarded

replicators

'macroevolutionary'

trends.

large-scale

But in

selection

t h e rest o f this

process

governing

chapter we

shall

concerned only with genetic fragments, and 'replicator' will be used as an a b b r e v i a t i o n for ' g e n e t i c r e p l i c a t o r ' . In principle, we m a y consider any portion of c h r o m o s o m e as a potential c a n d i d a t e for the title o f r e p l i c a t o r . N a t u r a l s e l e c t i o n m a y u s u a l l y b e s a f e l y r e g a r d e d a s the d i f f e r e n t i a l s u r v i v a l o f r e p l i c a t o r s r e l a t i v e t o t h e i r a l l e l e s . T h e w o r d allele is n o w a d a y s c u s t o m a r i l y used of cistrons b u t it is c l e a r l y e a s y , a n d i n t h e spirit o f this c h a p t e r , t o g e n e r a l i z e i t t o a n y p o r t i o n o f c h r o m o s o m e . I f w e l o o k a t a p o r t i o n o f c h r o m o s o m e f i v e c i s t r o n s l o n g , its a l l e l e s a r e t h e a l t e r n a t i v e sets o f f i v e c i s t r o n s t h a t e x i s t a t t h e h o m o l o g o u s l o c i o f a l l the c h r o m o s o m e s i n t h e p o p u l a t i o n . A n a l l e l e o f a n a r b i t r a r y s e q u e n c e of twenty-six codons is an alternative homologous sequence of twenty-six codons s o m e w h e r e i n the p o p u l a t i o n . A n y stretch o f D N A , b e g i n n i n g a n d e n d i n g at arbitrarily chosen points on the c h r o m o s o m e , c a n be considered to b e c o m p e t i n g w i t h a l l e l o m o r p h i c s t r e t c h e s for t h e r e g i o n o f c h r o m o s o m e c o n c e r n e d . It further follows that we c a n g e n e r a l i z e the terms h o m o z y g o u s and heterozygous. H a v i n g picked out an arbitrary length of c h r o m o s o m e as our c a n d i d a t e replicator, we look at the h o m o l o g o u s c h r o m o s o m e in the same diploid individual. whole

length

of the

If the t w o c h r o m o s o m e s are i d e n t i c a l o v e r the

replicator,

the

individual

homozygous

for

that

r e p l i c a t o r , o t h e r w i s e it is h e t e r o z y g o u s . W h e n I said 'arbitrarily c h o s e n portion of c h r o m o s o m e ' , I r e a l l y m e a n t arbitrarily. T h e twenty-six c o d o n s that I chose m i g h t w e l l span the b o r d e r b e t w e e n t w o c i s t r o n s . T h e s e q u e n c e still p o t e n t i a l l y f i t s t h e d e f i n i t i o n o f a r e p l i c a t o r , i t i s still p o s s i b l e t o t h i n k o f i t a s h a v i n g a l l e l e s , a n d i t still m a y b e thought of as h o m o z y g o u s or h e t e r o z y g o u s to the c o r r e s p o n d i n g portion of the h o m o l o g o u s c h r o m o s o m e i n a d i p l o i d candidate

replicator.

But

candidate

genotype.

should

This,

regarded

then, as

is our actual

r e p l i c a t o r o n l y i f i t possesses s o m e m i n i m u m d e g r e e o f l o n g e v i t y / f e c u n d i t y / fidelity ( t h e r e m a y b e trade-offs a m o n g t h e t h r e e ) . O t h e r t h i n g s b e i n g e q u a l , it is clear that larger candidates will h a v e l o w e r l o n g e v i t y / f e c u n d i t y / f i d e l i t y than smaller ones because they are m o r e v u l n e r a b l e to b e i n g b r o k e n by r e c o m b i n a t i o n e v e n t s . S o , how l a r g e a n d h o w s m a l l a p o r t i o n o f c h r o m o s o m e is it useful to t r e a t as a r e p l i c a t o r ? T h i s d e p e n d s o n t h e a n s w e r t o a n o t h e r q u e s t i o n : ' u s e f u l for w h a t ? ' T h e r e a s o n a r e p l i c a t o r is i n t e r e s t i n g to D a r w i n i a n s is t h a t it is p o t e n t i a l l y i m m o r t a l , o r a t least v e r y l o n g - l i v e d i n t h e f o r m o f c o p i e s . A s u c c e s s f u l

The Active Germ-line Replicator

r e p l i c a t o r i s o n e t h a t s u c c e e d s i n l a s t i n g , i n t h e f o r m o f c o p i e s , for a v e r y l o n g time measured in generations, and succeeds in p r o p a g a t i n g m a n y copies of itself. A n u n s u c c e s s f u l r e p l i c a t o r i s o n e t h a t p o t e n t i a l l y m i g h t h a v e b e e n l o n g - l i v e d , b u t in fact failed to survive, say because it caused the successive b o d i e s i n w h i c h i t f o u n d i t s e l f t o b e s e x u a l l y u n a t t r a c t i v e . W e m a y a p p l y the terms 'successful'

and

'unsuccessful'

to a n y arbitrarily defined portion of

c h r o m o s o m e . Its s u c c e s s i s m e a s u r e d r e l a t i v e t o its a l l e l e s , a n d , i f t h e r e i s h e t e r o z y g o s i t y at the r e p l i c a t o r locus in the p o p u l a t i o n , natural selection will change

the

relative

frequencies

of the

allelomorphic

replicators

the

population. B u t if the arbitrarily chosen portion of c h r o m o s o m e is very long it is n o t e v e n potentially l o n g - l i v e d in its p r e s e n t f o r m , for it is l i k e l y to be split a p a r t b y c r o s s i n g - o v e r i n a n y g i v e n g e n e r a t i o n , r e g a r d l e s s o f h o w successful i t m a y b e i n m a k i n g a b o d y s u r v i v e a n d r e p r o d u c e . T o g o t o a n e x t r e m e , i f the potential

replicator we

consider

a whole

chromosome,

the difference

b e t w e e n a 'successful' a n d an unsuccessful c h r o m o s o m e is of no significance, s i n c e b o t h a r e a l m o s t b o u n d t o b e split b y c r o s s i n g - o v e r b e f o r e t h e n e x t generation in a n y c a s e : their 'fidelity' is zero. This

can

put

another

way.

arbitrarily

defined

length

c h r o m o s o m e , o r p o t e n t i a l r e p l i c a t o r , m a y b e said t o h a v e a n e x p e c t e d halflife, m e a s u r e d i n g e n e r a t i o n s . T w o k i n d s o f f a c t o r w i l l affect this half-life. F i r s t l y , r e p l i c a t o r s w h o s e p h e n o t y p i c effects r e n d e r t h e m successful a t t h e i r business

of p r o p a g a t i n g

themselves

will

tend

have

long

half-life.

R e p l i c a t o r s w i t h l o n g e r half-lives than their alleles will c o m e to p r e d o m i n a t e i n t h e p o p u l a t i o n , a n d this i s t h e f a m i l i a r p r o c e s s o f n a t u r a l s e l e c t i o n . B u t i f w e set s e l e c t i o n p r e s s u r e s o n o n e s i d e , w e c a n s a y s o m e t h i n g a b o u t the halflife

of a

replicator

the

basis

o f its

length

alone.

If the

stretch

c h r o m o s o m e we c h o o s e to define as o u r r e p l i c a t o r of interest is long, it will t e n d to h a v e a s h o r t e r h a l f - l i f e t h a n a s h o r t e r r e p l i c a t o r , s i m p l y b e c a u s e it is more

likely

broken

crossing-over.

very

long

portion

c h r o m o s o m e c e a s e s t o d e s e r v e t h e title o f r e p l i c a t o r a t a l l . A c o r o l l a r y i s t h a t a l o n g p o r t i o n o f c h r o m o s o m e , e v e n i f successful i n t e r m s o f its p h e n o t y p i c effects, w i l l n o t b e r e p r e s e n t e d i n m a n y c o p i e s i n t h e p o p u l a t i o n . T h e Y c h r o m o s o m e e x c e p t e d , and d e p e n d i n g upon crossover rates, it seems u n l i k e l y that I share a n y w h o l e c h r o m o s o m e s w i t h a n y other individual.

assuredly share

m a n y small

portions of chromosomes with

others, a n d if we choose o u r portions small e n o u g h their likelihood of being s h a r e d b e c o m e s v e r y h i g h i n d e e d . I t i s n o t n o r m a l l y useful t o s p e a k o f interc h r o m o s o m e selection, therefore, since each c h r o m o s o m e is p r o b a b l y unique. N a t u r a l selection is the process by w h i c h replicators c h a n g e in frequency in the p o p u l a t i o n relative to their alleles. If the replicator under consideration i s s o l a r g e t h a t i t i s p r o b a b l y u n i q u e , i t c a n n o t b e said t o h a v e a ' f r e q u e n c y ' to c h a n g e . We must choose our arbitrary portion of c h r o m o s o m e so that it is s m a l l e n o u g h t o last, a t least p o t e n t i a l l y , for m a n y g e n e r a t i o n s b e f o r e b e i n g

The Active Germ-line Replicator

split

by crossing-over; small

enough to h a v e a

'frequency'

that can

c h a n g e d by n a t u r a l s e l e c t i o n . Is it p o s s i b l e to c h o o s e it loo s m a l l ? I s h a l l r e t u r n t o this q u e s t i o n b e l o w , after a p p r o a c h i n g i t f r o m a n o t h e r d i r e c t i o n . I

shall

make

attempt

specify

exactly

how

long

portion

c h r o m o s o m e c a n be permitted to be before it ceases to be usefully r e g a r d e d a s a r e p l i c a t o r . T h e r e i s n o h a r d a n d fast r u l e , a n d w e d o n ' t n e e d o n e . I t depends on the strength of the selection pressure of interest.

We are not

seeking an absolutely rigid definition, but 'a kind of fading-out definition, like t h e d e f i n i t i o n o f " b i g "

or " o l d " ' .

I f the selection pressure w e are

d i s c u s s i n g i s v e r y s t r o n g , t h a t i s i f o n e r e p l i c a t o r m a k e s its possessors v e r y m u c h m o r e l i k e l y t o s u r v i v e a n d r e p r o d u c e t h a n its a l l e l e s d o , t h e r e p l i c a t o r c a n b e q u i t e l a r g e a n d still b e u s e f u l l y r e g a r d e d a s a u n i t t h a t i s n a t u r a l l y selected.

If,

between

the other hand,

putative

replicator

the difference in survival

and

its

alleles

almost

consequences

negligible,

the

replicators under discussion w o u l d h a v e to be quite small if the difference in t h e i r s u r v i v a l v a l u e s i s t o m a k e i t s e l f felt. T h i s i s t h e r a t i o n a l e b e h i n d W i l l i a m s ' s ( 1 9 6 6 , p . 25) d e f i n i t i o n : ' I n e v o l u t i o n a r y t h e o r y , a g e n e c o u l d b e d e f i n e d a s a n y h e r e d i t a r y i n f o r m a t i o n for w h i c h t h e r e i s a f a v o r a b l e o r unfavorable

selection

bias

equal

several

many

times

its

rate

endogenous change.' T h e possibility o f strong linkage d i s e q u i l i b r i u m ( C l e g g 1978) does not w e a k e n the c a s e . I t s i m p l y i n c r e a s e s t h e s i z e o f t h e c h u n k o f g e n o m e t h a t w e can

usefully

treat

replicator.

If,

which

seems

disequilibrium is so strong that populations contain

doubtful,

linkage

'only a few g a m e t i c

types' ( L e w o n t i n 1974, p. 3 1 2 ) , the effective replicator will be a v e r y large c h u n k o f D N A . W h e n w h a t L e w o n t i n calls lc, the ' c h a r a c t e r i s t i c l e n g t h ' (the 'distance over

which

coupling

effective'),

only

fraction

of the

c h r o m o s o m e l e n g t h , e a c h g e n e i s o u t o f l i n k a g e e q u i l i b r i u m o n l y w i t h its neighbors but is assorted essentially i n d e p e n d e n t l y of other genes farther a w a y . T h e c h a r a c t e r i s t i c l e n g t h is, i n s o m e s e n s e , t h e u n i t o f e v o l u t i o n s i n c e genes within it are highly correlated. T h e c o n c e p t is a subtle one, h o w e v e r . It does not m e a n that the g e n o m e is b r o k e n up into discrete a d j a c e n t c h u n k s of length lc. E v e r y locus is the center of such a c o r r e l a t e d s e g m e n t a n d e v o l v e s i n l i n k a g e w i t h t h e g e n e s n e a r it' ( L e w o n t i n 1 9 7 4 ) . Similarly, Slatkin linkage

(1972) w r o t e that 'It is clear that w h e n p e r m a n e n t

disequilibrium

maintained

population,

the

higher

order

interactions are i m p o r t a n t a n d the c h r o m o s o m e tends to act as a unit. T h e d e g r e e t o w h i c h this i s t r u e i n a n y g i v e n s y s t e m i s a m e a s u r e o f w h e t h e r t h e g e n e or the c h r o m o s o m e is the unit of selection, or, m o r e a c c u r a t e l y , w h a t parts o f t h e g e n o m e c a n b e said t o b e a c t i n g i n u n i s o n ' . A n d T e m p l e t o n e t al. (1976)

wrote

that

' . . . t h e unit of selection

is a function

part of the

intensity of selection: the m o r e intense the selection, the m o r e the w h o l e g e n o m e t e n d s t o h o l d t o g e t h e r a s a u n i t ' . I t w a s i n this s p i r i t t h a t I p l a y f u l l y

The Active Germ-line Replicator

c o n t e m p l a t e d t i t l i n g an e a r l i e r w o r k The slightly selfish big bit of chromosome and the even more selfish little bit of chromosome ( D a w k i n s 1 9 7 6 a , p. 3 5 ) . It has often b e e n s u g g e s t e d to me that a fatal o b j e c t i o n to replicator selectionism is the existence of within-cistron crossing-over. If chromosomes w e r e like b e a d necklaces,

the a r g u m e n t runs, w i t h crossing-over a l w a y s

b r e a k i n g the n e c k l a c e b e t w e e n beads and not within them, you might hope to

define

discrete

replicators

the

population,

containing

integral

n u m b e r of cistrons. B u t since crossover can o c c u r a n y w h e r e (Watson 1976), not just b e t w e e n beads, all hope of defining discrete units disappears. T h i s criticism underestimates the elasticity that the replicator c o n c e p t is p e r m i t t e d b y t h e p u r p o s e for w h i c h i t w a s c o i n e d . A s I h a v e j u s t s h o w n , w e are

not

looking

for

discrete

units,

but

for

pieces

of chromosome

i n d e t e r m i n a t e l e n g t h w h i c h b e c o m e m o r e o r less n u m e r o u s t h a n a l t e r n a t i v e s of e x a c t l y the same length. M o r e o v e r , as M a r k R i d l e y reminds me, most w i t h i n - c i s t r o n c r o s s o v e r s a r e , i n a n y c a s e , i n d i s t i n g u i s h a b l e i n t h e i r effects from b e t w e e n - c i s t r o n crossovers. O b v i o u s l y , if the cistron c o n c e r n e d h a p p e n s t o b e h o m o z y g o u s , p a i r e d a t m e i o s i s w i t h a n i d e n t i c a l a l l e l e , t h e t w o sets o f g e n e t i c m a t e r i a l e x c h a n g e d in a crossover will be identical, and the crossover might just

well

never have happened.

If the cistrons c o n c e r n e d

are

h e t e r o z y g o u s , differing at one nucleotide locus, a n y within-cistron crossover that occurs 'north' of the h e t e r o z y g o u s nucleotide will be indistinguishable from

one

the

northern

boundary

of the

cistron;

crossover 'south' of the h e t e r o z y g o u s nucleotide will

any

within-cistron

be indistinguishable

f r o m o n e a t t h e s o u t h e r n b o u n d a r y o f t h e c i s t r o n . O n l y i f t h e c i s t r o n s differ a t t w o loci, a n d the crossover occurs b e t w e e n t h e m , will it be identifiable as a within-cistron crossover. T h e general point is that it does not particularly matter

where

crossovers

occur

relation

cistron

boundaries.

What

m a t t e r s i s w h e r e c r o s s o v e r s o c c u r i n r e l a t i o n t o h e t e r o z y g o u s n u c l e o t i d e s . If, for i n s t a n c e , a s e q u e n c e o f six a d j a c e n t c i s t r o n s h a p p e n s t o b e h o m o z y g o u s t h r o u g h o u t a n e n t i r e b r e e d i n g p o p u l a t i o n , a c r o s s o v e r a n y w h e r e w i t h i n the six w i l l b e e x a c t l y e q u i v a l e n t i n effect t o a c r o s s o v e r a t e i t h e r e n d o f t h e six. N a t u r a l s e l e c t i o n c a n c a u s e c h a n g e s i n f r e q u e n c y o n l y a t n u c l e o t i d e loci that

are

heterozygous

the

population.

If there

are

large

intervening

c h u n k s o f n u c l e o t i d e s e q u e n c e s t h a t n e v e r differ a m o n g i n d i v i d u a l s , these c a n n o t b e s u b j e c t t o n a t u r a l s e l e c t i o n , for t h e r e i s n o t h i n g t o c h o o s e b e t w e e n t h e m . N a t u r a l s e l e c t i o n m u s t f o c u s its a t t e n t i o n o n h e t e r o z y g o u s n u c l e o t i d e s . It

changes

evolutionarily

the

single

significant

nucleotide

phenotypic

level

changes,

that

are

although

responsible

for

the

course

u n v a r y i n g r e m a i n d e r of the g e n o m e is necessary to p r o d u c e a p h e n o t y p e at a l l . H a v e w e , t h e n , a r r i v e d a t a n a b s u r d l y r e d u c t i o n i s t i c reductio a d absurdum? S h a l l we w r i t e a b o o k c a l l e d

The Selfish Nucleotide? Is a d e n i n e e n g a g e d in a

r e m o r s e l e s s s t r u g g l e a g a i n s t c y t o s i n e for possession o f l o c u s n u m b e r 30004? A t t h e v e r y l e a s t , this i s n o t a h e l p f u l w a y t o e x p r e s s w h a t i s g o i n g o n . I t

T h e Active Germ-line Replicator

becomes d o w n r i g h t misleading if it suggests to the student that a d e n i n e at o n e l o c u s is, i n s o m e sense, a l l i e d w i t h a d e n i n e a t o t h e r l o c i , p u l l i n g t o g e t h e r for a n a d e n i n e t e a m . I f t h e r e i s a n y sense i n w h i c h p u r i n e s a n d p y r i m i d i n e s c o m p e t e w i t h e a c h o t h e r for h e t e r o z y g o u s l o c i , t h e s t r u g g l e a t e a c h l o c u s i s i n s u l a t e d from t h e s t r u g g l e a t o t h e r l o c i . T h e m o l e c u l a r b i o l o g i s t m a y , for his o w n important purposes ( C h a r g a f f cited in Judson

1979), count adenines

a n d c y t o s i n e s i n t h e g e n o m e a s a w h o l e , b u t t o d o s o i s a n i d l e e x e r c i s e for t h e student

of natural

selection.

If they

are

competitors

all,

they

are

c o m p e t i t o r s for e a c h l o c u s s e p a r a t e l y . T h e y a r e i n d i f f e r e n t t o t h e fate o f t h e i r e x a c t r e p l i c a s a t o t h e r l o c i (see a l s o C h a p t e r 8). B u t t h e r e i s a m o r e i n t e r e s t i n g r e a s o n for r e j e c t i n g t h e c o n c e p t o f t h e selfish n u c l e o t i d e , i n f a v o u r o f s o m e l a r g e r r e p l i c a t i n g e n t i t y . T h e w h o l e p u r p o s e o f o u r s e a r c h for a ' u n i t o f s e l e c t i o n ' i s t o d i s c o v e r a s u i t a b l e a c t o r t o p l a y the l e a d i n g r o l e i n o u r m e t a p h o r s o f p u r p o s e . W e l o o k a t a n a d a p t a t i o n a n d w a n t t o s a y , ' I t i s for t h e g o o d o f . . . ' . O u r q u e s t i n this c h a p t e r i s for t h e right w a y to c o m p l e t e that sentence. It is w i d e l y a d m i t t e d that serious error follows from

t h e u n c r i t i c a l a s s u m p t i o n t h a t a d a p t a t i o n s a r e for t h e g o o d

o f the s p e c i e s . I h o p e I s h a l l b e a b l e t o s h o w , i n this b o o k , t h a t y e t o t h e r t h e o r e t i c a l d a n g e r s , a l b e i t lesser o n e s , a t t e n d t h e a s s u m p t i o n t h a t a d a p t a t i o n s a r e for the g o o d o f the i n d i v i d u a l o r g a n i s m . I a m s u g g e s t i n g h e r e t h a t , s i n c e w e m u s t s p e a k o f a d a p t a t i o n s a s b e i n g for t h e g o o d o f s o m e t h i n g , t h e c o r r e c t something is the a c t i v e , g e r m - l i k e replicator. A n d w h i l e it m a y not be strictly w r o n g t o s a y t h a t a n a d a p t a t i o n i s for t h e g o o d o f t h e n u c l e o t i d e , i.e. t h e s m a l l e s t r e p l i c a t o r r e s p o n s i b l e for t h e p h e n o t y p i c d i f f e r e n c e s c o n c e r n e d i n the e v o l u t i o n a r y c h a n g e , i t i s n o t h e l p f u l t o d o s o . W e a r e g o i n g t o use t h e m e t a p h o r o f p o w e r . A n a c t i v e r e p l i c a t o r i s a c h u n k o f g e n o m e t h a t , w h e n c o m p a r e d t o its a l l e l e s , e x e r t s p h e n o t y p i c p o w e r o v e r its w o r l d , s u c h t h a t its f r e q u e n c y i n c r e a s e s o r d e c r e a s e s r e l a t i v e t o t h a t o f its a l l e l e s .

W h i l e it is u n d o u b t e d l y m e a n i n g f u l

to speak of a

single

n u c l e o t i d e a s e x e r t i n g p o w e r i n this sense, i t i s m u c h m o r e u s e f u l , s i n c e t h e nucleotide only exerts a given type of p o w e r w h e n e m b e d d e d in a larger unit,

treat

the larger unit as exerting p o w e r a n d

hence altering

the

f r e q u e n c y o f its c o p i e s . I t m i g h t b e t h o u g h t t h a t t h e s a m e a r g u m e n t c o u l d b e used t o j u s t i f y t r e a t i n g a n e v e n l a r g e r u n i t , s u c h a s t h e w h o l e g e n o m e , a s t h e u n i t t h a t e x e r t s t h e p o w e r . T h i s i s n o t s o , a t l e a s t for s e x u a l g e n o m e s . W e reject the w h o l e s e x u a l g e n o m e a s a c a n d i d a t e r e p l i c a t o r , b e c a u s e o f its h i g h risk o f b e i n g f r a g m e n t e d a t m e i o s i s . T h e s i n g l e n u c l e o t i d e d o e s n o t suffer from this p r o b l e m b u t , a s w e h a v e j u s t s e e n , i t raises a n o t h e r p r o b l e m . I t c a n n o t b e s a i d t o h a v e a p h e n o t y p i c effect e x c e p t i n t h e c o n t e x t o f t h e o t h e r n u c l e o t i d e s t h a t s u r r o u n d i t i n its c i s t r o n . I t i s m e a n i n g l e s s t o s p e a k o f the p h e n o t y p i c effect o f a d e n i n e . B u t i t i s e n t i r e l y s e n s i b l e t o s p e a k o f t h e p h e n o t y p i c effect o f s u b s t i t u t i n g a d e n i n e for c y t o s i n e a t a n a m e d l o c u s w i t h i n a n a m e d cistron. T h e case of a cistron w i t h i n a g e n o m e is not a n a l o g o u s .

The Active Germ-line Replicator

U n l i k e a n u c l e o t i d e , a c i s t r o n is l a r g e e n o u g h to h a v e a c o n s i s t e n t p h e n o t y p i c effect, r e l a t i v e l y , t h o u g h n o t c o m p l e t e l y , i n d e p e n d e n t l y o f w h e r e i t lies o n the c h r o m o s o m e ( b u t n o t r e g a r d l e s s o f w h a t o t h e r g e n e s s h a r e its g e n o m e ) . F o r a c i s t r o n , its s e q u e n t i a l c o n t e x t vis-a-vis o t h e r c i s t r o n s is n o t o v e r w h e l m i n g l y i m p o r t a n t i n d e t e r m i n i n g its p h e n o t y p i c effect i n c o m p a r i s o n w i t h its a l l e l e s . F o r a nucleotide's p h e n o t y p i c effect, o n t h e o t h e r h a n d , its s e q u e n t i a l c o n t e x t is e v e r y t h i n g . Bateson

(1981)

expresses

the

following

misgiving

about

'replicator

selection'. A w i n n i n g c h a r a c t e r i s d e f i n e d i n relation t o a n o t h e r o n e w h i l e g e n e t i c r e p l i c a t o r s a r e t h o u g h t a b o u t i n absolute a n d difficulty

brought

home

if y o u

ask

atomistic terms. T h e

yourself,

what

exactly

D a w k i n s ' r e p l i c a t o r ? Y o u m i g h t a n s w e r : ' T h a t bit o f genetic material m a k i n g the difference b e t w e e n the w i n n i n g a n d losing characters.' Y o u w o u l d h a v e stated that a replicator must be defined in relation to s o m e t h i n g else. A l t e r n a t i v e l y , y o u r r e p l y m i g h t b e :

'A replicator

c o n s i s t s o f a l l t h e g e n e s r e q u i r e d for t h e e x p r e s s i o n o f t h e s u r v i v i n g character'. In that case y o u are saddled with a c o m p l e x and unwieldy concept. Either w a y your answer would show how misleading it is to think of replicators as the atoms of e v o l u t i o n .

certainly

would join

Bateson

rejecting

the

second

o f his

two

a l t e r n a t i v e a n s w e r s , t h e u n w i e l d l y o n e . T h e f i r s t o f his a l t e r n a t i v e s , o n the other h a n d , expresses e x a c t l y my position, and

I do not share Bateson's

m i s g i v i n g s a b o u t it. F o r m y p u r p o s e s a g e n e t i c r e p l i c a t o r i s d e f i n e d b y r e f e r e n c e to its a l l e l e s , b u t this is n o t a w e a k n e s s of t h e c o n c e p t . O r , if it is d e e m e d t o b e a w e a k n e s s , i t i s a w e a k n e s s t h a t afflicts t h e w h o l e s c i e n c e o f p o p u l a t i o n g e n e t i c s , n o t j u s t the p a r t i c u l a r idea of g e n e t i c units of selection. It is a f u n d a m e n t a l t r u t h , t h o u g h it is n o t a l w a y s r e a l i z e d , t h a t whenever a geneticist studies a g e n e 'for' a n y p h e n o t y p i c c h a r a c t e r , he is a l w a y s referring to a difference b e t w e e n t w o a l l e l e s . T h i s is a r e c u r r i n g t h e m e t h r o u g h o u t this book. T o p r o v e t h e p u d d i n g , let m e s h o w h o w e a s y i t i s t o u s e t h e g e n e a s a c o n c e p t u a l unit of selection, w h i l e a d m i t t i n g that it is o n l y defined by c o m p a r i s o n w i t h its a l l e l e s . I t i s n o w a c c e p t e d t h a t a p a r t i c u l a r m a j o r g e n e for d a r k c o l o r a t i o n i n t h e p e p p e r e d m o t h Biston betularia h a s i n c r e a s e d i n frequency

industrial

areas

because

produces

phenotypes

that

are

superior in industrial areas ( K e t t l e w e l l 1 9 7 3 ) . At the s a m e time, we h a v e to a d m i t t h a t this g e n e i s o n l y o n e o f t h o u s a n d s t h a t a r e n e c e s s a r y i n o r d e r for t h e d a r k c o l o r a t i o n t o s h o w itself. A m o t h c a n n o t h a v e d a r k w i n g s unless i t has w i n g s , a n d it c a n n o t h a v e w i n g s unless it has h u n d r e d s of genes and hundreds

equally

necessary

environmental

factors.

But

this

all

The Active Germ-line Replicator

i r r e l e v a n t . T h e difference b e t w e e n t h e carbonaria a n d t h e typica p h e n o t y p e c a n still

be d u e

a difference

one

locus,

even

though

the p h e n o t y p e s

t h e m s e l v e s c o u l d n o t exist w i t h o u t t h e p a r t i c i p a t i o n o f t h o u s a n d s o f g e n e s . A n d it is the s a m e difference that is the basis of the n a t u r a l selection. B o t h g e n e t i c i s t s and n a t u r a l s e l e c t i o n a r e c o n c e r n e d w i t h d i f f e r e n c e s ! H o w e v e r c o m p l e x the g e n e t i c basis o f f e a t u r e s t h a t a l l m e m b e r s o f a s p e c i e s h a v e i n common, n a t u r a l s e l e c t i o n i s c o n c e r n e d w i t h d i f f e r e n c e s . E v o l u t i o n a r y c h a n g e is a l i m i t e d set of s u b s t i t u t i o n s at i d e n t i f i a b l e l o c i . F u r t h e r difficulties w i l l b e d e a l t w i t h i n t h e n e x t c h a p t e r . M e a n w h i l e , I e n d this c h a p t e r w i t h a s m a l l d i v e r s i o n w h i c h m a y b e h e l p f u l i n i l l u s t r a t i n g the r e p l i c a t o r o r ' g e n e ' s - e y e ' v i e w o f e v o l u t i o n . A n a p p e a l i n g a s p e c t o f t h e view appears if we look b a c k w a r d s in time. T h e replicators in frequent existence t o d a y constitute a relatively successful subset of those that h a v e existed in the past. A g i v e n replicator in me c o u l d , in theory, be traced b a c k w a r d s through a straight line of ancestors. T h e s e ancestors, and the e n v i r o n m e n t s t h a t t h e y p r o v i d e d for t h e r e p l i c a t o r , c a n b e r e g a r d e d a s t h e replicator's 'past e x p e r i e n c e ' . The

past

experience of autosomal

genetic

fragments

species

is,

s t a t i s t i c a l l y s p e a k i n g , s i m i l a r . I t consists o f a n e n s e m b l e o f t y p i c a l s p e c i e s bodies, approximately 50 per cent male and 50 per cent female bodies, bodies

which

grew

through

wide

spectrum

of ages

least

r e p r o d u c t i v e a g e ; a n d it includes a g o o d r a n d o m shuffling of ' c o m p a n i o n ' g e n e s a t o t h e r l o c i . T h e g e n e s t h a t exist t o d a y t e n d t o b e t h e o n e s t h a t a r e good at surviving in that statistical e n s e m b l e of bodies, a n d in c o m p a n y w i t h that statistical e n s e m b l e of c o m p a n i o n genes. As we shall see, it is selection in f a v o u r o f the q u a l i t i e s n e e d e d for s u r v i v a l i n company w i t h o t h e r , s i m i l a r l y s e l e c t e d , g e n e s , t h a t g i v e s rise t o t h e a p p e a r a n c e o f ' c o a d a p t e d g e n o m e s ' . I shall s h o w i n C h a p t e r 1 3 t h a t this i s a m u c h m o r e i l l u m i n a t i n g i n t e r p r e t a t i o n o f the p h e n o m e n o n o f c o a d a p t a t i o n t h a n its a l t e r n a t i v e , t h a t ' t h e c o a d a p t e d g e n o m e is the true unit of selection'. P r o b a b l y no t w o genes in an organism h a v e identical past experiences, though a linked pair m a y c o m e close, and, mutants aside, all the genes on a Y c h r o m o s o m e h a v e t r a v e l l e d t o g e t h e r t h r o u g h t h e s a m e set o f b o d i e s for a large n u m b e r of generations. But the e x a c t n a t u r e of a g e n e ' s past e x p e r i e n c e i s o f less i n t e r e s t t h a n t h e g e n e r a l i z a t i o n s o n e c a n m a k e a b o u t t h e p a s t e x p e r i e n c e s o f a l l g e n e s t h a t exist t o d a y . F o r i n s t a n c e , h o w e v e r v a r i a b l e t h e set o f m y a n c e s t o r s m a y b e , t h e y a l l h a d i n c o m m o n t h a t t h e y s u r v i v e d a t least t o r e p r o d u c t i v e a g e , t h e y c o p u l a t e d h e t e r o s e x u a l l y a n d w e r e f e r t i l e . T h e s a m e g e n e r a l i z a t i o n c a n n o t b e m a d e a b o u t t h e h i s t o r i c a l set o f b o d i e s that were not my ancestors. T h e bodies that p r o v i d e d the past e x p e r i e n c e of existing genes are a n o n - r a n d o m subset of all the b o d i e s that h a v e e v e r existed. T h e g e n e s t h a t exist t o d a y r e f l e c t t h e set o f e n v i r o n m e n t s t h a t t h e y h a v e

The Active Germ-line Replicator

e x p e r i e n c e d in the past. T h i s includes the internal e n v i r o n m e n t s p r o v i d e d by t h e b o d i e s t h e g e n e s h a v e i n h a b i t e d , a n d also e x t e r n a l e n v i r o n m e n t s , d e s e r t , forest, s e a s h o r e ,

predators,

p a r a s i t e s , s o c i a l c o m p a n i o n s , e t c . T h i s is, o f

c o u r s e , n o t b e c a u s e t h e e n v i r o n m e n t s h a v e i m p r i n t e d t h e i r q u a l i t i e s o n the g e n e s — t h a t w o u l d b e L a m a r c k i s m (see C h a p t e r 9 ) — b u t b e c a u s e the g e n e s t h a t e x i s t t o d a y a r e a s e l e c t e d set, a n d t h e q u a l i t i e s t h a t m a d e t h e m s u r v i v e reflect t h e q u a l i t i e s o f t h e e n v i r o n m e n t s i n w h i c h t h e y s u r v i v e d . I said t h a t a g e n e ' s e x p e r i e n c e consists of t i m e s p e n t in a p p r o x i m a t e l y 50 p e r c e n t m a l e a n d 5 0 p e r c e n t f e m a l e b o d i e s , b u t this i s n o t , o f c o u r s e , true o f genes

sex

chromosomes.

mammals,

assuming

Y-chromosome

c r o s s i n g - o v e r , a g e n e on a Y c h r o m o s o m e h a s e x p e r i e n c e d o n l y m a l e b o d i e s , a n d a g e n e o n a n X c h r o m o s o m e h a s s p e n t t w o - t h i r d s o f its h i s t o r y i n f e m a l e bodies and one-third in m a l e bodies. In birds, Y - c h r o m o s o m e genes h a v e e x p e r i e n c e d o n l y f e m a l e bodies, a n d in p a r t i c u l a r cases such as c u c k o o s we c a n s a y s o m e t h i n g f u r t h e r . F e m a l e Cuculus canorus a r e d i v i d e d i n t o ' g e n t e s ' , e a c h g e n s p a r a s i t i z i n g a d i f f e r e n t s p e c i e s o f host ( L a c k 1 9 6 8 ) . A p p a r e n t l y e a c h f e m a l e l e a r n s t h e q u a l i t i e s o f h e r o w n foster p a r e n t s a n d t h e i r nest, a n d returns w h e n adult to parasitize the same species. M a l e s do not seem to discriminate as to gens in their c h o i c e of m a t e , and therefore they act as v e h i c l e s for g e n e f l o w b e t w e e n g e n t e s . O f t h e g e n e s i n a f e m a l e c u c k o o , therefore, those on a u t o s o m e s a n d the X c h r o m o s o m e h a v e p r o b a b l y had r e c e n t e x p e r i e n c e o f a l l g e n t e s i n t h e p o p u l a t i o n , a n d b e e n ' r e a r e d ' b y foster parents b e l o n g i n g to all the species parasitized by the c u c k o o p o p u l a t i o n . But

the

chromosome,

uniquely,

confined

for

long

sequences

g e n e r a t i o n s t o o n e g e n s a n d o n e foster s p e c i e s . O f a l l t h e g e n e s s i t t i n g i n a r o b i n ' s nest, o n e s u b s e t — r o b i n g e n e s a n d c u c k o o Y - c h r o m o s o m e g e n e s ( a n d robin

flea

Another

genes)—has

subset—cuckoo

sat

robins'

autosomal

nests

and

for

many

generations

X-chromosome

back.

genes—has

ex-

p e r i e n c e d a m i x t u r e o f nests. O f c o u r s e t h e f i r s t s u b s e t s h a r e o n l y p a r t o f their e x p e r i e n c e , a l o n g series o f r o b i n nests. I n o t h e r a s p e c t s o f t h e i r e x p e r i e n c e , cuckoo Y - c h r o m o s o m e genes will have more in c o m m o n with other cuckoo genes

than

with

robin

genes.

But

a s far a s

certain

particular selection

p r e s s u r e s f o u n d i n nests a r e c o n c e r n e d , c u c k o o Y - c h r o m o s o m e g e n e s h a v e more in c o m m o n with robin genes than with c u c k o o autosome genes. It is n a t u r a l , t h e n , t h a t c u c k o o Y c h r o m o s o m e s s h o u l d h a v e e v o l v e d t o reflect their peculiar experience, w h i l e other c u c k o o genes simultaneously evolved to reflect their m o r e g e n e r a l e x p e r i e n c e — a kind of incipient intragenomic ' s p e c i a t i o n ' a t t h e c h r o m o s o m a l l e v e l . I t is, i n d e e d , w i d e l y a s s u m e d for this r e a s o n t h a t g e n e s for foster s p e c i e s - s p e c i f i c e g g m i m i c r y m u s t b e c a r r i e d o n t h e Y c h r o m o s o m e , w h i l e g e n e s for g e n e r a l p a r a s i t i c a d a p t a t i o n s m i g h t b e carried on any chromosome. I a m n o t s u r e w h e t h e r t h e f a c t h a s s i g n i f i c a n c e , b u t this b a c k w a r d s w a y o f l o o k i n g s h o w s X c h r o m o s o m e s , t o o , to h a v e a p e c u l i a r h i s t o r y . A g e n e on an

The Active Germ-line Replicator

autosome in a female c u c k o o is as likely to h a v e c o m e from the father as from the m o t h e r , i n w h i c h l a t t e r c a s e i t e x p e r i e n c e s t h e s a m e h o s t s p e c i e s for t w o g e n e r a t i o n s r u n n i n g . A g e n e on an X c h r o m o s o m e in a f e m a l e c u c k o o is b o u n d to h a v e c o m e from the father, a n d therefore is not e s p e c i a l l y likely to e x p e r i e n c e the s a m e host species t w o g e n e r a t i o n s r u n n i n g . A statistical 'runs test' o n the s e q u e n c e o f foster s p e c i e s e x p e r i e n c e d b y a n a u t o s o m a l g e n e w o u l d t h e r e f o r e r e v e a l a s l i g h t r u n s effect, g r e a t e r t h a n t h a t for a g e n e o n a n X c h r o m o s o m e , a n d m u c h less t h a n t h a t for a g e n e on a Y c h r o m o s o m e . In any animal, an inverted portion of c h r o m o s o m e m a y resemble a Y c h r o m o s o m e i n b e i n g u n a b l e t o cross o v e r . T h e ' e x p e r i e n c e ' o f a n y p a r t o f the ' i n v e r s i o n s u p e r g e n e ' t h e r e f o r e r e p e a t e d l y i n c l u d e s t h e o t h e r p a r t s o f t h e supergene

and

their

phenotypic

consequences.

habitat

selection

gene

a n y w h e r e in such a supergene, say a g e n e that m a k e s i n d i v i d u a l s c h o o s e d r y microclimates,

would

then

provide

a consistent

successive generations of the w h o l e s u p e r g e n e .

habitat

'experience'

for

Thus a given gene may

' e x p e r i e n c e ' c o n s i s t e n t l y d r y h a b i t a t s for t h e s a m e k i n d o f r e a s o n a s a g e n e o n a c u c k o o ' s Y c h r o m o s o m e c o n s i s t e n t l y e x p e r i e n c e s m e a d o w - p i p i t nests. T h i s will

provide

consistent

selection

pressure

bearing

upon

that

locus,

favouring alleles that are a d a p t e d to a d r y h a b i t a t in the s a m e w a y as alleles for m i m i c k i n g m e a d o w - p i p i t e g g s a r e f a v o u r e d i n Y c h r o m o s o m e s o f f e m a l e cuckoos o f the m e a d o w - p i p i t gens. T h i s p a r t i c u l a r inversion s u p e r g e n e w i l l t e n d t o b e f o u n d for g e n e r a t i o n s i n d r y h a b i t a t s , e v e n t h o u g h t h e rest o f t h e g e n o m e m a y b e r a n d o m l y shuffled o v e r t h e w h o l e r a n g e o f h a b i t a t s a v a i l a b l e t o the s p e c i e s . M a n y d i f f e r e n t l o c i o n t h e i n v e r t e d p o r t i o n o f c h r o m o s o m e m a y therefore c o m e to be a d a p t e d to a d r y c l i m a t e , a n d a g a i n s o m e t h i n g a k i n t o i n t r a g e n o m i c i n c i p i e n t s p e c i a t i o n m a y g o o n . I find this b a c k w a r d s w a y of l o o k i n g at the past ' e x p e r i e n c e ' of genetic replicators helpful. Germ-line replicators,

then,

are units

t h a t a c t u a l l y s u r v i v e o r fail

survive, the difference constituting n a t u r a l selection. A c t i v e replicators h a v e s o m e effect o n t h e w o r l d , w h i c h i n f l u e n c e s t h e i r c h a n c e s o f s u r v i v i n g . I t i s t h e effects o n t h e w o r l d o f s u c c e s s f u l a c t i v e g e r m - l i n e r e p l i c a t o r s t h a t w e see a s adaptations.

Fragments of D N A qualify as

active

germ-line

replicators.

W h e r e t h e r e i s s e x u a l r e p r o d u c t i o n , these f r a g m e n t s m u s t n o t b e d e f i n e d t o o large if they are to retain the p r o p e r t y of self-duplication. A n d they must not be defined too small if they are to be usefully r e g a r d e d as a c t i v e . I f t h e r e w e r e sex b u t n o c r o s s i n g - o v e r , e a c h c h r o m o s o m e w o u l d b e a r e p l i c a t o r , a n d w e s h o u l d s p e a k o f a d a p t a t i o n s a s b e i n g for t h e g o o d o f t h e c h r o m o s o m e . If there is no sex we c a n , by the s a m e token, treat the entire g e n o m e of an a s e x u a l o r g a n i s m as a r e p l i c a t o r . B u t t h e o r g a n i s m i t s e l f is not a r e p l i c a t o r . T h i s i s for t w o q u i t e d i s t i n c t r e a s o n s w h i c h s h o u l d n o t b e c o n f u s e d w i t h e a c h o t h e r . T h e first r e a s o n f o l l o w s f r o m t h e a r g u m e n t s d e v e l o p e d i n this

chapter,

and

applies

only

where

there

sexual

reproduction

and

m e i o s i s : m e i o s i s a n d s e x u a l fusion see t o i t t h a t n o t e v e n o u r g e n o m e s a r e

The Active Germ-line Replicator

replicators, so we ourselves are not replicators either. T h e second reason a p p l i e s t o a s e x u a l a s w e l l a s s e x u a l r e p r o d u c t i o n . I t w i l l b e e x p l a i n e d i n the n e x t c h a p t e r , w h i c h goes o n t o discuss w h a t o r g a n i s m s , a n d also groups o f o r g a n i s m s , are, g i v e n t h a t t h e y a r e n o t r e p l i c a t o r s .

6 O r g a n i s m s , G r o u p s and M e m e s : Replicators or V e h i c l e s ?

I h a v e m a d e s o m u c h o f t h e f r a g m e n t i n g effects o f m e i o s i s a s a r e a s o n for n o t r e g a r d i n g s e x u a l l y r e p r o d u c e d o r g a n i s m s a s r e p l i c a t o r s , t h a t i t i s t e m p t i n g t o see this a s t h e o n l y r e a s o n . I f this w e r e t r u e , i t s h o u l d f o l l o w t h a t asexually

reproduced

organisms

are

true

replicators,

and

that

where

r e p r o d u c t i o n i s a s e x u a l w e c o u l d l e g i t i m a t e l y s p e a k o f a d a p t a t i o n s a s 'for t h e g o o d o f t h e o r g a n i s m ' . B u t t h e f r a g m e n t i n g effect o f m e i o s i s i s n o t t h e o n l y r e a s o n for d e n y i n g t h a t o r g a n i s m s a r e t r u e r e p l i c a t o r s .

T h e r e is a m o r e

fundamental reason, and it applies to asexual organisms as m u c h as to sexual ones. To regard an organism as a replicator, even an asexual organism like a f e m a l e stick i n s e c t , i s t a n t a m o u n t t o a v i o l a t i o n o f t h e ' c e n t r a l d o g m a ' o f t h e non-inheritance replicator,

of a c q u i r e d that

may

characteristics. lay

out

stick

sequence

insect

consisting

looks

of daughter,

g r a n d d a u g h t e r , g r e a t - g r a n d d a u g h t e r , etc., in w h i c h e a c h a p p e a r s to be a r e p l i c a o f the p r e c e d i n g o n e i n t h e series. B u t s u p p o s e a f l a w o r b l e m i s h a p p e a r s s o m e w h e r e i n t h e c h a i n , s a y a stick i n s e c t i s u n f o r t u n a t e e n o u g h t o lose a l e g . T h e b l e m i s h m a y last for t h e w h o l e o f h e r l i f e t i m e , b u t i t i s n o t p a s s e d o n t o t h e n e x t l i n k i n t h e c h a i n . E r r o r s t h a t affect stick i n s e c t s b u t n o t t h e i r g e n e s a r e n o t p e r p e t u a t e d . N o w l a y o u t a p a r a l l e l series c o n s i s t i n g o f daughter's g e n o m e , etc.

genome,

granddaughter's

genome,

great-granddaughter's

I f a b l e m i s h a p p e a r s s o m e w h e r e a l o n g this series i t w i l l b e

passed o n t o all s u b s e q u e n t l i n k s i n t h e c h a i n . I t m a y a l s o b e r e f l e c t e d i n t h e b o d i e s o f all s u b s e q u e n t links i n the c h a i n , b e c a u s e i n e a c h g e n e r a t i o n t h e r e are c a u s a l a r r o w s l e a d i n g f r o m g e n e s t o b o d y . B u t t h e r e i s n o c a u s a l a r r o w l e a d i n g from b o d y to genes. No part of the stick insect's p h e n o t y p e is a r e p l i c a t o r . N o r i s h e r b o d y a s a w h o l e . I t i s w r o n g t o s a y t h a t 'just a s g e n e s c a n pass o n t h e i r s t r u c t u r e i n g e n e l i n e a g e s , o r g a n i s m s c a n pass o n t h e i r structure in organism lineages'. I a m s o r r y i f I a m a b o u t t o l a b o u r this a r g u m e n t , b u t I f e a r i t w a s m y failure t o b e c l e a r a b o u t i t b e f o r e t h a t l e d t o a n u n n e c e s s a r y d i s a g r e e m e n t 97

O r g a n i s m s , G r o u p s and M e m e s : Replicators or Vehicles?

w i t h B a t e s o n , a d i s a g r e e m e n t w h i c h i t i s w o r t h g o i n g t o s o m e t r o u b l e t o sort out.

Bateson

(1978b)

made

the

development are necessary but

point

that

n o t sufficient.

genetic A gene

determinants may

'program'

of a

p a r t i c u l a r bit of b e h a v i o u r ' w i t h o u t it b e i n g the o n l y thing to do so'. He goes on: D a w k i n s a c c e p t s a l l this b u t t h e n r e v e a l s his u n c e r t a i n t y a b o u t w h i c h l a n g u a g e h e i s u s i n g b y i m m e d i a t e l y g i v i n g s p e c i a l s t a t u s b a c k t o the gene as the p r o g r a m m e r . environmental

temperature

C o n s i d e r a case

which

during development

the a m b i e n t

is crucial

for

the

expression of a particular p h e n o t y p e . If the temperature changes by a few degrees the s u r v i v a l m a c h i n e is b e a t e n by a n o t h e r one. W o u l d not that g i v e as m u c h status to a necessary t e m p e r a t u r e v a l u e as to a necessary

gene?

The

temperature

value

also

required

for

the

e x p r e s s i o n o f a p a r t i c u l a r p h e n o t y p e . I t i s a l s o s t a b l e ( w i t h i n limits) f r o m o n e g e n e r a t i o n t o t h e n e x t . I t m a y e v e n b e t r a n s m i t t e d from o n e g e n e r a t i o n t o t h e n e x t i f t h e s u r v i v a l m a c h i n e m a k e s a nest for its offspring. I n d e e d , using D a w k i n s ' o w n style of teleological a r g u m e n t o n e c o u l d c l a i m t h a t t h e b i r d i s t h e nest's w a y o f m a k i n g a n o t h e r nest [Bateson 1978b]. I r e p l i e d t o B a t e s o n , b u t d i d s o t o o b r i e f l y , p i c k i n g o n t h e last r e m a r k a b o u t b i r d s ' nests a n d s a y i n g , ' A nest i s n o t a t r u e r e p l i c a t o r b e c a u s e a [ n o n g e n e t i c ] " m u t a t i o n " w h i c h o c c u r s i n t h e c o n s t r u c t i o n o f a nest, for e x a m p l e the a c c i d e n t a l i n c o r p o r a t i o n of a pine needle instead of the usual grass, is not p e r p e t u a t e d in future " g e n e r a t i o n s of nests".

Similarly, protein molecules

are not replicators, nor is messenger R N A ' (Dawkins 1978a). Bateson had taken the c a t c h p h r a s e a b o u t a bird being a gene's w a y of m a k i n g another g e n e , a n d i n v e r t e d it, s u b s t i t u t i n g ' n e s t ' for ' g e n e ' . B u t the p a r a l l e l i s n o t a v a l i d o n e . T h e r e i s a c a u s a l a r r o w g o i n g f r o m g e n e t o b i r d , b u t n o n e i n the reverse direction.

A changed gene may

perpetuate

itself b e t t e r

than

its

u n m u t a t e d a l l e l e . A c h a n g e d nest w i l l d o n o s u c h t h i n g u n l e s s , o f c o u r s e , the c h a n g e is d u e to a c h a n g e d g e n e , in w h i c h case it is the g e n e that is p e r p e t u a t e d , n o t t h e nest. A nest, l i k e a b i r d , is a g e n e ' s w a y of m a k i n g another gene. Bateson

worried

that

seem

give

'special

status'

genetic

d e t e r m i n a n t s o f b e h a v i o u r . H e fears t h a t a n e m p h a s i s o n t h e g e n e a s the e n t i t y for w h o s e b e n e f i t o r g a n i s m s l a b o u r , r a t h e r t h a n t h e o t h e r w a y a r o u n d , leads to an u n d u e e m p h a s i s on the i m p o r t a n c e of genetic as opposed to e n v i r o n m e n t a l d e t e r m i n a n t s o f d e v e l o p m e n t . T h e a n s w e r t o this i s t h a t w h e n w e a r e t a l k i n g a b o u t development i t i s a p p r o p r i a t e t o e m p h a s i z e n o n - g e n e t i c a s w e l l as g e n e t i c factors. B u t w h e n we are t a l k i n g a b o u t units of selection a d i f f e r e n t e m p h a s i s i s c a l l e d for, a n e m p h a s i s o n t h e p r o p e r t i e s o f r e p l i c a t o r s .

O r g a n i s m s , G r o u p s and M e m e s : R e p l i c a t o r s o r V e h i c l e s ?

T h e special

status

of genetic

factors

rather

than

non-genetic

factors

d e s e r v e d for o n e r e a s o n o n l y : g e n e t i c f a c t o r s r e p l i c a t e t h e m s e l v e s , b l e m i s h e s and all, but non-genetic factors do not. L e t u s g r a n t w i t h b o t h h a n d s t h a t t h e t e m p e r a t u r e i n t h e nest h o u s i n g a d e v e l o p i n g b i r d i s i m p o r t a n t b o t h for its i m m e d i a t e s u r v i v a l a n d for t h e w a y i t d e v e l o p s a n d t h e r e f o r e for its l o n g - t e r m s u c c e s s a s a n a d u l t . T h e i m m e d i a t e effects o f g e n e p r o d u c t s o n t h e b i o c h e m i c a l s p r i n g s o f d e v e l o p m e n t m a y , i n d e e d , c l o s e l y r e s e m b l e t h e effects o f t e m p e r a t u r e c h a n g e s 1957). We Bunsen

could

burners,

biochemical

tree

even

i m a g i n e the

selectively

applied

of embryonic

enzyme at

products

crucial

causation,

(Waddington

of genes

nodes

of the

controlling

little

branching

development

s e l e c t i v e c o n t r o l o f b i o c h e m i c a l r e a c t i o n r a t e s . A n e m b r y o l o g i s t r i g h t l y sees no

fundamental

distinction

between

genetic

and

environmental

causal

factors, a n d h e c o r r e c t l y r e g a r d s e a c h a s n e c e s s a r y b u t n o t s u f f i c i e n t . B a t e s o n was putting the e m b r y o l o g i s t ' s point of v i e w , a n d no ethologist is better q u a l i f i e d t o d o so. B u t I w a s n o t t a l k i n g e m b r y o l o g y . I w a s n o t c o n c e r n e d with the rival claims of d e t e r m i n a n t s of d e v e l o p m e n t . I w a s t a l k i n g a b o u t replicators surviving in evolutionary time, and Bateson certainly agrees that n e i t h e r a nest, n o r t h e t e m p e r a t u r e i n s i d e it, n o r t h e b i r d t h a t b u i l t it, a r e r e p l i c a t o r s . W e c a n q u i c k l y see t h a t t h e y a r e n o t r e p l i c a t o r s b y e x p e r i m e n t a l l y a l t e r i n g o n e o f t h e m . T h e c h a n g e m a y w r e a k h a v o c o n t h e a n i m a l , o n its d e v e l o p m e n t a n d its c h a n c e s of s u r v i v a l , but the change will not be passed on to the next generation. N o w m a k e a s i m i l a r m u t i l a t i o n ( m u t a t i o n ) to a g e n e in t h e g e r m - l i n e : t h e c h a n g e m a y o r m a y n o t affect t h e b i r d ' s d e v e l o p m e n t a n d its s u r v i v a l , b u t i t can b e p a s s e d o n t o t h e n e x t g e n e r a t i o n ; i t c a n b e r e p l i c a t e d . A s i s s o often t h e c a s e , a n a p p a r e n t d i s a g r e e m e n t t u r n s o u t t o b e d u e t o mutual

misunderstanding.

thought

that

Bateson

was

denying

proper

respect to the I m m o r t a l R e p l i c a t o r . Bateson t h o u g h t that I w a s d e n y i n g proper respect to the G r e a t N e x u s of c o m p l e x causal factors i n t e r a c t i n g in d e v e l o p m e n t . I n f a c t , e a c h o f u s w a s l a y i n g l e g i t i m a t e stress o n c o n s i d e r a t i o n s w h i c h a r e i m p o r t a n t for t w o d i f f e r e n t m a j o r fields o f b i o l o g y , t h e s t u d y o f d e v e l o p m e n t a n d the study of n a t u r a l selection. An

organism,

then,

not

replicator,

not

even

(despite

Lewontin

1 9 7 0 a â&#x20AC;&#x201D; s e e D a w k i n s i n press) a c r u d e r e p l i c a t o r w i t h p o o r c o p y i n g f i d e l i t y . I t i s t h e r e f o r e b e t t e r n o t t o s p e a k o f a d a p t a t i o n s a s b e i n g for t h e g o o d o f t h e organism.

W h a t a b o u t larger units,

groups of organisms,

species,

com-

munities of species, e t c . ? S o m e of these l a r g e r g r o u p i n g s are c l e a r l y subject to a version of the 'internal f r a g m e n t a t i o n destroys c o p y i n g fidelity' a r g u m e n t . T h e f r a g m e n t i n g a g e n t i n this c a s e i s n o t t h e r e c o m b i n i n g effects o f m e i o s i s , but i m m i g r a t i o n a n d e m i g r a t i o n , the destruction o f the integrity o f g r o u p s b y the m o v e m e n t o f i n d i v i d u a l s i n t o a n d o u t o f t h e m . A s I h a v e p u t i t b e f o r e , t h e y a r e l i k e c l o u d s i n t h e sky o r d u s t - s t o r m s i n t h e d e s e r t . temporary

aggregations

federations.

They

are

not

stable

T h e y are through

100 O r g a n i s m s , G r o u p s and M e m e s :

Replicators or Vehicles?

e v o l u t i o n a r y t i m e . P o p u l a t i o n s m a y last a l o n g w h i l e , b u t t h e y a r e c o n s t a n t l y b l e n d i n g w i t h o t h e r p o p u l a t i o n s a n d s o l o s i n g t h e i r i d e n t i t y . T h e y a r e also s u b j e c t to e v o l u t i o n a r y c h a n g e f r o m w i t h i n . A p o p u l a t i o n is n o t a d i s c r e t e e n o u g h entity to be a unit of natural selection, not stable and unitary enough to

'selected'

preference

another

population.

But, just

the

' f r a g m e n t a t i o n ' a r g u m e n t a p p l i e d o n l y to a subset of organisms, sexual ones, so it also applies o n l y to a subset at the g r o u p level. It applies to groups c a p a b l e of i n t e r b r e e d i n g , but it does not a p p l y to r e p r o d u c t i v e l y isolated species. L e t us, t h e n , e x a m i n e w h e t h e r s p e c i e s b e h a v e s u f f i c i e n t l y like c o h e r e n t e n t i t i e s , m u l t i p l y i n g a n d g i v i n g rise t o o t h e r s p e c i e s , t o d e s e r v e t o b e c a l l e d replicators. N o t e that that is not the same as Ghiselin's (1974b) logical claim that species are 'individuals'

(see a l s o H u l l

1976).

O r g a n i s m s , too, are

i n d i v i d u a l s in G h i s e l i n ' s sense, a n d I h o p e I h a v e established that organisms are not replicators. Do species, or, to be m o r e precise, do r e p r o d u c t i v e l y isolated g e n e - p o o l s , really a n s w e r to the definition of replicators? It is i m p o r t a n t to r e m e m b e r t h a t m e r e i m m o r t a l i t y is n o t a sufficient q u a l i f i c a t i o n . A l i n e a g e , s u c h a s a s e q u e n c e o f p a r e n t s a n d o f f s p r i n g from the l o n g - u n c h a n g e d b r a c h i o p o d g e n u s Lingula, i s u n e n d i n g i n t h e s a m e sense, a n d t o t h e s a m e e x t e n t , a s a l i n e a g e o f g e n e s . I n d e e d , for this e x a m p l e w e p e r h a p s n e e d n o t h a v e c h o s e n a ' l i v i n g fossil' l i k e Lingula. E v e n a r a p i d l y e v o l v i n g l i n e a g e c a n , in a sense, be treated as an entity w h i c h is either extinct or e x t a n t at a n y m o m e n t in g e o l o g i c a l time. N o w , certain kinds of lineage m a y be m o r e likely to go extinct than others, and we m a y be able to discern statistical l a w s of extinction. F o r e x a m p l e , lineages w h o s e females r e p r o d u c e a s e x u a l l y m a y b e s y s t e m a t i c a l l y m o r e o r less l i k e l y t o g o e x t i n c t than lineages w h o s e females stick to sex ( W i l l i a m s 1 9 7 5 ; M a y n a r d S m i t h 1978a). It has been suggested that a m m o n i t e and bivalve lineages with a h i g h r a t e o f e v o l v i n g l a r g e r s i z e (i.e. w i t h a h i g h r a t e o f o b e y i n g C o p e ' s R u l e ) are m o r e likely to go extinct than more slowly evolving lineages (Hallam 1 9 7 5 ) . L e i g h ( 1 9 7 7 ) m a k e s some excellent points a b o u t differential lineage e x t i n c t i o n , a n d its r e l a t i o n s h i p t o l o w e r l e v e l s o f s e l e c t i o n : ' . . . t h o s e s p e c i e s a r e f a v o r e d w h e r e s e l e c t i o n w i t h i n p o p u l a t i o n s w o r k s m o r e n e a r l y for the g o o d o f t h e s p e c i e s ' . S e l e c t i o n ' . . . f a v o r s s p e c i e s t h a t h a v e , for w h a t e v e r reason, evolved genetic systems w h e r e a gene's selective a d v a n t a g e more n e a r l y m a t c h e s its c o n t r i b u t i o n t o f i t n e s s ' . H u l l

(1980a,b)

is particularly

c l e a r a b o u t t h e l o g i c a l s t a t u s o f t h e l i n e a g e , a n d a b o u t its d i s t i n c t i o n from t h e r e p l i c a t o r a n d t h e i n t e r a c t o r ( H u l l ' s n a m e for w h a t I a m c a l l i n g the 'vehicle'). Differential lineage extinction, t h o u g h technically a form of selection, is not e n o u g h in itself to g e n e r a t e progressive e v o l u t i o n a r y c h a n g e . L i n e a g e s m a y b e ' s u r v i v o r s ' , b u t this d o e s n o t m a k e t h e m r e p l i c a t o r s . G r a i n s o f s a n d

O r g a n i s m s , G r o u p s and M e m e s : R e p l i c a t o r s o r V e h i c l e s ?

101

a r e s u r v i v o r s . H a r d g r a i n s , m a d e o f q u a r t z o r d i a m o n d , w i l l last l o n g e r t h a n soft g r a i n s m a d e o f c h a l k . B u t n o b o d y h a s e v e r i n v o k e d h a r d n e s s s e l e c t i o n a m o n g s a n d g r a i n s a s t h e basis for a n e v o l u t i o n a r y p r o g r e s s i o n . T h e r e a s o n , fundamentally, is that grains of sand do not m u l t i p l y . O n e g r a i n m a y survive a l o n g t i m e , b u t i t d o e s n o t m u l t i p l y a n d m a k e c o p i e s o f itself. D o s p e c i e s , o r other groups of organisms, m u l t i p l y ? Do they replicate? Alexander and

Borgia

(1978)

assert

that they do,

and

that

they are

t h e r e f o r e true r e p l i c a t o r s : ' S p e c i e s g i v e rise t o s p e c i e s ; s p e c i e s m u l t i p l y . ' T h e best c a s e I c a n m a k e for r e g a r d i n g s p e c i e s , o r r a t h e r t h e i r g e n e - p o o l s , a s m u l t i p l y i n g r e p l i c a t o r s arises f r o m t h e t h e o r y o f ' s p e c i e s s e l e c t i o n ' a s s o c i a t e d w i t h the p a l a e o n t o l o g i c a l i d e a o f ' p u n c t u a t e d e q u i l i b r i a ' ( E l d r e d g e & G o u l d 1972; Stanley 1975, 1979; Gould & Eldredge 1977; G o u l d 1977c, 1980a,b; L e v i n t o n & S i m o n 1 9 8 0 ) . I w i l l t a k e s o m e t i m e t o d i s c u s s this b o d y o f t h e o r y , since ' s p e c i e s s e l e c t i o n ' i s v e r y r e l e v a n t t o this c h a p t e r . A n o t h e r r e a s o n for t a k i n g t h e t i m e i s t h a t I r e g a r d the s u g g e s t i o n s o f E l d r e d g e a n d G o u l d a s o f g r e a t interest t o b i o l o g y g e n e r a l l y , b u t I a m a n x i o u s t h a t t h e y s h o u l d n o t b e oversold as more revolutionary than they actually are. G o u l d and E l d r e d g e ( 1 9 7 7 , p . 1 1 7 ) a r e t h e m s e l v e s c o n s c i o u s o f this d a n g e r , t h o u g h for d i f f e r e n t reasons. M y fear s t e m s f r o m t h e g r o w i n g i n f l u e n c e o f a v i g i l a n t c o r p s o f l a y c r i t i c s of

Darwinism,

either

religious

fundamentalists

Shavian/Koestlerian

L a m a r c k i s t s w h o , for r e a s o n s t h a t h a v e n o t h i n g t o d o w i t h s c i e n c e , e a g e r l y seize u p o n a n y t h i n g t h a t , w i t h i m p e r f e c t u n d e r s t a n d i n g , c a n b e m a d e t o sound a n t i - D a r w i n i a n . Journalists are often o n l y too r e a d y to p a n d e r to the unpopularity

of Darwinism

some

lay

circles.

One

of Britain's

least

d i s r e p u t a b l e d a i l y n e w s p a p e r s (The Guardian, 2 1 N o v e m b e r 1 9 7 8 ) s e r v e d u p a

journalistically

garbled

but

still

just

recognizable

version

the

E l d r e d g e / G o u l d theory in a l e a d i n g article, as e v i d e n c e that all is not w e l l with Darwinism.

P r e d i c t a b l y , this e l i c i t e d s o m e u n c o m p r e h e n d i n g f u n d a -

mentalist glee in the letter c o l u m n s of the paper, some of it from d i s q u i e t i n g l y influential

sources,

impression

that

and

even

the

'the

public could

scientists'

well

themselves

have

been

left

now

have

doubts

with

the

about

D a r w i n i s m . D r G o u l d i n f o r m s m e t h a t The Guardian d i d n o t f a v o u r h i m w i t h a r e p l y to his l e t t e r of p r o t e s t . A n o t h e r B r i t i s h n e w s p a p e r , (8 M a r c h

1981),

challenge Darwin', Eldredge/Gould

in a m u c h longer article called sensationally exaggerated

theory

and

other

versions

The Sunday Times

' T h e n e w clues that

the difference of Darwinism.

between The

the

British

B r o a d c a s t i n g C o r p o r a t i o n also g o t in on the a c t a r o u n d the s a m e time, in two separate p r o g r a m m e s m a d e by rival production teams. T h e y w e r e called The

Trouble with

Evolution

and

Did Darwin get it

Wrong?,

and

they

differed

h a r d l y a t all e x c e p t that o n e h a d E l d r e d g e a n d the o t h e r h a d G o u l d ! T h e second

programme

actually

went

the

lengths

of digging

some

102

O r g a n i s m s , G r o u p s and M e m e s : R e p l i c a t o r s o r V e h i c l e s ?

fundamentalists to c o m m e n t on the E l d r e d g e / G o u l d t h e o r y : not surprisingly, the ill-understood a p p e a r a n c e of dissension w i t h i n the ranks of Darwinists was meat and drink to them. J o u r n a l i s t i c s t a n d a r d s a r e n o t u n k n o w n i n l e a r n e d p e r i o d i c a l s t o o . Science (Vol.

210,

pp.

macroevolution

883 8 8 7 , under

1980)

reported

the d r a m a t i c

heading,

recent

conference

'Evolutionary

theory

under

fire', a n d w i t h the e q u a l l y sensational subtitle, ' A n historic conference in Chicago

challenges

the

four-decade

long

dominance

the

Modern

S y n t h e s i s ' (see c r i t i c i s m s b y F u t u y a m a e t al. 1 9 8 1 ) . A s M a y n a r d S m i t h i s quoted as saying at the same conference, ' Y o u are in d a n g e r of preventing understanding by suggesting that

there is intellectual antagonism

where

n o n e e x i s t s ' (see a l s o M a y n a r d S m i t h 1 9 8 1 ) . I n t h e f a c e o f a l l t h e b a l l y h o o , I am

anxious to be very clear about,

t o q u o t e o n e o f their o w n section

headings, exactly ' W h a t Eldredge and Gould Did Not (And Did) Say'. The

theory

of punctuated

equilibria

suggests

that

evolution

does not

consist in c o n t i n u o u s s m o o t h c h a n g e , 'stately unfolding', but goes in jerks, p u n c t u a t i n g l o n g p e r i o d s o f stasis. L a c k o f e v o l u t i o n a r y c h a n g e i n fossil l i n e a g e s s h o u l d n o t b e w r i t t e n off a s ' n o d a t a ' , b u t s h o u l d b e r e c o g n i z e d a s the n o r m , a n d a s w h a t w e s h o u l d r e a l l y e x p e c t t o see i f w e t a k e o u r m o d e r n s y n t h e s i s , p a r t i c u l a r l y its e m b e d d e d i d e a s o f a l l o p a t r i c s p e c i a t i o n , s e r i o u s l y : ' A s a c o n s e q u e n c e o f t h e a l l o p a t r i c t h e o r y , n e w fossil s p e c i e s d o not o r i g i n a t e i n t h e p l a c e w h e r e t h e i r a n c e s t o r s l i v e d . I t i s extremely i m p r o b a b l e t h a t w e shall be a b l e to trace the g r a d u a l splitting of a lineage m e r e l y by following a certain species up through a local rock c o l u m n ' (Eldredge & G o u l d 1972, p. 94). Of course microevolution by ordinary natural selection, w h a t I would call genetic replicator selection, goes on, but it is largely confined to brief b u r s t s o f a c t i v i t y a r o u n d t h e crisis t i m e s k n o w n a s s p e c i a t i o n e v e n t s . T h e s e bursts o f m i c r o e v o l u t i o n a r e u s u a l l y c o m p l e t e d t o o fast for p a l a e o n t o l o g i s t s t o t r a c k t h e m . A l l w e c a n see i s t h e s t a t e o f t h e l i n e a g e b e f o r e a n d after the n e w s p e c i e s i s f o r m e d . I t f o l l o w s t h a t ' g a p s ' i n t h e fossil r e c o r d b e t w e e n s p e c i e s , far f r o m b e i n g t h e e m b a r r a s s m e n t D a r w i n i a n s h a v e s o m e t i m e s t a k e n t h e m t o be, are exactly w h a t we should expect. T h e palaeontological evidence can be argued about

(Gingerich

1976;

G o u l d & E l d r e d g e 1 9 7 7 ; H a l l a m 1 9 7 8 ) , a n d I a m n o t q u a l i f i e d t o j u d g e it. A p p r o a c h i n g from a n o n - p a l a e o n t o l o g i c a l direction, indeed in lamentable ignorance

the

Wrightian/Mayrian

whole idea

Eldredge/Gould of

buffered

theory,

gene-pools

once

resisting

found

the

change,

but

o c c a s i o n a l l y s u c c u m b i n g to genetic revolutions, satisfyingly c o m p a t i b l e with one o f m y o w n enthusiasms, M a y n a r d Smith's (1974) 'evolutionarily stable strategy' concept: T h e g e n e p o o l w i l l b e c o m e a n evolutionarily stable set o f g e n e s , defined as a gene pool which cannot be invaded by any new gene. Most new

O r g a n i s m s , Groups and M e m e s : Replicators or Vehicles?

103

g e n e s w h i c h arise, e i t h e r b y m u t a t i o n o r r e a s s o r t m e n t o r i m m i g r a t i o n , are q u i c k l y p e n a l i z e d by n a t u r a l selection: the e v o l u t i o n a r i l y stable set

restored.

instability,

Occasionally . . . there

terminating

new

transitional

evolutionarily

period

stable

set . . . a

population might have more than one alternative stable point, and it m i g h t o c c a s i o n a l l y flip from o n e to a n o t h e r . P r o g r e s s i v e e v o l u t i o n m a y b e n o t s o m u c h a s t e a d y u p w a r d c l i m b a s a series o f d i s c r e t e steps from s t a b l e p l a t e a u t o s t a b l e p l a t e a u [ D a w k i n s 1 9 7 6 a , p . 9 3 ] . I a m also q u i t e i m p r e s s e d w i t h E l d r e d g e a n d G o u l d ' s r e i t e r a t e d p o i n t about time-scales: ' H o w can we view a steady progression yielding a 1 0 % increase in a million years as a n y t h i n g but a meaningless abstraction? C a n this v a r i e d w o r l d o f o u r s p o s s i b l y i m p o s e s u c h m i n u t e s e l e c t i o n p r e s s u r e s s o uninterruptedly

for

long?'

(Gould

Eldredge

1977).

'...to

see

g r a d u a l i s m a t all i n t h e fossil r e c o r d i m p l i e s s u c h a n e x c r u c i a t i n g l y s l o w r a t e o f p e r - g e n e r a t i o n c h a n g e t h a t w e m u s t s e r i o u s l y c o n s i d e r its i n v i s i b i l i t y t o natural selection in the c o n v e n t i o n a l m o d e â&#x20AC;&#x201D; c h a n g e s that confer m o m e n t a r y adaptive a d v a n t a g e s ' ( G o u l d 1980a). I suppose the following a n a l o g y m i g h t be m a d e . If a cork floats from one side of the A t l a n t i c to the other, t r a v e l l i n g steadily without d e v i a t i n g o r g o i n g b a c k w a r d s , w e m i g h t i n v o k e the G u l f S t r e a m o r T r a d e W i n d s i n e x p l a n a t i o n . T h i s w i l l seem p l a u s i b l e i f the time the c o r k t a k e s t o cross t h e o c e a n i s o f t h e r i g h t o r d e r o f m a g n i t u d e , s a y a f e w weeks or m o n t h s . B u t if the cork should t a k e a million y e a r s to cross the o c e a n , a g a i n n o t d e v i a t i n g o r g o i n g b a c k w a r d s b u t s t e a d i l y i n c h i n g its w a y a c r o s s , w e s h o u l d n o t b e satisfied w i t h a n y e x p l a n a t i o n i n t e r m s o f c u r r e n t s and winds. Currents and winds just don't m o v e that slowly, or if they do they will be so w e a k that the cork will be o v e r w h e l m i n g l y buffeted by o t h e r forces, b a c k w a r d s a s m u c h a s f o r w a r d s . I f w e f o u n d a c o r k s t e a d i l y m o v i n g a t such an e x t r e m e l y slow rate, we w o u l d h a v e to seek a w h o l l y different kind of explanation,

phenomenon

observed.

explanation

commensurate

with

the

time-scale

of the

Incidentally, there is a mildly interesting historical irony here. O n e of the e a r l y a r g u m e n t s u s e d a g a i n s t D a r w i n w a s t h a t t h e r e w a s n ' t e n o u g h t i m e for the p r o p o s e d a m o u n t o f e v o l u t i o n t o h a v e h a p p e n e d . i m a g i n e that selection pressures w e r e strong e n o u g h

It seemed hard to achieve

all

to that

e v o l u t i o n a r y c h a n g e in the short time then t h o u g h t to be a v a i l a b l e . T h e a r g u m e n t of E l d r e d g e a n d G o u l d just g i v e n is almost the e x a c t o p p o s i t e : it is h a r d to i m a g i n e a s e l e c t i o n p r e s s u r e weak e n o u g h to s u s t a i n s u c h a s l o w r a t e of unidirectional evolution over such a long period! Perhaps we should take w a r n i n g f r o m this h i s t o r i c a l t w i s t . B o t h a r g u m e n t s r e s o r t t o t h e ' h a r d t o i m a g i n e ' style of reasoning that D a r w i n so wisely c a u t i o n e d us against. Although

find

Eldredge

and

Gould's

time-scale

point

somewhat

p l a u s i b l e , I a m less c o n f i d e n t a b o u t i t t h a n t h e y a r e , s i n c e I d o f e a r t h e

104

O r g a n i s m s , G r o u p s and M e m e s : R e p l i c a t o r s o r V e h i c l e s ?

limitations o f m y o w n i m a g i n a t i o n . After all, the gradualist theory does not r e a l l y n e e d t o a s s u m e unidirectional e v o l u t i o n for l o n g p e r i o d s . I n t e r m s o f m y c o r k a n a l o g y , w h a t if the w i n d is so w e a k that the cork takes a million years to

cross

the

Atlantic?

Waves

and

local

currents

may

indeed

send

b a c k w a r d s a l m o s t a s m u c h a s f o r w a r d s . B u t w h e n all i s a d d e d u p , the n e t s t a t i s t i c a l d i r e c t i o n o f t h e c o r k m a y still

be determined

by a slow and

relentless w i n d . I a l s o w o n d e r w h e t h e r E l d r e d g e a n d G o u l d g i v e sufficient a t t e n t i o n t o the p o s s i b i l i t i e s o p e n e d u p b y ' a r m s r a c e s ' ( C h a p t e r 4 ) . I n c h a r a c t e r i z i n g the gradualist theory that they attack, they write: ' T h e postulated mechanism for g r a d u a l u n i - d i r e c t i o n a l c h a n g e i s " o r t h o s e l e c t i o n " , u s u a l l y v i e w e d a s a constant a d j u s t m e n t to a u n i - d i r e c t i o n a l c h a n g e in one or m o r e features of the p h y s i c a l e n v i r o n m e n t '

(Eldredge &

Gould

1972).

If the winds a n d

currents of the p h y s i c a l e n v i r o n m e n t pressed steadily in the same direction over g e o l o g i c a l time-scales, it m i g h t indeed seem likely that animal lineages would

reach

the

other

side

of their

evolutionary

ocean

fast

that

palaeontologists c o u l d not track their passage. B u t c h a n g e ' p h y s i c a l ' t o ' b i o l o g i c a l ' a n d t h i n g s m a y l o o k different. I f e a c h small

adaptive

step

one

lineage

calls

forth

counteradaptation

a n o t h e r l i n e a g e â&#x20AC;&#x201D; s a y its p r e d a t o r s â&#x20AC;&#x201D; s l o w , d i r e c t i o n a l o r t h o s e l e c t i o n looks rather m o r e plausible. T h e s a m e is true of intraspecific competition, w h e r e t h e o p t i m u m s i z e , s a y , for a n i n d i v i d u a l c a n b e s l i g h t l y l a r g e r t h a n the p r e s e n t p o p u l a t i o n m o d e , whatever the present population mode may be. ' . . . in the p o p u l a t i o n as a w h o l e t h e r e is a c o n s t a n t t e n d e n c y to f a v o r a s i z e s l i g h t l y a b o v e t h e m e a n . T h e s l i g h t l y l a r g e r a n i m a l s h a v e a v e r y s m a l l b u t i n the long run, in large populations, decisive a d v a n t a g e in competition . . . T h u s , p o p u l a t i o n s t h a t a r e r e g u l a r l y e v o l v i n g i n this w a y a r e a l w a y s w e l l a d a p t e d a s r e g a r d s s i z e i n t h e sense t h a t t h e o p t i m u m i s c o n t i n u o u s l y i n c l u d e d i n t h e i r normal

range of variation,

but a constant a s y m m e t r y in the centripetal

s e l e c t i o n f a v o r s a s l o w u p w a r d shift i n t h e m e a n ' ( S i m p s o n 1 9 5 3 , p . 1 5 1 ) . A l t e r n a t i v e l y (and shamelessly h a v i n g it b o t h w a y s ! ) , if e v o l u t i o n a r y trends r e a l l y a r e p u n c t u a t e d a n d s t e p p e d , p e r h a p s this i n i t s e l f c o u l d b e e x p l a i n e d by the arms r a c e c o n c e p t , g i v e n time-lags b e t w e e n a d a p t i v e a d v a n c e s on one side of the a r m s r a c e a n d responses by the other. B u t let u s p r o v i s i o n a l l y a c c e p t t h e t h e o r y o f p u n c t u a t e d e q u i l i b r i a a s a n e x c i t i n g l y d i f f e r e n t w a y o f l o o k i n g a t f a m i l i a r p h e n o m e n a , a n d t u r n t o the other side o f G o u l d a n d E l d r e d g e ' s ( 1 9 7 7 ) e q u a t i o n , ' p u n c t u a t e d equilibria + W r i g h t ' s r u l e = s p e c i e s s e l e c t i o n ' . W r i g h t ' s R u l e (not his o w n c o i n i n g ) i s ' t h e p r o p o s i t i o n t h a t a set o f m o r p h o l o g i e s p r o d u c e d b y s p e c i a t i o n e v e n t s i s essentially r a n d o m w i t h respect to the direction of e v o l u t i o n a r y trends within a c l a d e ' ( G o u l d & E l d r e d g e 1 9 7 7 ) . F o r e x a m p l e , even if there is an overall t r e n d t o w a r d s l a r g e r s i z e i n a set o f r e l a t e d l i n e a g e s , W r i g h t ' s R u l e suggests t h a t t h e r e i s n o s y s t e m a t i c t e n d e n c y for n e w l y b r a n c h e d - o f f s p e c i e s t o b e

O r g a n i s m s , Groups and M e m e s : Replicators or Vehicles?

larger than mutation

their parent species.

is clear,

and

T h e analogy with

this l e a d s d i r e c t l y t o

the

105

'randomness'

the right-hand

side of the

e q u a t i o n . I f n e w s p e c i e s differ f r o m t h e i r p r e d e c e s s o r s r a n d o m l y w i t h r e s p e c t to

major

trends,

major

trends

themselves

must

due

e x t i n c t i o n a m o n g those n e w s p e c i e s â&#x20AC;&#x201D; ' s p e c i e s s e l e c t i o n ' ,

differential

t o use S t a n l e y ' s

(1975) term. Gould

( 1 9 8 0 a ) r e g a r d s ' t h e t e s t i n g o f W r i g h t ' s r u l e a s a m a j o r task for

macroevolutionary

theory

and

paleobiology.

For

the

theory

of species

s e l e c t i o n , i n its p u r e f o r m , d e p e n d s u p o n it. C o n s i d e r , for e x a m p l e , a l i n e a g e displaying

C o p e ' s rule of increasing b o d y sizeâ&#x20AC;&#x201D;horses,

for e x a m p l e .

W r i g h t ' s r u l e b e v a l i d , a n d n e w s p e c i e s o f horses a r i s e e q u a l l y o f t e n a t sizes smaller and larger than their ancestors, then the trend is p o w e r e d by species s e l e c t i o n . B u t i f n e w s p e c i e s a r i s e p r e f e r e n t i a l l y a t sizes l a r g e r t h a n t h e i r ancestors,

then

don't

require

species

selection

all,

since

random

e x t i n c t i o n w o u l d still y i e l d t h e t r e n d . ' G o u l d h e r e s i m u l t a n e o u s l y s t i c k s his n e c k o u t a n d h a n d s O c c a m ' s R a z o r t o his o p p o n e n t s ! H e c o u l d e a s i l y h a v e c l a i m e d t h a t e v e n i f his m u t a t i o n - a n a l o g u e

(speciation)

was d i r e c t e d , t h e

t r e n d m i g h t still b e r e i n f o r c e d b y s p e c i e s s e l e c t i o n ( L e v i n t o n & S i m o n 1 9 8 0 ) . W i l l i a m s ( 1 9 6 6 , p . 99) i n a n i n t e r e s t i n g d i s c u s s i o n w h i c h I h a v e n o t s e e n c i t e d i n the l i t e r a t u r e o n p u n c t u a t e d e q u i l i b r i a , c o n s i d e r s a f o r m o f s p e c i e s s e l e c t i o n a c t i n g i n opposition to, a n d p e r h a p s o u t w e i g h i n g , t h e o v e r a l l t r e n d o f e v o l u t i o n w i t h i n s p e c i e s . H e a g a i n uses t h e h o r s e e x a m p l e , a n d t h e f a c t t h a t e a r l i e r fossils t e n d t o b e s m a l l e r t h a n l a t e r o n e s : F r o m this o b s e r v a t i o n , i t i s t e m p t i n g t o c o n c l u d e t h a t , a t l e a s t m o s t o f the

time

and

the

average,

larger

than

mean

size

was

a d v a n t a g e t o a n i n d i v i d u a l h o r s e i n its r e p r o d u c t i v e c o m p e t i t i o n w i t h the

rest

o f its

population.

the

component

populations

of the

T e r t i a r y horse-fauna are p r e s u m e d t o h a v e b e e n e v o l v i n g l a r g e r size most of the time a n d on the a v e r a g e . It is c o n c e i v a b l e , h o w e v e r , that precisely the opposite is true. It m a y be that at a n y g i v e n m o m e n t d u r i n g the T e r t i a r y , most of the horse p o p u l a t i o n s w e r e e v o l v i n g a s m a l l e r s i z e . T o a c c o u n t for t h e t r e n d t o w a r d s l a r g e r s i z e i t i s m e r e l y necessary

favoured

such

make a

the additional assumption tendency.

Thus,

while

only

that g r o u p selection a

minority

of the

populations m a y h a v e been e v o l v i n g a larger size, it c o u l d h a v e b e e n this m i n o r i t y t h a t g a v e rise t o m o s t o f t h e p o p u l a t i o n s o f a m i l l i o n years later.'

I do not find it hard to b e l i e v e that s o m e of the m a j o r m a c r o e v o l u t i o n a r y t r e n d s , o f the C o p e ' s R u l e t y p e ( b u t see H a l l a m 1 9 7 8 ) , o b s e r v e d b y p a l a e o n t o l ogists a r e d u e t o s p e c i e s s e l e c t i o n , i n t h e sense o f this p a s s a g e f r o m W i l l i a m s , w h i c h I think is the same as E l d r e d g e a n d G o u l d ' s sense. As I b e l i e v e all

106

O r g a n i s m s , G r o u p s and M e m e s : R e p l i c a t o r s o r V e h i c l e s ?

t h r e e a u t h o r s w o u l d a g r e e , this i s a v e r y d i f f e r e n t m a t t e r f r o m a c c e p t i n g g r o u p s e l e c t i o n a s a n e x p l a n a t i o n for i n d i v i d u a l s e l f - s a c r i f i c e : a d a p t a t i o n s for the g o o d o f the species. T h e r e w e are t a l k i n g a b o u t a n o t h e r kind o f g r o u p selection m o d e l , w h e r e the g r o u p is really seen not as a replicator but as a v e h i c l e for r e p l i c a t o r s . I s h a l l c o m e t o this s e c o n d k i n d o f g r o u p s e l e c t i o n later. M e a n w h i l e I shall a r g u e that a belief in the p o w e r of species selection t o s h a p e s i m p l e m a j o r t r e n d s i s n o t t h e s a m e a s a b e l i e f i n its p o w e r t o p u t together c o m p l e x adaptations such as eyes and brains. T h e m a j o r trends of p a l a e o n t o l o g y , simple increases in absolute size, or of r e l a t i v e sizes o f d i f f e r e n t p a r t s o f t h e b o d y , a r e i m p o r t a n t a n d i n t e r e s t i n g , b u t t h e y a r e , a b o v e all, s i m p l e . A c c e p t i n g E l d r e d g e a n d G o u l d ' s belief that n a t u r a l s e l e c t i o n i s a g e n e r a l t h e o r y t h a t c a n b e p h r a s e d o n m a n y l e v e l s , the putting together of a certain quantity of evolutionary c h a n g e demands a c e r t a i n m i n i m u m n u m b e r o f s e l e c t i v e r e p l i c a t o r - e l i m i n a t i o n s . W h e t h e r the replicators that are selectively eliminated are genes or species, a simple e v o l u t i o n a r y c h a n g e r e q u i r e s o n l y a few r e p l i c a t o r s u b s t i t u t i o n s . A l a r g e n u m b e r o f r e p l i c a t o r s u b s t i t u t i o n s , h o w e v e r , a r e n e e d e d for t h e e v o l u t i o n o f a

complex

adaptation.

The

minimum

replacement

cycle

time

when we

c o n s i d e r t h e g e n e a s r e p l i c a t o r i s o n e i n d i v i d u a l g e n e r a t i o n , from z y g o t e t o z y g o t e . I t i s m e a s u r e d i n y e a r s o r m o n t h s , o r s m a l l e r t i m e u n i t s . E v e n i n the l a r g e s t o r g a n i s m s i t i s m e a s u r e d i n o n l y tens o f y e a r s . W h e n w e c o n s i d e r the species as replicator, on the other h a n d , the r e p l a c e m e n t c y c l e time is the interval from speciation event to speciation event, and m a y be measured in t h o u s a n d s o f y e a r s , tens o f thousands, h u n d r e d s o f thousands. I n a n y given period of g e o l o g i c a l time, the n u m b e r of selective species extinctions that can h a v e t a k e n p l a c e i s m a n y o r d e r s o f m a g n i t u d e less t h a n

the n u m b e r of

selective allele replacements that can h a v e taken place. A g a i n it m a y be j u s t a limitation of the i m a g i n a t i o n , but w h i l e I c a n easily see

species

elongation

selection of horse

shaping legs,

simple

cannot

see

size such

trend slow

such

the

Tertiary

replicator-elimination

p u t t i n g t o g e t h e r a s u i t e o f a d a p t a t i o n s s u c h a s t h o s e o f w h a l e s t o a q u a t i c life. N o w , it m a y be said, surely that is unfair. H o w e v e r c o m p l e x the aquatic adaptations of whales m a y be w h e n taken as a w h o l e , c a n they not be broken d o w n i n t o a set o f s i m p l e s i z e t r e n d s w i t h a l l o m e t r i c c o n s t a n t s o f v a r y i n g m a g n i t u d e a n d sign in different parts of the b o d y ? If y o u can s t o m a c h oned i m e n s i o n a l e l o n g a t i o n in horses' legs as d u e to species selection, w h y not a w h o l e set o f e q u a l l y s i m p l e s i z e t r e n d s a d v a n c i n g i n p a r a l l e l , a n d e a c h o n e d r i v e n b y s p e c i e s s e l e c t i o n ? T h e w e a k n e s s i n this a r g u m e n t i s a s t a t i s t i c a l one. S u p p o s e there are ten such parallel trends, w h i c h is surely a highly c o n s e r v a t i v e e s t i m a t e for t h e e v o l u t i o n o f a q u a t i c a d a p t a t i o n s i n w h a l e s . I f W r i g h t ' s R u l e i s t o a p p l y t o a l l t e n , i n a n y o n e s p e c i a t i o n e v e n t e a c h o f the t e n t r e n d s i s a s l i k e l y t o b e r e v e r s e d a s t o b e a d v a n c e d . T h e c h a n c e t h a t all ten w i l l b e a d v a n c e d i n a n y o n e .speciation e v e n t i s o n e h a l f t o t h e p o w e r t e n ,

O r g a n i s m s , Groups and M e m e s : Replicators or Vehicles?

107

w h i c h i s less t h a n o n e i n a t h o u s a n d . I f t h e r e a r e t w e n t y p a r a l l e l t r e n d s , t h e chance of a n y one speciation event a d v a n c i n g all t w e n t y simultaneously is less t h a n o n e in a m i l l i o n . Admittedly,

some

advancement

towards

complex

multidimensional

a d a p t a t i o n m i g h t b e a c h i e v e d t h r o u g h s p e c i e s s e l e c t i o n e v e n i f n o t a l l t e n (or twenty) trends w e r e a d v a n c e d together in a n y o n e selective e v e n t . A f t e r all, m u c h the same critical point c a n b e m a d e a b o u t the selective d e a t h s o f i n d i v i d u a l o r g a n i s m s : i t i s r a r e t o find o n e i n d i v i d u a l a n i m a l t h a t i s o p t i m a l i n all the different d i m e n s i o n s o f m e a s u r e m e n t . T h e a r g u m e n t f i n a l l y r e t u r n s t o the d i f f e r e n c e i n c y c l e t i m e s . W e s h a l l h a v e t o m a k e a q u a n t i t a t i v e judgement

taking

into

account

the

vastly

greater

cycle

time

between

replicator deaths in the species selection case than in the g e n e selection case, a n d also t a k i n g i n t o a c c o u n t t h e c o m b i n a t o r i a l p r o b l e m r a i s e d a b o v e . I h a v e n e i t h e r t h e d a t a n o r t h e m a t h e m a t i c a l skills t o u n d e r t a k e this q u a n t i t a t i v e j u d g e m e n t , t h o u g h I h a v e a d i m f e e l i n g for t h e k i n d o f m e t h o d o l o g y t h a t w o u l d b e i n v o l v e d i n s e t t i n g u p a n a p p r o p r i a t e n u l l h y p o t h e s i s : i t w o u l d fall under the g e n e r a l

heading which

Thompson

might

have

appropriate

type

have

done

with

already

like a

been

think of as

computer', written

and

(Raup

'What

D'Arcy

programs et

al.

of the

1973).

provisional guess is that species selection will not be found to be a g e n e r a l l y satisfactory e x p l a n a t i o n o f c o m p l e x a d a p t a t i o n . Consider another adopt.

might

line protest

of argument that

that

the species

unreasonable

selectionist m i g h t

of me

base

combinatorial calculation on the assumption that the ten major trends in the evolution o f w h a l e s are i n d e p e n d e n t . S u r e l y the n u m b e r o f c o m b i n a t i o n s w e have to consider will be drastically reduced by correlations a m o n g the different t r e n d s ? I t i s i m p o r t a n t h e r e t o d i s t i n g u i s h t w o d i f f e r e n t s o u r c e s o f correlation,

which

may

called

incidental

correlation

and

adaptive

c o r r e l a t i o n . A n i n c i d e n t a l c o r r e l a t i o n i s a n i n t r i n s i c c o n s e q u e n c e o f t h e facts o f e m b r y o l o g y . F o r e x a m p l e , e l o n g a t i o n o f t h e left f o r e l e g i s u n l i k e l y t o b e independent o f e l o n g a t i o n o f the right foreleg. A n y m u t a t i o n that a c h i e v e s o n e i s i n t r i n s i c a l l y l i k e l y t o a c h i e v e t h e o t h e r s i m u l t a n e o u s l y . S l i g h t l y less obviously, the same m i g h t be partially true of e l o n g a t i o n of the forelegs a n d the h i n d l e g s . T h e r e a r e p r o b a b l y m a n y s i m i l a r c a s e s t h a t a r e less o b v i o u s still. An a d a p t i v e correlation, on the other h a n d , does not follow d i r ect l y from the m e c h a n i c s o f e m b r y o l o g y . A l i n e a g e t h a t m o v e s f r o m a t e r r e s t r i a l t o a n a q u a t i c e x i s t e n c e i s l i k e l y t o n e e d c h a n g e s t o its l o c o m o t o r y s y s t e m a n d its respiratory system, and there is no o b v i o u s reason to e x p e c t a n y intrinsic c o n n e c t i o n b e t w e e n t h e m . W h y should t r e n d s t h a t c o n v e r t w a l k i n g l i m b s t o flippers be intrinsically correlated w i t h trends to boost the efficiency of the l u n g s i n e x t r a c t i n g o x y g e n ? O f c o u r s e i t i s possible t h a t t w o s u c h c o a d a p t e d trends m i g h t b e c o r r e l a t e d a s a n i n c i d e n t a l c o n s e q u e n c e o f e m b r y o l o g i c a l

108

O r g a n i s m s , G r o u p s and M e m e s : Replicators or Vehicles?

mechanisms,

but

the

correlation

likely

to be positive

than

n e g a t i v e . W e are b a c k t o our c o m b i n a t o r i a l c a l c u l a t i o n , albeit w e must exercise care in counting our separate dimensions of change. F i n a l l y , the species selectionist m a y retreat and invoke ordinary low-level n a t u r a l selection to w e e d o u t i l l - c o a d a p t e d c o m b i n a t i o n s of c h a n g e , so that s p e c i a t i o n e v e n t s o n l y s e r v e u p a l r e a d y t r i e d a n d p r o v e d c o m b i n a t i o n s t o the s i e v e o f s p e c i e s s e l e c t i o n . B u t this ' s p e c i e s s e l e c t i o n i s t ' is, b y G o u l d ' s l i g h t s , n o species

selectionist

all!

has

conceded

that

all

the

interesting

e v o l u t i o n a r y c h a n g e results f r o m i n t e r - a l l e l e s e l e c t i o n a n d n o t f r o m i n t e r s p e c i e s s e l e c t i o n , a l b e i t i t m a y b e c o n c e n t r a t e d i n b r i e f bursts, p u n c t u a t i n g stasis. H e h a s c o n c e d e d t h e v i o l a t i o n o f W r i g h t ' s R u l e . A n d i f ' W r i g h t ' s R u l e ' n o w s e e m s u n f a i r l y e a s y t o v i o l a t e , t h a t i s w h a t I m e a n t w h e n I said t h a t G o u l d h a d s t u c k his n e c k o u t . I s h o u l d r e p e a t t h a t W r i g h t h i m s e l f i s n o t r e s p o n s i b l e for n a m i n g t h e r u l e . The

theory

of species a

selection,

equilibria,

stimulating

idea

dimensions

of quantitative c h a n g e

growing

which in

out

may

of that

well

of punctuated

explain

macroevolution.

some

would

single

be very

s u r p r i s e d i f i t c o u l d b e u s e d t o e x p l a i n t h e sort o f c o m p l e x m u l t i d i m e n s i o n a l a d a p t a t i o n t h a t I find i n t e r e s t i n g , t h e ' P a l e y ' s w a t c h ' , o r ' O r g a n s o f e x t r e m e Perfection a n d C o m p l i c a t i o n ' , kind of a d a p t a t i o n that seems to d e m a n d a s h a p i n g a g e n t a t l e a s t a s p o w e r f u l a s a d e i t y . R e p l i c a t o r s e l e c t i o n , w h e r e the replicators are alternative alleles,

m a y well be powerful

enough.

I f the

r e p l i c a t o r s a r e a l t e r n a t i v e species, h o w e v e r , I d o u b t if it is p o w e r f u l e n o u g h , b e c a u s e i t i s t o o s l o w . E l d r e d g e a n d C r a c r a f t ( 1 9 8 0 , p . 269) a p p e a r t o a g r e e : 'The

concept

reproduction roborated,

natural

selection

of individuals

within

within-population

(fitness

differences,

populations)

phenomenon,

appears

and

differential

constitutes

the

corbest

a v a i l a b l e e x p l a n a t i o n for t h e o r i g i n , m a i n t e n a n c e , a n d p o s s i b l e m o d i f i c a t i o n o f a d a p t a t i o n s . ' I f this i s i n d e e d t h e o p i n i o n o f ' p u n c t u a t i o n i s t s ' a n d ' s p e c i e s s e l e c t i o n i s t s ' g e n e r a l l y , i t i s h a r d t o see w h a t a l l t h e fuss i s a b o u t . F o r simplicity I h a v e discussed the theory of species selection as one in w h i c h the species is treated as a replicator. T h e reader will have noticed, however,

that

this

rather

speaking

of an

asexually

reproducing

o r g a n i s m a s a r e p l i c a t o r . E a r l i e r i n this c h a p t e r , w e s a w t h a t t h e test o f m u t i l a t i o n f o r c e s us s t r i c t l y to l i m i t t h e title of r e p l i c a t o r to t h e genome of, s a y , a s t i c k i n s e c t , n o t t h e s t i c k i n s e c t itself. S i m i l a r l y , i n t h e s p e c i e s s e l e c t i o n m o d e l , it is n o t t h e s p e c i e s t h a t is t h e r e p l i c a t o r b u t t h e gene-pool.

It is

t e m p t i n g , n o w , t o say, ' I n that case, w h y not g o the w h o l e h o g a n d regard the

gene

replicator

rather

than

some

larger

unit,

even

the

E l d r e d g e / G o u l d m o d e l ? ' T h e answer i s t h a t i f t h e y a r e r i g h t a b o u t a g e n e p o o l b e i n g a c o a d a p t e d unit, h o m e o s t a t i c a l l y buffered against c h a n g e , it m i g h t h a v e t h e s a m e k i n d o f r i g h t t o b e t r e a t e d a s a s i n g l e r e p l i c a t o r a s has t h e g e n o m e o f a s t i c k i n s e c t . T h e g e n e - p o o l h a s this r i g h t , h o w e v e r , o n l y i f i t

O r g a n i s m s , G r o u p s and M e m e s : R e p l i c a t o r s o r V e h i c l e s ?

109

is r e p r o d u c t i v e l y isolated, just as the g e n o m e has that right o n l y if it is reproduced asexually. E v e n then the right is a tenuous one. E a r l i e r i n this c h a p t e r , w e e s t a b l i s h e d t h a t a n o r g a n i s m i s d e f i n i t e l y n o t a r e p l i c a t o r , a l t h o u g h its g e n o m e m a y b e i f i t i s a s e x u a l l y r e p r o d u c e d . W e h a v e n o w s e e n t h a t t h e r e m a y b e a c a s e for r e g a r d i n g t h e g e n e - p o o l o f a reproductively isolated

g r o u p , such as a species,

as a replicator.

If we

p r o v i s i o n a l l y a c c e p t t h e l o g i c o f this c a s e , w e c a n v i s u a l i z e e v o l u t i o n d i r e c t e d b y s e l e c t i o n a m o n g s u c h r e p l i c a t o r s , b u t I h a v e j u s t c o n c l u d e d t h a t this k i n d of selection is unlikely to explain c o m p l e x a d a p t a t i o n . A p a r t from the small genetic fragment, w h i c h we discussed in the previous c h a p t e r , are there a n y o t h e r p l a u s i b l e c a n d i d a t e s for t h e title o f r e p l i c a t o r ? I h a v e p r e v i o u s l y s u p p o r t e d t h e c a s e for a c o m p l e t e l y n o n - g e n e t i c k i n d o f replicator, w h i c h flourishes o n l y i n the e n v i r o n m e n t p r o v i d e d b y c o m p l e x , communicating

brains.

called

the

'meme'

(Dawkins

1976a).

Unfortunately, unlike C l o a k (1975) but, if I understand t h e m aright, like L u m s d e n and W i l s o n (1980), I w a s insufficiently c l e a r a b o u t the distinction b e t w e e n the m e m e itself, a s r e p l i c a t o r , o n t h e o n e h a n d , a n d its ' p h e n o t y p i c effects' o r ' m e m e p r o d u c t s ' o n t h e o t h e r . A m e m e s h o u l d b e r e g a r d e d a s a unit of information residing in a brain ( C l o a k ' s ' i - c u l t u r e ' ) . It has a definite s t r u c t u r e , r e a l i z e d i n w h a t e v e r p h y s i c a l m e d i u m t h e b r a i n uses for s t o r i n g information.

the

brain

stores

information

pattern

of synaptic

c o n n e c t i o n s , a m e m e s h o u l d in p r i n c i p l e be v i s i b l e u n d e r a m i c r o s c o p e as a definite

pattern

of synaptic

structure.

If the

b r a i n stores

information

'distributed' form (Pribram 1974), the m e m e w o u l d not be l o c a l i z a b l e on a m i c r o s c o p e s l i d e , b u t still I w o u l d w a n t t o r e g a r d i t a s p h y s i c a l l y r e s i d i n g i n t h e b r a i n . T h i s i s t o d i s t i n g u i s h i t f r o m its p h e n o t y p i c effects, w h i c h a r e its consequences in the outside w o r l d ( C l o a k ' s ' m - c u l t u r e ' ) . T h e p h e n o t y p i c effects o f a m e m e m a y b e i n t h e f o r m o f w o r d s , m u s i c , v i s u a l i m a g e s , s t y l e s o f c l o t h e s , f a c i a l o r h a n d g e s t u r e s , skills s u c h a s o p e n i n g m i l k b o t t l e s i n tits, o r p a n n i n g w h e a t i n J a p a n e s e m a c a q u e s . T h e y a r e t h e o u t w a r d and visible (audible, etc.) manifestations of the m e m e s w i t h i n the b r a i n . T h e y m a y b e p e r c e i v e d b y t h e sense o r g a n s o f o t h e r i n d i v i d u a l s , a n d t h e y m a y s o i m p r i n t t h e m s e l v e s o n the b r a i n s o f t h e r e c e i v i n g i n d i v i d u a l s that a c o p y (not necessarily e x a c t ) of the o r i g i n a l m e m e is g r a v e n in the receiving brain. T h e n e w c o p y of the m e m e is then in a position to b r o a d c a s t its p h e n o t y p i c effects, w i t h t h e r e s u l t t h a t f u r t h e r c o p i e s o f i t s e l f m a y b e m a d e in yet other brains. R e t u r n i n g , for c l a r i f i c a t i o n ,

to D N A as our archetypal replicator,

its

consequences on the w o r l d are of t w o i m p o r t a n t types. Firstly, it m a k e s c o p i e s o f itself,

m a k i n g use o f t h e c e l l u l a r a p p a r a t u s

of replicases,

etc.

S e c o n d l y , i t h a s effects o n t h e o u t s i d e w o r l d , w h i c h i n f l u e n c e t h e c h a n c e s o f its c o p i e s ' s u r v i v i n g . T h e f i r s t o f these t w o effects c o r r e s p o n d s t o t h e m e m e ' s use o f t h e a p p a r a t u s o f i n t e r - i n d i v i d u a l

communication

and

imitation

O r g a n i s m s , G r o u p s and M e m e s : R e p l i c a t o r s o r V e h i c l e s ?

m a k e c o p i e s o f itself. I f i n d i v i d u a l s l i v e i n a s o c i a l c l i m a t e i n w h i c h i m i t a t i o n i s c o m m o n , this c o r r e s p o n d s t o a c e l l u l a r c l i m a t e r i c h i n e n z y m e s for c o p y i n g DNA. B u t w h a t a b o u t t h e s e c o n d k i n d o f effect o f D N A , t h e k i n d c o n v e n t i o n a l l y c a l l e d ' p h e n o t y p i c ' ? H o w d o a m e m e ' s p h e n o t y p i c effects c o n t r i b u t e t o its s u c c e s s o r f a i l u r e i n b e i n g r e p l i c a t e d ? T h e a n s w e r i s t h e s a m e a s for the g e n e t i c r e p l i c a t o r . A n y effect t h a t a m e m e h a s o n t h e b e h a v i o u r o f a b o d y b e a r i n g it m a y influence that m e m e ' s c h a n c e of surviving. A m e m e that m a d e its b o d i e s r u n o v e r cliffs w o u l d h a v e a fate l i k e t h a t o f a g e n e for m a k i n g its b o d i e s r u n o v e r cliffs. I t w o u l d t e n d t o b e e l i m i n a t e d from the m e m e - p o o l . B u t j u s t as p r o m o t i n g b o d i l y s u r v i v a l is only part of w h a t constitutes s u c c e s s i n g e n e t i c r e p l i c a t o r s , s o t h e r e a r e m a n y o t h e r w a y s i n w h i c h m e m e s m a y w o r k p h e n o t y p i c a l l y for t h e i r o w n p r e s e r v a t i o n . I f t h e p h e n o t y p i c effect of a m e m e is a t u n e , t h e c a t c h i e r it is t h e m o r e l i k e l y it is to be c o p i e d . If i t i s a s c i e n t i f i c i d e a , its c h a n c e s o f s p r e a d i n g t h r o u g h t h e w o r l d ' s scientific b r a i n s w i l l b e i n f l u e n c e d b y its c o m p a t i b i l i t y w i t h t h e a l r e a d y e s t a b l i s h e d c o r p u s o f i d e a s . I f i t i s a p o l i t i c a l o r r e l i g i o u s i d e a , i t m a y assist its o w n surv i v a l i f o n e o f its p h e n o t y p i c effects i s t o m a k e its b o d i e s v i o l e n t l y i n t o l e r a n t o f n e w a n d u n f a m i l i a r i d e a s . A m e m e h a s its o w n o p p o r t u n i t i e s for r e p l i c a t i o n , a n d its o w n p h e n o t y p i c effects, a n d t h e r e i s n o r e a s o n w h y s u c c e s s i n a m e m e should h a v e a n y c o n n e c t i o n w h a t e v e r with genetic success. T h i s is r e g a r d e d by m a n y of my biological correspondents as the weakest point in the w h o l e m e m e theory (Greene

1 9 7 8 ; A l e x a n d e r 1980, p . 7 8 ;

S t a d d o n i n p r e s s ) . I d o n ' t see t h e p r o b l e m ; o r , r a t h e r , I d o see t h e p r o b l e m b u t I d o n ' t t h i n k i t i s a n y g r e a t e r for m e m e s a s r e p l i c a t o r s t h a n i t i s for g e n e s . T i m e and again, my sociobiological colleagues have upbraided me as a t u r n c o a t , b e c a u s e I w i l l n o t a g r e e w i t h t h e m t h a t t h e ultimate c r i t e r i o n for the s u c c e s s o f a m e m e m u s t b e its c o n t r i b u t i o n t o D a r w i n i a n 'fitness'. A t b o t t o m , t h e y insist, a ' g o o d m e m e ' s p r e a d s b e c a u s e b r a i n s a r e r e c e p t i v e t o it, a n d the receptiveness of brains is ultimately shaped by (genetic) natural selection. T h e v e r y fact that a n i m a l s i m i t a t e other a n i m a l s a t all must u l t i m a t e l y b e explicable in terms of their D a r w i n i a n fitness. B u t t h e r e i s n o t h i n g m a g i c a b o u t D a r w i n i a n f i t n e s s i n t h e g e n e t i c sense. T h e r e is no l a w g i v i n g it priority as the f u n d a m e n t a l q u a n t i t y that is m a x i m i z e d . F i t n e s s i s j u s t a w a y o f t a l k i n g a b o u t the s u r v i v a l o f r e p l i c a t o r s , i n this c a s e g e n e t i c r e p l i c a t o r s . I f a n o t h e r k i n d o f e n t i t y arises, w h i c h a n s w e r s to

the definition of an

replicator that

active germ-line replicator,

w o r k for t h e i r o w n

survival

will

variants of the n e w

tend

become more

numerous. To be consistent, we could invent a new kind of 'individual f i t n e s s ' , w h i c h m e a s u r e d t h e s u c c e s s o f a n i n d i v i d u a l i n p r o p a g a t i n g his memes. I t is, o f c o u r s e , t r u e t h a t ' M e m e s a r e u t t e r l y d e p e n d e n t u p o n g e n e s , b u t g e n e s c a n exist a n d c h a n g e q u i t e i n d e p e n d e n t l y o f m e m e s ' ( B o n n e r 1980).

O r g a n i s m s , Groups and M e m e s : Replicators or Vehicles? 111

B u t this d o e s n o t m e a n

that the ultimate

c r i t e r i o n for s u c c e s s i n m e m e

selection is g e n e survival. It does not m e a n that success goes to those m e m e s t h a t f a v o u r t h e g e n e s o f t h e i n d i v i d u a l s b e a r i n g t h e m . T o b e s u r e , this w i l l s o m e t i m e s b e so. O b v i o u s l y a m e m e t h a t c a u s e s i n d i v i d u a l s b e a r i n g i t t o k i l l t h e m s e l v e s h a s a g r a v e d i s a d v a n t a g e , b u t n o t n e c e s s a r i l y a f a t a l o n e . J u s t as a g e n e for s u i c i d e s o m e t i m e s s p r e a d s i t s e l f b y a r o u n d a b o u t r o u t e ( e . g . i n s o c i a l insect workers, or p a r e n t a l sacrifice), so a suicidal m e m e c a n s p r e a d , as w h e n a d r a m a t i c a n d w e l l - p u b l i c i z e d m a r t y r d o m i n s p i r e s o t h e r s t o d i e for a d e e p l y l o v e d c a u s e , a n d this i n t u r n i n s p i r e s o t h e r s t o d i e , a n d s o o n ( V i d a l 1 9 5 5 ) . It is true that the relative survival success of a m e m e will d e p e n d critically o n t h e s o c i a l a n d b i o l o g i c a l c l i m a t e i n w h i c h i t f i n d s itself, a n d this c l i m a t e will certainly be influenced by the genetic m a k e - u p of the population. B u t it w i l l a l s o d e p e n d o n the m e m e s t h a t a r e a l r e a d y n u m e r o u s i n t h e m e m e - p o o l . Genetic

evolutionists

are

already

happy

with

the

idea

that

the

relative

success o f t w o a l l e l e s c a n d e p e n d u p o n w h i c h g e n e s a t o t h e r l o c i d o m i n a t e the g e n e - p o o l , a n d I h a v e a l r e a d y m e n t i o n e d this i n c o n n e c t i o n w i t h t h e evolution o f ' c o a d a p t e d g e n o m e s ' . T h e statistical structure o f the g e n e - p o o l sets u p a c l i m a t e o r e n v i r o n m e n t w h i c h affects t h e s u c c e s s o f a n y o n e g e n e r e l a t i v e t o its a l l e l e s . A g a i n s t o n e g e n e t i c b a c k g r o u n d o n e a l l e l e m a y b e f a v o u r e d ; a g a i n s t a n o t h e r g e n e t i c b a c k g r o u n d its a l l e l e m a y b e f a v o u r e d . For e x a m p l e , if the g e n e - p o o l is d o m i n a t e d by genes that m a k e a n i m a l s seek dry places,

this w i l l set u p s e l e c t i o n p r e s s u r e s i n f a v o u r o f g e n e s for a n

i m p e r m e a b l e s k i n . B u t a l l e l e s for a m o r e p e r m e a b l e s k i n w i l l b e f a v o u r e d i f the g e n e - p o o l h a p p e n s t o b e d o m i n a t e d b y g e n e s for s e e k i n g d a m p p l a c e s . The

point

the

obvious

one

that

selection

any

one

locus

not

independent of selection at other loci. O n c e a lineage begins e v o l v i n g in a p a r t i c u l a r d i r e c t i o n , m a n y l o c i w i l l fall i n t o s t e p , a n d t h e r e s u l t i n g p o s i t i v e feedbacks will tend to p r o p e l the lineage in the s a m e direction, in spite of pressures f r o m t h e o u t s i d e w o r l d . A n i m p o r t a n t a s p e c t o f t h e e n v i r o n m e n t w h i c h selects b e t w e e n a l l e l e s a t a n y o n e l o c u s w i l l b e t h e g e n e s t h a t a l r e a d y d o m i n a t e the g e n e - p o o l a t o t h e r l o c i . Similarly, an important aspect of selection on a n y one m e m e will be the other

memes

that

already

happen

dominate

the

meme-pool

(Wilson

1 9 7 5 ) . I f the society i s a l r e a d y d o m i n a t e d b y M a r x i s t , o r N a z i m e m e s , a n y n e w m e m e ' s r e p l i c a t i o n s u c c e s s w i l l b e i n f l u e n c e d b y its c o m p a t i b i l i t y w i t h this e x i s t i n g b a c k g r o u n d . P o s i t i v e f e e d b a c k s w i l l p r o v i d e a m o m e n t u m w h i c h can carry meme-based evolution in directions unconnected with, or even contradictory

to,

the

directions

that

would

favoured

gene-based

evolution. I agree w i t h P u l l i a m and D u n f o r d (1980) that cultural e v o l u t i o n ' o w e s its o r i g i n a n d its r u l e s t o g e n e t i c e v o l u t i o n , b u t i t h a s a m o m e n t u m a l l its o w n ' . There

are,

of course,

significant

gene-based selection processes

differences

(Cavalli-Sforza

between &

meme-based

Feldman

1973,

and

1981).

112

O r g a n i s m s , G r o u p s and M e m e s : R e p l i c a t o r s o r V e h i c l e s ?

M e m e s are not strung out a l o n g linear c h r o m o s o m e s , a n d it is not clear that t h e y o c c u p y a n d c o m p e t e for d i s c r e t e ' l o c i ' , o r t h a t t h e y h a v e i d e n t i f i a b l e 'alleles'. P r e s u m a b l y , as in the case of genes, we c a n strictly only talk a b o u t p h e n o t y p i c effects i n t e r m s o f d i f f e r e n c e s , e v e n i f w e j u s t m e a n t h e d i f f e r e n c e b e t w e e n the b e h a v i o u r p r o d u c e d by a brain c o n t a i n i n g the m e m e a n d that of a b r a i n n o t c o n t a i n i n g it. T h e c o p y i n g p r o c e s s i s p r o b a b l y m u c h less p r e c i s e than in the case of g e n e s : there m a y be a certain 'mutational' element in e v e r y c o p y i n g e v e n t , a n d this, b y t h e w a y , i s a l s o t r u e o f t h e ' s p e c i e s selection' discussed earlier in the c h a p t e r . M e m e s m a y partially blend with e a c h other in a w a y that genes do not. N e w 'mutations' m a y be 'directed' rather than r a n d o m w i t h respect to evolutionary trends. T h e equivalent of Weismannism

less

rigid

for

memes

than

for

genes:

there

may

' L a m a r c k i a n ' c a u s a l a r r o w s l e a d i n g from p h e n o t y p e to replicator, as well as t h e o t h e r w a y a r o u n d . T h e s e d i f f e r e n c e s m a y p r o v e sufficient t o r e n d e r the analogy

with

genetic

natural

selection

worthless

even

positively

m i s l e a d i n g . M y o w n f e e l i n g i s t h a t its m a i n v a l u e m a y lie n o t s o m u c h i n helping us to understand h u m a n culture as in sharpening our perception of genetic natural selection. T h i s is the only reason I am presumptuous enough t o d i s c u s s it, for I d o n o t k n o w n e n o u g h a b o u t t h e e x i s t i n g l i t e r a t u r e o n h u m a n c u l t u r e t o m a k e a n a u t h o r i t a t i v e c o n t r i b u t i o n t o it. W h a t e v e r t h e c l a i m s o f m e m e s t o b e r e g a r d e d a s r e p l i c a t o r s i n the s a m e sense a s g e n e s ,

t h e f i r s t p a r t o f this c h a p t e r e s t a b l i s h e d

that individual

organisms are not replicators. Nevertheless, they are obviously functional units of g r e a t i m p o r t a n c e , a n d it is n o w necessary to establish e x a c t l y w h a t t h e i r r o l e is. I f t h e o r g a n i s m i s n o t a r e p l i c a t o r , w h a t i s i t ? T h e a n s w e r i s t h a t it is a c o m m u n a l vehicle for r e p l i c a t o r s . A v e h i c l e is an e n t i t y in w h i c h replicators (genes a n d m e m e s ) travel a b o u t , an entity whose attributes are a f f e c t e d b y t h e r e p l i c a t o r s i n s i d e it, a n e n t i t y w h i c h m a y b e seen a s a c o m p o u n d tool of replicator p r o p a g a t i o n . B u t i n d i v i d u a l organisms are not t h e o n l y e n t i t i e s t h a t m i g h t b e r e g a r d e d a s v e h i c l e s i n this sense. T h e r e i s a h i e r a r c h y of entities e m b e d d e d in larger entities, a n d in theory the c o n c e p t of v e h i c l e m i g h t b e a p p l i e d t o a n y level o f the h i e r a r c h y . T h e concept of hierarchy is a generally important one. Chemists believe t h a t m a t t e r i s m a d e o f a b o u t a h u n d r e d different k i n d s o f a t o m s , i n t e r a c t i n g w i t h e a c h other by m e a n s of their electrons. A t o m s are gregarious, forming h u g e assemblages w h i c h are g o v e r n e d by laws at their o w n level. W i t h o u t c o n t r a d i c t i n g the laws of chemistry, therefore, we find it convenient to ignore atoms w h e n we are thinking about large lumps of matter. W h e n explaining t h e w o r k i n g s o f a m o t o r c a r w e f o r g e t a t o m s a n d v a n d e r W a a l ' s forces a s units of e x p l a n a t i o n , a n d prefer to talk of cylinders and sparking plugs. T h i s lesson a p p l i e s n o t j u s t t o t h e t w o l e v e l s o f a t o m s a n d c y l i n d e r h e a d s . T h e r e i s a h i e r a r c h y , r a n g i n g from f u n d a m e n t a l particles b e l o w the a t o m i c level up

O r g a n i s m s , G r o u p s and M e m e s : Replicators or V e h i c l e s ?

through

molecules

and

crystals

the

macroscopic

chunks

113

which

our

u n a i d e d sense o r g a n s a r e b u i l t t o a p p r e c i a t e . Living matter introduces complexity:

a w h o l e n e w set o f r u n g s

the

ladder of

m a c r o m o l e c u l e s folding themselves into their tertiary forms,

intracellular membranes and organelles, populations,

communities

and

cells,

ecosystems.

tissues, o r g a n s , o r g a n i s m s , similar

hierarchy

of units

e m b e d d e d in larger units e p i t o m i z e s the c o m p l e x artificial p r o d u c t s of l i v i n g thingsâ&#x20AC;&#x201D;semiconductor crystals,

transistors,

integrated

circuits,

computers

and e m b e d d e d units that c a n o n l y b e u n d e r s t o o d i n terms o f 'software'. A t every level the units interact w i t h e a c h other f o l l o w i n g laws a p p r o p r i a t e to that level, l a w s w h i c h are not c o n v e n i e n t l y r e d u c i b l e to l a w s at l o w e r levels. T h i s has all b e e n said m a n y times before, a n d is so o b v i o u s as to be a l m o s t platitudinous. B u t one sometimes has to repeat platitudes in o r d e r to p r o v e that one's heart is in the right p l a c e ! E s p e c i a l l y if o n e wishes to e m p h a s i z e a s l i g h t l y u n c o n v e n t i o n a l sort o f h i e r a r c h y , for this m a y b e m i s t a k e n for a ' r e d u c t i o n i s t ' a t t a c k o n t h e i d e a o f h i e r a r c h y itself. R e d u c t i o n i s m i s a d i r t y word,

and

fashionable.

kind I

of 'holistier than

enthusiastically

thou'

self-righteousness

this

fashion

when

has

talking

become about

mechanisms within individual bodies, and have a d v o c a t e d 'neuro-economic' and

'software'

explanations

neurophysiological ones approach

of behaviour

(Dawkins

1976b).

to individual development.

preference

conventional

I w o u l d favour an analogous

B u t there

are

times

w h e n holistic

p r e a c h i n g b e c o m e s a n e a s y s u b s t i t u t e for t h o u g h t , a n d I b e l i e v e t h e d i s p u t e a b o u t u n i t s o f s e l e c t i o n p r o v i d e s e x a m p l e s o f this. T h e n e o - W e i s m a n n i s t v i e w o f life w h i c h this b o o k a d v o c a t e s l a y s stress o n the g e n e t i c r e p l i c a t o r a s a f u n d a m e n t a l u n i t o f e x p l a n a t i o n . I b e l i e v e i t h a s an atom-like role to p l a y in functional, t e l e o n o m i c e x p l a n a t i o n . If we wish to s p e a k o f a d a p t a t i o n s a s b e i n g 'for t h e g o o d o f s o m e t h i n g , t h a t s o m e t h i n g i s the a c t i v e , g e r m - l i n e r e p l i c a t o r . T h i s i s a s m a l l c h u n k o f D N A , a s i n g l e ' g e n e ' a c c o r d i n g to some definitions of the w o r d . B u t I am of course not s u g g e s t i n g that small genetic units w o r k in isolation from e a c h other, a n y m o r e than a chemist thinks that atoms d o . L i k e atoms, genes are h i g h l y g r e g a r i o u s . T h e y a r e often s t r u n g t o g e t h e r a l o n g c h r o m o s o m e s , c h r o m o s o m e s a r e w r a p p e d u p in groups in nuclear membranes, enveloped in cytoplasm and enclosed in cell m e m b r a n e s . C e l l s too are n o r m a l l y not isolated, b u t c l o n e d to form the h u g e conglomerates we k n o w as organisms. We are n o w p l u g g e d into the familiar e m b e d d e d hierarchy, and need go no further. F u n c t i o n a l l y s p e a k i n g , too, g e n e s a r e g r e g a r i o u s . T h e y h a v e p h e n o t y p i c effects o n b o d i e s , b u t t h e y d o n o t d o s o i n i s o l a t i o n . I stress this o v e r a n d o v e r a g a i n i n this b o o k . T h e r e a s o n I m a y s o u n d r e d u c t i o n i s t i c i s t h a t I insist o n a n a t o m i s t i c v i e w o f units o f s e l e c t i o n , i n t h e sense o f t h e u n i t s t h a t a c t u a l l y s u r v i v e o r fail t o

O r g a n i s m s , G r o u p s and M e m e s : Replicators or Vehicles?

114

s u r v i v e , w h i l e b e i n g w h o l e - h e a r t e d l y i n t e r a c t i o n i s t w h e n i t c o m e s t o the d e v e l o p m e n t o f t h e p h e n o t y p i c means b y w h i c h t h e y s u r v i v e : Of course

true

that

the

phenotypic

effect

of a

gene

m e a n i n g l e s s c o n c e p t o u t s i d e t h e c o n t e x t o f m a n y , o r e v e n a l l , o f the o t h e r g e n e s i n t h e g e n o m e . Y e t , h o w e v e r c o m p l e x a n d i n t r i c a t e the o r g a n i s m m a y be, h o w e v e r m u c h w e m a y a g r e e that the organism i s a u n i t of function, selection.

Genes

I still t h i n k it is m i s l e a d i n g to c a l l it a u n i t of may

interact,

even

"blend",

their

effects

e m b r y o n i c d e v e l o p m e n t , as m u c h as y o u please. But they do not b l e n d w h e n it c o m e s to b e i n g passed on to future generations. I am n o t t r y i n g to belittle the i m p o r t a n c e of the i n d i v i d u a l p h e n o t y p e in e v o l u t i o n . I a m m e r e l y t r y i n g t o sort o u t e x a c t l y w h a t its r o l e is. I t i s t h e a l l i m p o r t a n t i n s t r u m e n t of r e p l i c a t o r p r e s e r v a t i o n : it is not t h a t w h i c h is preserved [Dawkins 1978a, p. 69].

I n this b o o k I a m u s i n g t h e w o r d ' v e h i c l e ' for a n i n t e g r a t e d a n d c o h e r e n t 'instrument of replicator preservation'. A v e h i c l e is a n y unit, discrete e n o u g h to seem w o r t h n a m i n g , w h i c h houses a c o l l e c t i o n o f r e p l i c a t o r s a n d w h i c h w o r k s a s a u n i t for t h e p r e s e r v a t i o n a n d p r o p a g a t i o n of t h o s e r e p l i c a t o r s . I r e p e a t , a v e h i c l e is n o t a r e p l i c a t o r . A r e p l i c a t o r ' s s u c c e s s i s m e a s u r e d b y its c a p a c i t y t o s u r v i v e i n t h e f o r m o f c o p i e s . A v e h i c l e ' s s u c c e s s i s m e a s u r e d b y its c a p a c i t y t o p r o p a g a t e t h e r e p l i c a t o r s t h a t r i d e i n s i d e it. T h e o b v i o u s a n d a r c h e t y p a l v e h i c l e i s t h e i n d i v i d u a l o r g a n i s m , b u t this m a y n o t b e t h e o n l y l e v e l i n t h e h i e r a r c h y o f life a t w h i c h t h e title i s a p p l i c a b l e . W e c a n e x a m i n e a s c a n d i d a t e v e h i c l e s c h r o m o s o m e s a n d cells b e l o w the o r g a n i s m level, g r o u p s a n d c o m m u n i t i e s a b o v e it. A t a n y l e v e l , i f a v e h i c l e i s d e s t r o y e d , a l l t h e r e p l i c a t o r s inside i t w i l l b e d e s t r o y e d . N a t u r a l s e l e c t i o n w i l l t h e r e f o r e , a t least t o s o m e e x t e n t , f a v o u r r e p l i c a t o r s t h a t c a u s e t h e i r v e h i c l e s t o resist b e i n g d e s t r o y e d . p r i n c i p l e this c o u l d

a p p l y to g r o u p s of o r g a n i s m s as w e l l as to single

o r g a n i s m s , for i f a g r o u p i s d e s t r o y e d a l l t h e g e n e s i n s i d e i t a r e d e s t r o y e d t o o . V e h i c l e survival i s o n l y p a r t o f t h e s t o r y , h o w e v e r . R e p l i c a t o r s t h a t w o r k for t h e ' r e p r o d u c t i o n ' o f v e h i c l e s a t v a r i o u s l e v e l s m i g h t t e n d t o d o b e t t e r t h a n r i v a l r e p l i c a t o r s t h a t w o r k m e r e l y for v e h i c l e s u r v i v a l . R e p r o d u c t i o n a t the

organism

level

familiar

enough

need

further

discussion.

R e p r o d u c t i o n at the g r o u p level is more problematic. In principle a group m a y b e s a i d t o h a v e r e p r o d u c e d i f i t s e n d s off a ' p r o p a g u l e ' , s a y a b a n d o f y o u n g o r g a n i s m s w h o g o o u t a n d found a n e w g r o u p . T h e i d e a o f a nested h i e r a r c h y of levels at w h i c h selection m i g h t take p l a c e â&#x20AC;&#x201D; v e h i c l e selection in my termsâ&#x20AC;&#x201D;is e m p h a s i z e d in W i l s o n ' s (1975) c h a p t e r on g r o u p selection (e.g. his f i g u r e 5 - 1 ) . I h a v e p r e v i o u s l y g i v e n r e a s o n s for s h a r i n g i n t h e g e n e r a l s c e p t i c i s m a b o u t

O r g a n i s m s , G r o u p s and M e m e s : R e p l i c a t o r s o r V e h i c l e s ?

115

' g r o u p selection' a n d selection at other h i g h levels, a n d n o t h i n g in the recent l i t e r a t u r e t e m p t s m e t o c h a n g e m y m i n d . B u t t h a t i s n o t t h e p o i n t a t issue here. T h e point here is that we must be clear a b o u t the difference b e t w e e n those t w o d i s t i n c t k i n d s o f c o n c e p t u a l u n i t s , r e p l i c a t o r s a n d v e h i c l e s . I h a v e s u g g e s t e d t h a t t h e best w a y o f u n d e r s t a n d i n g E l d r e d g e a n d G o u l d ' s t h e o r y o f ' s p e c i e s s e l e c t i o n ' i s i n t e r m s o f s p e c i e s a s replicators. B u t t h e m a j o r i t y o f models ordinarily called ' g r o u p selection', i n c l u d i n g all those r e v i e w e d by W i l s o n ( 1 9 7 5 ) , a n d most o f those r e v i e w e d b y W a d e ( 1 9 7 8 ) , are i m p l i c i t l y t r e a t i n g g r o u p s a s v e h i c l e s . T h e e n d result o f t h e s e l e c t i o n d i s c u s s e d i s a c h a n g e i n g e n e f r e q u e n c i e s , for e x a m p l e a n i n c r e a s e o f ' a l t r u i s t i c g e n e s ' a t t h e e x p e n s e o f 'selfish g e n e s ' .

I t i s still g e n e s t h a t a r e r e g a r d e d a s t h e

r e p l i c a t o r s w h i c h a c t u a l l y s u r v i v e (or fail t o s u r v i v e ) a s a c o n s e q u e n c e o f t h e (vehicle) selection process. A s for g r o u p s e l e c t i o n itself, m y p r e j u d i c e i s t h a t i t h a s s o a k e d u p m o r e t h e o r e t i c a l i n g e n u i t y t h a n its b i o l o g i c a l i n t e r e s t w a r r a n t s . I a m i n f o r m e d b y the e d i t o r o f a l e a d i n g m a t h e m a t i c s j o u r n a l t h a t h e i s c o n t i n u a l l y p l a g u e d b y ingenious papers p u r p o r t i n g to h a v e s q u a r e d the circle. S o m e t h i n g a b o u t the fact t h a t this h a s b e e n p r o v e d t o b e i m p o s s i b l e i s s e e n a s a n i r r e s i s t i b l e challenge

certain

type

of intellectual

dilettante.

Perpetual

motion

m a c h i n e s h a v e a s i m i l a r f a s c i n a t i o n for s o m e a m a t e u r i n v e n t o r s . T h e c a s e o f group

selection

hardly

analogous:

has

never

been

proved

i m p o s s i b l e , a n d n e v e r c o u l d b e . N e v e r t h e l e s s , I h o p e I m a y b e f o r g i v e n for w o n d e r i n g w h e t h e r part of g r o u p selection's e n d u r i n g r o m a n t i c a p p e a l stems from the a u t h o r i t a t i v e h a m m e r i n g t h e t h e o r y h a s r e c e i v e d e v e r s i n c e W y n n e E d w a r d s (1962) did us the v a l u a b l e service of b r i n g i n g it out into the open. Anti-group

selectionism

has

been

embraced

orthodox, and, as M a y n a r d Smith

(1976a)

notes,

the

establishment

'It is in the nature of

science that o n c e a position b e c o m e s o r t h o d o x it should be subjected to c r i t i c i s m . . . ' T h i s is, n o d o u b t , h e a l t h y , b u t M a y n a r d S m i t h d r i l y g o e s o n : 'It does not follow that, b e c a u s e a position is o r t h o d o x , it is w r o n g . . . ' M o r e generous recent treatments of g r o u p selection are g i v e n by G i l p i n ( 1 9 7 5 ) , E. O. Wilson (1975), W a d e (1978), Boorman and Levitt (1980), and D. S. W i l s o n ( 1 9 8 0 , b u t see c r i t i c i s m b y G r a f e n 1 9 8 0 , i n p r e s s ) . I am not g o i n g to go a g a i n into the d e b a t e o v e r g r o u p selection versus i n d i v i d u a l s e l e c t i o n . T h i s i s b e c a u s e t h e m a i n p u r p o s e o f this b o o k i s t o d r a w attention to the weaknesses of the w h o l e v e h i c l e c o n c e p t , w h e t h e r the v e h i c l e is an individual organism or a g r o u p .

S i n c e e v e n the staunchest g r o u p

s e l e c t i o n i s t w o u l d a g r e e t h a t t h e i n d i v i d u a l o r g a n i s m i s a far m o r e c o h e r e n t and

important

'unit of selection',

shall c o n c e n t r a t e my a t t a c k on

the

individual organism as my representative vehicle, rather than on the g r o u p . T h e case against the g r o u p should b e strengthened b y default. It m a y seem that I h a v e invented my o w n c o n c e p t , the v e h i c l e , as an A u n t S a l l y t o b e e a s i l y k n o c k e d d o w n . T h i s i s n o t so. I s i m p l y use t h e n a m e v e h i c l e

116

O r g a n i s m s , G r o u p s and M e m e s : Replicators or Vehicles?

to g i v e expression to a c o n c e p t w h i c h is f u n d a m e n t a l to the p r e d o m i n a n t orthodox

approach

natural

selection.

admitted

that,

some

f u n d a m e n t a l s e n s e , n a t u r a l s e l e c t i o n consists i n t h e d i f f e r e n t i a l s u r v i v a l o f g e n e s (or l a r g e r g e n e t i c r e p l i c a t o r s ) . B u t g e n e s a r e n o t n a k e d , t h e y w o r k t h r o u g h b o d i e s (or g r o u p s , e t c . ) . A l t h o u g h t h e u l t i m a t e u n i t o f s e l e c t i o n m a y i n d e e d be the genetic replicator, the p r o x i m a l unit of selection is usually regarded as something larger, usually an individual organism. T h u s M a y r (1963) d e v o t e s a w h o l e c h a p t e r to d e m o n s t r a t i n g the functional c o h e r e n c e of the w h o l e g e n o m e of an i n d i v i d u a l o r g a n i s m . I shall discuss M a y r ' s points in d e t a i l i n C h a p t e r 1 3 . F o r d ( 1 9 7 5 , p . 185) d i s d a i n f u l l y w r i t e s o f f t h e ' e r r o r ' that 'the unit of selection is the g e n e , w h e r e a s it is the i n d i v i d u a l ' . G o u l d (1977b) says:

S e l e c t i o n s i m p l y c a n n o t see g e n e s a n d p i c k a m o n g t h e m d i r e c t l y . I t must use bodies as an i n t e r m e d i a r y . A g e n e is a bit of D N A hidden w i t h i n a cell. S e l e c t i o n views bodies. It favors some bodies because they are stronger, better insulated, earlier in their sexual maturation, fiercer in c o m b a t , or m o r e b e a u t i f u l to b e h o l d . . . If, in f a v o r i n g a s t r o n g e r b o d y , s e l e c t i o n a c t e d d i r e c t l y u p o n a g e n e for s t r e n g t h , t h e n D a w k i n s might be vindicated. If bodies were u n a m b i g u o u s maps of t h e i r g e n e s , t h e n b a t t l i n g bits o f D N A w o u l d d i s p l a y t h e i r c o l o r s e x t e r n a l l y a n d selection m i g h t act u p o n t h e m directly. B u t bodies are no

such

t h i n g . . . Bodies

cannot

atomized

into

parts,

each

constructed by an individual gene. Hundreds of genes contribute to the b u i l d i n g of most b o d y parts and their action is channeled through a k a l e i d o s c o p i c series o f e n v i r o n m e n t a l i n f l u e n c e s :

embryonic and

postnatal, internal and external.

N o w i f this w e r e r e a l l y a g o o d a r g u m e n t , i t w o u l d b e a n a r g u m e n t a g a i n s t t h e w h o l e o f M e n d e l i a n g e n e t i c s , j u s t a s m u c h a s a g a i n s t t h e i d e a o f the g e n e as the unit of selection. T h e L a m a r c k i a n fanatic H. G. C a n n o n , indeed, e x p l i c i t l y uses i t a s s u c h : ' A l i v i n g b o d y i s n o t s o m e t h i n g i s o l a t e d , n e i t h e r i s i t a c o l l e c t i o n of p a r t s as D a r w i n e n v i s a g e d it, l i k e , as I h a v e s a i d b e f o r e , so m a n y m a r b l e s in a b o x . T h a t is the t r a g e d y of m o d e r n genetics. T h e devotees of the n e o - M e n d e l i a n hypothesis regard the o r g a n i s m as so m a n y characters c o n t r o l l e d b y s o m a n y g e n e s . S a y w h a t t h e y like a b o u t p o l y g e n e s â&#x20AC;&#x201D; t h a t i s t h e essence of their fantastic hypothesis' ( C a n n o n 1959, p. 1 3 1 ) . Most

people

would

agree

that

this

not

good

argument

against

M e n d e l i a n g e n e t i c s , a n d n o m o r e i s i t a g o o d a r g u m e n t a g a i n s t t r e a t i n g the g e n e as the unit of selection. T h e mistake w h i c h both G o u l d and C a n n o n m a k e i s t h a t t h e y fail t o d i s t i n g u i s h g e n e t i c s f r o m e m b r y o l o g y . M e n d e l i s m i s a

theory

particulate

inheritance,

not

particulate

embryology.

The

a r g u m e n t of C a n n o n and G o u l d is a valid argument against particulate

O r g a n i s m s , G r o u p s and M e m e s : R e p l i c a t o r s o r V e h i c l e s ?

117

embryology and in favour of blending e m b r y o l o g y . I myself give similar a r g u m e n t s e l s e w h e r e i n this b o o k ( e . g . t h e c a k e a n a l o g y i n t h e s e c t i o n o f Chapter 9 called ' T h e poverty of preformationism'). Genes do indeed blend, a s far a s t h e i r effects o n d e v e l o p i n g p h e n o t y p e s a r e c o n c e r n e d . B u t , a s I h a v e already e m p h a s i z e d sufficiently,

t h e y d o not b l e n d a s t h e y r e p l i c a t e a n d

r e c o m b i n e d o w n t h e g e n e r a t i o n s . I t i s this t h a t m a t t e r s for t h e g e n e t i c i s t , a n d i t i s also this t h a t m a t t e r s for the s t u d e n t o f u n i t s o f s e l e c t i o n . G o u l d goes o n : So parts are not translated genes, and selection doesn't e v e n w o r k d i r e c t l y o n p a r t s . I t a c c e p t s o r rejects e n t i r e o r g a n i s m s b e c a u s e suites o f parts, interacting i n c o m p l e x w a y s , confer a d v a n t a g e s . T h e i m a g e o f i n d i v i d u a l g e n e s , p l o t t i n g the c o u r s e o f t h e i r o w n s u r v i v a l , b e a r s little r e l a t i o n s h i p Dawkins

will

t o d e v e l o p m e n t a l g e n e t i c s a s w e u n d e r s t a n d it.

need

another

metaphor:

genes

caucusing,

forming

a l l i a n c e s , s h o w i n g d e f e r e n c e for a c h a n c e t o j o i n a p a c t , g a u g i n g probable environments. But w h e n you a m a l g a m a t e so m a n y genes a n d tie t h e m t o g e t h e r i n h i e r a r c h i c a l c h a i n s o f a c t i o n m e d i a t e d b y environments, we call the resultant object a b o d y . G o u l d comes closer to the truth here, but the truth is subtler, as I h o p e to show in C h a p t e r

13. T h e point was alluded to in the previous chapter.

B r i e f l y , t h e sense i n w h i c h g e n e s m a y b e s a i d t o ' c a u c u s ' a n d f o r m ' a l l i a n c e s ' is the f o l l o w i n g . S e l e c t i o n f a v o u r s t h o s e g e n e s w h i c h s u c c e e d in the presence of other genes, which in turn succeed in the presence of them.

Therefore mutually

c o m p a t i b l e sets o f g e n e s a r i s e i n g e n e - p o o l s . T h i s i s m o r e s u b t l e a n d m o r e useful t h a n t o s a y t h a t ' w e c a l l t h e r e s u l t a n t o b j e c t a b o d y ' . Of course g e n e s a r e n o t d i r e c t l y v i s i b l e to s e l e c t i o n .

Obviously t h e y a r e

s e l e c t e d b y v i r t u e o f t h e i r p h e n o t y p i c effects, a n d c e r t a i n l y t h e y c a n o n l y b e said t o have p h e n o t y p i c effects i n c o n c e r t w i t h h u n d r e d s o f o t h e r g e n e s . B u t i t i s t h e thesis o f this b o o k t h a t w e s h o u l d n o t b e t r a p p e d i n t o a s s u m i n g t h a t those p h e n o t y p i c effects a r e best r e g a r d e d a s b e i n g n e a t l y w r a p p e d u p i n d i s c r e t e b o d i e s (or o t h e r d i s c r e t e v e h i c l e s ) . T h e d o c t r i n e o f t h e e x t e n d e d p h e n o t y p e is t h a t t h e p h e n o t y p i c effect of a g e n e ( g e n e t i c r e p l i c a t o r ) is b e s t seen a s a n effect u p o n t h e w o r l d a t l a r g e , a n d o n l y i n c i d e n t a l l y u p o n t h e i n d i v i d u a l o r g a n i s m â&#x20AC;&#x201D; o r a n y o t h e r v e h i c l e â&#x20AC;&#x201D; i n w h i c h i t h a p p e n s t o sit.

7 Selfish W a s p or Selfish Strategy?

T h i s is a chapter about practical research m e t h o d o l o g y . T h e r e will be t h o s e w h o a c c e p t t h e thesis o f this b o o k a t a t h e o r e t i c a l l e v e l b u t w h o w i l l o b j e c t t h a t , i n p r a c t i c e , f i e l d w o r k e r s f i n d i t useful t o focus t h e i r a t t e n t i o n o n individual a d v a n t a g e . In a t h e o r e t i c a l sense, t h e y w i l l s a y , it is r i g h t to see the natural w o r l d as a b a t t l e g r o u n d of replicators, but in real research we are obliged

measure

and

compare

the

D a r w i n i a n fitness of individual

o r g a n i s m s . I w a n t to discuss a p a r t i c u l a r piece of research in detail to show t h a t this i s n o t n e c e s s a r i l y t h e c a s e . I n s t e a d o f c o m p a r i n g t h e s u c c e s s o f i n d i v i d u a l o r g a n i s m s , i t i s often i n p r a c t i c e m o r e useful t o c o m p a r e t h e success of 'strategies' ( M a y n a r d S m i t h 1974) or ' p r o g r a m s ' or 'subroutines', averaged

across

the individuals

that

use

them.

O f the

many

pieces of

r e s e a r c h t h a t I c o u l d h a v e d i s c u s s e d , for i n s t a n c e t h e w o r k o n ' o p t i m a l foraging' (Pyke, Pulliam & C h a r n o v 1 9 7 7 ; K r e b s 1978), Parker's (1978a) d u n g f l i e s , o r a n y o f t h e e x a m p l e s r e v i e w e d b y D a v i e s (in p r e s s ) , I c h o o s e B r o c k m a n n ' s study of digger wasps purely because I am very familiar with it (Brockmann,

Grafen

Dawkins

1979;

Brockmann

Dawkins

1979;

D a w k i n s & B r o c k m a n n 1980). I s h a l l use t h e w o r d ' p r o g r a m ' i n e x a c t l y t h e s a m e sense a s M a y n a r d S m i t h uses ' s t r a t e g y ' .

I prefer ' p r o g r a m ' to 'strategy' because experience

w a r n s t h a t ' s t r a t e g y ' i s q u i t e l i k e l y t o b e m i s u n d e r s t o o d , i n a t least t w o different English

ways

Dictionary

(Dawkins and

1980).

standard

And

incidentally,

American

usage,

following prefer

the

Oxford

'program'

' p r o g r a m m e ' w h i c h a p p e a r s to be a nineteenth-century affectation imported f r o m t h e F r e n c h . A p r o g r a m (or s t r a t e g y ) is a r e c i p e for a c t i o n , a set of notional instructions that an a n i m a l seems to be ' o b e y i n g ' , just as a computer o b e y s its p r o g r a m . A c o m p u t e r p r o g r a m m e r w r i t e s o u t his p r o g r a m i n a l a n g u a g e s u c h a s A l g o l o r F o r t r a n , w h i c h m a y l o o k r a t h e r like i m p e r a t i v e E n g l i s h . T h e m a c h i n e r y o f t h e c o m p u t e r i s s o set u p t h a t i t b e h a v e s a s i f 118

Selfish W a s p or Selfish S t r a t e g y ?

119

o b e y i n g these q u a s i - E n g l i s h i n s t r u c t i o n s . B e f o r e i t c a n r u n , t h e p r o g r a m i s t r a n s l a t e d ( b y c o m p u t e r ) i n t o a set o f m o r e e l e m e n t a r y ' m a c h i n e l a n g u a g e ' instructions, closer to the h a r d w a r e a n d further from easy h u m a n c o m p r e h e n sion. I n a sense i t i s these m a c h i n e l a n g u a g e i n s t r u c t i o n s t h a t a r e ' a c t u a l l y ' o b e y e d r a t h e r t h a n t h e q u a s i - E n g l i s h p r o g r a m , a l t h o u g h i n a n o t h e r sense b o t h a r e o b e y e d , a n d i n y e t a n o t h e r sense n e i t h e r i s ! A person w a t c h i n g a n d a n a l y s i n g the b e h a v i o u r of a c o m p u t e r w h o s e program

had

been

lost m i g h t ,

principle,

be able

to reconstruct the

p r o g r a m o r its f u n c t i o n a l e q u i v a l e n t . T h e last f o u r w o r d s a r e c r u c i a l . F o r his o w n convenience he will write the reconstructed p r o g r a m in some particular l a n g u a g e â&#x20AC;&#x201D; A l g o l , Fortran, a flow chart, some p a r t i c u l a r rigorous subset of English. B u t there is no w a y of k n o w i n g in w h i c h , if a n y , of these l a n g u a g e s the p r o g r a m w a s o r i g i n a l l y w r i t t e n . I t m a y h a v e b e e n d i r e c t l y w r i t t e n i n m a c h i n e l a n g u a g e , or ' h a r d - w i r e d ' into the m a c h i n e r y of the c o m p u t e r at m a n u f a c t u r e . T h e end result is the s a m e in a n y c a s e : the c o m p u t e r performs s o m e useful task s u c h a s c a l c u l a t i n g s q u a r e r o o t s , a n d a h u m a n c a n u s e f u l l y t r e a t t h e c o m p u t e r as if it w a s ' o b e y i n g ' a set of i m p e r a t i v e i n s t r u c t i o n s w r i t t e n o u t in a l a n g u a g e t h a t is c o n v e n i e n t for h u m a n s to u n d e r s t a n d . I t h i n k t h a t for m a n y p u r p o s e s s u c h

'software explanations'

of behaviour

m e c h a n i s m s a r e j u s t a s v a l i d a n d useful a s t h e m o r e o b v i o u s ' h a r d w a r e explanations' favoured by neurophysiologists. A biologist looking at an a n i m a l is in s o m e w h a t the s a m e position as an e n g i n e e r l o o k i n g a t a c o m p u t e r r u n n i n g a lost p r o g r a m . T h e a n i m a l i s behaving in w h a t appears to be an organized, purposeful w a y , as if it was obeying a program, an orderly sequence of imperative instructions. T h e a n i m a l ' s p r o g r a m h a s n o t a c t u a l l y b e e n lost, for i t n e v e r w a s w r i t t e n o u t . R a t h e r , natural selection c o b b l e d together the e q u i v a l e n t of a h a r d - w i r e d machine code

program,

favouring mutations

generations of nervous systems to b e h a v e

that

altered

successive

(and to learn to c h a n g e their

b e h a v i o u r ) i n a p p r o p r i a t e w a y s . A p p r o p r i a t e m e a n s , i n this c a s e , a p p r o p r i a t e for the s u r v i v a l

and

p r o p a g a t i o n of the genes

concerned.

Nevertheless,

although no p r o g r a m was ever written d o w n , just as in the case of the c o m p u t e r r u n n i n g a p r o g r a m w h i c h h a s b e e n lost, i t i s c o n v e n i e n t for u s t o think

of the

animal

'obeying'

program

'written'

some

easily

understood l a n g u a g e such as English. O n e of the things we c a n then do is to imagine alternative programs or subroutines w h i c h might 'compete' with e a c h o t h e r for ' c o m p u t e r t i m e ' i n the n e r v o u s s y s t e m s o f t h e p o p u l a t i o n . T h o u g h we must treat the a n a l o g y w i t h c i r c u m s p e c t i o n , as I shall s h o w , we can

usefully

alternative

imagine natural selection

programs

subroutines,

and

acting directly treat

individual

pool

organisms

t e m p o r a r y e x e c u t o r s a n d p r o p a g a t o r s o f these a l t e r n a t i v e p r o g r a m s . I n a p a r t i c u l a r m o d e l o f a n i m a l f i g h t i n g , for e x a m p l e , M a y n a r d S m i t h ( 1 9 7 2 , p . 19) p o s t u l a t e d five a l t e r n a t i v e ' s t r a t e g i e s ' ( p r o g r a m s ) :

1 2 0

Selfish W a s p o r Selfish S t r a t e g y ?

1 F i g h t c o n v e n t i o n a l l y ; retreat if o p p o n e n t proves to be stronger or if opponent escalates. 2 Fight at escalated level. Retreat only if injured. 3 Start c o n v e n t i o n a l l y . Escalate only if opponent escalates. 4 Start conventionally.

Escalate only if opponent continues to fight

conventionally. 5 F i g h t at escalated level. R e t r e a t before getting hurt if opponent does likewise. F o r t h e p u r p o s e o f c o m p u t e r s i m u l a t i o n i t w a s n e c e s s a r y t o d e f i n e these five 'strategies' imperative

more rigorously,

English

notation

b u t for h u m a n u n d e r s t a n d i n g the s i m p l e preferable.

T h e important

point

for this

c h a p t e r is that the five strategies w e r e t h o u g h t of as if they (rather than i n d i v i d u a l animals) w e r e c o m p e t i n g entities in their o w n right. R u l e s w e r e set

the

computer

simulation

for

the

'reproduction'

o f successful

s t r a t e g i e s ( p r e s u m a b l y i n d i v i d u a l s a d o p t i n g successful s t r a t e g i e s r e p r o d u c e d a n d p a s s e d o n g e n e t i c t e n d e n c i e s t o a d o p t t h o s e s a m e s t r a t e g i e s , b u t the d e t a i l s o f this w e r e i g n o r e d ) . T h e q u e s t i o n a s k e d w a s a b o u t s t r a t e g y s u c c e s s , not i n d i v i d u a l success. A further i m p o r t a n t point is that M a y n a r d S m i t h w a s seeking the 'best' s t r a t e g y i n o n l y a s p e c i a l s e n s e . I n fact h e w a s s e e k i n g a n ' e v o l u t i o n a r i l y stable s t r a t e g y ' o r E S S . T h e E S S has b e e n rigorously defined Smith

1974),

successful

b u t it c a n

be c r u d e l y encapsulated

(Maynard

as a strategy

that is

w h e n c o m p e t i n g w i t h c o p i e s o f itself. T h i s m a y s e e m a n o d d

p r o p e r t y to single out, but the rationale is really very powerful. If a p r o g r a m o r s t r a t e g y i s s u c c e s s f u l , this m e a n s t h a t c o p i e s o f i t w i l l t e n d t o b e c o m e m o r e n u m e r o u s in the p o p u l a t i o n of programs and will ultimately b e c o m e almost u n i v e r s a l . I t w i l l t h e r e f o r e c o m e t o b e s u r r o u n d e d b y c o p i e s o f itself. I f i t i s t o r e m a i n u n i v e r s a l , t h e r e f o r e , i t m u s t b e successful w h e n c o m p e t i n g a g a i n s t c o p i e s o f itself, s u c c e s s f u l c o m p a r e d w i t h r a r e different s t r a t e g i e s t h a t m i g h t arise by m u t a t i o n or invasion. A p r o g r a m that w a s not e v o l u t i o n a r i l y stable i n this s e n s e w o u l d n o t last l o n g i n t h e w o r l d , a n d w o u l d t h e r e f o r e n o t p r e s e n t i t s e l f for o u r e x p l a n a t i o n . I n t h e c a s e o f t h e f i v e s t r a t e g i e s listed a b o v e , M a y n a r d S m i t h w a n t e d t o know what

would

happen

p o p u l a t i o n c o n t a i n i n g c o p i e s o f all f i v e

p r o g r a m s . W a s there o n e of the five w h i c h , if it c a m e to p r e d o m i n a t e , w o u l d retain

its

numerical

superiority

against

all

comers?

concluded

that

p r o g r a m n u m b e r 3 i s a n E S S : w h e n i t h a p p e n s t o b e v e r y n u m e r o u s i n the p o p u l a t i o n n o o t h e r p r o g r a m f r o m t h e list d o e s b e t t e r t h a n p r o g r a m 3 itself ( a c t u a l l y t h e r e i s a p r o b l e m o v e r this p a r t i c u l a r e x a m p l e â&#x20AC;&#x201D; D a w k i n s 1980, p . 7 â&#x20AC;&#x201D; b u t I shall ignore it h e r e ) . W h e n we talk of a p r o g r a m as ' d o i n g better' or as b e i n g 'successful' we are notionally m e a s u r i n g success as c a p a c i t y to p r o p a g a t e c o p i e s o f t h e s a m e p r o g r a m i n t h e n e x t g e n e r a t i o n : i n r e a l i t y this

Selfish W a s p or Selfish S t r a t e g y ?

121

i s l i k e l y t o m e a n t h a t a successful p r o g r a m i s o n e w h i c h p r o m o t e s t h e s u r v i v a l a n d r e p r o d u c t i o n o f the a n i m a l a d o p t i n g it. W h a t M a y n a r d Smith, together with Price and Parker ( M a y n a r d Smith & Price

1973;

Maynard

Smith

Parker

1976),

has done is to take the

m a t h e m a t i c a l theory o f g a m e s a n d w o r k out the c r u c i a l respect i n w h i c h that t h e o r y m u s t b e m o d i f i e d t o suit t h e D a r w i n i s t ' s p u r p o s e . T h e c o n c e p t o f t h e E S S , a s t r a t e g y t h a t d o e s r e l a t i v e l y w e l l a g a i n s t c o p i e s of itself, is t h e r e s u l t . I h a v e a l r e a d y m a d e t w o attempts a t a d v o c a t i n g the i m p o r t a n c e o f the E S S c o n c e p t a n d e x p l a i n i n g its b r o a d a p p l i c a b i l i t y i n e t h o l o g y ( D a w k i n s 1 9 7 6 a , 1980), a n d I s h a l l n o t r e p e a t m y s e l f u n n e c e s s a r i l y h e r e . H e r e m y p u r p o s e i s t o d e v e l o p t h e r e l e v a n c e o f this w a y o f t h i n k i n g for t h e s u b j e c t o f t h e p r e s e n t b o o k , the d e b a t e a b o u t t h e l e v e l a t w h i c h n a t u r a l s e l e c t i o n a c t s . I s h a l l b e g i n by r e c o u n t i n g a specific piece of research that used the E S S c o n c e p t . A l l the facts I s h a l l g i v e a r e f r o m t h e field o b s e r v a t i o n s o f D r J a n e B r o c k m a n n , reported in detail elsewhere and briefly m e n t i o n e d in C h a p t e r 3. I shall h a v e to g i v e a brief a c c o u n t of the research itself before I c a n relate it to the m e s s a g e o f this c h a p t e r . Sphex ichneumcneus is a s o l i t a r y w a s p , s o l i t a r y in t h e sense t h a t t h e r e a r e no s o c i a l g r o u p s a n d n o sterile w o r k e r s , a l t h o u g h t h e f e m a l e s d o t e n d t o d i g t h e i r nests i n l o o s e a g g r e g a t i o n s . E a c h f e m a l e l a y s h e r o w n e g g s , a n d a l l l a b o u r on b e h a l f of the y o u n g is c o m p l e t e d before the e g g is l a i d â&#x20AC;&#x201D; t h e w a s p s are

not

'progressive

underground

nest

provisioners'.

which

she has

The

female

previously

lays

provisioned

one with

egg

stung and

paralysed k a t y d i d s (long-horned grasshoppers). T h e n she closes up that nest, l e a v i n g t h e l a r v a t o feed o n t h e k a t y d i d s , w h i l e s h e h e r s e l f starts w o r k o n a n e w nest. T h e life o f a n a d u l t f e m a l e i s l i m i t e d t o a b o u t six s u m m e r w e e k s . I f o n e w i s h e d t o m e a s u r e it, t h e s u c c e s s o f a f e m a l e c o u l d b e a p p r o x i m a t e d a s t h e n u m b e r o f e g g s t h a t she s u c c e s s f u l l y l a y s o n a d e q u a t e p r o v i s i o n s d u r i n g this t i m e . T h e thing that especially interested us w a s that the wasps s e e m e d to h a v e t w o a l t e r n a t i v e w a y s o f a c q u i r i n g a nest. E i t h e r a f e m a l e w o u l d d i g h e r o w n nest i n t h e g r o u n d , o r s h e w o u l d a t t e m p t t o t a k e o v e r a n e x i s t i n g n e s t w h i c h a n o t h e r w a s p h a d d u g . W e c a l l e d t h e s e t w o b e h a v i o u r p a t t e r n s digging a n d entering, r e s p e c t i v e l y . N o w , h o w c a n t w o a l t e r n a t i v e w a y s o f a c h i e v i n g t h e s a m e e n d , i n this c a s e t w o a l t e r n a t i v e w a y s o f a c q u i r i n g a nest, c o e x i s t i n o n e p o p u l a t i o n ? S u r e l y o n e o r t h e o t h e r o u g h t t o b e m o r e s u c c e s s f u l , a n d t h e less successful o n e s h o u l d b e r e m o v e d f r o m t h e p o p u l a t i o n b y n a t u r a l s e l e c t i o n ? T h e r e a r e t w o g e n e r a l r e a s o n s w h y this m i g h t n o t h a p p e n , w h i c h I w i l l e x p r e s s i n t h e j a r g o n o f E S S t h e o r y : firstly, d i g g i n g a n d e n t e r i n g m i g h t b e two outcomes of one 'conditional strategy'; secondly, they might be equally successful a t s o m e c r i t i c a l f r e q u e n c y m a i n t a i n e d

by frequency-dependent

selectionâ&#x20AC;&#x201D;part of a 'mixed E S S ' ( M a y n a r d Smith 1974,

1 9 7 9 ) . I f t h e first

possibility w e r e correct, all w a s p s w o u l d b e p r o g r a m m e d w i t h the s a m e

1 2 2

Selfish W a s p o r Selfish S t r a t e g y ?

c o n d i t i o n a l r u l e : ' I f X i s t r u e , d i g , o t h e r w i s e e n t e r ' ; for i n s t a n c e , ' I f y o u h a p p e n t o b e a s m a l l w a s p , d i g , o t h e r w i s e use y o u r s u p e r i o r s i z e t o t a k e o v e r a n o t h e r w a s p ' s b u r r o w ' . W e failed t o f i n d a n y e v i d e n c e for a c o n d i t i o n a l p r o g r a m o f this o r a n y o t h e r k i n d . I n s t e a d , w e c o n v i n c e d o u r s e l v e s t h a t the s e c o n d p o s s i b i l i t y , t h e ' m i x e d E S S ' , f i t t e d t h e facts. T h e r e are in theory two kinds of mixed E S S , or rather two extremes with a c o n t i n u u m b e t w e e n . T h e f i r s t e x t r e m e i s a b a l a n c e d p o l y m o r p h i s m . I n this c a s e , i f w e w a n t t o use t h e i n i t i a l s ' E S S ' , t h e f i n a l S s h o u l d b e t h o u g h t o f a s s t a n d i n g for state o f t h e p o p u l a t i o n r a t h e r t h a n s t r a t e g y o f t h e i n d i v i d u a l . I f this p o s s i b i l i t y o b t a i n e d , t h e r e w o u l d b e t w o d i s t i n c t k i n d s o f w a s p s , d i g g e r s a n d enterers, w h o w o u l d tend t o b e e q u a l l y successful. equally

successful,

natural

selection

would

tend

If they were not eliminate

the

less

successful o n e from the p o p u l a t i o n . It is too m u c h to h o p e that, by sheer c o i n c i d e n c e , t h e n e t costs a n d benefits o f d i g g i n g w o u l d e x a c t l y b a l a n c e the net

costs

and

dependent

benefits

selection.

of entering.

postulate

Rather, a

critical

are

invoking frequency-

equilibrium

proportion

d i g g e r s , p*, a t w h i c h t h e t w o k i n d s o f w a s p s a r e e q u a l l y s u c c e s s f u l . T h e n , i f t h e p r o p o r t i o n o f d i g g e r s i n t h e p o p u l a t i o n falls b e l o w t h e c r i t i c a l f r e q u e n c y , d i g g e r s w i l l b e f a v o u r e d b y s e l e c t i o n , w h i l e i f i t rises a b o v e t h e c r i t i c a l f r e q u e n c y e n t e r e r s w i l l b e f a v o u r e d . I n this w a y the p o p u l a t i o n w o u l d h o v e r a r o u n d the e q u i l i b r i u m frequency. I t i s e a s y t o t h i n k o f p l a u s i b l e r e a s o n s w h y benefit m i g h t b e f r e q u e n c y d e p e n d e n t i n this w a y . C l e a r l y , s i n c e n e w b u r r o w s c o m e i n t o e x i s t e n c e o n l y w h e n d i g g e r s d i g t h e m , t h e f e w e r d i g g e r s t h e r e a r e i n t h e p o p u l a t i o n the s t r o n g e r w i l l b e t h e c o m p e t i t i o n a m o n g e n t e r e r s for b u r r o w s , a n d the l o w e r the benefit to a t y p i c a l enterer. C o n v e r s e l y , w h e n diggers are v e r y numerous, a v a i l a b l e b u r r o w s a b o u n d and enterers tend to prosper.

But,

said,

frequency-dependent p o l y m o r p h i s m is only one end of a continuum. We now turn to the other end. At the other end of the c o n t i n u u m

there is no p o l y m o r p h i s m

among

i n d i v i d u a l s . I n t h e s t a b l e s t a t e a l l w a s p s o b e y the s a m e p r o g r a m , b u t t h a t p r o g r a m i s i t s e l f a m i x t u r e . E v e r y w a s p i s o b e y i n g the i n s t r u c t i o n , ' D i g w i t h p r o b a b i l i t y p, e n t e r w i t h p r o b a b i l i t y I â&#x20AC;&#x201D; p'; for i n s t a n c e , ' D i g on 70 p e r c e n t of occasions, enter on 30 per cent of occasions'.

I f this i s r e g a r d e d a s a

' p r o g r a m ' , w e c o u l d p e r h a p s refer t o d i g g i n g a n d e n t e r i n g t h e m s e l v e s a s 'subroutines'.

Every

programmed

wasp

choose

one

equipped or

the

with

other

both on

subroutines.

each

occasion

She

with

c h a r a c t e r i s t i c p r o b a b i l i t y , p. Although

there

polymorphism

of diggers

and

enterers

here,

s o m e t h i n g m a t h e m a t i c a l l y e q u i v a l e n t to f r e q u e n c y - d e p e n d e n t selection can go on. H e r e is h o w it w o u l d w o r k . As before, there is a critical population f r e q u e n c y o f d i g g i n g , p*, a t w h i c h e n t e r i n g w o u l d y i e l d e x a c t l y the s a m e ' p a y - o f f ' a s d i g g i n g . p * is, t h e n , t h e e v o l u t i o n a r i l y s t a b l e d i g g i n g p r o b a b i l i t y .

Selfish W a s p o r Selfish S t r a t e g y ?

I f t h e s t a b l e p r o b a b i l i t y i s 0.7,

programs instructing wasps

123

to follow

different r u l e , s a y ' D i g w i t h p r o b a b i l i t y 0 . 7 5 ' , o r ' D i g w i t h p r o b a b i l i t y 0 . 6 5 ' , w o u l d d o less w e l l . T h e r e i s a w h o l e f a m i l y o f ' m i x e d s t r a t e g i e s ' o f t h e f o r m ' D i g w i t h p r o b a b i l i t y p, enter w i t h p r o b a b i l i t y 1 â&#x20AC;&#x201D;p', a n d o n l y o n e of these is the E S S . I said t h a t the t w o e x t r e m e s w e r e j o i n e d b y a c o n t i n u u m . I m e a n t t h a t t h e s t a b l e p o p u l a t i o n f r e q u e n c y o f d i g g i n g , p * (70 p e r c e n t o r w h a t e v e r i t i s ) , could be achieved by any of a large n u m b e r of combinations of pure and mixed individual strategies. T h e r e might be a w i d e distribution of p values in individual nervous systems in the p o p u l a t i o n , i n c l u d i n g some p u r e diggers and

pure enterers.

But,

provided

the

total

frequency of d i g g i n g in

the

p o p u l a t i o n i s e q u a l t o t h e c r i t i c a l v a l u e p*, i t w o u l d still b e t r u e t h a t d i g g i n g and entering w e r e e q u a l l y successful, a n d n a t u r a l selection w o u l d not act to c h a n g e the r e l a t i v e f r e q u e n c y o f t h e t w o s u b r o u t i n e s i n t h e n e x t g e n e r a t i o n . T h e p o p u l a t i o n w o u l d b e i n a n e v o l u t i o n a r i l y stable state. T h e a n a l o g y w i t h F i s h e r ' s ( 1 9 3 0 a ) t h e o r y o f sex r a t i o e q u i l i b r i u m w i l l b e c l e a r . P r o c e e d i n g from the c o n c e i v a b l e t o the a c t u a l , B r o c k m a n n ' s d a t a s h o w conclusively that

these w a s p s a r e n o t i n a n y s i m p l e sense p o l y m o r p h i c .

Individuals sometimes d u g and sometimes entered. We c o u l d not e v e n detect a n y s t a t i s t i c a l t e n d e n c y for i n d i v i d u a l s t o s p e c i a l i z e i n d i g g i n g o r e n t e r i n g . E v i d e n t l y , if the w a s p p o p u l a t i o n is in a m i x e d e v o l u t i o n a r i l y stable state, it lies a w a y f r o m t h e p o l y m o r p h i s m e n d o f t h e c o n t i n u u m . W h e t h e r i t i s a t t h e other

extremeâ&#x20AC;&#x201D;all

individuals

running

the

same

stochastic

programâ&#x20AC;&#x201D;or

whether there is some m o r e c o m p l e x m i x t u r e of pure and m i x e d i n d i v i d u a l p r o g r a m s , w e d o n o t k n o w . I t i s o n e o f t h e c e n t r a l m e s s a g e s o f this c h a p t e r that, for o u r r e s e a r c h p u r p o s e , w e d i d n o t need t o k n o w . B e c a u s e w e r e f r a i n e d from t a l k i n g a b o u t i n d i v i d u a l s u c c e s s , b u t t h o u g h t i n s t e a d a b o u t s u b r o u t i n e success a v e r a g e d o v e r a l l i n d i v i d u a l s , w e w e r e a b l e t o d e v e l o p a n d test a successful m o d e l o f t h e m i x e d E S S w h i c h left o p e n t h e q u e s t i o n o f w h e r e a l o n g the c o n t i n u u m o u r w a s p s l a y . I s h a l l r e t u r n t o this p o i n t after g i v i n g s o m e p e r t i n e n t facts a n d after o u t l i n i n g t h e m o d e l itself. W h e n a w a s p d i g s a b u r r o w , she m a y e i t h e r s t a y w i t h i t a n d p r o v i s i o n it, o r she m a y a b a n d o n it.

R e a s o n s for a b a n d o n i n g nests w e r e n o t a l w a y s

obvious, but they i n c l u d e d invasion by ants and other undesirable aliens. A w a s p w h o m o v e s i n t o a b u r r o w t h a t a n o t h e r h a s d u g m a y find t h a t t h e o r i g i n a l o w n e r is still in r e s i d e n c e . In this c a s e s h e is s a i d to have joined t h e p r e v i o u s o w n e r , a n d t h e t w o w a s p s u s u a l l y w o r k o n t h e s a m e n e s t for a w h i l e , b o t h i n d e p e n d e n t l y b r i n g i n g k a t y d i d s t o it. A l t e r n a t i v e l y , t h e e n t e r i n g w a s p m a y b e f o r t u n a t e e n o u g h t o hit u p o n a nest t h a t h a s b e e n a b a n d o n e d b y its o r i g i n a l o w n e r , i n w h i c h c a s e she h a s i t t o herself. T h e e v i d e n c e i n d i c a t e s t h a t e n t e r i n g w a s p s c a n n o t d i s t i n g u i s h a nest t h a t h a s b e e n a b a n d o n e d f r o m o n e t h a t i s still o c c u p i e d b y its p r e v i o u s o w n e r . T h i s f a c t i s n o t s o s u r p r i s i n g as it m a y seem, since both wasps spend most of their time out hunting, so t w o

124

Selfish W a s p or Selfish S t r a t e g y ?

w a s p s ' s h a r i n g ' t h e s a m e nest s e l d o m m e e t . W h e n t h e y d o m e e t t h e y f i g h t , a n d i n a n y c a s e o n l y o n e o f t h e m s u c c e e d s i n l a y i n g a n e g g i n t h e nest u n d e r dispute. W h a t e v e r h a d p r e c i p i t a t e d t h e a b a n d o n i n g o f a nest b y t h e o r i g i n a l o w n e r s e e m e d u s u a l l y t o b e a t e m p o r a r y i n c o n v e n i e n c e , a n d a n a b a n d o n e d nest constituted a desirable resource w h i c h w a s soon used by a n o t h e r w a s p . A w a s p w h o e n t e r s a n a b a n d o n e d b u r r o w s a v e s h e r s e l f t h e costs a s s o c i a t e d w i t h d i g g i n g o n e . O n t h e o t h e r h a n d , s h e r u n s t h e risk t h a t t h e b u r r o w she enters h a s n o t b e e n a b a n d o n e d . I t m a y still c o n t a i n t h e o r i g i n a l o w n e r , o r i t m a y c o n t a i n a n o t h e r e n t e r i n g w a s p w h o g o t t h e r e f i r s t . I n e i t h e r o f these cases the e n t e r i n g w a s p lets h e r s e l f in for a h i g h risk of a c o s t l y fight, a n d a h i g h risk that she w i l l not be the o n e to l a y the e g g at the end of a costly period of p r o v i s i o n i n g t h e nest. We d e v e l o p e d a n d tested a m a t h e m a t i c a l m o d e l ( B r o c k m a n n , G r a f e n & D a w k i n s 1 9 7 9 ) w h i c h d i s t i n g u i s h e d f o u r different ' o u t c o m e s ' o r fates t h a t c o u l d befall a w a s p in a n y particular nesting episode. 1 S h e c o u l d b e f o r c e d t o a b a n d o n t h e nest, s a y b y a n a n t r a i d . 2 S h e c o u l d e n d u p a l o n e , i n sole c h a r g e o f t h e nest. 3 S h e c o u l d be j o i n e d by a second w a s p . 4 She could join an already incumbent wasp. O u t c o m e s 1 to 3 c o u l d r e s u l t f r o m an i n i t i a l d e c i s i o n to d i g a b u r r o w . O u t c o m e s 2 to 4 c o u l d result from an initial decision to enter. B r o c k m a n n ' s d a t a e n a b l e d us to m e a s u r e , in terms of p r o b a b i l i t y of l a y i n g an e g g per unit t i m e , t h e r e l a t i v e ' p a y o f f s ' a s s o c i a t e d w i t h e a c h o f these four o u t c o m e s . F o r instance, in one study population in Exeter, N e w Hampshire, O u t c o m e 4, ' j o i n i n g ' , h a d a p a y o f f s c o r e o f 0.35 e g g s p e r obtained

100 h o u r s . T h i s s c o r e w a s

by a v e r a g i n g o v e r all occasions w h e n w a s p s e n d e d up in that

o u t c o m e . T o c a l c u l a t e i t w e s i m p l y a d d e d u p t h e t o t a l n u m b e r o f e g g s laid by wasps w h o , on the occasion concerned, had j o i n e d an already incumbent w a s p , a n d d i v i d e d b y t h e t o t a l t i m e s p e n t b y w a s p s o n nests t h a t t h e y h a d joined.

The

corresponding

subsequently joined was

score

for

wasps

who

began

alone

but

were

1.06 e g g s p e r 100 h o u r s , a n d t h a t for w a s p s w h o

r e m a i n e d a l o n e w a s 1.93 e g g s p e r 100 h o u r s . I f a w a s p c o u l d c o n t r o l w h i c h o f t h e f o u r o u t c o m e s she e n d e d u p i n , she s h o u l d ' p r e f e r ' t o e n d u p a l o n e s i n c e this o u t c o m e c a r r i e d t h e h i g h e s t p a y o f f rate, b u t h o w m i g h t she a c h i e v e this? It w a s a k e y assumption of our m o d e l that the four o u t c o m e s did not correspond to decisions that were a v a i l a b l e to a w a s p . A w a s p c a n ' d e c i d e ' to d i g or to enter. She c a n n o t decide to be j o i n e d or to be alone a n y m o r e than a m a n can decide not to get cancer. T h e s e are o u t c o m e s that d e p e n d o n c i r c u m s t a n c e s b e y o n d the individual's c o n t r o l . I n this c a s e t h e y d e p e n d o n w h a t t h e o t h e r w a s p s i n t h e p o p u l a t i o n

Selfish W a s p or Selfish S t r a t e g y ?

125

d o . B u t j u s t a s a m a n m a y s t a t i s t i c a l l y r e d u c e his c h a n c e s o f g e t t i n g c a n c e r , by taking the decision to stop s m o k i n g , so a w a s p ' s 'task' is to m a k e the o n l y decision open to h e r â&#x20AC;&#x201D; d i g or enterâ&#x20AC;&#x201D;in such a w a y as to m a x i m i z e her c h a n c e s o f e n d i n g u p i n a d e s i r a b l e o u t c o m e . M o r e s t r i c t l y , w e seek t h e stable v a l u e of p, p*, such that w h e n p* of the decisions in the p o p u l a t i o n are digging decisions, no m u t a n t gene l e a d i n g to the a d o p t i o n of some other value of p will be favoured by natural selection. T h e probability that an entering decision will lead to s o m e p a r t i c u l a r outcome, such as

the d e s i r a b l e

'alone' outcome,

frequency of entering decisions in

d e p e n d s on the overall

the p o p u l a t i o n .

If a

large

a m o u n t of

e n t e r i n g i s g o i n g o n i n the p o p u l a t i o n , t h e n u m b e r o f a v a i l a b l e a b a n d o n e d burrows goes d o w n , and the chances go up that a w a s p that decides to enter w i l l find h e r s e l f i n the u n d e s i r a b l e p o s i t i o n o f j o i n i n g a n i n c u m b e n t . O u r model enables us to take a n y given v a l u e of p, the overall frequency of d i g g i n g in the p o p u l a t i o n , a n d predict the p r o b a b i l i t y that an i n d i v i d u a l that decides to d i g , or an i n d i v i d u a l that d e c i d e s to enter, w i l l end that e p i s o d e i n e a c h o f t h e four o u t c o m e s . T h e a v e r a g e p a y o f f t o a w a s p t h a t decides to dig,

t h e r e f o r e , c a n b e p r e d i c t e d for a n y n a m e d f r e q u e n c y o f

d i g g i n g versus entering in the p o p u l a t i o n as a w h o l e . It is s i m p l y the sum, o v e r t h e four o u t c o m e s , o f t h e e x p e c t e d p a y o f f y i e l d e d b y e a c h o u t c o m e , multiplied by the p r o b a b i l i t y that a w a s p that digs will end up in that o u t c o m e . T h e e q u i v a l e n t s u m c a n b e w o r k e d o u t for a w a s p t h a t d e c i d e s t o enter, a g a i n

for a n y n a m e d

frequency of d i g g i n g versus entering in

the

population. Finally, making certain plausible additional assumptions which a r e listed i n t h e o r i g i n a l p a p e r , w e s o l v e a n e q u a t i o n t o find t h e p o p u l a t i o n d i g g i n g frequency at w h i c h the a v e r a g e e x p e c t e d benefit to a w a s p that digs is exactly e q u a l to the a v e r a g e e x p e c t e d benefit to a w a s p that enters. T h a t is our

predicted

equilibrium

frequency

which

can

compare

with

the

o b s e r v e d f r e q u e n c y i n the w i l d p o p u l a t i o n . O u r e x p e c t a t i o n i s t h a t t h e r e a l p o p u l a t i o n s h o u l d e i t h e r b e s i t t i n g a t t h e e q u i l i b r i u m f r e q u e n c y o r else i n t h e process o f e v o l v i n g t o w a r d s the e q u i l i b r i u m f r e q u e n c y .

T h e m o d e l also

predicts the proportion of wasps e n d i n g up in e a c h of the four o u t c o m e s at e q u i l i b r i u m , a n d these figures t o o c a n b e tested a g a i n s t t h e o b s e r v e d d a t a . The

model's

equilibrium

theoretically

stable

that

predicts

that

deviations from e q u i l i b r i u m will be corrected by n a t u r a l selection. Brockmann studied two populations of wasps, one in M i c h i g a n and one in New Hampshire.

The

results w e r e d i f f e r e n t

the

two

populations.

M i c h i g a n t h e m o d e l failed t o p r e d i c t t h e o b s e r v e d results, a n d w e c o n c l u d e d t h a t i t w a s q u i t e i n a p p l i c a b l e t o t h e M i c h i g a n p o p u l a t i o n , for u n k n o w n reasons as discussed population

has

now

the

gone

original extinct

paper is

(the

probably

fact

that

the

fortuitous!).

Michigan The

New

Hampshire population, on the other hand, g a v e a c o n v i n c i n g fit to the p r e d i c t i o n s o f the m o d e l . T h e p r e d i c t e d e q u i l i b r i u m f r e q u e n c y o f e n t e r i n g

126

Selfish W a s p or Selfish S t r a t e g y ?

w a s 0.44, a n d t h e o b s e r v e d f r e q u e n c y w a s 0 . 4 1 . T h e m o d e l also successfully p r e d i c t e d t h e f r e q u e n c y o f e a c h o f t h e four ' o u t c o m e s ' i n t h e N e w H a m p s h i r e population.

Perhaps most importantly,

t h e a v e r a g e p a y o f f r e s u l t i n g from

d i g g i n g d e c i s i o n s d i d n o t differ s i g n i f i c a n t l y f r o m t h e a v e r a g e p a y o f f r e s u l t i n g from entering decisions. T h e p o i n t o f m y t e l l i n g this s t o r y i n t h e p r e s e n t b o o k has n o w f i n a l l y a r r i v e d . I w a n t t o c l a i m t h a t w e w o u l d h a v e f o u n d i t difficult t o d o this r e s e a r c h i f w e h a d t h o u g h t i n t e r m s o f individual s u c c e s s , r a t h e r t h a n i n t e r m s o f strategy ( p r o g r a m ) success a v e r a g e d o v e r all i n d i v i d u a l s . I f the m i x e d E S S h a d h a p p e n e d t o lie a t t h e b a l a n c e d p o l y m o r p h i s m e n d o f t h e c o n t i n u u m , i t w o u l d , i n d e e d , h a v e m a d e sense t o ask s o m e t h i n g l i k e t h e f o l l o w i n g . I s the s u c c e s s o f w a s p s t h a t d i g e q u a l t o t h e success o f w a s p s t h a t e n t e r ? W e w o u l d h a v e classified w a s p s a s d i g g e r s o r e n t e r e r s , a n d c o m p a r e d t h e t o t a l l i f e t i m e ' s e g g - l a y i n g success of i n d i v i d u a l s of the t w o types, p r e d i c t i n g that the t w o s u c c e s s s c o r e s s h o u l d b e e q u a l . B u t a s w e h a v e seen these w a s p s a r e n o t p o l y m o r p h i c . E a c h i n d i v i d u a l sometimes digs and sometimes enters. I t m i g h t b e t h o u g h t t h a t i t w o u l d h a v e b e e n e a s y t o d o s o m e t h i n g like the f o l l o w i n g . C l a s s i f y a l l i n d i v i d u a l s i n t o those t h a t e n t e r e d w i t h a p r o b a b i l i t y less t h a n 0 . 1 , t h o s e t h a t e n t e r e d w i t h a p r o b a b i l i t y b e t w e e n 0.1

a n d 0.2,

t h o s e w i t h a p r o b a b i l i t y b e t w e e n 0.2 a n d 0.3, b e t w e e n 0.3 a n d 0.4, 0.4 a n d 0.5, e t c . T h e n c o m p a r e t h e l i f e t i m e r e p r o d u c t i v e successes o f w a s p s i n the d i f f e r e n t c l a s s e s . B u t s u p p o s i n g w e d i d this, e x a c t l y w h a t w o u l d the E S S t h e o r y p r e d i c t ? A h a s t y first t h o u g h t is t h a t t h o s e w a s p s w i t h a p v a l u e close to the e q u i l i b r i u m p* should enjoy a h i g h e r success score than wasps with s o m e o t h e r v a l u e o f p : t h e g r a p h o f success a g a i n s t p s h o u l d p e a k a t a n ' o p t i m u m ' at p*. B u t p* is n o t r e a l l y an o p t i m u m v a l u e , it is an e v o l u t i o n a r i l y stable v a l u e . T h e t h e o r y expects that, w h e n p* is a c h i e v e d in the p o p u l a t i o n as a w h o l e , d i g g i n g a n d e n t e r i n g should be e q u a l l y successful. At e q u i l i b r i u m , therefore, we e x p e c t no correlation b e t w e e n a wasp's d i g g i n g probability and her success. If the p o p u l a t i o n deviates from e q u i l i b r i u m in the direction of t o o m u c h e n t e r i n g , t h e ' o p t i m u m ' c h o i c e r u l e b e c o m e s ' a l w a y s d i g ' (not ' d i g w i t h p r o b a b i l i t y p * ' ) . I f t h e p o p u l a t i o n d e v i a t e s f r o m e q u i l i b r i u m i n the other direction, the ' o p t i m u m ' policy is ' a l w a y s enter'.

If the p o p u l a t i o n

f l u c t u a t e s a t r a n d o m a r o u n d t h e e q u i l i b r i u m v a l u e , a n a l o g y w i t h sex r a t i o t h e o r y s u g g e s t s t h a t i n t h e l o n g r u n g e n e t i c t e n d e n c i e s t o a d o p t e x a c t l y the e q u i l i b r i u m v a l u e , p*, w i l l b e f a v o u r e d o v e r t e n d e n c i e s t o a d o p t a n y o t h e r c o n s i s t e n t v a l u e o f p ( W i l l i a m s 1 9 7 9 ) . B u t i n a n y o n e y e a r this a d v a n t a g e i s n o t p a r t i c u l a r l y l i k e l y t o b e e v i d e n t . T h e s e n s i b l e e x p e c t a t i o n o f the t h e o r y i s t h a t t h e r e s h o u l d b e n o s i g n i f i c a n t d i f f e r e n c e i n s u c c e s s r a t e s a m o n g the classes o f w a s p s . I n a n y c a s e this m e t h o d o f d i v i d i n g w a s p s u p i n t o classes p r e s u p p o s e s t h a t there is some consistent variation a m o n g wasps in d i g g i n g tendency. T h e

Selfish W a s p or Selfish S t r a t e g y ?

127

theory gives us no particular reason to expect that there should be any such variation. positive

I n d e e d , the a n a l o g y w i t h sex ratio t h e o r y just m e n t i o n e d g i v e s grounds

probability.

for

expecting

that

wasps

I n a c c o r d a n c e w i t h this,

should

not

vary

digging

a s t a t i s t i c a l test o n t h e a c t u a l d a t a

revealed no evidence of inter-individual variation in digging tendency. E v e n if there w e r e some i n d i v i d u a l v a r i a t i o n , the m e t h o d of c o m p a r i n g the success o f i n d i v i d u a l s w i t h different p v a l u e s w o u l d h a v e b e e n a c r u d e a n d i n s e n s i t i v e o n e for c o m p a r i n g t h e s u c c e s s r a t e s o f d i g g i n g a n d e n t e r i n g . T h i s c a n b e s e e n by an analogy. An agriculturalist wishes to c o m p a r e the efficacy of t w o fertilizers, A a n d B . H e t a k e s ten fields a n d d i v i d e s e a c h o f t h e m i n t o a l a r g e n u m b e r o f s m a l l plots. E a c h plot is treated, at r a n d o m , w i t h either A or B, a n d w h e a t is s o w n i n a l l the p l o t s o f a l l t h e fields. N o w , h o w s h o u l d h e c o m p a r e t h e t w o fertilizers? T h e s e n s i t i v e w a y i s t o t a k e t h e y i e l d s o f a l l t h e p l o t s t r e a t e d w i t h A and c o m p a r e t h e m w i t h the yields of all the plots treated w i t h B, across all ten f i e l d s . B u t t h e r e i s a n o t h e r , m u c h c r u d e r w a y . I t h a p p e n s t h a t i n t h e r a n d o m a l l o c a t i o n o f fertilizers t o p l o t s , s o m e o f t h e t e n f i e l d s r e c e i v e d a relatively large a m o u n t of fertilizer A, w h i l e others h a p p e n e d to be g i v e n a relatively large a m o u n t of B. T h e agriculturalist c o u l d , then, plot the overall yield of each of the ten fields against the p r o p o r t i o n of the field that w a s treated

with

fertilizer A

rather

than

If there

very

pronounced

d i f f e r e n c e i n q u a l i t y b e t w e e n t h e t w o f e r t i l i z e r s , this m e t h o d m i g h t j u s t s h o w i t u p , b u t far m o r e p r o b a b l y t h e d i f f e r e n c e w o u l d b e m a s k e d . T h e m e t h o d o f c o m p a r i n g the y i e l d s o f t h e t e n f i e l d s w o u l d b e efficient o n l y i f t h e r e i s v e r y h i g h b e t w e e n - f i e l d v a r i a n c e , a n d t h e r e i s n o p a r t i c u l a r r e a s o n t o e x p e c t this. I n the a n a l o g y , t h e t w o f e r t i l i z e r s s t a n d for d i g g i n g a n d e n t e r i n g . T h e fields a r e the w a s p s . T h e p l o t s a r e t h e e p i s o d e s o f t i m e t h a t i n d i v i d u a l w a s p s devote either to d i g g i n g or to entering. T h e crude m e t h o d of c o m p a r i n g d i g g i n g and entering is to plot the lifetime success of i n d i v i d u a l w a s p s against their p r o p o r t i o n a t e d i g g i n g t e n d e n c y .

The

sensitive

way

the

one

actually employed. We m a d e a detailed and exhaustive inventory of the time spent by e a c h w a s p o n e a c h b u r r o w w i t h w h i c h she w a s associated. individual duration,

female's each

adult

episode

lifetime

into

being designated

consecutive a digging

We divided each

episodes episode

of if the

known wasp

c o n c e r n e d b e g a n h e r a s s o c i a t i o n w i t h t h e b u r r o w b y d i g g i n g it. O t h e r w i s e , i t was designated an entering episode. T h e end of each episode was signalled b y t h e w a s p ' s l e a v i n g t h e nest for t h e last t i m e . T h i s i n s t a n t w a s a l s o t r e a t e d a s t h e start o f t h e n e x t b u r r o w e p i s o d e , e v e n t h o u g h t h e n e x t b u r r o w site had not, at the time, b e e n chosen. T h a t is to say, in o u r time a c c o u n t i n g , the t i m e s p e n t s e a r c h i n g for a n e w b u r r o w t o e n t e r , o r s e a r c h i n g for a p l a c e t o dig a new burrow, was designated retroactively as time 'spent' on that n e w

128

Selfish W a s p or Selfish S t r a t e g y ?

burrow.

It was

added

the

time

subsequently spent

p r o v i s i o n i n g the

b u r r o w w i t h k a t y d i d s , f i g h t i n g o t h e r w a s p s , f e e d i n g , s l e e p i n g , e t c . , u n t i l the w a s p left t h e n e w b u r r o w for t h e last t i m e . At the e n d of the season, therefore, we c o u l d a d d up the total n u m b e r of w a s p h o u r s s p e n t o n d u g - b u r r o w e p i s o d e s , a n d also the t o t a l n u m b e r o f w a s p h o u r s s p e n t o n e n t e r e d - b u r r o w e p i s o d e s . F o r t h e N e w H a m p s h i r e s t u d y these two

figures

were

8518.7

hours

and

6747.4

hours,

respectively.

This is

r e g a r d e d as t i m e s p e n t , or i n v e s t e d , for a r e t u r n , a n d t h e r e t u r n is m e a s u r e d i n n u m b e r s o f e g g s . T h e t o t a l n u m b e r o f e g g s l a i d a t t h e e n d o f the d u g b u r r o w e p i s o d e s (i.e. b y w a s p s t h a t h a d d u g t h e b u r r o w c o n c e r n e d ) i n t h e w h o l e N e w H a m p s h i r e p o p u l a t i o n d u r i n g t h e y e a r o f s t u d y w a s 82. T h e c o r r e s p o n d i n g n u m b e r for e n t e r e d - b u r r o w e p i s o d e s w a s 5 7 e g g s . T h e success r a t e o f t h e d i g g i n g s u b r o u t i n e w a s , t h e r e f o r e , 8 2 / 8 5 1 8 . 7 = 0.96 e g g s p e r 100 h o u r s . T h e s u c c e s s r a t e o f t h e e n t e r i n g s u b r o u t i n e w a s 5 7 / 6 7 4 7 . 4 = 0.84 e g g s p e r 100 h o u r s . T h e s e s u c c e s s scores a r e a v e r a g e d a c r o s s all t h e i n d i v i d u a l s w h o used the t w o subroutines. Instead of c o u n t i n g the n u m b e r of eggs laid in her lifetime b y a n i n d i v i d u a l w a s p â&#x20AC;&#x201D; t h e e q u i v a l e n t o f m e a s u r i n g the w h e a t y i e l d o f e a c h o f t h e ten f i e l d s i n t h e a n a l o g y â&#x20AC;&#x201D; w e c o u n t t h e n u m b e r o f e g g s l a i d ' b y ' t h e d i g g i n g (or e n t e r i n g ) s u b r o u t i n e p e r u n i t ' r u n n i n g t i m e ' o f the subroutine. T h e r e i s a n o t h e r r e s p e c t i n w h i c h i t w o u l d h a v e b e e n difficult for u s t o h a v e d o n e this a n a l y s i s i f w e h a d insisted o n t h i n k i n g i n t e r m s o f i n d i v i d u a l success. In o r d e r to solve the e q u a t i o n to predict the e q u i l i b r i u m entering f r e q u e n c y , w e h a d t o h a v e e m p i r i c a l e s t i m a t e s o f t h e e x p e c t e d payoffs o f e a c h of the

four

'outcomes'

(abandons,

remains

alone,

is joined, joins).

o b t a i n e d p a y o f f s c o r e s for t h e f o u r o u t c o m e s i n the s a m e w a y a s w e o b t a i n e d s u c c e s s s c o r e s for e a c h o f t h e t w o s t r a t e g i e s , d i g a n d e n t e r . W e a v e r a g e d o v e r a l l i n d i v i d u a l s , d i v i d i n g t h e t o t a l n u m b e r o f e g g s l a i d i n e a c h o u t c o m e b y the total time spent on episodes that ended up in that o u t c o m e . Since most i n d i v i d u a l s e x p e r i e n c e d a l l f o u r o u t c o m e s a t different t i m e s , i t i s n o t c l e a r h o w w e c o u l d h a v e o b t a i n e d t h e n e c e s s a r y e s t i m a t e s o f o u t c o m e payoffs i f w e h a d t h o u g h t in terms of i n d i v i d u a l success. N o t i c e t h e i m p o r t a n t r o l e o f time i n t h e c o m p u t a t i o n o f t h e ' s u c c e s s ' o f the d i g g i n g a n d e n t e r i n g subroutines (and o f the p a y o f f g i v e n b y e a c h o u t c o m e ) . T h e total n u m b e r of eggs laid ' b y ' the d i g g i n g subroutine is a poor measure of success until it has been d i v i d e d by the time spent on the subroutine. T h e n u m b e r of eggs laid by the t w o subroutines m i g h t be e q u a l , but if d i g g i n g episodes are on a v e r a g e t w i c e as l o n g as entering episodes, natural selection w i l l p r e s u m a b l y f a v o u r e n t e r i n g . I n fact r a t h e r m o r e e g g s w e r e l a i d ' b y ' the d i g g i n g s u b r o u t i n e t h a n by the entering one, but c o r r e s p o n d i n g l y m o r e time w a s spent on the d i g g i n g s u b r o u t i n e so the o v e r a l l success rates of the t w o w e r e a p p r o x i m a t e l y e q u a l . N o t i c e t o o t h a t w e d o n o t s p e c i f y w h e t h e r the e x t r a t i m e s p e n t o n d i g g i n g i s a c c o u n t e d for b y a g r e a t e r n u m b e r o f w a s p s

Selfish W a s p or Selfish S t r a t e g y ?

129

digging, or by each digging episode lasting longer. T h e distinction m a y be i m p o r t a n t for s o m e p u r p o s e s , b u t i t d o e s n ' t m a t t e r for t h e k i n d o f e c o n o m i c analysis we undertook. I t w a s c l e a r l y s t a t e d i n the o r i g i n a l p a p e r ( B r o c k m a n n , G r a f e n & D a w k i n s 1979), a n d must be repeated here, that the m e t h o d we used d e p e n d e d u p o n some

assumptions.

assumed,

for

instance,

that

wasp's

choice

s u b r o u t i n e o n a n y p a r t i c u l a r o c c a s i o n d i d n o t affect h e r s u r v i v a l o r s u c c e s s r a t e after t h e e n d o f t h e e p i s o d e c o n c e r n e d . T h u s t h e costs o f d i g g i n g w e r e assumed to be reflected totally in the time spent on d i g g i n g episodes, a n d the costs o f e n t e r i n g r e f l e c t e d i n t h e t i m e s p e n t o n e n t e r i n g e p i s o d e s . I f t h e a c t o f d i g g i n g h a d i m p o s e d s o m e e x t r a c o s t , s a y a risk o f w e a r a n d t e a r t o t h e l i m b s , s h o r t e n i n g life e x p e c t a t i o n , o u r s i m p l e t i m e - c o s t a c c o u n t i n g w o u l d n e e d t o be a m e n d e d . T h e success rates of the d i g g i n g a n d the e n t e r i n g subroutines would

have

expressed,

not

eggs

per

hour,

but

eggs

per

' o p p o r t u n i t y c o s t ' . O p p o r t u n i t y cost m i g h t still b e m e a s u r e d i n u n i t s o f t i m e , but d i g g i n g time w o u l d h a v e to be scaled up in a costlier c u r r e n c y than entering time, b e c a u s e e a c h h o u r spent in d i g g i n g shortens the e x p e c t a t i o n of effective

life

of the

individual.

Under

such

circumstances

might

n e c e s s a r y , i n spite o f a l l the difficulties, t o t h i n k i n t e r m s o f i n d i v i d u a l s u c c e s s rather than subroutine success. It is for this k i n d of r e a s o n t h a t C l u t t o n - B r o c k el al. (in press) a r e p r o b a b l y wise in their a m b i t i o n to m e a s u r e the total lifetime r e p r o d u c t i v e success rates o f t h e i r i n d i v i d u a l red d e e r s t a g s . I n t h e c a s e o f B r o c k m a n n ' s w a s p s , w e h a v e reason to think that our assumptions w e r e c o r r e c t , a n d that we w e r e justified in

ignoring individual

success

and

concentrating on

subroutine

success.

Therefore w h a t N. B. D a v i e s , in a lecture, j o c u l a r l y called the ' O x f o r d method'

(measuring

subroutine

(measuring i n d i v i d u a l success)

success)

and

the

'Cambridge

method'

m a y e a c h be justified in different c i r c u m -

stances. I am not s a y i n g that the O x f o r d m e t h o d should a l w a y s be used. T h e v e r y fact t h a t it is sometimes p r e f e r a b l e is sufficient to a n s w e r t h e c l a i m t h a t f i e l d w o r k e r s i n t e r e s t e d i n m e a s u r i n g costs a n d b e n e f i t s a l w a y s h a v e t o t h i n k in t e r m s of individual costs a n d b e n e f i t s . W h e n c o m p u t e r chess t o u r n a m e n t s a r e h e l d , a l a y m a n m i g h t i m a g i n e t h a t one c o m p u t e r plays against another. It is m o r e pertinent to describe the tournament as being between programs. A good p r o g r a m will consistently beat a poor p r o g r a m , and it doesn't m a k e a n y difference w h i c h physical computer cither program is running on.

Indeed the t w o p r o g r a m s could

swap physical computers every other g a m e , each one running alternately in a n I B M a n d a n I C L c o m p u t e r , a n d t h e result a t t h e e n d o f t h e t o u r n a m e n t will be the s a m e as if one p r o g r a m consistently ran in the I B M a n d the other consistently ran in the

ICL.

Similarly, to return to the a n a l o g y at the

b e g i n n i n g o f this c h a p t e r , the d i g g i n g s u b r o u t i n e ' r u n s ' i n a l a r g e n u m b e r o f different p h y s i c a l w a s p n e r v o u s s y s t e m s . E n t e r i n g i s t h e n a m e o f a r i v a l

130

Selfish W a s p or Selfish S t r a t e g y ?

subroutine

which

also

runs

many

different

wasp

nervous

systems,

i n c l u d i n g s o m e o f t h e s a m e p h y s i c a l n e r v o u s s y s t e m s as, a t o t h e r t i m e s , r u n the d i g g i n g s u b r o u t i n e . J u s t a s a p a r t i c u l a r I B M o r I C L c o m p u t e r f u n c t i o n s as the p h y s i c a l m e d i u m t h r o u g h w h i c h a n y of a v a r i e t y of chess p r o g r a m s c a n a c t o u t t h e i r skills, s o o n e i n d i v i d u a l w a s p i s t h e p h y s i c a l m e d i u m t h r o u g h w h i c h s o m e t i m e s the d i g g i n g subroutine, at other times the entering s u b r o u t i n e , a c t s o u t its c h a r a c t e r i s t i c b e h a v i o u r . As already explained, than programs,

I call d i g g i n g and entering 'subroutines', rather

b e c a u s e we h a v e a l r e a d y used

' p r o g r a m ' for the o v e r a l l

lifetime c h o o s i n g rules of an i n d i v i d u a l . An i n d i v i d u a l is r e g a r d e d as being p r o g r a m m e d w i t h a r u l e for c h o o s i n g t h e d i g g i n g o r t h e e n t e r i n g s u b r o u t i n e w i t h s o m e p r o b a b i l i t y p. In the special case of a p o l y m o r p h i s m , w h e r e each i n d i v i d u a l is e i t h e r a l i f e l o n g d i g g e r or a l i f e l o n g e n t e r e r , p b e c o m e s 1 or 0, and the categories p r o g r a m and subroutine b e c o m e synonymous. T h e beauty of c a l c u l a t i n g the e g g - l a y i n g success rates of subroutines rather than of i n d i v i d u a l s is that the p r o c e d u r e we a d o p t is the s a m e regardless of w h e r e on the

mixed

continuum

strategy we

continuum

still

predict

our

animals

that

the

are.

digging

Anywhere subroutine

along

the

should,

e q u i l i b r i u m , enjoy a success rate e q u a l to that of the entering subroutine. I t i s t e m p t i n g , t h o u g h r a t h e r m i s l e a d i n g , t o p u s h this l i n e o f t h o u g h t t o w h a t a p p e a r s t o b e its l o g i c a l c o n c l u s i o n , a n d t h i n k i n t e r m s o f s e l e c t i o n acting directly on subroutines in a subroutine pool. T h e population's nervous tissue, its d i s t r i b u t e d c o m p u t e r h a r d w a r e , i s i n h a b i t e d b y m a n y c o p i e s o f the d i g g i n g subroutine and m a n y copies of the entering subroutine. At any given time the p r o p o r t i o n of r u n n i n g copies of the d i g g i n g subroutine is p. T h e r e is a

critical

value

of p,

subroutines is equal. subroutine

pool,

c a l l e d p*,

which

the

success

rate

of the

two

I f e i t h e r o f t h e t w o b e c o m e s t o o n u m e r o u s i n the

natural

selection

penalizes

and

the

equilibrium

restored. The

reason

this

misleading

that

selection

really

works

the

d i f f e r e n t i a l s u r v i v a l o f a l l e l e s i n a g e n e p o o l . E v e n w i t h the m o s t l i b e r a l i m a g i n a b l e interpretation of w h a t we m e a n by g e n e control, there is no useful sense i n w h i c h t h e d i g g i n g s u b r o u t i n e a n d t h e e n t e r i n g s u b r o u t i n e c o u l d b e t h o u g h t o f a s b e i n g c o n t r o l l e d b y a l t e r n a t i v e a l l e l e s . I f for n o o t h e r r e a s o n , this i s b e c a u s e t h e w a s p s , a s w e h a v e s e e n , a r e n o t p o l y m o r p h i c , b u t a r e p r o g r a m m e d w i t h a s t o c h a s t i c r u l e for c h o o s i n g t o d i g o r e n t e r o n a n y g i v e n o c c a s i o n . N a t u r a l s e l e c t i o n m u s t f a v o u r g e n e s t h a t a c t o n the s t o c h a s t i c p r o g r a m o f i n d i v i d u a l s , i n p a r t i c u l a r c o n t r o l l i n g the v a l u e o f p , t h e d i g g i n g p r o b a b i l i t y . N e v e r t h e l e s s , a l t h o u g h i t i s m i s l e a d i n g i f t a k e n t o o l i t e r a l l y , the m o d e l o f s u b r o u t i n e s c o m p e t i n g d i r e c t l y for r u n n i n g t i m e i n n e r v o u s s y s t e m s p r o v i d e s s o m e useful s h o r t c u t s t o g e t t i n g t h e r i g h t a n s w e r . T h e i d e a of selection in a n o t i o n a l pool of subroutines also leads us to think about yet another time-scale on which an analogue of frequency-dependent

Selfish W a s p o r Selfish S t r a t e g y ?

131

selection m i g h t o c c u r . T h e present m o d e l a l l o w s that from d a y t o d a y the observed n u m b e r o f r u n n i n g copies o f the d i g g i n g s u b r o u t i n e m i g h t c h a n g e , as individual wasps o b e y i n g their stochastic p r o g r a m s switch their h a r d w a r e from o n e s u b r o u t i n e t o a n o t h e r . S o far I h a v e i m p l i e d t h a t a g i v e n w a s p i s born

with

built-in

predilection

dig

with

certain

characteristic

probability. But it is also theoretically possible that wasps m i g h t be e q u i p p e d t o m o n i t o r t h e p o p u l a t i o n a r o u n d t h e m w i t h t h e i r sense o r g a n s , a n d c h o o s e to dig or enter a c c o r d i n g l y . In E S S j a r g o n focusing on the i n d i v i d u a l l e v e l , this w o u l d b e r e g a r d e d a s a c o n d i t i o n a l s t r a t e g y , e a c h w a s p o b e y i n g a n ' i f c l a u s e ' o f t h e f o l l o w i n g f o r m : ' I f y o u see a l a r g e a m o u n t o f e n t e r i n g g o i n g on around you, dig, otherwise enter.' M o r e practically, each w a s p might be p r o g r a m m e d t o f o l l o w a r u l e o f t h u m b s u c h a s : ' S e a r c h for a b u r r o w t o e n t e r ; i f y o u h a v e n o t f o u n d o n e after a t i m e t , g i v e u p a n d d i g y o u r o w n . ' A s it

happens

our

evidence

goes

against

such

'conditional

strategy'

( B r o c k m a n n & D a w k i n s 1 9 7 9 ) , but the theoretical possibility is interesting. F r o m t h e p r e s e n t p o i n t o f v i e w w h a t i s p a r t i c u l a r l y i n t e r e s t i n g i s this. W e could

still

analyse

the

data

terms

of a

notional

selection

between

subroutines in a subroutine p o o l , even t h o u g h the selection process l e a d i n g to the r e s t o r a t i o n o f t h e e q u i l i b r i u m w h e n p e r t u r b e d w o u l d n o t b e n a t u r a l selection on a g e n e r a t i o n a l time-scale. It w o u l d be a d e v e l o p m e n t a l l y stable s t r a t e g y o r D S S ( D a w k i n s 1980) r a t h e r t h a n a n E S S , b u t t h e m a t h e m a t i c s c o u l d b e m u c h the s a m e ( H a r l e y 1 9 8 1 ) . I m u s t w a r n t h a t a n a l o g i c a l r e a s o n i n g o f this sort i s a l u x u r y t h a t w e d a r e not i n d u l g e unless we are c a p a b l e of c l e a r l y seeing the limitations of the analogy.

T h e r e are real

and

important distinctions

between

Darwinian

selection and b e h a v i o u r a l assessment, just as there w e r e real a n d i m p o r t a n t distinctions b e t w e e n a b a l a n c e d p o l y m o r p h i s m and

true m i x e d

evol-

utionarily stable strategy. Just as the v a l u e of p, the i n d i v i d u a l ' s d i g g i n g probability, w a s considered to be adjusted by n a t u r a l selection, so, in the b e h a v i o u r a l a s s e s s m e n t m o d e l , t , t h e i n d i v i d u a l ' s c r i t e r i o n for r e s p o n d i n g t o the frequency of d i g g i n g in the p o p u l a t i o n , is p r e s u m a b l y influenced by natural

selection.

The

concept

of selection

among

subroutines

subroutine pool blurs some important distinctions while p o i n t i n g up some i m p o r t a n t s i m i l a r i t i e s : t h e w e a k n e s s e s o f this w a y o f t h i n k i n g a r e l i n k e d t o its strengths. W h a t I do r e m e m b e r is that, w h e n we w e r e a c t u a l l y wrestling w i t h the difficulties o f t h e w a s p a n a l y s i s , o n e o f o u r m a i n l e a p s f o r w a r d occurred w h e n , u n d e r the influence o f A . G r a f e n , w e k i c k e d the h a b i t o f worrying imaginary

about world

individual where

reproductive

'digging'

success

competed

and

directly

switched with

'entering';

c o m p e t e d for ' r u n n i n g t i m e ' i n f u t u r e n e r v o u s s y s t e m s . T h i s chapter has been an interlude, a digression. I h a v e not been trying to a r g u e that 'subroutines', or 'strategies' are really true replicators, true units of natural selection. T h e y are not. G e n e s and fragments of g e n o m e s are true

132

Selfish W a s p or Selfish S t r a t e g y ?

r e p l i c a t o r s . S u b r o u t i n e s a n d s t r a t e g i e s c a n b e t h o u g h t o f for c e r t a i n p u r p o s e s as if they w e r e replicators, but w h e n those purposes h a v e been served we m u s t r e t u r n t o r e a l i t y . N a t u r a l s e l e c t i o n r e a l l y h a s t h e effect o f c h o o s i n g b e t w e e n alleles in w a s p gene-pools, alleles w h i c h influence the probability t h a t i n d i v i d u a l w a s p s w i l l e n t e r o r d i g . W e t e m p o r a r i l y l a i d this k n o w l e d g e a s i d e a n d e n t e r e d a n i m a g i n a r y w o r l d o f ' i n t e r - s u b r o u t i n e s e l e c t i o n ' for a s p e c i f i c m e t h o d o l o g i c a l p u r p o s e . W e w e r e j u s t i f i e d i n d o i n g this b e c a u s e w e w e r e a b l e to m a k e certain assumptions a b o u t the wasps, and because of the a l r e a d y d e m o n s t r a t e d m a t h e m a t i c a l e q u i v a l e n c e b e t w e e n the various w a y s in w h i c h a m i x e d evolutionarily stable strategy can be put together. As in the case of C h a p t e r 4,

t h e p u r p o s e o f this c h a p t e r h a s b e e n t o

u n d e r m i n e our c o n f i d e n c e in the i n d i v i d u a l - c e n t r e d v i e w of teleonomy, in this c a s e b y s h o w i n g t h a t i t i s n o t a l w a y s useful, i n p r a c t i c e , t o m e a s u r e i n d i v i d u a l s u c c e s s i f w e a r e t o s t u d y n a t u r a l s e l e c t i o n i n the f i e l d . T h e n e x t t w o chapters discuss a d a p t a t i o n s w h i c h , b y their v e r y nature, w e c a n n o t e v e n b e g i n t o u n d e r s t a n d i f w e insist o n t h i n k i n g i n t e r m s o f i n d i v i d u a l benefit.

8 O u t l a w s and Modifiers

N a t u r a l selection is the process w h e r e b y replicators o u t - p r o p a g a t e e a c h o t h e r . T h e y d o this b y e x e r t i n g p h e n o t y p i c effects o n t h e w o r l d , a n d i t i s often c o n v e n i e n t t o see t h o s e p h e n o t y p i c effects a s g r o u p e d t o g e t h e r i n discrete 'vehicles' such as i n d i v i d u a l organisms. T h i s gives s u b s t a n c e to the orthodox doctrine that each i n d i v i d u a l b o d y c a n be t h o u g h t of as a unitary agent m a x i m i z i n g one quantityâ&#x20AC;&#x201D;'fitness', various notions of w h i c h will be discussed i n C h a p t e r 1 0 . B u t the i d e a o f i n d i v i d u a l b o d i e s m a x i m i z i n g o n e q u a n t i t y relies o n t h e a s s u m p t i o n t h a t r e p l i c a t o r s a t d i f f e r e n t l o c i w i t h i n a b o d y can be e x p e c t e d to ' c o o p e r a t e ' . In other w o r d s we must assume that the a l l e l e t h a t s u r v i v e s best a t a n y g i v e n l o c u s t e n d s t o b e t h e o n e t h a t i s b e s t for the g e n o m e as a w h o l e . T h i s is i n d e e d o f t e n t h e c a s e . A r e p l i c a t o r t h a t e n s u r e s its o w n s u r v i v a l a n d p r o p a g a t i o n d o w n t h e g e n e r a t i o n s b y c o n f e r r i n g o n its s u c c e s s i v e b o d i e s r e s i s t a n c e t o a d a n g e r o u s d i s e a s e , s a y , w i l l t h e r e b y b e n e f i t all the o t h e r g e n e s i n t h e s u c c e s s i v e g e n o m e s o f w h i c h i t i s a m e m b e r . B u t i t i s a l s o e a s y t o i m a g i n e c a s e s w h e r e a g e n e m i g h t p r o m o t e its o w n survival while

h a r m i n g the s u r v i v a l c h a n c e s of most

of the

rest o f t h e

genome. Following A l e x a n d e r and Borgia (1978) I shall call such genes outlaws. I d i s t i n g u i s h t w o m a i n classes o f o u t l a w s . A n ' a l l e l i c o u t l a w ' i s d e f i n e d a s a r e p l i c a t o r t h a t h a s a p o s i t i v e s e l e c t i o n c o e f f i c i e n t a t its o w n l o c u s b u t for w h i c h , a t m o s t o t h e r l o c i , t h e r e i s s e l e c t i o n i n f a v o u r o f r e d u c i n g its effect a t its o w n l o c u s . A n e x a m p l e i s a ' s e g r e g a t i o n d i s t o r t e r ' o r ' m e i o t i c d r i v e ' g e n e . I t i s f a v o u r e d a t its o w n l o c u s t h r o u g h g e t t i n g i t s e l f i n t o m o r e t h a n 5 0 p e r c e n t o f the g a m e t e s p r o d u c e d . A t t h e s a m e t i m e , g e n e s a t o t h e r l o c i w h o s e effect i s t o r e d u c e t h e s e g r e g a t i o n d i s t o r t i o n w i l l b e f a v o u r e d b y s e l e c t i o n a t their respective loci. H e n c e the s e g r e g a t i o n distorter is an o u t l a w . T h e other m a i n class o f o u t l a w , t h e ' l a t e r a l l y s p r e a d i n g o u t l a w ' , i s less f a m i l i a r . I t w i l l b e discussed i n the n e x t c h a p t e r . F r o m t h e v i e w p o i n t o f this b o o k t h e r e i s a sense i n w h i c h w e e x p e c t a l l genes to be potential o u t l a w s , so m u c h so that the v e r y t e r m m i g h t seem 133

134

O u t l a w s and M o d i f i e r s

s u p e r f l u o u s . O n t h e o t h e r h a n d i t c a n b e a r g u e d , firstly, t h a t o u t l a w s a r e u n l i k e l y to be f o u n d in n a t u r e b e c a u s e at a n y g i v e n locus the allele that is best a t s u r v i v i n g w i l l n e a r l y a l w a y s t u r n o u t t o b e t h e a l l e l e t h a t i s best a t promoting

the

survival

and

reproduction

of the

organism

whole.

S e c o n d l y various authors, following L e i g h ( 1 9 7 1 ) , h a v e argued that, even if o u t l a w s did arise a n d w e r e t e m p o r a r i l y favoured by selection, they are likely, i n A l e x a n d e r a n d B o r g i a ' s w o r d s , ' t o h a v e t h e i r effects n u l l i f i e d , a t least t o t h e e x t e n t t h a t t h e y a r e o u t n u m b e r e d b y t h e o t h e r g e n e s i n the g e n o m e ' . I t d o e s , i n d e e d , f o l l o w f r o m t h e d e f i n i t i o n o f a n o u t l a w t h a t this s h o u l d t e n d t o h a p p e n . T h e s u g g e s t i o n b e i n g m a d e i s t h a t , w h e n e v e r a n o u t l a w arises, s e l e c t i o n w i l l f a v o u r m o d i f i e r g e n e s a t s o m a n y o t h e r loci t h a t n o t r a c e w i l l r e m a i n o f t h e p h e n o t y p i c effects o f t h e o u t l a w . O u t l a w s w i l l t h e r e f o r e , t h e suggestion goes, be transient p h e n o m e n a . T h i s w o u l d not, h o w e v e r , make t h e m n e g l i g i b l e : i f g e n o m e s a r e r i d d l e d w i t h o u t l a w - s u p p r e s s i n g g e n e s , this, i n itself, i s a n i m p o r t a n t effect o f o u t l a w g e n e s , e v e n i f n o t r a c e r e m a i n s o f t h e i r o r i g i n a l p h e n o t y p i c effects. I s h a l l d i s c u s s t h e r e l e v a n c e o f m o d i f i e r g e n e s in a l a t e r s e c t i o n . T h e r e is a sense in w h i c h a ' v e h i c l e ' is w o r t h y of the n a m e in inverse proportion to the n u m b e r of o u t l a w replicators that it contains. T h e idea of a discrete v e h i c l e m a x i m i z i n g a u n i t a r y q u a n t i t y â&#x20AC;&#x201D; f i t n e s s â&#x20AC;&#x201D; d e p e n d s on the a s s u m p t i o n t h a t t h e r e p l i c a t o r s t h a t i t s e r v e s a l l s t a n d t o g a i n f r o m the s a m e properties a n d b e h a v i o u r of their shared vehicle. If some replicators w o u l d b e n e f i t f r o m t h e v e h i c l e ' s d o i n g a c t X , w h i l e o t h e r r e p l i c a t o r s w o u l d benefit f r o m its d o i n g a c t Y , t h a t v e h i c l e i s c o r r e s p o n d i n g l y less l i k e l y t o b e h a v e a s a coherent unit. governed

It will h a v e the attributes of a h u m a n o r g a n i z a t i o n that is a

quarrelsome

committeeâ&#x20AC;&#x201D;pulled

this

way

and

that,

and

unable to show decisiveness and consistency of purpose. T h e r e is a superficial a n a l o g y here with g r o u p selection.

O n e o f the

p r o b l e m s of the t h e o r y that g r o u p s of o r g a n i s m s function as effective g e n e v e h i c l e s i s t h a t o u t l a w s (from t h e g r o u p ' s p o i n t o f v i e w ) a r e v e r y l i k e l y t o a r i s e a n d b e f a v o u r e d b y s e l e c t i o n . I f w e a r e h y p o t h e s i z i n g the e v o l u t i o n o f individual restraint through g r o u p selection, a gene that makes individuals b e h a v e selfishly i n a n o t h e r w i s e a l t r u i s t i c g r o u p i s a n a l o g o u s t o a n o u t l a w . I t is the n e a r i n e v i t a b i l i t y of such ' o u t l a w s ' arising that has d a s h e d the hopes of m a n y a g r o u p selection modeller. T h e i n d i v i d u a l b o d y i s a m u c h m o r e p e r s u a s i v e g e n e v e h i c l e t h a n the g r o u p b e c a u s e , a m o n g o t h e r r e a s o n s , o u t l a w r e p l i c a t o r s w i t h i n the b o d y a r e not v e r y likely to be strongly favoured over their alleles. T h e fundamental r e a s o n for

this

the drilled

formality of the

mechanisms of individual

r e p r o d u c t i o n , t h e ' g a v o t t e o f c h r o m o s o m e s ' a s H a m i l t o n ( 1 9 7 5 b ) c a l l e d it. I f all replicators ' k n o w ' that their o n l y h o p e of g e t t i n g into the next generation is v i a the o r t h o d o x b o t t l e n e c k of i n d i v i d u a l r e p r o d u c t i o n , all will h a v e the s a m e 'interests at h e a r t ' ; s u r v i v a l of the shared b o d y to r e p r o d u c t i v e age,

O u t l a w s and M o d i f i e r s

135

successful c o u r t s h i p a n d r e p r o d u c t i o n o f t h e s h a r e d b o d y , a n d a successful o u t c o m e to the parental enterprise of the shared b o d y .

E n l i g h t e n e d self-

interest d i s c o u r a g e s o u t l a w r y w h e n all r e p l i c a t o r s h a v e a n e q u a l s t a k e i n t h e normal r e p r o d u c t i o n of the same shared b o d y . Where

reproduction

asexual

the

stake

equal

and

total,

for

all

r e p l i c a t o r s h a v e t h e s a m e 100 p e r c e n t c h a n c e o f f i n d i n g t h e m s e l v e s i n e v e r y child

produced

their joint

c o r r e s p o n d i n g c h a n c e for

efforts.

Where

reproduction

is sexual

each replicator is only half as great,

but

the the

ritualized courtliness of meiosis, H a m i l t o n ' s ' g a v o t t e ' , l a r g e l y succeeds in g u a r a n t e e i n g to e a c h allele an equal c h a n c e of r e a p i n g the benefits of the success o f t h e j o i n t r e p r o d u c t i v e e n t e r p r i s e . I t is, o f c o u r s e , a n o t h e r q u e s t i o n why t h e g a v o t t e

of t h e c h r o m o s o m e s

is so c o u r t l y .

immensely

important question w h i c h I shall e v a d e on a simple p l e a of c o w a r d i c e . It is one o f a set o f q u e s t i o n s a b o u t t h e e v o l u t i o n o f g e n e t i c s y s t e m s w i t h w h i c h b e t t e r m i n d s t h a n m i n e h a v e w r e s t l e d m o r e o r less u n s u c c e s s f u l l y ( W i l l i a m s 1 9 7 5 , 1 9 8 0 ; M a y n a r d S m i t h 1 9 7 8 a ) , a set o f q u e s t i o n s w h i c h m o v e d W i l l i a m s t o r e m a r k t h a t ' t h e r e i s a k i n d o f crisis a t h a n d i n e v o l u t i o n a r y b i o l o g y ' . I d o n ' t u n d e r s t a n d w h y m e i o s i s i s t h e w a y i t is, b u t g i v e n t h a t i t i s m u c h f o l l o w s . I n particular the o r g a n i z e d

f a i r - d e a l i n g o f m e i o s i s h e l p s t o a c c o u n t for t h e

c o h e r e n c e a n d h a r m o n y w h i c h u n i t e s t h e p a r t s o f a n i n d i v i d u a l o r g a n i s m . If, a t t h e l e v e l o f t h e group o f i n d i v i d u a l s a s p o t e n t i a l v e h i c l e , t h e p r i v i l e g e o f reproduction was g r a n t e d w i t h the same scrupulous p r o b i t y in a similarly well-disciplined 'gavotte of the organisms', g r o u p selection m i g h t b e c o m e a more plausible theory of e v o l u t i o n . But, w i t h the possible e x c e p t i o n of the v e r y s p e c i a l c a s e o f t h e s o c i a l insects, g r o u p ' r e p r o d u c t i o n ' i s a n a r c h i c a l a n d favourable to individual o u t l a w r y . E v e n social insect colonies will never s e e m fully h a r m o n i o u s a g a i n after T r i v e r s a n d H a r e ' s i n g e n i o u s a n a l y s i s o f sex r a t i o c o n f l i c t s (see C h a p t e r 4 ) . T h i s c o n s i d e r a t i o n tells u s w h e r e w e s h o u l d l o o k first i f w e w a n t t o d i s c o v e r o u t l a w s w i t h i n the i n d i v i d u a l b o d y a s v e h i c l e . A n y r e p l i c a t o r t h a t m a n a g e d t o s u b v e r t t h e rules o f m e i o s i s s o t h a t i t e n j o y e d m o r e t h a n t h e o r d a i n e d 5 0 per cent c h a n c e of e n d i n g up in a g a m e t e w o u l d , other things b e i n g e q u a l , tend t o b e f a v o u r e d o v e r its a l l e l e s i n n a t u r a l s e l e c t i o n . S u c h g e n e s a r e k n o w n t o g e n e t i c i s t s u n d e r the n a m e o f m e i o t i c d r i v e g e n e s o r s e g r e g a t i o n d i s t o r t e r s . I h a v e already used

them

as an e x a m p l e to illustrate my definition of an

outlaw.

'Genes that beat the system' T h e a c c o u n t of segregation distorters that I shall m a i n l y follow is that of C r o w ( 1 9 7 9 ) , w h o uses l a n g u a g e c o n g e n i a l t o t h e s p i r i t o f this b o o k . H i s paper is called ' G e n e s that violate M e n d e l ' s rules', and it ends as follows: 'The

Mendelian

system

works

with

maximum

efficiency

only

if it

s c r u p u l o u s l y fair t o all g e n e s . I t i s i n c o n s t a n t d a n g e r , h o w e v e r , o f b e i n g

136

O u t l a w s and M o d i f i e r s

upset

genes

that

subvert

the

meiotic

process

their

own

a d v a n t a g e . . . T h e r e are m a n y refinements of meiosis a n d sperm formation whose purpose is a p p a r e n t l y to render such cheating unlikely. A n d yet some genes h a v e m a n a g e d to beat the system.' C r o w suggests that segregation distorters m a y b e m u c h m o r e c o m m o n t h a n w e o r d i n a r i l y r e a l i z e , for t h e m e t h o d s o f g e n e t i c i s t s a r e n o t w e l l g e a r e d t o d e t e c t i n g t h e m , e s p e c i a l l y i f t h e y p r o d u c e o n l y s l i g h t , q u a n t i t a t i v e effects. T h e S D g e n e s i n Drosophila a r e p a r t i c u l a r l y w e l l s t u d i e d , a n d h e r e t h e r e i s some

indication

homologous

the

chromosomes

actual are

still

mechanism paired

of distortion. during

'While

meiosis,

c h r o m o s o m e m i g h t do something to its n o r m a l p a r t n e r ( a n d r i v a l )

the

the SD

that later

causes a dysfunction of the sperm r e c e i v i n g the n o r m a l c h r o m o s o m e . . . SD might

actually break

the other c h r o m o s o m e '

(Crow

1979,

my macabre

emphasis). T h e r e is e v i d e n c e that, in S D - h e t e r o z y g o u s individuals, sperms not c o n t a i n i n g the S D c h r o m o s o m e h a v e a b n o r m a l , a n d p r e s u m a b l y faulty, tails.

might

thought,

then,

that

the faulty

tail

results f r o m s o m e

s a b o t a g e t o t h e n o n - S D c h r o m o s o m e i n t h e s p e r m s c o n t a i n i n g it. T h i s c a n n o t be the w h o l e story, as C r o w points out, because sperms h a v e been shown to b e c a p a b l e o f d e v e l o p i n g n o r m a l tails w i t h o u t a n y c h r o m o s o m e s a t a l l . I n d e e d , the w h o l e sperm p h e n o t y p e seems usually to be u n d e r the control of t h e d i p l o i d g e n o t y p e o f t h e f a t h e r , n o t its o w n h a p l o i d g e n o t y p e ( B e a t t y & G l u e c k s o h n - W a e l s c h 1 9 7 2 ; see b e l o w ) . ' T h e effect o f t h e S D c h r o m o s o m e o n its h o m o l o g u e c a n n o t , t h e n , b e s i m p l y t o i n a c t i v a t e s o m e f u n c t i o n , b e c a u s e n o f u n c t i o n i s r e q u i r e d . S D m u s t s o m e h o w i n d u c e its p a r t n e r t o c o m m i t a positive act of sabotage.' S e g r e g a t i o n distorters prosper w h e n rare, because the chances are then g o o d that their v i c t i m s are alleles, not copies. W h e n c o m m o n , the distorter t e n d s t o o c c u r h o m o z y g o u s l y , a n d t h e r e f o r e s a b o t a g e s c o p i e s o f itself, m a k i n g t h e o r g a n i s m v i r t u a l l y s t e r i l e . T h e s t o r y i s m o r e c o m p l i c a t e d t h a n this, b u t c o m p u t e r simulations described by C r o w suggest that a stable proportion of segregation distorter genes will be maintained

a frequency somewhat

g r e a t e r t h a n w o u l d b e a c c o u n t e d for b y r e c u r r e n t m u t a t i o n a l o n e . T h e r e i s s o m e e v i d e n c e t h a t this i s s o i n r e a l life. In order to qualify as an o u t l a w , a segregation distorter must do harm to m o s t o f t h e rest o f t h e g e n o m e , n o t j u s t t o its a l l e l e s . S e g r e g a t i o n distorters c o u l d h a v e this effect b y r e d u c i n g t h e t o t a l g a m e t e c o u n t o f t h e i n d i v i d u a l . E v e n i f t h e y d i d n o t d o this, t h e r e i s a m o r e g e n e r a l r e a s o n for e x p e c t i n g there to be selection at other loci in favour of suppressing them ( C r o w 1979). T h e a r g u m e n t needs to be d e v e l o p e d stage by stage. Firstly m a n y genes, w h e n c o m p a r e d w i t h t h e i r a l l e l e s , h a v e s e v e r a l p l e i o t r o p i c effects. L e w o n t i n ( 1 9 7 4 ) g o e s s o far a s t o s p e a k o f ' . . . t h e u n d o u b t e d t r u t h t h a t e v e r y g e n e affects e v e r y c h a r a c t e r . . .'. W h i l e t o c a l l this a n ' u n d o u b t e d t r u t h ' m a y b e ,

O u t l a w s and M o d i f i e r s

137

t o p u t i t m i l d l y , a n e n t h u s i a s t i c e x a g g e r a t i o n , for m y p u r p o s e s I n e e d o n l y a s s u m e t h a t m o s t n e w m u t a t i o n s h a v e s e v e r a l p l e i o t r o p i c effects. N o w i t i s r e a s o n a b l e t o e x p e c t t h a t m o s t s u c h p l e i o t r o p i c effects w i l l b e d e l e t e r i o u s â&#x20AC;&#x201D; m u t a t i o n a l effects u s u a l l y a r e . I f a g e n e i s f a v o u r e d b y s e l e c t i o n r e s u l t i n g f r o m o n e b e n e f i c i a l effect, this w i l l b e b e c a u s e t h e a d v a n t a g e s o f its b e n e f i c i a l effect q u a n t i t a t i v e l y o u t w e i g h t h e d i s a d v a n t a g e s o f its o t h e r effects. Normally,

'beneficial'

and

'deleterious',

deleterious to the w h o l e o r g a n i s m .

mean

beneficial

and

In the case of a segregation distorter,

h o w e v e r , t h e b e n e f i c i a l effect w e a r e t a l k i n g a b o u t i s b e n e f i c i a l t o t h e g e n e a l o n e . A n y p l e i o t r o p i c effects t h a t i t m a y h a v e o n t h e b o d y a r e p r e t t y l i k e l y to be deleterious to the w h o l e b o d y ' s s u r v i v a l a n d r e p r o d u c t i o n . S e g r e g a t i o n distorters a r e t h e r e f o r e , o n t h e w h o l e , l i k e l y t o b e o u t l a w s : w e e x p e c t t h a t s e l e c t i o n w i l l f a v o u r g e n e s a t o t h e r l o c i w h o s e p h e n o t y p i c effect i s t o r e d u c e the s e g r e g a t i o n d i s t o r t i o n . T h i s b r i n g s u s t o t h e t o p i c o f m o d i f i e r s .

Modifiers T h e classic p r o v i n g g r o u n d for t h e t h e o r y o f m o d i f i e r g e n e s w a s R . A . F i s h e r ' s e x p l a n a t i o n o f t h e e v o l u t i o n o f d o m i n a n c e . F i s h e r ( 1 9 3 0 a , b u t see C h a r l e s w o r t h 1 9 7 9 ) s u g g e s t e d t h a t t h e b e n e f i c i a l effects o f a g i v e n g e n e t e n d t o b e c o m e d o m i n a n t t h r o u g h t h e s e l e c t i o n o f m o d i f i e r s , w h i l e its d e l e t e r i o u s effects t e n d t o b e c o m e r e c e s s i v e . H e n o t e d t h a t d o m i n a n c e a n d r e c e s s i v e n e s s are not properties of genes themselves, b u t properties of their p h e n o t y p i c effects. I n d e e d a g i v e n g e n e c a n b e d o m i n a n t i n o n e o f its p l e i o t r o p i c effects a n d r e c e s s i v e i n a n o t h e r . A p h e n o t y p i c effect o f a g e n e i s t h e j o i n t p r o d u c t o f itself a n d its e n v i r o n m e n t , a n e n v i r o n m e n t w h i c h i n c l u d e s t h e rest o f t h e g e n o m e . T h i s i n t e r a c t i v e v i e w o f g e n e a c t i o n , w h i c h F i s h e r h a d t o a r g u e for at length in 1930, h a d b e c o m e so well a c c e p t e d by 1958 that he w a s a b l e to t a k e i t for g r a n t e d i n t h e s e c o n d e d i t i o n o f his g r e a t b o o k . I t f o l l o w s f r o m i t t h a t d o m i n a n c e o r r e c e s s i v e n e s s , l i k e a n y o t h e r p h e n o t y p i c effect, m a y i t s e l f e v o l v e , t h r o u g h t h e s e l e c t i o n o f o t h e r g e n e s e l s e w h e r e i n t h e g e n o m e , a n d this w a s the basis o f F i s h e r ' s t h e o r y o f d o m i n a n c e . A l t h o u g h t h e s e o t h e r g e n e s a r e k n o w n as modifiers, it is n o w realized that there is no separate c a t e g o r y of modifier genes as distinct from major genes. R a t h e r , a n y g e n e m a y serve as m o d i f i e r o f t h e p h e n o t y p i c effects o f a n y o t h e r g e n e . I n d e e d , a n y g i v e n g e n e ' s p h e n o t y p i c effects a r e s u s c e p t i b l e t o m o d i f i c a t i o n b y m a n y o t h e r g e n e s i n t h e genome, genes w h i c h themselves m a y h a v e m a n y other major and minor effects

(Mayr

theoretical

1963).

purposes,

Modifiers for

have

instance

been the

invoked

for

various

other

Medawar/Williams/Hamilton

progression of theories of the e v o l u t i o n of senescence ( K i r k w o o d & H o l l i d a y 1979)T h e r e l e v a n c e o f modifiers t o the subject o f o u t l a w genes has a l r e a d y b e e n alluded

to.

Since

any

gene's

phenotypic

effects

may

subject

138

O u t l a w s and M o d i f i e r s

modification by genes at other loci, and since outlaws, by definition, work to t h e d e t r i m e n t o f t h e rest o f t h e g e n o m e , w e s h o u l d e x p e c t s e l e c t i o n t o f a v o u r g e n e s t h a t h a p p e n t o h a v e t h e effect o f n e u t r a l i z i n g the o u t l a w ' s d e l e t e r i o u s effects o n t h e b o d y a s a w h o l e . S u c h m o d i f i e r s w o u l d b e f a v o u r e d o v e r alleles t h a t d i d n o t i n f l u e n c e t h e o u t l a w ' s effects. H i c k e y a n d C r a i g ( 1 9 6 6 ) , s t u d y i n g a s e x - r a t i o d i s t o r t i n g g e n e (see b e l o w ) in t h e y e l l o w - f e v e r m o s q u i t o Aedes aegypti, f o u n d e v i d e n c e for e v o l u t i o n a r y d i m i n u t i o n o f t h e d i s t o r t i n g effect which

could

interpreted

r e s u l t i n g from

the selection of modifiers

(though their o w n interpretation was slightly different). If outlaws do, in general,

call

forth

the

selection

of suppressing

modifiers,

there

will

p r e s u m a b l y b e a n a r m s r a c e b e t w e e n e a c h o u t l a w a n d its m o d i f i e r s . A s i n a n y o t h e r a r m s r a c e ( C h a p t e r 4 ) , w e n o w ask w h e t h e r t h e r e i s a n y g e n e r a l r e a s o n t o e x p e c t o n e side t o p r e v a i l o v e r t h e o t h e r . L e i g h ( 1 9 7 1 , 1 9 7 7 ) , A l e x a n d e r a n d B o r g i a ( 1 9 7 8 ) , K u r l a n d ( 1 9 7 9 , 1 9 8 0 ) , H a r t u n g (in p r e s s ) , a n d o t h e r s s u g g e s t t h a t t h e r e i s j u s t s u c h a g e n e r a l r e a s o n . S i n c e , for a n y single o u t l a w , suppressing modifiers m a y arise a n y w h e r e in the g e n o m e , t h e o u t l a w w i l l b e o u t n u m b e r e d . A s L e i g h ( 1 9 7 1 ) p u t s it, ' I t i s a s i f w e h a d t o d o w i t h a p a r l i a m e n t o f g e n e s : e a c h a c t s i n its o w n self-interest, b u t i f its acts h u r t t h e o t h e r s , t h e y w i l l c o m b i n e t o g e t h e r t o s u p p r e s s i t . . . H o w e v e r , a t loci s o c l o s e l y l i n k e d t o a d i s t o r t e r t h a t t h e benefits o f " r i d i n g its c o a t t a i l s " o u t w e i g h t h e d a m a g e o f its d i s e a s e , s e l e c t i o n t e n d s t o e n h a n c e the d i s t o r t i o n effect. T h u s a s p e c i e s m u s t h a v e m a n y c h r o m o s o m e s if, w h e n a d i s t o r t e r arises, s e l e c t i o n at m o s t l o c i is to f a v o r its s u p p r e s s i o n . J u s t as t o o s m a l l a p a r l i a m e n t m a y be p e r v e r t e d by the C a b a l s of a few, a species w i t h only one, slightly linked c h r o m o s o m e is an easy prey to distorters' ( L e i g h 1971, p. 249). I am not sure w h a t I think a b o u t L e i g h ' s point a b o u t chromosome numbers,

b u t his m o r e g e n e r a l p o i n t t h a t t h e r e i s s o m e sense i n w h i c h

o u t l a w s m a y b e ' o u t n u m b e r e d ' ( A l e x a n d e r & B o r g i a 1 9 7 8 , p . 4 5 8 ) b y their modifiers seems to me to h a v e promise. I suppose ' o u t n u m b e r i n g ' could, in practice, work in two main ways. F i r s t l y , i f d i f f e r e n t m o d i f i e r s e a c h c a u s e a q u a n t i t a t i v e d i m i n u t i o n o f the o u t l a w ' s effect, s e v e r a l m o d i f i e r s m i g h t c o m b i n e a d d i t i v e l y . S e c o n d l y , i f a n y o n e o f s e v e r a l m o d i f i e r s w o u l d suffice t o n e u t r a l i z e t h e o u t l a w , t h e c h a n c e o f effective n e u t r a l i z a t i o n goes up w i t h the n u m b e r of a v a i l a b l e modifier loci. Alexander and Borgia's metaphor of 'outnumbering', and Leigh's metaphor of the p o w e r of the c o l l e c t i v e in a ' p a r l i a m e n t ' of the m a n y , c o u l d be given m e a n i n g i n e i t h e r o r b o t h o f these t w o w a y s . I t i s i m p o r t a n t for t h e a r g u m e n t t h a t s e g r e g a t i o n d i s t o r t e r s a t different l o c i c o u l d n o t , i n a n y o b v i o u s sense, ' p o o l t h e i r efforts'. T h e y a r e n o t w o r k i n g for s o m e c o m m o n e n d o f ' g e n e r a l segregation distortion'. R a t h e r , e a c h one is w o r k i n g to distort segregation in f a v o u r o f itself, a n d this w i l l h u r t o t h e r s e g r e g a t i o n d i s t o r t e r s j u s t a s m u c h a s it hurts non-distorters.

Suppressors of segregation distorters, on the other

h a n d , c o u l d , in a sense, p o o l t h e i r efforts.

O u t l a w s and M o d i f i e r s

139

T h e p a r l i a m e n t o f genes i s o n e o f those m e t a p h o r s w h i c h , i f w e are not c a r e f u l , tricks u s i n t o t h i n k i n g t h a t i t e x p l a i n s m o r e t h a n i t d o e s . L i k e all humans,

but

unlike

genes,

human

Members

of Parliament

are

highly

sophisticated c o m p u t e r s c a p a b l e of using foresight a n d l a n g u a g e to conspire and reach agreements. O u t l a w s m a y seem to be suppressed by a g r e e m e n t of a collective in the p a r l i a m e n t of genes, but w h a t is really g o i n g on is the selection of modifier genes in preference to n o n - m o d i f y i n g alleles at their respective

loci.

Needless

to say,

Leigh

and

the

other

a d v o c a t e s of the

' p a r l i a m e n t o f g e n e s ' h y p o t h e s i s a r e w e l l a w a r e o f this. I n o w w a n t t o e x t e n d the list o f o u t l a w s .

Sex-linked outlaws If a segregation distorter occurs on a sex c h r o m o s o m e , it is not o n l y an outlaw in conflict with suppression

population

with

t h e rest o f t h e g e n o m e a n d

modifiers:

extinction.

also,

This

incidentally,

because,

therefore subject threatens

addition

the to

whole

ordinary

d e t r i m e n t a l side effects, i t a l s o distorts t h e sex r a t i o , a n d m a y e v e n e l i m i n a t e one

sex

from

the

population

altogether.

one

of Hamilton's

(1967)

c o m p u t e r simulations, a single m u t a n t m a l e w i t h a ' d r i v i n g Y' c h r o m o s o m e c a u s i n g m a l e s t o h a v e o n l y sons a n d n o d a u g h t e r s , w a s i n t r o d u c e d i n t o a p o p u l a t i o n o f 1000 m a l e s a n d 1000 f e m a l e s . I t t o o k o n l y f i f t e e n g e n e r a t i o n s t o d r i v e t h e m o d e l p o p u l a t i o n e x t i n c t for l a c k o f f e m a l e s . S o m e t h i n g l i k e this effect h a s b e e n d e m o n s t r a t e d i n t h e l a b o r a t o r y ( L y t t l e 1 9 7 7 ) . T h e p o s s i b i l i t y o f u s i n g a d r i v i n g Y g e n e i n t h e c o n t r o l o f s e r i o u s pests l i k e t h e y e l l o w - f e v e r mosquito did not escape H i c k e y a n d C r a i g ( 1 9 6 6 ) . It is a m e t h o d w i t h sinister e l e g a n c e b e c a u s e i t i s s o c h e a p : a l l t h e w o r k o f s p r e a d i n g t h e p e s t c o n t r o l a g e n t i s d o n e b y t h e pests t h e m s e l v e s t o g e t h e r w i t h n a t u r a l s e l e c t i o n . It is like ' g e r m w a r f a r e ' e x c e p t that the lethal ' g e r m ' is not an e x t r a n e o u s virus but a g e n e in the species's o w n g e n e - p o o l . P e r h a p s the distinction is not a fundamental one a n y w a y (Chapter 9). X - l i n k e d d r i v e i s l i k e l y t o h a v e t h e s a m e sort o f d e t r i m e n t a l effect o n populations

Y-linked

extinguish the population

drive,

but

(Hamilton

tends 1967).

take

generations

T h e driving gene on

c h r o m o s o m e c a u s e s m a l e s t o h a v e d a u g h t e r s r a t h e r t h a n sons birds,

Lepidoptera,

etc.).

saw

Chapter

to X

(except in

if haploid

male

H y m e n o p t e r a c o u l d influence the a m o u n t of care d e v o t e d to their spouses' offspring, t h e y w o u l d f a v o u r d a u g h t e r s r a t h e r t h a n sons, s i n c e m a l e s pass n o g e n e s o n t o sons. T h e m a t h e m a t i c s o f this s i t u a t i o n a r e a n a l o g o u s t o t h e c a s e o f X - l i n k e d drive, the w h o l e g e n o m e o f the m a l e h y m e n o p t e r a n f u n c t i o n i n g like a n X c h r o m o s o m e ( H a m i l t o n 1 9 6 7 , p . 481 a n d f o o t n o t e 1 8 ) . I t i s often t h e c a s e t h a t X c h r o m o s o m e s cross o v e r w i t h e a c h o t h e r b u t n o t w i t h Y c h r o m o s o m e s . It follows that all genes on X c h r o m o s o m e s c o u l d stand t o g a i n from t h e p r e s e n c e i n t h e g e n e - p o o l o f a d r i v i n g X g e n e w h i c h d i s t o r t s

140

O u t l a w s and Modifiers

g a m e t o g e n e s i s i n t h e h e t e r o g a m e t i c sex i n f a v o u r o f X g a m e t e s a n d a g a i n s t Y g a m e t e s . G e n e s on X c h r o m o s o m e s a r e , in a sense, u n i t e d a g a i n s t Y g e n e s , in a kind of 'anti linkage g r o u p ' , simply because they h a v e no c h a n c e of finding themselves on a Y c h r o m o s o m e . Modifiers to suppress X - l i n k e d meiotic drive i n t h e h e t e r o g a m e t i c s e x m i g h t w e l l n o t b e f a v o u r e d i f t h e y a r o s e a t o t h e r loci on X c h r o m o s o m e s . T h e y w o u l d be favoured if they arose on autosomes. T h i s is different from the case of segregation distorters on a u t o s o m e s : here there m i g h t w e l l be selection in favour of suppressing them by modifiers at other

loci

even

the same

chromosome.

X-linked

distorters

affecting

g a m e t e p r o d u c t i o n i n t h e h e t e r o g a m e t i c s e x a r e , t h e n , o u t l a w s from the p o i n t o f v i e w o f t h e a u t o s o m a l p a r t o f t h e g e n e - p o o l , b u t n o t from the p o i n t o f v i e w o f t h e rest o f t h e X - c h r o m o s o m a l p a r t o f t h e g e n e - p o o l . T h i s p o t e n t i a l ' s o l i d a r i t y ' a m o n g t h e g e n e s o n sex c h r o m o s o m e s s u g g e s t s t h a t the c o n c e p t o f the o u t l a w g e n e m a y be too simple. It c o n v e y s the i m a g e of a single rebel s t a n d i n g o u t a g a i n s t t h e rest o f t h e g e n o m e . A t t i m e s w e m i g h t , i n s t e a d , d o b e t t e r t o t h i n k i n t e r m s o f w a r s b e t w e e n r i v a l g a n g s o f g e n e s , for i n s t a n c e the X - c h r o m o s o m e g e n e s a g a i n s t t h e rest. C o s m i d e s a n d T o o b y ( 1 9 8 1 ) c o i n the useful t e r m ' c o r e p l i c o n ' for s u c h a g a n g o f g e n e s t h a t r e p l i c a t e t o g e t h e r a n d therefore tend

t o w o r k for t h e s a m e e n d s .

I n m a n y cases n e i g h b o u r i n g

coreplicons will blur into each other. G a n g i n g up by Y - c h r o m o s o m e genes is even more to be expected. As long as Y c h r o m o s o m e s do n o t cross o v e r , it is c l e a r t h a t all g e n e s on a Y c h r o m o s o m e s t a n d t o g a i n from t h e p r e s e n c e o f a Y - l i n k e d d i s t o r t e r e v e r y bit a s m u c h a s t h e d i s t o r t e r g e n e itself. H a m i l t o n ( 1 9 6 7 ) m a d e t h e i n t e r e s t i n g s u g g e s t i o n t h a t t h e r e a s o n for t h e w e l l - k n o w n i n e r t n e s s o f Y c h r o m o s o m e s (hairy ears seems to be the o n l y c o n s p i c u o u s Y - l i n k e d trait in m a n ) is that Ys u p p r e s s i n g m o d i f i e r s h a v e b e e n p o s i t i v e l y s e l e c t e d e l s e w h e r e i n the g e n o m e . I t i s n o t o b v i o u s h o w a m o d i f i e r m i g h t g o a b o u t s u p p r e s s i n g the p h e n o t y p i c a c t i v i t y o f a n e n t i r e c h r o m o s o m e , s i n c e t h e v a r i o u s p h e n o t y p i c effects o f a single c h r o m o s o m e are usually so heterogeneous. ( W h y w o u l d selection not s u p p r e s s o n l y t h e effects o f t h e d r i v i n g g e n e s , l e a v i n g o t h e r Y - l i n k e d effects intact?) I suppose it m i g h t do it by p h y s i c a l l y d e l e t i n g large chunks of Y c h r o m o s o m e , o r b y c o n t r i v i n g t o q u a r a n t i n e t h e Y c h r o m o s o m e from the cell's transcription machinery. A w e i r d e x a m p l e of a d r i v i n g r e p l i c a t o r w h i c h is p r o b a b l y n o t a g e n e in t h e o r d i n a r y sense o f t h e w o r d i s g i v e n b y W e r r e n , S k i n n e r a n d C h a r n o v (in p r e p a r a t i o n ) . T h e y s t u d i e d t h e p a r a s i t o i d w a s p Nasonia vitripennis, i n w h i c h there

variety

of males

called

Dl,

'daughterless'.

Wasps

being

h a p l o d i p l o i d , m a l e s pass t h e i r g e n e s o n l y t o d a u g h t e r s : a m a l e ' s m a t e m a y h a v e sons, b u t t h o s e sons a r e h a p l o i d a n d fatherless. W h e n D l m a l e s m a t e w i t h f e m a l e s , t h e y c a u s e t h e m t o p r o d u c e all m a l e b r o o d s . M o s t o f t h e sons o f females m a t e d to Dl males are themselves Dl males. A l t h o u g h no nuclear g e n e s pass from f a t h e r t o s o n , t h e r e f o r e , t h e D l f a c t o r s o m e h o w d o e s pass

O u t l a w s and Modifiers

141

f r o m father t o 'son'. T h e D l factor r a p i d l y spreads, i n e x a c t l y the s a m e w a y as a driving Y c h r o m o s o m e w o u l d .

It is not k n o w n w h a t the Dl factor

p h y s i c a l l y consists of. I t i s c e r t a i n l y n o t n u c l e a r g e n e t i c m a t e r i a l , a n d i t i s theoretically possible that it is not e v e n c o m p o s e d of nucleic acid, a l t h o u g h W e r r e n e t al. s u s p e c t t h a t i t p r o b a b l y i s c y t o p l a s m i c a l l y b o r n e n u c l e i c a c i d . T h e o r e t i c a l l y , any k i n d o f p h y s i c a l o r c h e m i c a l i n f l u e n c e o f a D l m a l e o n his m a t e , w h i c h c a u s e s h e r t o h a v e D l sons, w o u l d s p r e a d l i k e a d r i v i n g Y c h r o m o s o m e , a n d w o u l d q u a l i f y a s a n a c t i v e g e r m - l i n e r e p l i c a t o r i n t h e sense of C h a p t e r 5. It is a l s o an o u t l a w par excellence, for it s p r e a d s i t s e l f at t h e t o t a l e x p e n s e o f a l l t h e n u c l e a r g e n e s i n t h e m a l e s t h a t b e a r it.

Selfish sperm W i t h some e x c e p t i o n s , all the d i p l o i d cells of an o r g a n i s m are g e n e t i c a l l y i d e n t i c a l , b u t the h a p l o i d g a m e t e s i t p r o d u c e s a r e a l l d i f f e r e n t . O n l y o n e o u t of m a n y sperms in an ejaculate c a n fertilize an e g g , a n d there is therefore potential

for c o m p e t i t i o n a m o n g t h e m .

A n y gene that found

phenotypic

e x p r e s s i o n w h e n i n the h a p l o i d s t a t e i n a s p e r m c e l l c o u l d b e f a v o u r e d o v e r its alleles i f i t i m p r o v e d the c o m p e t i t i v e a b i l i t y o f t h e s p e r m . S u c h a g e n e w o u l d not necessarily be sex-linked: it could be found on any c h r o m o s o m e . I f i t w a s s e x - l i n k e d i t w o u l d h a v e t h e effect o f b i a s i n g t h e s e x r a t i o , a n d w o u l d b e a n o u t l a w . I f i t w a s o n a n a u t o s o m e i t w o u l d still q u a l i f y a s a n o u t l a w for t h e g e n e r a l k i n d o f r e a s o n a l r e a d y g i v e n for a n y s e g r e g a t i o n distorter: ' . . . if there were genes affecting sperm-cell function there w o u l d be competition a m o n g sperm cells, a n d a g e n e that i m p r o v e d the ability to fertilize w o u l d i n c r e a s e i n t h e p o p u l a t i o n . I f s u c h a g e n e h a p p e n e d t o c a u s e , say, m a l f u n c t i o n o f the liver, that w o u l d b e j u s t too b a d ; the g e n e w o u l d i n c r e a s e a n y w a y , s i n c e s e l e c t i o n for g o o d h e a l t h i s m u c h less e f f e c t i v e t h a n selection by c o m p e t i t i o n a m o n g sperm cells'

(Crow

1 9 7 9 ) . T h e r e is, o f

course, no particular reason w h y a sperm competition g e n e should h a p p e n to cause malfunction of the liver but, as a l r e a d y p o i n t e d out, most m u t a t i o n s are d e l e t e r i o u s , s o s o m e u n d e s i r a b l e side effect i s p r e t t y l i k e l y . W h y d o e s C r o w assert t h a t s e l e c t i o n for g o o d h e a l t h i s m u c h less e f f e c t i v e than selection by competition a m o n g sperm cells? T h e r e must inevitably be a q u a n t i t a t i v e t r a d e - o f f i n v o l v i n g the m a g n i t u d e o f t h e effect o n h e a l t h . B u t , t h a t a s i d e , a n d e v e n a l l o w i n g for t h e c o n t r o v e r s i a l p o s s i b i l i t y t h a t o n l y a minority of sperms are v i a b l e ( C o h e n 1 9 7 7 ) , the a r g u m e n t a p p e a r s to h a v e force b e c a u s e t h e c o m p e t i t i o n b e t w e e n s p e r m c e l l s i n a n e j a c u l a t e w o u l d s e e m to be so f i e r c e .

A million million spermatozoa, All of them alive: O u t of their c a t a c l y s m but one poor N o a h Dare hope to survive.

142

O u t l a w s and M o d i f i e r s

A n d of that billion minus one Might have chanced to be Shakespeare, another Newton, a new D o n n e â&#x20AC;&#x201D; But the O n e w a s M e . S h a m e to h a v e ousted y o u r betters thus. T a k i n g ark while the others remained outside! B e t t e r for a l l o f us, f r o w a r d H o m u n c u l u s , If you'd quietly died! Aldous

Huxley

O n e m i g h t i m a g i n e t h a t a m u t a n t g e n e t h a t e x p r e s s e d itself w h e n i n the haploid g e n o t y p e of a spermatozoon, causing increased competitive ability, s a y a n i m p r o v e d s w i m m i n g t a i l o r t h e s e c r e t i o n o f a s p e r m i c i d e t o w h i c h the sperm itself w a s i m m u n e , w o u l d be i m m e d i a t e l y favoured by a selection pressure

gigantic

enough

outweigh

all

but

the

most

catastrophic

d e l e t e r i o u s s i d e effects o n the d i p l o i d b o d y . B u t a l t h o u g h i t m a y b e t r u e t h a t only one in

hundreds of millions of sperms

'dare hope to survive',

the

c a l c u l a t i o n l o o k s v e r y different f r o m t h e p o i n t o f v i e w o f a s i n g l e g e n e . I f w e f o r g e t l i n k a g e g r o u p s a n d b r a n d - n e w m u t a t i o n s for a m o m e n t , h o w e v e r r a r e a g e n e m a y b e i n t h e g e n e - p o o l , i f a g i v e n m a l e h a s i t i n his d i p l o i d g e n o t y p e , a t least 5 0 p e r c e n t o f his s p e r m s m u s t h a v e it. I f o n e s p e r m h a s r e c e i v e d a g e n e g i v i n g i t c o m p e t i t i v e a d v a n t a g e , 5 0 p e r c e n t o f its r i v a l s i n t h e s a m e e j a c u l a t e w i l l h a v e r e c e i v e d t h e s a m e g e n e . O n l y i f t h e m u t a t i o n h a s arisen d e novo d u r i n g astronomical

the genesis of a single sperm will in

magnitude.

the selection pressure be

U s u a l l y it will be a m o r e modest selection

p r e s s u r e , n o t o f m i l l i o n s t o o n e b u t o n l y t w o t o o n e . I f w e t a k e l i n k a g e effects into c o n s i d e r a t i o n the c a l c u l a t i o n is m o r e c o m p l i c a t e d , and the selection pressure in favour of c o m p e t i t i v e sperms will increase s o m e w h a t . In a n y c a s e , it is a s t r o n g e n o u g h p r e s s u r e for us to e x p e c t t h a t , if g e n e s expressed themselves w h e n in the h a p l o i d g e n o t y p e of the sperm, outlaws w o u l d b e f a v o u r e d , t o t h e d e t r i m e n t o f t h e rest o f t h e g e n e s i n t h e d i p l o i d f a t h e r ' s g e n o m e . I t s e e m s , t o s a y t h e least, f o r t u n a t e t h a t s p e r m p h e n o t y p e s are, as a m a t t e r of fact, usually not u n d e r the control of their o w n haploid genotypes (Beatty & Gluecksohn-Waelsch types

must

under

some

genetic

1972). Of course sperm pheno-

control,

and

natural

selection

has

doubtless w o r k e d on the genes c o n t r o l l i n g sperm p h e n o t y p e s to perfect sperm a d a p t a t i o n . B u t t h o s e g e n e s s e e m t o e x p r e s s t h e m s e l v e s w h e n i n the d i p l o i d g e n o t y p e of the father, not w h e n in the h a p l o i d g e n o t y p e of the sperm. W h e n in the sperm they are passively carried. T h e p a s s i v i t y o f t h e i r g e n o t y p e s m a y b e a n i m m e d i a t e c o n s e q u e n c e o f the lack

of cytoplasm

spermatozoa:

gene

cannot

achieve

phenotypic

O u t l a w s and M o d i f i e r s

143

expression e x c e p t v i a c y t o p l a s m . T h i s is a p r o x i m a l e x p l a n a t i o n . B u t it is at least w o r t h t o y i n g w i t h r e v e r s i n g t h e p r o p o s i t i o n

to obtain an ultimate

functional e x p l a n a t i o n : sperms are m a d e small, as an a d a p t a t i o n to p r e v e n t the p h e n o t y p i c e x p r e s s i o n o f t h e h a p l o i d g e n o t y p e . O n this h y p o t h e s i s w e a r e proposing an arms race between competitive

ability

among

(haploid-expressed)

spermatozoa

the

g e n e s for i n c r e a s e d

one

hand,

and

genes

e x p r e s s i n g t h e m s e l v e s w h e n i n the d i p l o i d g e n o t y p e o f t h e f a t h e r o n t h e o t h e r hand,

causing sperms

b e c o m e smaller and

therefore

unable

give

phenotypic expression to their o w n haploid g e n o t y p e s . T h i s hypothesis does not e x p l a i n w h y eggs are larger than s p e r m s ; it assumes the basic fact of anisogamy, and therefore does not aspire to be an alternative to theories of the o r i g i n s o f a n i s o g a m y ( P a r k e r 1 9 7 8 b ; M a y n a r d S m i t h 1 9 7 8 a ; A l e x a n d e r & Borgia

1 9 7 9 ) . M o r e o v e r not all sperms are small, as S i v i n s k i

(1980)

r e m i n d s u s i n a m o s t i n t r i g u i n g r e v i e w . B u t t h e p r e s e n t e x p l a n a t i o n still deserves consideration as an ancillary to others. It is a n a l o g o u s to H a m i l t o n ' s ( 1 9 6 7 ) e x p l a n a t i o n for t h e i n e r t n e s s o f Y c h r o m o s o m e s , t o w h i c h I h a v e already alluded.

Green beards and armpits S o m e of the outlaws I h a v e been considering h a v e been realistic, a n d are a c t u a l l y k n o w n t o g e n e t i c i s t s . S o m e o f the s u g g e s t e d o u t l a w s t h a t I s h a l l n o w c o m e t o a r e , f r a n k l y , p r e t t y i m p r o b a b l e . I m a k e n o a p o l o g y for this. I see them as t h o u g h t e x p e r i m e n t s . T h e y p l a y the s a m e role in h e l p i n g me to think straight a b o u t reality as i m a g i n a r y trains t r a v e l l i n g at n e a r l y the speed of l i g h t d o for p h y s i c i s t s . So,

this

spirit

of t h o u g h t

experiment,

imagine

gene

c h r o m o s o m e w h i c h m a k e s its possessor kill his d a u g h t e r s a n d f e e d t h e m t o his sons. T h i s i s c l e a r l y a b e h a v i o u r a l v e r s i o n o f a d r i v i n g Y - c h r o m o s o m e effect. I f i t a r o s e i t w o u l d t e n d t o s p r e a d for t h e s a m e r e a s o n , a n d i t w o u l d b e a n o u t l a w i n t h e s a m e sense t h a t its p h e n o t y p i c effect w o u l d b e d e t r i m e n t a l t o the rest o f t h e m a l e ' s g e n e s . M o d i f i e r s , o n a n y c h r o m o s o m e o t h e r t h a n t h e Y c h r o m o s o m e , w h i c h t e n d e d t o r e d u c e t h e p h e n o t y p i c effect o f t h e d a u g h t e r killing g e n e w o u l d be favoured over their alleles. In a sense the o u t l a w g e n e is u s i n g t h e sex of t h e m a l e ' s c h i l d r e n as a c o n v e n i e n t label for t h e p r e s e n c e or a b s e n c e o f itself: a l l sons a r e l a b e l l e d a s d e f i n i t e possessors o f t h e g e n e , a l l d a u g h t e r s a s d e f i n i t e n o n - p o s s e s s o r s o f it. A s i m i l a r a r g u m e n t c a n b e m a d e for X c h r o m o s o m e s . H a m i l t o n ( 1 9 7 2 , p . 201) p o i n t e d o u t t h a t i n n o r m a l d i p l o i d s p e c i e s a g e n e o n a n X c h r o m o s o m e i n the h o m o g a m e t i c sex h a s t h r e e - q u a r t e r s o f a c h a n c e o f b e i n g i d e n t i c a l b y descent with a g e n e in a sibling of the h o m o g a m e t i c sex. T h u s the ' X c h r o m o s o m e r e l a t e d n e s s ' o f h u m a n sisters i s a s h i g h a s t h e o v e r a l l r e l a t e d n e s s o f h y m e n o p t e r a n sisters, a n d h i g h e r t h a n t h e o v e r a l l r e l a t e d n e s s o f h u m a n sisters. H a m i l t o n w e n t s o far a s t o w o n d e r w h e t h e r a n X - c h r o m o s o m e effect

144

O u t l a w s and Modifiers

m i g h t a c c o u n t for t h e f a c t t h a t h e l p e r s a t the nest i n b i r d s s e e m , u s u a l l y , t o be elder brothers,

r a t h e r t h a n sisters,

o f the n e s t l i n g s

(the m a l e sex i s

h o m o g a m e t i c in birds). He noted that the X c h r o m o s o m e in birds accounts for s o m e 1 0 p e r c e n t o f t h e w h o l e g e n o m e , a n d t h a t i t i s t h e r e f o r e n o t too i m p r o b a b l e t h a t t h e g e n e t i c basis for b r o t h e r l y c a r e m i g h t lie o n t h e X c h r o m o s o m e . I f so, b r o t h e r l y c a r e m i g h t b e f a v o u r e d b y t h e s a m e k i n d o f s e l e c t i o n p r e s s u r e a s H a m i l t o n h a d e a r l i e r s u g g e s t e d for sisterly c a r e i n H y m e n o p t e r a . Perhaps significantly, S y r e n and L u y c k x (1977) point out t h a t i n s o m e t e r m i t e s , t h e o n l y n o n - h a p l o d i p l o i d g r o u p t o h a v e a c h i e v e d full eusociality, ' a p p r o x i m a t e l y h a l f the g e n o m e is m a i n t a i n e d as a linkage g r o u p w i t h t h e sex c h r o m o s o m e ' ( L a c y 1 9 8 0 ) . Wickler

(1977),

commenting

Hamilton's X - c h r o m o s o m e idea, potentially

even

Whitney's

(1976)

rediscovery

s u g g e s t s t h a t Y - c h r o m o s o m e effects are

powerful

than

X-chromosome

effects,

but

c h r o m o s o m e s a s a r u l e d o n ' t m a k e u p s u c h a h i g h p r o p o r t i o n o f the g e n o m e . I n a n y c a s e ' s e x - l i n k e d a l t r u i s m ' m u s t b e discriminating: i n d i v i d u a l s a c t i n g under

the

influence

their

sex

chromosomes

should

tend

show

f a v o u r i t i s m t o w a r d s c l o s e r e l a t i v e s o f t h e s a m e sex r a t h e r t h a n o f the o p p o s i t e s e x . G e n e s for s e x - b l i n d s i b l i n g c a r e w o u l d n o t b e o u t l a w s . T h e v a l u e o f the o u t l a w e d s e x - c h r o m o s o m e t h o u g h t e x p e r i m e n t does not lie i n its p l a u s i b i l i t y â&#x20AC;&#x201D; w h i c h , l i k e H a m i l t o n , I d o n o t r a t e h i g h l y â&#x20AC;&#x201D; b u t i n the fact t h a t i t f o c u s e s o u r a t t e n t i o n o n t h e i m p o r t a n c e o f this d i s c r i m i n a t i o n . T h e sex of a n o t h e r i n d i v i d u a l is u s e d as a label to i d e n t i f y it as a m e m b e r of a class

of individuals

ordinary

theory

about

of kin

whose genetics

selection,

something

relatedness

(or

known.

rather some

the

proximate

c o r r e l a t e o f r e l a t e d n e s s s u c h a s p r e s e n c e i n o n e ' s o w n nest) i s used a s a l a b e l i n d i c a t i n g h i g h e r t h a n a v e r a g e p r o b a b i l i t y o f s h a r i n g a g e n e . F r o m the p o i n t of v i e w of a g e n e on a Y c h r o m o s o m e , t h e sex of a s i b l i n g is a l a b e l w h i c h signifies t h e d i f f e r e n c e b e t w e e n c e r t a i n t y o f s h a r i n g t h e g e n e a n d c e r t a i n t y o f n o t s h a r i n g it. N o t e , by the w a y , the ineptness of notions of individual fitness, or even i n c l u s i v e f i t n e s s a s o r d i n a r i l y u n d e r s t o o d , a t d e a l i n g w i t h s i t u a t i o n s like this. T h e n o r m a l c a l c u l a t i o n o f i n c l u s i v e f i t n e s s m a k e s use o f a c o e f f i c i e n t o f relationship w h i c h is s o m e m e a s u r e of the p r o b a b i l i t y that a pair of relatives will

approximation

particular provided

gene, the

identical

genes

concerned

descent. have

This no

better

good

way

' r e c o g n i z i n g ' c o p i e s o f t h e m s e l v e s i n o t h e r i n d i v i d u a l s . I f a g e n e i s o n a sex c h r o m o s o m e a n d c a n u s e t h e sex o f r e l a t i v e s a s a l a b e l , h o w e v e r , its best ' e s t i m a t e ' of the p r o b a b i l i t y that a relative shares a c o p y of itself will be a b e t t e r e s t i m a t e t h a n t h a t p r o v i d e d b y t h e c o e f f i c i e n t o f r e l a t i o n s h i p . I n its most general form, the principle of genes a p p e a r i n g to 'recognize' copies of t h e m s e l v e s i n o t h e r i n d i v i d u a l s h a s b e e n d u b b e d t h e ' g r e e n - b e a r d effect' ( D a w k i n s 1976a, p. 96, following H a m i l t o n 1964b, p. 25). G r e e n - b e a r d or

O u t l a w s and M o d i f i e r s

'recognition

alleles'

have

been

described

the

literature

145

outlaws

( A l e x a n d e r & B o r g i a 1 9 7 8 ; A l e x a n d e r 1980), a n d they should therefore be discussed i n this c h a p t e r , e v e n t h o u g h , a s w e s h a l l s e e , t h e i r s t a t u s a s o u t l a w s needs careful e x a m i n a t i o n ( R i d l e y & G r a f e n in press). T h e g r e e n - b e a r d effect r e d u c e s t h e p r i n c i p l e o f ' g e n e s e l f - r e c o g n i t i o n ' t o its b a r e essentials i n a n u n r e a l i s t i c a l l y h y p o t h e t i c a l , b u t n e v e r t h e l e s s i n s t r u c t i v e , w a y . A g e n e i s p o s t u l a t e d w h i c h h a s t w o p l e i o t r o p i c effects. O n e effect i s t o c o n f e r a c o n s p i c u o u s l a b e l , t h e ' g r e e n b e a r d ' . T h e o t h e r effect i s t o c o n f e r a tendency to b e h a v e altruistically t o w a r d s bearers of the l a b e l . S u c h a g e n e , if it ever arose, could easily be favoured by natural selection, a l t h o u g h it w o u l d be vulnerable to a m u t a n t arising w h i c h conferred the label w i t h o u t the altruism. G e n e s a r e n o t c o n s c i o u s little d e v i l s , a b l e t o r e c o g n i z e c o p i e s o f t h e m s e l v e s i n o t h e r i n d i v i d u a l s a n d t o a c t a c c o r d i n g l y . T h e o n l y w a y for t h e g r e e n b e a r d effect t o arise i s b y i n c i d e n t a l p l e i o t r o p y . A m u t a t i o n m u s t a r i s e w h i c h j u s t h a p p e n s t o h a v e t w o c o m p l e m e n t a r y effects: t h e l a b e l o r ' g r e e n b e a r d ' , a n d the t e n d e n c y t o b e h a v e a l t r u i s t i c a l l y t o w a r d s l a b e l l e d i n d i v i d u a l s . I h a v e a l w a y s t h o u g h t s u c h a f o r t u i t o u s c o n j u n c t i o n o f p l e i o t r o p i c effects t o o g o o d to be true. H a m i l t o n also noted the idea's i n h e r e n t i m p l a u s i b i l i t y , b u t h e w e n t o n ' . . . e x a c t l y t h e s a m e a priori o b j e c t i o n s m i g h t b e m a d e t o t h e evolution of assortative m a t i n g w h i c h manifestly has e v o l v e d , p r o b a b l y m a n y t i m e s i n d e p e n d e n t l y a n d d e s p i t e its o b s c u r e a d v a n t a g e s ' ( H a m i l t o n 1 9 6 4 b , p . 2 5 ) . I t i s w o r t h b r i e f l y e x a m i n i n g this c o m p a r i s o n w i t h a s s o r t a t i v e m a t i n g , w h i c h for p r e s e n t p u r p o s e s I s h a l l t a k e t o m e a n t h e t e n d e n c y o f i n d i v i d u a l s t o prefer t o m a t e w i t h i n d i v i d u a l s t h a t g e n e t i c a l l y r e s e m b l e t h e m . W h y i s i t t h a t t h e g r e e n - b e a r d effect s e e m s s o m u c h m o r e f a r - f e t c h e d t h a n assortative m a t i n g ? It is not just that assortative m a t i n g is positively k n o w n to occur. I suggest another reason. T h i s is that w h e n we think of assortative m a t i n g w e i m p l i c i t l y a s s u m e self-inspection a s a m e a n s o f f a c i l i t a t i n g t h e effect. If black individuals prefer to m a t e with b l a c k individuals, and w h i t e w i t h w h i t e , w e d o n o t find this h a r d t o b e l i e v e b e c a u s e w e t a c i t l y a s s u m e t h a t i n d i v i d u a l s p e r c e i v e t h e i r own c o l o u r . E a c h i n d i v i d u a l , w h a t e v e r his c o l o u r , i s a s s u m e d t o b e o b e y i n g t h e same r u l e : i n s p e c t y o u r s e l f (or m e m b e r s o f y o u r o w n family) and choose a m a t e of the same colour. T h i s p r i n c i p l e does not stretch our credulity by d e m a n d i n g that t w o specific effectsâ&#x20AC;&#x201D;colour a n d behavioural preferenceâ&#x20AC;&#x201D;are controlled pleiotropically by the s a m e gene. If there

general

advantage

mating

with

similar

partners,

natural

selection will favour the self-inspection rule regardless of the e x a c t n a t u r e of the r e c o g n i t i o n c h a r a c t e r u s e d . I t d o e s n o t h a v e t o b e s k i n c o l o u r . A n y conspicuous

and

variable

character

would

work

with

the

identical

behavioural rule. No far-fetched pleiotropism need be postulated. W e l l t h e n , w i l l t h e s a m e k i n d o f m e c h a n i s m w o r k for t h e g r e e n - b e a r d effect? M i g h t a n i m a l s o b e y a b e h a v i o u r a l r u l e o f t h e f o r m : ' I n s p e c t y o u r s e l f

146

O u t l a w s and Modifiers

and b e h a v e altruistically towards other individuals that resemble y o u ' ? T h e a n s w e r i s t h a t t h e y m i g h t , b u t this w o u l d n o t b e a t r u e e x a m p l e o f t h e g r e e n beard

effect.

Instead,

call

the

'armpit

effect'.

the

paradigm

h y p o t h e t i c a l e x a m p l e , t h e a n i m a l i s s u p p o s e d t o s m e l l its o w n a r m p i t s , a n d b e h a v e altruistically towards other individuals with a similar smell.

(The

r e a s o n for c h o o s i n g a n o l f a c t o r y n a m e i s t h a t p o l i c e d o g trials h a v e s h o w n that

dogs

presented

with

handkerchiefs

held

under

human

armpits can

distinguish the sweats of a n y t w o i n d i v i d u a l h u m a n s e x c e p t identical twins ( K a l m u s 1 9 5 5 ) . T h i s suggests that there is an e n o r m o u s l y v a r i a b l e richness of g e n e t i c l a b e l l i n g i n m o l e c u l e s o f s w e a t . I n t h e l i g h t o f t h e result w i t h i d e n t i c a l t w i n s , o n e feels i n c l i n e d t o b e t t h a t p o l i c e d o g s c o u l d b e t r a i n e d t o sniff o u t t h e c o e f f i c i e n t o f r e l a t i o n s h i p b e t w e e n p a i r s o f h u m a n s a n d t h a t , for i n s t a n c e , t h e y c o u l d b e t r a i n e d t o t r a c k d o w n a c r i m i n a l i f g i v e n a sniff o f his b r o t h e r . B e t h a t a s i t m a y , ' a r m p i t effect' i s h e r e b e i n g used a s a g e n e r a l n a m e for a n y case

of an

animal

inspecting

himself,

known

relative,

and

discriminating in favour of other individuals with a similar smell or with some other perceived similarity.) T h e e s s e n t i a l d i f f e r e n c e b e t w e e n t h e g r e e n - b e a r d effect a n d t h e a r m p i t s e l f - i n s p e c t i o n effect i s a s f o l l o w s . T h e a r m p i t s e l f - i n s p e c t i o n b e h a v i o u r a l r u l e will lead

to the detection of other individuals that are similar in some

r e s p e c t , p e r h a p s i n m a n y r e s p e c t s , b u t i t w i l l n o t s p e c i f i c a l l y l e a d t o the detection

of individuals

that

possess

copies

of the

gene

mediating

the

b e h a v i o u r a l r u l e itself. T h e a r m p i t r u l e m i g h t p r o v i d e a n a d m i r a b l e m e a n s o f d e t e c t i n g t r u e k i n f r o m n o n - k i n , o r o f d e t e c t i n g w h e t h e r a b r o t h e r w a s a full brother or only a half brother. T h i s could be very important, and it might p r o v i d e t h e basis for s e l e c t i o n i n f a v o u r o f s e l f - i n s p e c t i n g b e h a v i o u r , b u t the selection w o u l d b e c o n v e n t i o n a l , familiar kin selection. T h e self-inspection rule w o u l d be functioning simply as a kin-recognition d e v i c e , a n a l o g o u s to a rule like: ' B e h a v e altruistically towards individuals that g r e w up in y o u r o w n nest.' T h e g r e e n - b e a r d effect i s q u i t e d i f f e r e n t . H e r e t h e i m p o r t a n t t h i n g i s t h a t a g e n e (or c l o s e l i n k a g e g r o u p ) p r o g r a m s t h e r e c o g n i t i o n s p e c i f i c a l l y o f c o p i e s o f itself. T h e g r e e n - b e a r d effect i s n o t a m e c h a n i s m for t h e r e c o g n i t i o n o f k i n . R a t h e r , kin recognition and ' g r e e n - b e a r d ' recognition are alternative w a y s in w h i c h genes could b e h a v e as if discriminating in favour of copies of themselves. T o r e t u r n t o H a m i l t o n ' s c o m p a r i s o n w i t h a s s o r t a t i v e m a t i n g , w e c a n see that

does

not

really

provide

good

grounds

for

optimism

over

the

p l a u s i b i l i t y o f t h e g r e e n - b e a r d effect. A s s o r t a t i v e m a t i n g i s m u c h m o r e l i k e l y to i n v o l v e s e l f - i n s p e c t i o n . If, for w h a t e v e r r e a s o n , it is an a d v a n t a g e in g e n e r a l for l i k e t o m a t e w i t h l i k e , s e l e c t i o n w o u l d f a v o u r a n a r m p i t t y p e o f b e h a v i o u r a l r u l e : Inspect yourself, a n d choose a m a t e that resembles y o u . T h i s will a c h i e v e the desired resultâ&#x20AC;&#x201D;an optimal b a l a n c e between outbreed-

O u t l a w s and M o d i f i e r s

147

ing and inbreeding (Bateson 1978a) or w h a t e v e r the a d v a n t a g e m a y b e â&#x20AC;&#x201D; r e g a r d l e s s o f the e x a c t n a t u r e o f t h e c h a r a c t e r i s t i c s b y w h i c h i n d i v i d u a l s differ. Assortative m a t i n g is not the o n l y a n a l o g y H a m i l t o n m i g h t h a v e chosen. A n o t h e r o n e i s t h e c a s e o f c r y p t i c m o t h s c h o o s i n g t o sit o n a b a c k g r o u n d t h a t m a t c h e s t h e i r o w n c o l o u r . K e t t l e w e l l ( 1 9 5 5 ) g a v e d a r k - c o l o u r e d carbonaria a n d l i g h t - c o l o u r e d t y p i c a l m o r p h s o f t h e p e p p e r e d m o t h Biston betularia t h e o p p o r t u n i t y t o sit o n d a r k - o r l i g h t - c o l o u r e d b a c k g r o u n d s . T h e r e w a s a s t a t i s t i c a l l y s i g n i f i c a n t t e n d e n c y for m o t h s t o c h o o s e a b a c k g r o u n d m a t c h i n g t h e i r o w n b o d y c o l o u r . T h i s c o u l d b e d u e t o p l e i o t r o p i s m (or g e n e s for c o l o u r b e i n g c l o s e l y l i n k e d t o g e n e s for b a c k g r o u n d c h o i c e ) . I f this w e r e so, a s Sargent (1969a) believes, it might, by analogy, reduce our scepticism about the

inherent

plausibility of the

green-beard

effect.

Kettlewell

believed,

h o w e v e r , that the moths a c h i e v e d the m a t c h i n g b y the simpler m e c h a n i s m o f ' c o n t r a s t c o n f l i c t ' . H e s u g g e s t e d t h a t a m o t h c o u l d see a s m a l l p o r t i o n o f its o w n b o d y , a n d t h a t i t m o v e d a r o u n d u n t i l t h e o b s e r v e d c o n t r a s t b e t w e e n its o w n b o d y and the b a c k g r o u n d r e a c h e d a m i n i m u m . It is easy to b e l i e v e that natural

selection

minimizing

might

favour

behavioural

rule,

the

genetic

because

basis

would

for

such

work

contrast-

automatically

conjunction with any colour, including a newly mutated colour.

It is of

c o u r s e a n a l o g o u s t o t h e ' a r m p i t s e l f - i n s p e c t i o n ' effect, a n d i s p l a u s i b l e for t h e same reason. S a r g e n t ' s ( 1 9 6 9 a ) i n t u i t i o n differs f r o m K e t t l e w e l l ' s . H e d o u b t s t h e selfinspection

theory,

and

thinks

that

the

two

morphs

of B.

betularia differ

genetically in their b a c k g r o u n d preference. He has no e v i d e n c e a b o u t B. betularia itself, b u t h a s d o n e s o m e i n g e n i o u s e x p e r i m e n t s o n o t h e r s p e c i e s . F o r e x a m p l e , he took m e m b e r s of a d a r k species and of a light species, and painted

the

c i r c u m - o c u l a r hairs

in an

attempt

'fool'

the moths into

choosing a b a c k g r o u n d that m a t c h e d the p a i n t e d hairs. T h e y obstinately persisted

choosing

background

that

matched

their

genetically

d e t e r m i n e d c o l o u r ( S a r g e n t 1 9 6 8 ) . U n f o r t u n a t e l y , h o w e v e r , this i n t e r e s t i n g result w a s o b t a i n e d

w i t h t w o different species,

not with dark and

light

morphs of one species. I n a n o t h e r e x p e r i m e n t w h i c h w a s d o n e w i t h a d i m o r p h i c s p e c i e s , Phigalia titea, S a r g e n t ( 1 9 6 9 a ) s i m p l y failed t o g e t t h e r e s u l t K e t t l e w e l l h a d w i t h B . betularia. T h e P . titea i n d i v i d u a l s , w h e t h e r t h e d a r k o r t h e l i g h t m o r p h , c h o s e t o sit o n l i g h t b a c k g r o u n d s , p r e s u m a b l y t h e a p p r o p r i a t e b a c k g r o u n d for t h e l i g h t a n c e s t r a l f o r m o f t h e s p e c i e s . W h a t i s n e e d e d i s for s o m e b o d y t o r e p e a t S a r g e n t ' s k e y e x p e r i m e n t o f p a i n t i n g the p a r t s o f a m o t h ' s b o d y t h a t i t c a n see, b u t u s i n g a d i m o r p h i c s p e c i e s like B. betularia w h i c h is k n o w n to s h o w morph-specific b a c k g r o u n d choice. K e t t l e w e l l ' s theory w o u l d predict that moths p a i n t e d b l a c k will select b l a c k b a c k g r o u n d s , a n d m o t h s p a i n t e d light will select light b a c k g r o u n d s , regardless of w h e t h e r t h e y are g e n e t i c a l l y

148

O u t l a w s and M o d i f i e r s

carbonaria or typica. A p u r e l y g e n e t i c t h e o r y w o u l d p r e d i c t t h a t carbonaria w i l l c h o o s e d a r k b a c k g r o u n d s a n d typica l i g h t b a c k g r o u n d s ,

regardless of h o w

they are painted. I f t h e l a t t e r t h e o r y t u r n e d o u t t o b e r i g h t , w o u l d this result g i v e a i d a n d c o m f o r t t o t h e g r e e n - b e a r d t h e o r y ? A little, p e r h a p s , s i n c e i t w o u l d s u g g e s t that a m o r p h o l o g i c a l character and behavioural recognition of something resembling that morphological character can be, or can rapidly become, closely linked g e n e t i c a l l y . It must be r e m e m b e r e d , here, that in the m o t h crypsis e x a m p l e there is no suggestion that we are dealing with an outlaw effect.

If there

are

two

genes,

one

controlling

colour

and

the

other

b a c k g r o u n d c h o i c e b e h a v i o u r , b o t h s t a n d t o g a i n f r o m t h e p r e s e n c e o f the a p p r o p r i a t e o t h e r o n e , a n d n e i t h e r o f t h e t w o i s i n a n y sense a n o u t l a w . I f the t w o genes started out distantly linked, selection w o u l d favour closer and c l o s e r l i n k a g e . I t i s n o t c l e a r t h a t s e l e c t i o n w o u l d s i m i l a r l y f a v o u r t h e close l i n k a g e o f a ' g r e e n - b e a r d g e n e ' a n d a g e n e for g r e e n - b e a r d r e c o g n i t i o n . I t s e e m s t h a t t h e a s s o c i a t i o n b e t w e e n t h e effects w o u l d h a v e t o b e t h e r e b y l u c k r i g h t f r o m t h e start. T h e g r e e n - b e a r d effect i s a l l a b o u t o n e selfish g e n e l o o k i n g after c o p i e s o f i t s e l f i n o t h e r i n d i v i d u a l s , r e g a r d l e s s of, i n d e e d i n spite of, the p r o b a b i l i t y that those i n d i v i d u a l s will share genes in g e n e r a l . T h e g r e e n - b e a r d g e n e ' s p o t s ' c o p i e s o f itself, a n d i t t h e r e b y s e e m s t o w o r k a g a i n s t the interests o f the rest o f t h e g e n o m e . I t a p p e a r s t o b e a n o u t l a w i n t h e sense t h a t i t m a k e s i n d i v i d u a l s w o r k a n d p a y costs, for t h e b e n e f i t o f o t h e r i n d i v i d u a l s w h o a r e n o t p a r t i c u l a r l y l i k e l y t o s h a r e g e n e s o t h e r t h a n t h e o u t l a w itself. T h i s i s the r e a s o n A l e x a n d e r a n d B o r g i a ( 1 9 7 8 ) c a l l i t a n o u t l a w , a n d i t i s o n e o f the r e a s o n s for t h e i r s c e p t i c i s m a b o u t t h e e x i s t e n c e o f g r e e n - b e a r d g e n e s . But it is actually not obvious that green-beard genes w o u l d , if they ever arose, be outlaws. T h e following caution is urged by R i d l e y and Grafen (in p r e s s ) . O u r d e f i n i t i o n o f a n o u t l a w m a k e s r e f e r e n c e t o its p r o v o k i n g o f m o d i f i e r s a t o t h e r l o c i w h i c h t e n d t o s u p p r e s s its p h e n o t y p i c effects. A t first sight it seems clear that g r e e n - b e a r d genes w o u l d indeed p r o v o k e suppressing modifiers, b e c a u s e the modifiers w o u l d not tend to h a v e copies in the bodies of the

(unrelated)

g r e e n - b e a r d e d i n d i v i d u a l s c a r e d for.

But we must not

f o r g e t t h a t a m o d i f i e r , i f i t i s t o h a v e a n y effect o n t h e p h e n o t y p i c e x p r e s s i o n of a g r e e n - b e a r d g e n e , is l i k e l y itself to be in a g r e e n - b e a r d e d b o d y , a n d is t h e r e f o r e in a p o s i t i o n to b e n e f i t f r o m receiving a l t r u i s m f r o m o t h e r g r e e n b e a r d e d i n d i v i d u a l s . M o r e o v e r , s i n c e those o t h e r g r e e n - b e a r d e d d o n o r s a r e n o t p a r t i c u l a r l y l i k e l y t o b e r e l a t i v e s , t h e costs o f t h e i r a l t r u i s m w i l l not b e felt b y c o p i e s o f t h e w o u l d - b e m o d i f i e r s . A c a s e c o u l d t h e r e f o r e b e m a d e t h a t w o u l d - b e m o d i f i e r s a t o t h e r l o c i w i l l g a i n r a t h e r t h a n lose f r o m s h a r i n g a b o d y w i t h a g r e e n - b e a r d g e n e . T o this i t c a n n o t b e o b j e c t e d t h a t t h e costs o f p a y i n g o u t a l t r u i s m t o o t h e r g r e e n - b e a r d e d i n d i v i d u a l s m a y o u t w e i g h the b e n e f i t s o f r e c e i v i n g a l t r u i s m f r o m o t h e r g r e e n - b e a r d e d i n d i v i d u a l s : i f this

O u t l a w s and Modifiers

149

w e r e true there w o u l d be no question of the g r e e n - b e a r d g e n e s p r e a d i n g in the first p l a c e . T h e e s s e n c e o f R i d l e y a n d G r a f e n ' s p o i n t i s t h a t i f ( w h i c h i s unlikely)

the g r e e n - b e a r d g e n e has w h a t it takes to spread

through the

p o p u l a t i o n a t all, t h e costs a n d b e n e f i t s o f t h e s i t u a t i o n w i l l b e s u c h a s t o f a v o u r m o d i f i e r s t h a t e n h a n c e r a t h e r t h a n r e d u c e t h e effect. I n e v a l u a t i n g this p o i n t , e v e r y t h i n g d e p e n d s o n t h e e x a c t n a t u r e o f w h a t w e are c a l l i n g the g r e e n - b e a r d p h e n o t y p e .

If the entire p l e i o t r o p i c d u a l

p h e n o t y p e â&#x20AC;&#x201D; g r e e n beard plus altruism towards g r e e n - b e a r d e d i n d i v i d u a l s â&#x20AC;&#x201D; is regarded as a p a c k a g e deal, w h i c h modifiers c a n suppress or e n h a n c e only as a unit, then R i d l e y and G r a f e n are surely right that g r e e n - b e a r d genes are n o t o u t l a w s . B u t , o f c o u r s e , a s t h e y t h e m s e l v e s stress, a m o d i f i e r t h a t c o u l d d e t a c h t h e t w o p h e n o t y p i c effects f r o m e a c h o t h e r , s u p p r e s s i n g t h e a l t r u i s t i c p h e n o t y p e of the g r e e n - b e a r d g e n e w h i l e not suppressing the g r e e n b e a r d itself w o u l d c e r t a i n l y b e f a v o u r e d . A t h i r d p o s s i b i l i t y i s t h e s p e c i a l c a s e o f a green-beard g e n e that caused parents to discriminate in f a v o u r of those of their c h i l d r e n that h a p p e n e d to share the r e c o g n i t i o n c h a r a c t e r . S u c h a g e n e w o u l d be analogous to a meiotic-drive gene, a n d w o u l d be a true o u t l a w . W h a t e v e r w e m a y feel a b o u t R i d l e y a n d G r a f e n ' s p o i n t a b o u t t h e g r e e n b e a r d effect, i t i s c l e a r t h a t g e n e s m e d i a t i n g a l t r u i s m t o w a r d s c l o s e k i n , a n d favoured by c o n v e n t i o n a l kin-selection pressure, are definitely not o u t l a w s . A l l the g e n e s i n t h e g e n o m e h a v e t h e s a m e s t a t i s t i c a l o d d s o f g a i n i n g f r o m t h e kin a l t r u i s m b e h a v i o u r , for a l l h a v e t h e s a m e s t a t i s t i c a l o d d s o f b e i n g p o s s e s s e d b y t h e i n d i v i d u a l b e n e f i t e d . A ' k i n - s e l e c t i o n g e n e ' is, i n a s e n s e , w o r k i n g for itself a l o n e , b u t i t b e n e f i t s t h e o t h e r g e n e s i n its g e n o m e a s w e l l . T h e r e w i l l t h e r e f o r e n o t b e s e l e c t i o n i n f a v o u r o f m o d i f i e r s t h a t s u p p r e s s it. A r m p i t selfinspection genes w o u l d be a special case of kin-recognition genes, and are likewise not o u t l a w s . I h a v e b e e n n e g a t i v e a b o u t t h e p l a u s i b i l i t y o f t h e g r e e n - b e a r d effect. T h e postulated favouritism based on sex c h r o m o s o m e s , w h i c h

I have already

m e n t i o n e d , i s a s p e c i a l c a s e o f t h e g r e e n - b e a r d effect, a n d i s p e r h a p s t h e l e a s t implausible one. I discussed it in the context of w i t h i n - f a m i l y favouritism: elder siblings w e r e supposed to discriminate a m o n g their y o u n g e r siblings on the basis o f p r o b a b i l i t y o f s h a r i n g sex c h r o m o s o m e s , s e x i t s e l f b e i n g u s e d a s the l a b e l ( ' g r e e n b e a r d ' ) . T h i s i s n o t t o o w i l d l y i m p r o b a b l e b e c a u s e , i f Y chromosomes do not pleiotropic

cross o v e r ,

green-beard

chromosome'.

'gene'

instead of h a v i n g to postulate a single

can

postulate

whole

'green-beard

I t i s sufficient t h a t t h e g e n e t i c b a s i s for s e x u a l f a v o u r i t i s m

s h o u l d o c c u r a n y w h e r e o n t h e sex c h r o m o s o m e c o n c e r n e d . O n e m i g h t m a k e a s i m i l a r a r g u m e n t for a n y s u b s t a n t i a l p o r t i o n o f a c h r o m o s o m e w h i c h , s a y b e c a u s e o f i n v e r s i o n , d i d n o t cross o v e r . I t i s c o n c e i v a b l e , t h e r e f o r e , t h a t a true g r e e n - b e a r d effect o f s o m e k i n d m i g h t o n e d a y b e d i s c o v e r e d . I suspect that all present e x a m p l e s of w h a t m i g h t a p p e a r to be g r e e n - b e a r d effects a r e , i n f a c t , v e r s i o n s o f t h e a r m p i t s e l f - i n s p e c t i o n effect. T h u s W u e t al.

150

O u t l a w s and M o d i f i e r s

( 1 9 8 0 ) p l a c e d i n d i v i d u a l m o n k e y s , Macaca nemestrina, in a c h o i c e a p p a r a t u s w h e r e t h e y h a d t o c h o o s e t o sit n e x t t o o n e o f t w o offered c o m p a n i o n s . I n e a c h c a s e o n e o f t h e t w o c o m p a n i o n s offered w a s a h a l f s i b l i n g , r e l a t e d t h r o u g h the father b u t not the m o t h e r ; the other w a s an unrelated control. T h e r e s u l t w a s a s t a t i s t i c a l l y s i g n i f i c a n t t e n d e n c y for i n d i v i d u a l s t o c h o o s e t o sit n e x t t o h a l f s i b l i n g s r a t h e r t h a n u n r e l a t e d c o n t r o l s . N o t e t h a t the h a l f s i b l i n g s c o n c e r n e d w e r e n o t r e l a t e d i n t h e m a t e r n a l l i n e : this m e a n s t h a t there is no possibility of their r e c o g n i z i n g an o d o u r a c q u i r e d from

the

mother, say.

the

W h a t e v e r the m o n k e y s are recognizing,

i t c o m e s from

s h a r e d f a t h e r , a n d this s u g g e s t s , i n s o m e sense, r e c o g n i t i o n o f s h a r e d g e n e s . My bet is that the m o n k e y s recognize resemblances of relatives to perceived f e a t u r e s o f t h e m s e l v e s . W u e t al. a r e o f t h e s a m e o p i n i o n . Greenberg zephyrum.

(1979)

(Seger,

studied

t h e p r i m i t i v e l y s o c i a l s w e a t b e e Lasioglossum

1 9 8 0 , refers t o this w o r k u n d e r t h e p i c t u r e s q u e h e a d i n g ,

' D o b e e s h a v e g r e e n s e t a e ? ' . ) W h e r e W u e t al. u s e d c h o i c e o f s i t t i n g p a r t n e r as a b e h a v i o u r a l assay, G r e e n b e r g used the decision of a g u a r d w o r k e r w h e t h e r t o a d m i t o r e x c l u d e a n o t h e r w o r k e r s e e k i n g e n t r a n c e t o t h e nest. He

plotted

the

probability

of a

worker's

being

admitted

against

her

coefficient of relationship w i t h the sentinel. N o t o n l y w a s there an excellent p o s i t i v e c o r r e l a t i o n : t h e s l o p e o f t h e l i n e w a s a l m o s t e x a c t l y o n e , s o the p r o b a b i l i t y of a s e n t i n e l a d m i t t i n g a s t r a n g e r w a s a p p r o x i m a t e l y equal to the coefficient o f r e l a t i o n s h i p ! G r e e n b e r g ' s e v i d e n c e c o n v i n c e d him that ' T h e g e n e t i c c o m p o n e n t i s t h e r e f o r e i n o d o r p r o d u c t i o n a n d a p p a r e n t l y n o t i n the p e r c e p t u a l s y s t e m ' (p. 1096). I n m y t e r m i n o l o g y , G r e e n b e r g ' s w o r d s a m o u n t t o t h e s t a t e m e n t t h a t h e i s d e a l i n g w i t h t h e a r m p i t effect, n o t w i t h t h e g r e e n b e a r d effect. O f c o u r s e t h e b e e s m a y , a s G r e e n b e r g b e l i e v e s , h a v e i n s p e c t e d relatives

with

whom

they

were

already

familiar

rather

than

their

own

' a r m p i t s ' ( H o l l d o b l e r & M i c h e n e r 1 9 8 0 ) . I t i s still e s s e n t i a l l y a n e x a m p l e o f t h e a r m p i t r a t h e r t h a n t h e g r e e n - b e a r d effect, i n w h i c h c a s e t h e r e i s n o question of the genes responsible being outlaws. A particularly elegant study w h i c h c o m e s t o a s i m i l a r c o n c l u s i o n i s t h a t o f L i n s e n m a i r ( 1 9 7 2 ) o n the f a m i l y - s p e c i f i c c h e m i c a l ' b a d g e ' o f t h e s o c i a l d e s e r t w o o d l o u s e Hemilepistus reaumuri.

Similarly, Bateson

(in p r e p a r a t i o n )

provides intriguing evidence

that J a p a n e s e q u a i l d i s c r i m i n a t e their first cousins from their siblings and from m o r e distant relatives, using learned visual cues. W a l d m a n and A d l e r (1979) h a v e investigated w h e t h e r tadpoles preferentially

associate

with

siblings.

Colour-marked

tadpoles

taken

from

two

c l u t c h e s w e r e a l l o w e d t o s w i m freely a r o u n d a t a n k ; t h e n a g r i d w a s l o w e r e d into the tank, t r a p p i n g e a c h tadpole in one of sixteen compartments. T h e r e was a statistically significant

t e n d e n c y for t a d p o l e s

to end

up closer to

siblings than to non-siblings. P e r h a p s unfortunately, the e x p e r i m e n t a l design d o e s n o t r u l e o u t a p o s s i b l e c o n f o u n d i n g effect o f g e n e t i c a l l y d e t e r m i n e d 'habitat selection'.

I f t h e r e w a s a g e n e t i c a l l y d e t e r m i n e d t e n d e n c y to, s a y ,

O u t l a w s and M o d i f i e r s

151

h u g the e d g e s o f t h e t a n k r a t h e r t h a n t h e m i d d l e , g e n e t i c r e l a t i v e s m i g h t a s a consequence be e x p e c t e d to end up in the same parts of the tank. T h e experiment does not, therefore, u n e q u i v o c a l l y d e m o n s t r a t e recognition of r e l a t i v e s o r a p r e f e r e n c e for a s s o c i a t i n g w i t h r e l a t i v e s a s s u c h , b u t for m a n y theoretical

purposes

this d o e s

not

matter.

The

authors

introduced

their

paper with reference to Fisher's (1930a) kin selection theory of the e v o l u t i o n o f a p o s e m a t i s m , a n d for p u r p o s e s o f t h a t t h e o r y r e l a t i v e s s i m p l y h a v e t o e n d up together. It doesn't matter whether they are together because of shared habitat preference or b e c a u s e of true relative-recognition. F o r o u r present purpose, h o w e v e r , it is w o r t h n o t i n g that, if further e x p e r i m e n t s confirm the r u l e o f ' i n c i d e n t a l h a b i t a t s e l e c t i o n ' for t h e t a d p o l e s , this w o u l d r u l e o u t t h e 'armpit' theory but w o u l d not rule out the g r e e n - b e a r d theory. S h e r m a n (1979) invokes the i d e a of genetic favouritism in an ingenious theory a b o u t c h r o m o s o m e n u m b e r s in social insects. He presents e v i d e n c e t h a t e u s o c i a l insects t e n d t o h a v e h i g h e r c h r o m o s o m e n u m b e r s t h a n t h e i r nearest

non-social

phylogenetic

relatives.

Seger

(1980)

independently

d i s c o v e r e d t h e effect, a n d h a s his o w n t h e o r y t o a c c o u n t for it. T h e e v i d e n c e for the effect i s s o m e w h a t e q u i v o c a l a n d w o u l d p e r h a p s b e n e f i t f r o m a demanding

analysis

using

the

statistical

methods

developed

modern

students of the c o m p a r a t i v e m e t h o d (e.g. H a r v e y & M a c e in press). B u t what I

a m c o n c e r n e d w i t h h e r e i s n o t t h e t r u t h o f t h e effect i t s e l f b u t

S h e r m a n ' s t h e o r y t o a c c o u n t for it. H e c o r r e c t l y n o t e s t h a t h i g h c h r o m o s o m e numbers tend to r e d u c e the v a r i a n c e in fraction of shared genes a m o n g siblings. To take an e x t r e m e case, if a species has o n l y one c h r o m o s o m e pair w i t h n o c r o s s i n g - o v e r , a n y p a i r o f full s i b l i n g s w i l l s h a r e ( i d e n t i c a l b y d e s c e n t ) either all, none, or h a l f of their genes w i t h a m e a n of 50 per cent. If there are hundreds of chromosomes, on the other hand, the n u m b e r of genes shared (identical by descent) a m o n g siblings will be n a r r o w l y distributed a b o u t the same m e a n of 50 per cent. C r o s s i n g - o v e r c o m p l i c a t e s the issue, b u t it r e m a i n s true that a high c h r o m o s o m e n u m b e r in a species tends to go w i t h l o w genetic variance a m o n g siblings in that species. It follows that if social insect workers wished to discriminate in favour of those o f t h e i r s i b l i n g s w i t h w h o m t h e y h a p p e n e d t o s h a r e t h e m o s t g e n e s , i t w o u l d b e e a s i e r for t h e m t o d o s o i f t h e s p e c i e s ' s c h r o m o s o m e n u m b e r w e r e low than if it were high. S u c h preferential discrimination by workers w o u l d b e d e t r i m e n t a l t o t h e f i t n e s s o f the q u e e n , w h o w o u l d ' p r e f e r ' a m o r e e v e n h a n d e d t r e a t m e n t o f h e r o f f s p r i n g . S h e r m a n t h e r e f o r e s u g g e s t s , i n effect, t h a t the h i g h c h r o m o s o m e c o u n t i n e u s o c i a l i n s e c t s i s a n a d a p t a t i o n t o c a u s e "offsprings' r e p r o d u c t i v e interests to m o r e closely c o i n c i d e w i t h those of their m o t h e r " . W e should not forget, b y the w a y , that w o r k e r s w i l l not b e unanimous. E a c h worker might show favouritism towards y o u n g e r siblings t h a t r e s e m b l e h e r , b u t o t h e r w o r k e r s w i l l t e n d t o resist h e r f a v o u r i t i s m , for the s a m e r e a s o n a s t h e q u e e n w i l l resist it. T h e w o r k e r s c a n n o t b e t r e a t e d a s

152

O u t l a w s and M o d i f i e r s

a m o n o l i t h i c p a r t y in opposition to the q u e e n , in the same w a y as T r i v e r s a n d H a r e ( 1 9 7 6 ) w e r e a b l e to treat t h e m in their theory of conflict o v e r the sex r a t i o . S h e r m a n v e r y f a i r l y lists t h r e e w e a k n e s s e s o f his h y p o t h e s i s , b u t t h e r e a r e t w o m o r e s e r i o u s p r o b l e m s w i t h it, F i r s t l y , u n l e s s w e a r e c a r e f u l t o q u a l i f y i t further, the hypothesis a p p e a r s to c o m e d a n g e r o u s l y close to a fallacy w h i c h I h a v e d u b b e d ' M i s u n d e r s t a n d i n g N u m b e r II' ( D a w k i n s 1979a) or the ' A c e of Spades

Fallacy'

(Chapter

10).

Sherman

assumes

that

the

extent of

c o o p e r a t i o n a m o n g c o n s p e c i f i c s i s r e l a t e d t o t h e ' m e a n fraction o f a l l e l e s t h e y s h a r e ' ( m y e m p h a s i s ) w h e r e a s h e s h o u l d t h i n k i n t e r m s o f the probability t h a t a g e n e ' f o r ' c o o p e r a t i o n i s s h a r e d (see a l s o P a r t r i d g e & N u n n e y 1 9 7 7 ) . O n t h e l a t t e r a s s u m p t i o n his h y p o t h e s i s , a s a t p r e s e n t e x p r e s s e d , w o u l d n o t w o r k (Seger

1980).

Sherman

could

r e s c u e his h y p o t h e s i s f r o m

this p a r t i c u l a r

c r i t i c i s m b y i n v o k i n g t h e ' a r m p i t s e l f - r e c o g n i t i o n ' effect. I s h a l l n o t spell t h e a r g u m e n t o u t i n d e t a i l , b e c a u s e I s u s p e c t t h a t S h e r m a n a c c e p t s it.

(The

e s s e n t i a l p o i n t i s t h a t t h e a r m p i t effect c a n use w e a k l i n k a g e w i t h i n a f a m i l y , w h i l e t h e g r e e n - b e a r d effect r e q u i r e s p l e i o t r o p y o r l i n k a g e d i s e q u i l i b r i u m . I f workers

inspect

themselves,

and

show

favouritism

those

their

r e p r o d u c t i v e siblings that share features that they p e r c e i v e themselves to possess,

ordinary

hypothesis

linkage

could

escape

effects the

become

'Ace

all-important

of Spades

Fallacy'.

and It

Sherman's would

also,

i n c i d e n t a l l y , e s c a p e t h e first o f S h e r m a n ' s o w n o b j e c t i o n s , n a m e l y t h a t the hypothesis ' d e p e n d s on the existence of alleles that e n a b l e their bearers to recognize

their

covered ...',

alleles'.

'Such

recognition

alleles

have

never

been dis-

and, by implication, are pretty implausible. S h e r m a n could

m a k e t h i n g s e a s i e r for h i m s e l f b y t y i n g his h y p o t h e s i s t o t h e a r m p i t r a t h e r t h a n t h e g r e e n - b e a r d effect.) My

second

attention

difficulty

by J.

with

Maynard

Sherman's

Smith

hypothesis

(personal

was

brought

communication).

Taking

the

' a r m p i t ' version of the theory, it is indeed c o n c e i v a b l e that workers might be s e l e c t e d t o i n s p e c t t h e m s e l v e s , a n d s h o w f a v o u r i t i s m t o w a r d s those o f t h e i r r e p r o d u c t i v e s i b l i n g s t h a t s h a r e t h e i r o w n i n d i v i d u a l c h a r a c t e r i s t i c s . I t i s also t r u e t h a t q u e e n s w o u l d t h e n b e s e l e c t e d t o s u p p r e s s this f a v o u r i t i s m i f t h e y c o u l d , for i n s t a n c e b y p h e r o m o n a l m a n i p u l a t i o n . B u t , i n o r d e r t o b e s e l e c t e d , a n y s u c h m o v e o n t h e p a r t o f a q u e e n w o u l d h a v e t o h a v e a n effect a s soon a s it a r o s e as a m u t a t i o n . W o u l d this be t r u e of a m u t a t i o n t h a t i n c r e a s e d a queen's c h r o m o s o m e n u m b e r ? No it w o u l d not. An increase in chromosome n u m b e r w o u l d c h a n g e the selection pressures b e a r i n g o n w o r k e r favouritism, and m a n y generations later it might produce an evolutionary change which w o u l d b e t o t h e a d v a n t a g e o f q u e e n s i n g e n e r a l . B u t this w o u l d n o t h e l p the original

mutant

queen,

programming and

would

whose

workers

be oblivious

would

their

own

genetic

t o c h a n g e s i n s e l e c t i o n pressures.

C h a n g e s i n s e l e c t i o n p r e s s u r e s e x e r t t h e i r effects o v e r t h e l o n g e r t i m e - s c a l e o f

O u t l a w s and Modifiers

153

generations. A q u e e n c a n n o t be e x p e c t e d to initiate a p r o g r a m of artificial s e l e c t i o n for t h e l o n g - t e r m b e n e f i t o f f u t u r e q u e e n s ! T h e h y p o t h e s i s m a y b e r e s c u e d from this o b j e c t i o n b y s u g g e s t i n g t h a t h i g h c h r o m o s o m e n u m b e r s a r e not an a d a p t a t i o n to facilitate q u e e n m a n i p u l a t i o n of w o r k e r s , b u t rather are a p r e a d a p t a t i o n . T h o s e g r o u p s t h a t h a p p e n e d , for o t h e r r e a s o n s , t o h a v e high chromosome

numbers,

were the most likely

to evolve eusociality.

S h e r m a n m e n t i o n s this v e r s i o n o f his h y p o t h e s i s , b u t sees n o r e a s o n t o f a v o u r i t o v e r the m o r e p o s i t i v e , m a t e r n a l - m a n i p u l a t i o n v e r s i o n .

In conclusion,

Sherman's hypothesis can be m a d e theoretically sound, if it is phrased in terms of p r e a d a p t a t i o n rather t h a n a d a p t a t i o n , a n d in terms of the a r m p i t effect r a t h e r t h a n t h e g r e e n - b e a r d effect. T h e g r e e n - b e a r d effect m a y b e i m p l a u s i b l e , b u t i t i s i n s t r u c t i v e . T h e s t u d e n t o f k i n s e l e c t i o n w h o first u n d e r s t a n d s t h e h y p o t h e t i c a l g r e e n - b e a r d effect, a n d t h e n a p p r o a c h e s k i n s e l e c t i o n t h e o r y i n t e r m s o f its s i m i l a r i t i e s t o a n d d i f f e r e n c e s f r o m ' g r e e n - b e a r d t h e o r y ' , i s u n l i k e l y t o fall p r e y t o t h e m a n y t e m p t i n g o p p o r t u n i t i e s for e r r o r t h a t k i n s e l e c t i o n t h e o r y offers

(Dawkins

1 9 7 9 a ) . M a s t e r y o f the g r e e n - b e a r d m o d e l will c o n v i n c e h i m that altruism t o w a r d s k i n i s n o t a n e n d i n itself, s o m e t h i n g t h a t a n i m a l s a r e m y s t e r i o u s l y e x p e c t e d t o p r a c t i s e i n a c c o r d a n c e w i t h s o m e c l e v e r m a t h e m a t i c s t h a t field workers don't understand. Rather, kinship provides just one w a y in w h i c h genes can b e h a v e as if they recognized and favoured copies of themselves in o t h e r i n d i v i d u a l s . H a m i l t o n h i m s e l f i s e m p h a t i c o n this p o i n t : ' . . . k i n s h i p should be considered just one w a y of getting positive regression of g e n o t y p e i n t h e r e c i p i e n t , a n d . . . i t i s this p o s i t i v e r e g r e s s i o n t h a t i s v i t a l l y n e c e s s a r y for a l t r u i s m . T h u s the i n c l u s i v e fitness c o n c e p t i s m o r e g e n e r a l t h a n " k i n selection"' (Hamilton 1975a, p. 140-141). H a m i l t o n is here using w h a t he earlier described as 'the extended m e a n i n g o f i n c l u s i v e fitness' ( H a m i l t o n 1 9 6 4 b , p . 2 5 ) . T h e c o n v e n t i o n a l m e a n i n g o f inclusive

fitness,

the

meaning

upon

which

Hamilton

himself based

his

d e t a i l e d m a t h e m a t i c s , i s i n c a p a b l e o f h a n d l i n g t h e g r e e n - b e a r d effect a n d , indeed, o u t l a w s such as meiotic-drive genes. T h i s is b e c a u s e it is firmly tied to t h e i d e a of t h e

individual organism

'vehicle'

' m a x i m i z i n g entity'.

O u t l a w g e n e s d e m a n d t o b e t r e a t e d a s selfish m a x i m i z i n g e n t i t i e s i n t h e i r o w n r i g h t , a n d t h e y c o n s t i t u t e a s t r o n g w e a p o n i n t h e c a s e a g a i n s t t h e 'selfish o r g a n i s m ' p a r a d i g m . N o w h e r e i s this b e t t e r e x e m p l i f i e d t h a n i n H a m i l t o n ' s o w n i n g e n i o u s e x t e n s i o n s o f F i s h e r ' s sex r a t i o t h e o r y ( H a m i l t o n 1 9 6 7 ) . T h e green-beard t h o u g h t e x p e r i m e n t is instructive in further w a y s . A n y o n e w h o thinks a b o u t genes literally as m o l e c u l a r entities is in d a n g e r of b e i n g m i s l e d b y p a s s a g e s l i k e ' W h a t i s t h e selfish g e n e ? I t i s n o t j u s t o n e s i n g l e p h y s i c a l bit o f D N A . . . I t i s all replicas o f a p a r t i c u l a r b i t o f D N A , d i s t r i b u t e d throughout the w o r l d . . . a distributed a g e n c y , existing in m a n y different i n d i v i d u a l s a t o n c e . . . a g e n e m i g h t b e a b l e t o assist replicas o f i t s e l f w h i c h a r e s i t t i n g i n o t h e r b o d i e s . ' T h e w h o l e o f k i n s e l e c t i o n t h e o r y rests o n this g e n e r a l

154

O u t l a w s and Modifiers

p r e m i s e , y e t i t w o u l d b e m y s t i c a l a n d w r o n g t o t h i n k t h a t g e n e s assist c o p i e s o f e a c h o t h e r because t h o s e c o p i e s a r e i d e n t i c a l m o l e c u l e s t o t h e m s e l v e s . A g r e e n b e a r d t h o u g h t e x p e r i m e n t h e l p s t o e x p l a i n this. C h i m p a n z e e s a n d g o r i l l a s a r e s o s i m i l a r t h a t a g e n e i n o n e s p e c i e s m i g h t b e p h y s i c a l l y i d e n t i c a l i n its m o l e c u l a r d e t a i l s to a g e n e in t h e o t h e r . Is this m o l e c u l a r i d e n t i t y a sufficient reason to e x p e c t selection to favour genes in one species ' r e c o g n i z i n g ' copies of themselves in the other species, a n d extending them a helping h a n d ? T h e a n s w e r i s n o , a l t h o u g h a n a i v e a p p l i c a t i o n o f 'selfish g e n e ' r e a s o n i n g a t the m o l e c u l a r level m i g h t lead us to think otherwise. N a t u r a l selection at the g e n e level is c o n c e r n e d w i t h c o m p e t i t i o n a m o n g a l l e l e s for a p a r t i c u l a r c h r o m o s o m a l slot in a s h a r e d g e n e - p o o l . A g r e e n b e a r d g e n e i n t h e c h i m p a n z e e g e n e p o o l i s n o t a c a n d i d a t e for a slot o n a n y g o r i l l a c h r o m o s o m e , a n d n o r i s a n y o f its a l l e l e s . I t i s t h e r e f o r e indifferent t o t h e fate o f its s t r u c t u r a l l y i d e n t i c a l c o u n t e r p a r t i n t h e g o r i l l a g e n e - p o o l . (It not

counterpart

might

indifferent the

gorilla

molecular identity.)

the

fate

gene-pool,

but

its that

phenotypically

identical

has

do with

nothing

A s far a s t h e p r e s e n t a r g u m e n t i s c o n c e r n e d , c h i m p

g e n e s a n d g o r i l l a g e n e s a r e n o t c o p i e s o f e a c h o t h e r i n a n i m p o r t a n t sense. T h e y a r e c o p i e s o f e a c h o t h e r o n l y i n t h e t r i v i a l sense t h a t t h e y h a p p e n t o h a v e the i d e n t i c a l m o l e c u l a r structure. T h e unconscious, m e c h a n i c a l laws o f n a t u r a l s e l e c t i o n g i v e u s n o g r o u n d s for e x p e c t i n g t h e m t o assist m o l e c u l a r c o p i e s , j u s t b e c a u s e t h e y are m o l e c u l a r c o p i e s . Conversely,

we m i g h t be justified

i n e x p e c t i n g t o see g e n e s assisting

m o l e c u l a r l y different alleles at their o w n locus w i t h i n a species g e n e - p o o l , p r o v i d e d t h e y h a d t h e s a m e p h e n o t y p i c effects. A p h e n o t y p i c a l l y n e u t r a l mutation at a locus changes molecular identity but does nothing to weaken a n y selection there m a y be in favour of m u t u a l assistance.

Green-beard

a l t r u i s m c o u l d still i n c r e a s e t h e i n c i d e n c e o f g r e e n - b e a r d p h e n o t y p e s i n the population,

even

t h o u g h g e n e s w e r e assisting o t h e r g e n e s t h a t w e r e not

s t r i c t c o p i e s o f t h e m s e l v e s i n t h e m o l e c u l a r sense.

It is the incidence of

phenotypes

not

that

are

interested

explaining,

the

incidence

m o l e c u l a r c o n f i g u r a t i o n s o f D N A . A n d i f a n y r e a d e r t h i n k s t h a t last r e m a r k c o n t r a d i c t s m y b a s i c thesis, I m u s t h a v e failed t o m a k e m y b a s i c thesis c l e a r ! L e t m e use t h e g r e e n b e a r d i n o n e m o r e i n s t r u c t i v e t h o u g h t e x p e r i m e n t , t o c l a r i f y t h e t h e o r y o f r e c i p r o c a l a l t r u i s m . I h a v e c a l l e d t h e g r e e n - b e a r d effect i m p l a u s i b l e , w i t h t h e p o s s i b l e e x c e p t i o n o f t h e sex c h r o m o s o m e s p e c i a l cases. But

there

another

special

case

which

could

conceivably

have some

c o u n t e r p a r t in reality. I m a g i n e a g e n e p r o g r a m m i n g the b e h a v i o u r a l rule: ' I f y o u see a n o t h e r i n d i v i d u a l p e r f o r m i n g a n a l t r u i s t i c a c t , r e m e m b e r t h e incident,

and

individual in

i f t h e o p p o r t u n i t y arises b e h a v e a l t r u i s t i c a l l y t o w a r d s future'

'altruism-recognition

(Dawkins effect.'

1976a,

Using

the

96).

This m a y be called

legendary

example

that the

of Haldane's

(1955) j u m p i n g into the river to save a d r o w n i n g person, the g e n e that I am

O u t l a w s and M o d i f i e r s

155

p o s t u l a t i n g m i g h t s p r e a d b e c a u s e i t w a s , i n effect, r e c o g n i z i n g c o p i e s o f itself. I t is, i n fact, a k i n d o f g r e e n - b e a r d g e n e . I n s t e a d o f u s i n g a n i n c i d e n t a l p l e i o t r o p i c r e c o g n i t i o n c h a r a c t e r s u c h as a g r e e n b e a r d , it uses a n o n i n c i d e n t a l o n e : t h e b e h a v i o u r p a t t e r n o f a l t r u i s t i c r e s c u i n g itself. R e s c u e r s tend t o s a v e o n l y o t h e r s w h o h a v e r e s c u e d s o m e b o d y i n t h e i r t i m e , s o t h e gene tends to save copies of itself (setting aside p r o b l e m s of h o w the system c o u l d g e t s t a r t e d , e t c . ) . M y p o i n t i n b r i n g i n g this h y p o t h e t i c a l e x a m p l e u p h e r e i s t o e m p h a s i z e its d i s t i n c t n e s s f r o m t w o o t h e r , s u p e r f i c i a l l y s i m i l a r cases. T h e f i r s t i s t h e o n e H a l d a n e h i m s e l f w a s i l l u s t r a t i n g , t h e s a v i n g o f c l o s e kin;

thanks

Hamilton

now

understand

this

well.

T h e second

reciprocal altruism (Trivers 1 9 7 1 ) . A n y resemblance b e t w e e n true reciprocal a l t r u i s m a n d the h y p o t h e t i c a l a l t r u i s m - r e c o g n i t i o n c a s e I a m n o w d i s c u s s i n g is purely accidental (Rothstein 1981). T h e resemblance, h o w e v e r , sometimes muddles students of the t h e o r y of r e c i p r o c a l altruism, w h i c h is w h y I am m a k i n g use o f g r e e n - b e a r d t h e o r y t o d i s p e l t h e m u d d l e . I n true r e c i p r o c a l a l t r u i s m , t h e ' a l t r u i s t ' s t a n d s t o g a i n i n t h e f u t u r e f r o m the p r e s e n c e o f the individual b e n e f i c i a r y o f his a l t r u i s m . T h e effect w o r k s e v e n i f t h e t w o s h a r e n o g e n e s , a n d e v e n (contra R o t h s t e i n

1981) if they

b e l o n g t o different s p e c i e s , a s i n T r i v e r s ' s e x a m p l e o f t h e m u t u a l i s m b e t w e e n cleaner fish and

their clients.

Genes mediating such reciprocal

altruism

benefit t h e rest o f t h e g e n o m e n o less t h a n t h e y b e n e f i t t h e m s e l v e s , a n d a r e clearly

not

outlaws.

They

are

favoured

ordinary,

familiar

natural

selection, albeit some p e o p l e (e.g. Sahlins 1 9 7 7 , p p . 8 5 - 8 7 ) seem to h a v e difficulty i n u n d e r s t a n d i n g t h e p r i n c i p l e , a p p a r e n t l y b e c a u s e t h e y o v e r l o o k the f r e q u e n c y - d e p e n d e n t n a t u r e o f t h e s e l e c t i o n a n d t h e c o n s e q u e n t n e e d t o think i n g a m e - t h e o r e t i c t e r m s ( D a w k i n s 1 9 7 6 a , p p . 1 9 7 â&#x20AC;&#x201D; 2 0 1 ; A x e l r o d a n d H a m i l t o n 1 9 8 1 ) . T h e a l t r u i s m - r e c o g n i t i o n effect i s f u n d a m e n t a l l y different, t h o u g h s u p e r f i c i a l l y s i m i l a r . T h e r e i s n o n e e d for t h e a l t r u i s m r e c o g n i z e r i n d i v i d u a l t o r e p a y a g o o d t u r n d o n e t o himself. H e s i m p l y r e c o g n i z e s g o o d d e e d s d o n e t o a n y b o d y , a n d s i n g l e s o u t t h e a l t r u i s t for his o w n l a t e r f a v o u r s . It w o u l d be impossible to g i v e a sensible a c c o u n t of o u t l a w s in terms of i n d i v i d u a l s m a x i m i z i n g t h e i r f i t n e s s . T h a t i s t h e r e a s o n for g i v i n g t h e m p r o m i n e n c e i n this b o o k . A t t h e b e g i n n i n g o f t h e c h a p t e r I d i v i d e d o u t l a w s into 'allelic o u t l a w s ' a n d 'laterally spreading o u t l a w s ' . A l l the suggested o u t l a w s w e h a v e s o far c o n s i d e r e d h a v e b e e n a l l e l i c : t h e y a r e f a v o u r e d o v e r their a l l e l e s a t t h e i r o w n l o c i , w h i l e b e i n g o p p o s e d b y m o d i f i e r s a t o t h e r l o c i . I n o w turn to laterally s p r e a d i n g o u t l a w s . T h e s e are o u t l a w s u n r u l y e n o u g h to break a w a y a l t o g e t h e r from the discipline of allelic c o m p e t i t i o n w i t h i n the confines o f a l o c u s . T h e y s p r e a d t o o t h e r l o c i , e v e n c r e a t e n e w l o c i for t h e m s e l v e s b y i n c r e a s i n g t h e size o f the g e n o m e . T h e y a r e c o n v e n i e n t l y discussed

under

the

heading

'Selfish

DNA',

catch-phrase

which

has

r e c e n t l y a c q u i r e d c u r r e n c y i n t h e p a g e s o f Nature. T h i s w i l l b e t h e s u b j e c t o f the f i r s t p a r t o f t h e n e x t c h a p t e r .

9 Selfish D N A , J u m p i n g Genes, and a L a m a r c k i a n Scare

This

chapter

will

somewhat

miscellaneous

one,

gathering

t o g e t h e r t h e results o f m y b r i e f a n d f o o l h a r d y i n c u r s i o n s i n t o t h e h i n t e r l a n d s o f fields far f r o m m y o w n , m o l e c u l a r a n d c e l l b i o l o g y , i m m u n o l o g y a n d e m b r y o l o g y . T h e b r e v i t y I justify on the grounds that greater length w o u l d be

even

foolhardy.

The

foolhardiness

less d e f e n s i b l e ,

but

may

p e r h a p s be forgiven on the g r o u n d s that an e q u a l l y rash earlier raid yielded the g e r m o f a n i d e a w h i c h s o m e m o l e c u l a r biologists n o w take seriously under the n a m e o f Selfish D N A .

Selfish D N A . . . it a p p e a r s that the a m o u n t of D N A in organisms is m o r e than is s t r i c t l y n e c e s s a r y for b u i l d i n g t h e m : a l a r g e f r a c t i o n o f t h e D N A i s n e v e r translated into protein. F r o m the point of v i e w of the i n d i v i d u a l organism

this

seems

supervise

the

b u i l d i n g of b o d i e s ,

paradoxical.

I f the it

'purpose'

of D N A is

is s u r p r i s i n g to find

a large

quantity of D N A w h i c h does no such thing. Biologists are racking t h e i r b r a i n s t r y i n g t o t h i n k w h a t this s u r p l u s D N A i s d o i n g . B u t from t h e p o i n t o f v i e w o f t h e selfish g e n e s t h e m s e l v e s , t h e r e i s n o p a r a d o x . T h e t r u e ' p u r p o s e ' o f D N A i s t o s u r v i v e , n o m o r e a n d n o less. T h e simplest w a y to e x p l a i n the surplus D N A is to suppose that it is a p a r a s i t e , or at best a h a r m l e s s b u t useless p a s s e n g e r , h i t c h i n g a r i d e in the survival m a c h i n e s created b y the other D N A [ D a w k i n s 1976a, p. 47]. T h i s i d e a w a s d e v e l o p e d f u r t h e r a n d w o r k e d o u t m o r e fully b y m o l e c u l a r biologists

two

stimulating

papers

published

simultaneously

Nature

(Doolittle & S a p i e n z a 1980; O r g e l & C r i c k 1980). T h e s e papers provoked c o n s i d e r a b l e d i s c u s s i o n , i n l a t e r issues o f Nature ( s y m p o s i a i n V o l . 285, p p . 617-620

and

Vol.

288,

pp.

645-648) 156

and

elsewhere

(e.g.

BBC

radio

Selfish D N A , J u m p i n g G e n e s , a n d a L a m a r c k i a n S c a r e

157

d i s c u s s i o n ) . T h e i d e a is, o f c o u r s e , h i g h l y c o n g e n i a l t o t h e w h o l e thesis b e i n g a d v a n c e d i n this b o o k . T h e facts a r e a s f o l l o w s . T h e t o t a l a m o u n t o f D N A i n different o r g a n i s m s i s v e r y v a r i a b l e , a n d t h e v a r i a t i o n d o e s n o t m a k e o b v i o u s sense i n t e r m s o f phylogeny.

This

implausible

that

the

so-called

number

'C-value

of radically

paradox'. different

'It

genes

seems

totally

needed

s a l a m a n d e r is 20 t i m e s t h a t f o u n d in a m a n ' ( O r g e l & C r i c k 1 9 8 0 ) . It is e q u a l l y i m p l a u s i b l e t h a t s a l a m a n d e r s o n t h e W e s t side o f N o r t h A m e r i c a should need m a n y times m o r e D N A than c o n g e n e r i c s a l a m a n d e r s o n the E a s t side. A l a r g e p e r c e n t a g e o f t h e D N A i n e u k a r y o t i c g e n o m e s i s n e v e r t r a n s l a t e d . T h i s ' j u n k D N A ' m a y lie b e t w e e n c i s t r o n s , i n w h i c h c a s e i t i s k n o w n a s s p a c e r D N A , o r i t m a y consist o f u n e x p r e s s e d ' i n t r o n s ' w i t h i n cistrons,

interspersed with

(Crick

1979).

the expressed parts of the cistron,

the

'exons'

T h e apparently surplus D N A m a y b e t o v a r y i n g extents

repetitive and meaningless in terms of the genetic c o d e . S o m e is p r o b a b l y never transcribed into R N A . O t h e r portions m a y b e transcribed into R N A , but then 'spliced out' before the R N A is translated into a m i n o a c i d sequences. Either w a y , it is never expressed phenotypically, if by p h e n o t y p i c expression we m e a n expression v i a the o r t h o d o x route of c o n t r o l l i n g protein synthesis (Doolittle & S a p i e n z a 1980). T h i s does not m e a n , h o w e v e r , that the so-called j u n k D N A i s n o t subject t o n a t u r a l s e l e c t i o n . V a r i o u s ' f u n c t i o n s ' for i t h a v e b e e n p r o p o s e d , w h e r e 'function'

means

adaptive

benefit

the

organism.

The

'function'

extra D N A m a y 'simply b e t o separate the g e n e s ' ( C o h e n 1 9 7 7 , p . 1 7 2 ) . E v e n if a stretch of D N A is not itself transcribed, it c a n increase the f r e q u e n c y of c r o s s o v e r s b e t w e e n g e n e s s i m p l y b y o c c u p y i n g s p a c e b e t w e e n t h e m , a n d this is a kind of p h e n o t y p i c expression. S p a c e r D N A m i g h t , therefore, in s o m e sense b e f a v o u r e d b y n a t u r a l s e l e c t i o n b e c a u s e o f its effects o n c r o s s o v e r frequencies. It w o u l d not, h o w e v e r , be c o m p a t i b l e w i t h c o n v e n t i o n a l usage to describe a length of spacer D N A as e q u i v a l e n t to a ' g e n e for' a g i v e n r e c o m b i n a t i o n r a t e . T o q u a l i f y for this title, a g e n e m u s t h a v e a n effect o n r e c o m b i n a t i o n r a t e s in comparison with its alleles. It is m e a n i n g f u l to s p e a k of a given

length

spacer

DNA

having

allelesâ&#x20AC;&#x201D;differing

sequences

o c c u p y i n g the same space on other c h r o m o s o m e s in the p o p u l a t i o n . B u t since the p h e n o t y p i c effect o f s p a c i n g o u t g e n e s i s a r e s u l t s o l e l y o f t h e l e n g t h o f t h e stretch o f s p a c e r D N A , a l l a l l e l e s a t a g i v e n ' l o c u s ' m u s t h a v e t h e s a m e 'phenotypic expression' if they all h a v e the same length. If the 'function' of surplus D N A is 'to' s p a c e o u t genes, therefore, the w o r d function is b e i n g used i n a n u n u s u a l w a y . T h e n a t u r a l s e l e c t i o n p r o c e s s i n v o l v e d i s n o t t h e ordinary

natural

selection

among

alleles

locus.

Rather,

the

perpetuation of a feature of the genetic systemâ&#x20AC;&#x201D;distance b e t w e e n genes. A n o t h e r p o s s i b l e ' f u n c t i o n ' for t h e n o n - e x p r e s s e d D N A i s t h a t s u g g e s t e d b y C a v a l i e r - S m i t h ( 1 9 7 8 ) . H i s t h e o r y i s e n c a p s u l a t e d i n his t i t l e : ' N u c l e a r

158

Selfish D N A , J u m p i n g G e n e s , and a L a m a r c k i a n Scare

v o l u m e c o n t r o l b y n u c l e o s k e l e t a l D N A , s e l e c t i o n for c e l l v o l u m e a n d cell g r o w t h rate, a n d the solution o f the D N A C - v a l u e p a r a d o x . ' H e thinks that 'K-selected' organisms

need

l a r g e r cells

than

'r-selected'

ones,

and

that

v a r y i n g the total a m o u n t of D N A per cell is a g o o d w a y of controlling cell s i z e . H e asserts t h a t ' t h e r e i s a g o o d c o r r e l a t i o n b e t w e e n s t r o n g r - s e l e c t i o n , small cells a n d l o w C - v a l u e s on the one h a n d a n d b e t w e e n K-selection, large cells a n d h i g h C - v a l u e s o n t h e o t h e r ' . I t w o u l d b e i n t e r e s t i n g t o test for this correlation

statistically,

taking

account

the

difficulties

inherent

q u a n t i t a t i v e c o m p a r a t i v e s u r v e y s ( H a r v e y & M a c e i n p r e s s ) . T h e r\K dist i n c t i o n itself, t o o , s e e m s t o a r o u s e w i d e s p r e a d d o u b t s a m o n g e c o l o g i s t s , for reasons that h a v e n e v e r b e e n quite clear to m e , and sometimes seem unclear to t h e m too.

I t i s o n e o f t h o s e c o n c e p t s t h a t i s often u s e d ,

but almost

a l w a y s a c c o m p a n i e d by a ritualistic a p o l o g y , the intellectual e q u i v a l e n t of touching wood.

S o m e o b j e c t i v e i n d e x o f a s p e c i e s ' s p o s i t i o n o n the r / K

c o n t i n u u m w o u l d b e n e e d e d b e f o r e a r i g o r o u s test o f t h e c o r r e l a t i o n c o u l d b e undertaken. While

awaiting

further

evidence

for

and

against

hypotheses

o f the

C a v a l i e r - S m i t h v a r i e t y , the thing to notice in the present c o n t e x t is that they are hypotheses m a d e in the traditional m o u l d ; they are based on the idea that D N A , like a n y o t h e r aspect of an o r g a n i s m , is selected b e c a u s e it does the

organism

some

good.

The

selfish

DNA

hypothesis

based

i n v e r s i o n o f this a s s u m p t i o n : p h e n o t y p i c c h a r a c t e r s a r e t h e r e b e c a u s e t h e y h e l p D N A t o r e p l i c a t e itself, a n d i f D N A c a n find q u i c k e r a n d e a s i e r w a y s t o r e p l i c a t e itself, p e r h a p s b y p a s s i n g c o n v e n t i o n a l p h e n o t y p i c e x p r e s s i o n , i t w i l l b e s e l e c t e d t o d o s o . E v e n i f t h e E d i t o r o f Nature ( V o l . 2 8 5 , p . 604, 1980) g o e s a bit far in d e s c r i b i n g it as ' m i l d l y s h o c k i n g ' , t h e t h e o r y of selfish D N A is in a w a y r e v o l u t i o n a r y . B u t o n c e w e d e e p l y i m b i b e the f u n d a m e n t a l truth that an o r g a n i s m is a tool of D N A , rather than the other w a y a r o u n d , the idea of 'selfish D N A ' b e c o m e s c o m p e l l i n g , e v e n o b v i o u s . T h e l i v i n g c e l l , e s p e c i a l l y t h e n u c l e u s i n e u k a r y o t e s , i s p a c k e d w i t h the active

machinery

of nucleic

polymerase readily whether or not

that

catalyses D N A is

acid

replication

and

the replication of any meaningful in

recombination. DNA,

DNA

regardless of

terms of the genetic code.

' S n i p p i n g o u t ' o f D N A , a n d ' s p l i c i n g i n ' o f o t h e r bits o f D N A , a r e also p a r t s o f t h e n o r m a l s t o c k i n t r a d e o f t h e c e l l u l a r a p p a r a t u s , for t h e y o c c u r e v e r y t i m e there is a crossover or other t y p e of r e c o m b i n a t i o n event. T h e fact that i n v e r s i o n s a n d o t h e r t r a n s l o c a t i o n s s o r e a d i l y o c c u r , f u r t h e r testifies t o the c a s u a l e a s e w i t h w h i c h c h u n k s o f D N A m a y b e c u t o u t o f o n e p a r t o f the g e n o m e , a n d spliced into another part. R e p l i c a b i l i t y and 'spliceability' seem t o b e a m o n g t h e m o s t s a l i e n t f e a t u r e s o f D N A i n its n a t u r a l e n v i r o n m e n t ( R i c h m o n d 1979) of cellular machinery. G i v e n the possibilities of such an e n v i r o n m e n t , g i v e n the existence of c e l l u l a r f a c t o r i e s set u p for t h e r e p l i c a t i o n a n d s p l i c i n g o f D N A , i t i s o n l y t o b e e x p e c t e d that natural selection w o u l d favour D N A variants that are able

Selfish D N A , J u m p i n g G e n e s , a n d a L a m a r c k i a n S c a r e

159

t o e x p l o i t t h e c o n d i t i o n s t o t h e i r o w n a d v a n t a g e . A d v a n t a g e , i n this c a s e , simply means multiple replication in germ-lines. A n y variety of D N A whose properties h a p p e n to m a k e it readily replicated will a u t o m a t i c a l l y b e c o m e c o m m o n e r i n the w o r l d . W h a t might such properties be? Paradoxically, we are most familiar w i t h the

indirect,

elaborate,

and

roundabout

methods

which

DNA

m o l e c u l e s s e c u r e t h e i r f u t u r e . T h e s e a r e t h e i r p h e n o t y p i c effects o n b o d i e s , a c h i e v e d by the p r o x i m a l route of c o n t r o l l i n g protein synthesis, a n d h e n c e by

the

distal

routes

controlling

embryonic

development

m o r p h o l o g y , physiology and b e h a v i o u r . B u t there are also m u c h m o r e direct and simple w a y s i n w h i c h varieties o f D N A c a n spread a t the e x p e n s e o f rival varieties. It is b e c o m i n g increasingly evident that, in addition to the large, orderly c h r o m o s o m e s w i t h their w e l l - r e g i m e n t e d g a v o t t e , cells are h o m e to a m o t l e y riff-raff o f D N A a n d

R N A fragments,

cashing in

the perfect

e n v i r o n m e n t p r o v i d e d by the cellular a p p a r a t u s . T h e s e replicating fellow-travellers go by various n a m e s d e p e n d i n g on size and properties: plasmids, episomes, insertion sequences, plasmons, virions, transposons, replicons, viruses. W h e t h e r they should be r e g a r d e d as rebels who have

broken

a w a y from

the c h r o m o s o m a l g a v o t t e ,

or as invading

p a r a s i t e s f r o m o u t s i d e , s e e m s t o m a t t e r less a n d less. T o t a k e a p a r a l l e l , w e m a y r e g a r d a p o n d , or a forest, as a c o m m u n i t y w i t h a c e r t a i n s t r u c t u r e , a n d e v e n a c e r t a i n s t a b i l i t y . B u t the s t r u c t u r e a n d s t a b i l i t y a r e m a i n t a i n e d i n t h e face

of a

constant

turnover

of participants.

Individuals

immigrate

and

emigrate, n e w ones are b o r n a n d old ones die. T h e r e is a fluidity, a j u m p i n g in and out of c o m p o n e n t parts, so that it b e c o m e s m e a n i n g l e s s to try to distinguish 'true' c o m m u n i t y m e m b e r s from foreign invaders. So it is w i t h the g e n o m e . It is n o t a s t a t i c s t r u c t u r e , b u t a fluid c o m m u n i t y . ' J u m p i n g genes' immigrate and emigrate (Cohen 1976).

S i n c e t h e r a n g e o f p o s s i b l e hosts i n n a t u r e a t l e a s t for t r a n s f o r m i n g D N A a n d for p l a s m i d s s u c h a s R P 4 i s s o l a r g e , o n e feels t h a t a t least i n G r a m - n e g a t i v e b a c t e r i a all p o p u l a t i o n s m a y i n d e e d b e c o n n e c t e d . I t i s k n o w n that b a c t e r i a l D N A c a n b e expressed i n w i d e l y different host

species . . . It

may

indeed

impossible

view

bacterial

evolution in terms of simple family trees; rather, a n e t w o r k , w i t h converging as well as diverging junctions, m a y be a more appropriate metaphor [Broda 1979, p. 140]. Some

authors

speculate

that

the

network

not

confined

bacterial

evolution (e.g. M a r g u l i s 1976). T h e r e i s s u b s t a n t i a l e v i d e n c e t h a t o r g a n i s m s a r e n o t l i m i t e d for t h e i r evolution

to genes that b e l o n g to the g e n e pool of their species.

R a t h e r it seems m o r e plausible that in the time-scale of e v o l u t i o n the

160

Selfish D N A , J u m p i n g G e n e s , and a L a m a r c k i a n Scare

w h o l e o f t h e g e n e p o o l o f the b i o s p h e r e i s a v a i l a b l e t o a l l o r g a n i s m s and

t h a t t h e m o r e d r a m a t i c steps a n d

apparent discontinuities in

e v o l u t i o n a r e i n f a c t a t t r i b u t a b l e t o v e r y r a r e e v e n t s i n v o l v i n g the a d o p t i o n of part or all of a foreign g e n o m e . O r g a n i s m s and genomes m a y thus be r e g a r d e d as c o m p a r t m e n t s of the biosphere through w h i c h genes

general circulate at various

rates and

in which

i n d i v i d u a l g e n e s a n d o p e r o n s m a y b e i n c o r p o r a t e d i f o f sufficient a d v a n t a g e . . .' [ J e o n & D a n i e l l i 1 9 7 1 ] . T h a t e u k a r y o t e s , i n c l u d i n g o u r s e l v e s , m a y not

b e i n s u l a t e d from this

h y p o t h e t i c a l g e n e t i c traffic i s s u g g e s t e d b y t h e f a s t - g r o w i n g s u c c e s s o f the technology definition

'genetic

of g e n e

engineering',

manipulation

gene

Britain

manipulation. is

'the

The

formation

legal

of new

c o m b i n a t i o n s of heritable material by the insertion of nucleic acid molecules, p r o d u c e d by w h a t e v e r m e a n s outside the cell,

into a n y virus, bacterial

p l a s m i d o r o t h e r v e c t o r s y s t e m s o a s t o a l l o w t h e i r i n c o r p o r a t i o n i n t o a host organism in w h i c h they do not naturally occur but in w h i c h they are capable o f c o n t i n u e d p r o p a g a t i o n ' ( O l d & P r i m r o s e 1980, p . 1 ) . B u t o f c o u r s e h u m a n genetic engineers are beginners in the g a m e . T h e y are just learning to tap the expertise of the n a t u r a l g e n e t i c engineers, the viruses a n d plasmids that h a v e b e e n selected to m a k e their living at the trade. P e r h a p s t h e g r e a t e s t f e a t o f n a t u r a l g e n e t i c e n g i n e e r i n g o n the g r a n d s c a l e is the c o m p l e x of manipulations associated with sexual reproduction in eukaryotes:

meiosis, crossing-over a n d fertilization. T w o o f our foremost

m o d e r n e v o l u t i o n i s t s h a v e f a i l e d t o e x p l a i n t o t h e i r o w n s a t i s f a c t i o n the advantage

o f this

extraordinary

procedure

for

the

individual

organism

(Williams 1 9 7 5 ; M a y n a r d Smith 1978a). As M a y n a r d Smith (1978a, p. 113) a n d W i l l i a m s ( 1 9 7 9 ) b o t h n o t e , this m a y b e o n e a r e a w h e r e , i f n o w h e r e else, w e s h a l l h a v e t o s w i t c h o u r a t t e n t i o n a w a y from i n d i v i d u a l o r g a n i s m s t o t r u e replicators. W h e n w e try t o solve the p a r a d o x o f the cost o f meiosis, perhaps i n s t e a d o f w o r r y i n g a b o u t h o w s e x h e l p s t h e organism w e s h o u l d s e a r c h for r e p l i c a t i n g 'engineers' of meiosis, intracellular agents w h i c h actually cause meiosis to h a p p e n . T h e s e h y p o t h e t i c a l engineers, fragments of nucleic acid w h i c h m i g h t lie i n s i d e o r o u t s i d e t h e c h r o m o s o m e s , w o u l d h a v e t o a c h i e v e their o w n r e p l i c a t i o n success as a b y p r o d u c t of forcing meiosis u p o n the organism. In bacteria, r e c o m b i n a t i o n is a c h i e v e d by a separate fragment of D N A o r ' s e x f a c t o r ' w h i c h , i n o l d e r t e x t b o o k s , w a s t r e a t e d a s a p a r t o f the bacterium's o w n adaptive machinery, but w h i c h is better regarded as a r e p l i c a t i n g g e n e t i c e n g i n e e r w o r k i n g for its o w n g o o d . I n a n i m a l s , c e n t r i o l e s are

thought

mitochondria,

self-replicating

entities

with

their

own

DNA,

a l t h o u g h u n l i k e m i t o c h o n d r i a t h e y often pass t h r o u g h the

m a l e as w e l l as the female line. A l t h o u g h at present it is just a j o k e to picture c h r o m o s o m e s b e i n g d r a g g e d k i c k i n g and s c r e a m i n g into the second anaphase

Selfish D N A , J u m p i n g G e n e s , a n d a L a m a r c k i a n S c a r e

161

b y r u t h l e s s l y selfish c e n t r i o l e s o r o t h e r m i n i a t u r e g e n e t i c e n g i n e e r s , s t r a n g e r ideas h a v e

b e c o m e c o m m o n p l a c e in the past.

And,

after a l l ,

orthodox

t h e o r i z i n g h a s s o far failed t o d e n t t h e p a r a d o x o f t h e c o s t o f m e i o s i s . O r g e l a n d C r i c k ( 1 9 8 0 ) s a y m u c h t h e s a m e a b o u t t h e lesser p a r a d o x o f v a r i a b l e C v a l u e s a n d a b o u t the selfish D N A t h e o r y t o a c c o u n t for i t : ' T h e m a i n facts a r e , a t first s i g h t , s o o d d t h a t o n l y a s o m e w h a t u n c o n v e n t i o n a l idea is likely to e x p l a i n t h e m . ' By a c o m b i n a t i o n of fact a n d d a y d r e a m e d e x t r a p o l a t i o n , I h a v e t r i e d t o set a s t a g e o n t o w h i c h selfish D N A i t s e l f c a n e n t e r a l m o s t u n n o t i c e d ; t o p a i n t a b a c k d r o p a g a i n s t w h i c h selfish D N A w i l l appear,

not

unconventional

but

almost

inescapable.

DNA

that

not

translated into protein, w h o s e c o d o n s w o u l d spell m e a n i n g l e s s g i b b e r i s h if t h e y e v e r w e r e t r a n s l a t e d , m a y y e t v a r y i n its r e p l i c a b i l i t y , its s p l i c e a b i l i t y , a n d its r e s i s t a n c e t o d e t e c t i o n a n d d e l e t i o n b y t h e d e b u g g i n g r o u t i n e s o f t h e cellular

machinery.

'Intragenomic

selection'

can

therefore

lead

i n c r e a s e i n the a m o u n t o f c e r t a i n t y p e s o f m e a n i n g l e s s , o r u n t r a n s c r i b e d , D N A , littered a r o u n d a n d cluttering u p the c h r o m o s o m e s . T r a n s l a t e d D N A , too, m a y b e s u b j e c t t o this k i n d o f s e l e c t i o n , a l t h o u g h h e r e t h e i n t r a g e n o m i c selection pressures will p r o b a b l y be s w a m p e d by m o r e p o w e r f u l pressures, p o s i t i v e a n d n e g a t i v e , r e s u l t i n g f r o m c o n v e n t i o n a l p h e n o t y p i c effects. C o n v e n t i o n a l s e l e c t i o n results i n c h a n g e s i n t h e f r e q u e n c y o f r e p l i c a t o r s relative to their alleles at defined loci on the c h r o m o s o m e s of p o p u l a t i o n s . I n t r a g e n o m i c s e l e c t i o n o f selfish D N A i s a d i f f e r e n t k i n d o f s e l e c t i o n . H e r e we are not d e a l i n g w i t h the relative success of alleles at o n e locus in a g e n e p o o l , b u t w i t h t h e s p r e a d a b i l i t y o f c e r t a i n k i n d s o f D N A t o different l o c i o r the c r e a t i o n o f n e w l o c i . M o r e o v e r , t h e s e l e c t i o n o f selfish D N A i s n o t l i m i t e d to the time-scale of i n d i v i d u a l g e n e r a t i o n s ; it c a n selectively increase in a n y mitotic cell division in the germ-lines of d e v e l o p i n g bodies. In

conventional

selection,

the

variation

which

selection

acts

produced, ultimately, by mutation, but we usually think of it as mutation within the constraints of an o r d e r l y system of l o c i : m u t a t i o n p r o d u c e s a variant gene at a n a m e d locus. It is therefore possible to think of selection as c h o o s i n g a m o n g a l l e l e s a t s u c h a d i s c r e t e l o c u s . M u t a t i o n i n t h e l a r g e r sense, h o w e v e r , includes m o r e r a d i c a l c h a n g e s in the g e n e t i c system, m i n o r ones such as inversions, and major ones such as c h a n g e s in c h r o m o s o m e n u m b e r or ploidy, a n d c h a n g e s from s e x u a l i t y to a s e x u a l i t y a n d v i c e versa. T h e s e l a r g e r m u t a t i o n s ' c h a n g e t h e r u l e s o f t h e g a m e ' b u t t h e y a r e still, i n v a r i o u s senses, s u b j e c t t o n a t u r a l s e l e c t i o n . I n t r a g e n o m i c s e l e c t i o n for selfish D N A b e l o n g s i n t h e list o f u n c o n v e n t i o n a l t y p e s o f s e l e c t i o n , n o t i n v o l v i n g c h o i c e a m o n g alleles at a discrete locus. Selfish D N A i s s e l e c t e d for its p o w e r t o s p r e a d ' l a t e r a l l y ' , t o g e t i t s e l f duplicated into n e w loci elsewhere in the g e n o m e . It does not spread at the e x p e n s e o f a p a r t i c u l a r set o f a l l e l e s ,

in the w a y that,

say,

a g e n e for

m e l a n i s m i n m o t h s s p r e a d s i n i n d u s t r i a l a r e a s a t t h e e x p e n s e o f its a l l e l e s a t

Selfish D N A , J u m p i n g G e n e s , and a L a m a r c k i a n Scare

the s a m e locus.

It is this t h a t d i s t i n g u i s h e s it,

as a ' l a t e r a l l y s p r e a d i n g

o u t l a w ' , from the 'allelic o u t l a w s ' w h i c h w e r e the subject of the previous c h a p t e r . L a t e r a l s p r e a d i n g to n e w loci is like the spread of a virus through a p o p u l a t i o n , or like the spread of c a n c e r cells t h r o u g h a b o d y . O r g e l and C r i c k i n d e e d refer t o t h e s p r e a d i n g o f f u n c t i o n l e s s r e p l i c a t o r s a s a ' c a n c e r o f the g e n o m e ' . A s for t h e q u a l i t i e s w h i c h a r e a c t u a l l y l i k e l y t o b e f a v o u r e d i n the s e l e c t i o n o f selfish D N A , I w o u l d h a v e t o b e a m o l e c u l a r b i o l o g i s t i n o r d e r t o p r e d i c t them in detail. O n e does not h a v e to be a molecular biologist, however, to s u r m i s e t h a t t h e y m i g h t b e classified i n t o t w o m a i n c l a s s e s : q u a l i t i e s t h a t m a k e for e a s e o f d u p l i c a t i o n

and

insertion,

and

qualities

that

make

difficult for d e f e n c e m e c h a n i s m s o f t h e c e l l t o seek t h e m o u t a n d d e s t r o y t h e m . J u s t a s a c u c k o o e g g seeks p r o t e c t i o n b y m i m i c k i n g the host e g g s w h i c h l e g i t i m a t e l y i n h a b i t t h e nest, s o selfish D N A m i g h t e v o l v e m i m e t i c q u a l i t i e s t h a t ' m a k e i t m o r e l i k e o r d i n a r y D N A a n d so, p e r h a p s , less e a s y t o r e m o v e ' ( O r g e l & C r i c k ) . J u s t a s a full u n d e r s t a n d i n g o f c u c k o o a d a p t a t i o n s is l i k e l y to r e q u i r e a k n o w l e d g e of t h e p e r c e p t u a l s y s t e m s of hosts, so a full a p p r e c i a t i o n o f t h e d e t a i l s o f selfish D N A a d a p t a t i o n s w i l l r e q u i r e d e t a i l e d knowledge of exactly how D N A polymerase works, exactly how snipping and s p l i c i n g o c c u r , e x a c t l y w h a t g o e s o n i n m o l e c u l a r ' p r o o f - r e a d i n g ' . W h i l e full k n o w l e d g e o f t h e s e m a t t e r s c a n o n l y c o m e f r o m d e t a i l e d r e s e a r c h w o r k o f the k i n d t h a t m o l e c u l a r b i o l o g i s t s h a v e s o b r i l l i a n t l y s u c c e e d e d i n b e f o r e , i t is, perhaps, not too m u c h to h o p e that m o l e c u l a r biologists m i g h t be aided in t h e i r r e s e a r c h b y t h e r e a l i z a t i o n t h a t D N A i s n o t w o r k i n g for t h e g o o d o f the c e l l b u t for t h e g o o d o f itself. T h e m a c h i n e r y o f r e p l i c a t i o n , s p l i c i n g , a n d p r o o f - r e a d i n g m a y b e b e t t e r u n d e r s t o o d i f i t i s s e e n a s i n p a r t the p r o d u c t o f a ruthless a r m s r a c e . T h e point m a y be e m p h a s i z e d w i t h the aid of an analogy. I m a g i n e t h a t M a r s i s a U t o p i a i n w h i c h t h e r e i s c o m p l e t e trust, t o t a l h a r m o n y , n o selfishness a n d n o d e c e i t . N o w i m a g i n e a scientist f r o m M a r s t r y i n g t o m a k e s e n s e o f h u m a n life a n d t e c h n o l o g y . S u p p o s e h e s t u d i e d o n e o f o u r l a r g e d a t a p r o c e s s i n g c e n t r e s â&#x20AC;&#x201D; a n e l e c t r o n i c c o m p u t e r w i t h its a s s o c i a t e d machinery

of duplication,

assumptionâ&#x20AC;&#x201D;natural designed

for

the

editing

his

common

own

and

error-correction.

societyâ&#x20AC;&#x201D;that

good,

would

the go

If he

machinery a

long

made had

way

the been

towards

u n d e r s t a n d i n g it. E r r o r - c o r r e c t i n g d e v i c e s , for i n s t a n c e , w o u l d c l e a r l y b e designed

combat

the

inevitable

and

non-malevolent

Second

L a w of

T h e r m o d y n a m i c s . But certain aspects w o u l d remain p u z z l i n g . H e would m a k e n o sense o f the e l a b o r a t e a n d costly systems o f security a n d p r o t e c t i o n : secret passwords a n d c o d e n u m b e r s that h a v e to be typed in by c o m p u t e r users. If o u r M a r t i a n e x a m i n e d a military electronic c o m m u n i c a t i o n system h e m i g h t d i a g n o s e its p u r p o s e a s t h e r a p i d a n d efficient t r a n s m i s s i o n o f useful i n f o r m a t i o n , a n d h e m i g h t t h e r e f o r e b e baffled b y t h e t r o u b l e a n d e x p e n s e t o

Selfish D N A , J u m p i n g G e n e s , a n d a L a m a r c k i a n S c a r e

163

w h i c h t h e s y s t e m s e e m s t o g o i n o r d e r t o e n c o d e its m e s s a g e s i n a w a y w h i c h i s o b s c u r e a n d h a r d t o d e c o d e . I s this n o t w a n t o n a n d a b s u r d i n e f f i c i e n c y ? B r o u g h t up as he is in a trusting U t o p i a , it m i g h t require a m a j o r flash of r e v o l u t i o n a r y i n s i g h t for o u r M a r t i a n t o see t h a t m u c h o f h u m a n t e c h n o l o g y o n l y m a k e s sense w h e n y o u r e a l i z e t h a t h u m a n s distrust e a c h o t h e r , t h a t s o m e h u m a n s w o r k a g a i n s t the best i n t e r e s t s o f o t h e r h u m a n s . T h e r e i s a s t r u g g l e b e t w e e n those w h o w i s h t o o b t a i n i l l i c i t i n f o r m a t i o n f r o m a c o m m u n i c a t i o n s y s t e m a n d those w h o w i s h t o w i t h h o l d t h a t i n f o r m a t i o n f r o m t h e m . M u c h o f h u m a n t e c h n o l o g y is the p r o d u c t of arms races a n d c a n o n l y be u n d e r s t o o d in those t e r m s . S p e c t a c u l a r as their a c h i e v e m e n t s h a v e been, is it possible that m o l e c u l a r biologists h a v e hitherto, like biologists at other levels, b e e n in s o m e t h i n g like the p o s i t i o n o f o u r M a r t i a n ? B y a s s u m i n g t h a t t h e c e l l i s a p l a c e w h e r e m o l e c u l a r m a c h i n e r y w h i r r s for the g o o d o f t h e o r g a n i s m , t h e y h a v e c o m e a long w a y . T h e y m a y g o further i f they n o w c u l t i v a t e a m o r e c y n i c a l v i e w a n d c o u n t e n a n c e the p o s s i b i l i t y t h a t s o m e m o l e c u l e s m a y b e u p t o n o g o o d f r o m the p o i n t o f v i e w o f t h e rest. O b v i o u s l y t h e y a l r e a d y d o this w h e n t h e y contemplate viruses and other i n v a d i n g parasites. A l l that is n e e d e d is to t u r n the s a m e c y n i c a l e y e o n t h e c e l l ' s ' o w n ' D N A . I t i s b e c a u s e t h e y a r e s t a r t i n g t o d o j u s t this t h a t I f i n d t h e p a p e r s o f D o o l i t t l e a n d S a p i e n z a a n d O r g e l and C r i c k so exciting, in comparison w i t h the objections of C a v a l i e r S m i t h (1980), D o v e r (1980) a n d others, a l t h o u g h o f course the objectors m a y be right in

the

particular detailed

points

they make.

Orgel

and

Crick

s u m m a r i z e the message w e l l :

I n s h o r t , w e m a y e x p e c t a k i n d o f m o l e c u l a r s t r u g g l e for e x i s t e n c e w i t h i n the D N A o f the c h r o m o s o m e s , using the process o f n a t u r a l s e l e c t i o n . T h e r e i s n o r e a s o n t o b e l i e v e t h a t this i s l i k e l y t o b e m u c h simpler or more easy to predict than evolution at a n y other level. At b o t t o m , t h e e x i s t e n c e o f selfish D N A i s p o s s i b l e b e c a u s e D N A i s a m o l e c u l e w h i c h i s r e p l i c a t e d v e r y e a s i l y a n d b e c a u s e selfish D N A occurs in an environment in w h i c h D N A replication is a necessity. It thus has the o p p o r t u n i t y of s u b v e r t i n g these essential m e c h a n i s m s to its o w n p u r p o s e . I n w h a t sense i s selfish D N A a n o u t l a w ? I t i s a n o u t l a w t o t h e e x t e n t t h a t organisms

would

b e t t e r off w i t h o u t it.

Perhaps

wastes

space

and

molecular raw materials, perhaps it wastefully consumes v a l u a b l e running t i m e o n the d u p l i c a t i n g a n d p r o o f r e a d i n g m a c h i n e r y . I n a n y e v e n t w e m a y e x p e c t t h a t s e l e c t i o n w i l l t e n d t o e l i m i n a t e selfish D N A f r o m t h e g e n o m e . W e m a y d i s t i n g u i s h t w o k i n d s o f 'anti-selfish D N A ' s e l e c t i o n . F i r s t l y , s e l e c t i o n might favour positive adaptations

t o rid o r g a n i s m s o f selfish D N A .

For

e x a m p l e , the a l r e a d y discovered proofreading p r i n c i p l e m i g h t b e e x t e n d e d .

Selfish D N A , J u m p i n g G e n e s , a n d a L a m a r c k i a n Scare

L o n g s e q u e n c e s m i g h t b e e x a m i n e d for ' s e n s e ' a n d e x c i s e d i f f o u n d w a n t i n g . I n p a r t i c u l a r , h i g h l y r e p e t i t i v e D N A m i g h t b e r e c o g n i z e d b y its statistical uniformity. T h e s e positive adaptations are w h a t I had in mind in my above d i s c u s s i o n o f a r m s r a c e s , ' m i m i c r y ' , e t c . W e a r e t a l k i n g , h e r e , a b o u t the e v o l u t i o n o f anti-selfish D N A m a c h i n e r y w h i c h c o u l d b e a s e l a b o r a t e and a s s p e c i a l i z e d a s t h e a n t i p r e d a t o r a d a p t a t i o n s o f insects. T h e r e is, h o w e v e r , a s e c o n d k i n d o f s e l e c t i o n t h a t c o u l d a c t a g a i n s t selfish D N A , w h i c h i s m u c h simpler and cruder. A n y organism that h a p p e n e d t o e x p e r i e n c e a r a n d o m d e l e t i o n o f p a r t o f its selfish D N A w o u l d , b y d e f i n i t i o n , be a m u t a n t o r g a n i s m . T h e deletion itself w o u l d be a m u t a t i o n , a n d it w o u l d b e f a v o u r e d b y n a t u r a l s e l e c t i o n t o t h e e x t e n t t h a t o r g a n i s m s possessing i t benefited from wastage

it,

of space,

p r e s u m a b l y because they did materials

and

time

n o t suffer t h e e c o n o m i c

t h a t selfish

D N A brings.

Mutant

o r g a n i s m s w o u l d , o t h e r things b e i n g e q u a l , r e p r o d u c e at a h i g h e r rate than the

loaded

down

'wild-type'

individuals,

and

the

deletion

would

con-

s e q u e n t l y b e c o m e m o r e c o m m o n in the g e n e pool. N o t e that I am not n o w t a l k i n g a b o u t s e l e c t i o n i n f a v o u r o f t h e capacity t o d e l e t e selfish D N A : t h a t w a s t h e s u b j e c t o f t h e p r e v i o u s p a r a g r a p h . H e r e w e a r e r e c o g n i z i n g t h a t the d e l e t i o n itself, t h e absence of t h e selfish D N A , is itself a r e p l i c a t i n g e n t i t y (a replicating absence!), w h i c h can be favoured by selection. It is t e m p t i n g to include under the h e a d i n g of outlaws somatic mutations that c a u s e cells to o u t - r e p r o d u c e the n o n - m u t a n t cells of a b o d y , to the u l t i m a t e d e t r i m e n t o f t h e b o d y itself. B u t a l t h o u g h t h e r e i s a k i n d o f q u a s i D a r w i n i a n s e l e c t i o n t h a t c a n g o o n i n c a n c e r t u m o u r s , a n d C a i r n s ( 1 9 7 5 ) has ingeniously d r a w n attention to w h a t appear to be bodily adaptations to forestall s u c h w i t h i n - b o d y selection, I think that to a p p l y the o u t l a w c o n c e p t h e r e w o u l d n o t b e h e l p f u l . N o t , t h a t i s t o s a y , u n l e s s the m u t a n t g e n e s concerned

somehow

manage

propagate

themselves

indefinitely.

They

c o u l d d o this e i t h e r b y g e t t i n g t h e m s e l v e s t r a n s p o r t e d i n v i r u s - l i k e v e c t o r s , say t h r o u g h the air, or by s o m e h o w b u r r o w i n g into the n u c l e a r germ-line. In either of these t w o cases they w o u l d qualify as ' g e r m - l i n e replicators' as d e f i n e d i n C h a p t e r 5 a n d t h e title o f o u t l a w w o u l d b e a p p r o p r i a t e . There

has

been

one

startling recent

suggestion

that genes w h i c h

are

b e n e f i c i a r i e s o f s o m a t i c s e l e c t i o n m i g h t i n d e e d b u r r o w i n t o the g e r m - l i n e , t h o u g h i n this c a s e t h e y a r e n o t c a n c e r o u s a n d n o t n e c e s s a r i l y o u t l a w s . I w a n t t o m e n t i o n this w o r k b e c a u s e i t h a s b e e n g i v e n p u b l i c i t y a s a w o u l d - b e resuscitator of the so-called

' L a m a r c k i a n ' theory of evolution.

S i n c e the

t h e o r e t i c a l p o s i t i o n a d o p t e d i n this b o o k i s f a i r l y d e s c r i b a b l e a s ' e x t r e m e Weismannism',

I a m b o u n d t o see a n y s e r i o u s r e v i v a l o f L a m a r c k i s m a s

u n d e r m i n i n g m y p o s i t i o n . I t i s t h e r e f o r e n e c e s s a r y t o discuss it.

A L a m a r c k i a n scare I use t h e w o r d ' s c a r e ' b e c a u s e , t o b e p a i n f u l l y h o n e s t , I c a n t h i n k o f few

Selfish D N A , J u m p i n g G e n e s , and a L a m a r c k i a n S c a r e

165

things t h a t w o u l d m o r e d e v a s t a t e m y w o r l d v i e w t h a n a d e m o n s t r a t e d n e e d to

return

the

theory

of evolution

that

traditionally

attributed

L a m a r c k . I t i s o n e o f t h e f e w c o n t i n g e n c i e s for w h i c h I m i g h t offer t o e a t m y h a t . It is t h e r e f o r e all t h e m o r e i m p o r t a n t to g i v e a full a n d fair h e a r i n g to some claims m a d e on b e h a l f of Steele (1979) (1980,

1981). Before Steele's (1979)

and Gorczynski and Steele

book w a s available in Britain,

The

Sunday Times o f L o n d o n ( 1 3 J u l y 1980) p r i n t e d a f u l l - p a g e a r t i c l e a b o u t his ideas and 'astonishing e x p e r i m e n t w h i c h seems t o c h a l l e n g e D a r w i n i s m a n d r e s u r r e c t L a m a r c k ' . T h e B B C h a v e g i v e n t h e results s i m i l a r p u b l i c i t y , i n a t least t w o t e l e v i s i o n p r o g r a m m e s a n d s e v e r a l r a d i o p r o g r a m m e s : a s w e h a v e a l r e a d y seen, ' s c i e n t i f i c ' j o u r n a l i s t s a r e c o n s t a n t l y o n t h e a l e r t for a n y t h i n g that s o u n d s l i k e a c h a l l e n g e t o D a r w i n . N o less a s c i e n t i s t t h a n S i r P e t e r M e d a w a r forced us to take Steele's w o r k seriously by d o i n g so himself. He was quoted as b e i n g properly cautious a b o u t the need to repeat the w o r k , and as c o n c l u d i n g : 'I h a v e no i d e a w h a t the o u t c o m e w i l l be, b u t I h o p e S t e e l e is r i g h t '

(The Sunday

Times).

N a t u r a l l y a n y scientist h o p e s t h a t t h e t r u t h , w h a t e v e r i t is, w i l l o u t . B u t a scientist i s also e n t i t l e d t o his i n n e r m o s t h o p e s a s t o w h a t t h a t t r u t h w i l l t u r n out to b e — a revolution in one's head is b o u n d to be a painful e x p e r i e n c e — a n d I confess t h a t m y o w n h o p e s d i d n o t i n i t i a l l y c o i n c i d e w i t h S i r P e t e r ' s ! I h a d m y d o u b t s a b o u t w h e t h e r his c o u l d r e a l l y c o i n c i d e w i t h t h o s e a t t r i b u t e d t o h i m , u n t i l I r e c a l l e d his, t o m e a l w a y s s l i g h t l y p u z z l i n g (see p a g e 2 2 ) , r e m a r k t h a t ' T h e m a i n w e a k n e s s o f m o d e r n e v o l u t i o n a r y t h e o r y i s its l a c k o f a fully w o r k e d o u t t h e o r y o f v a r i a t i o n , t h a t is, o f candidature for e v o l u t i o n , o f the f o r m i n w h i c h g e n e t i c v a r i a n t s a r e p r o f f e r e d for s e l e c t i o n .

We have

therefore n o c o n v i n c i n g a c c o u n t o f e v o l u t i o n a r y p r o g r e s s — o f the o t h e r w i s e inexplicable tendency of organisms to adopt ever more c o m p l i c a t e d solutions o f the p r o b l e m s o f r e m a i n i n g a l i v e ' ( M e d a w a r 1 9 6 7 ) . M e d a w a r i s o n e o f those w h o h a v e , m o r e r e c e n t l y , t r i e d v e r y h a r d , a n d y e t f a i l e d , t o r e p l i c a t e S t e e l e ' s f i n d i n g s ( B r e n t et al. 1 9 8 1 ) . T o a n t i c i p a t e t h e c o n c l u s i o n I s h a l l c o m e to, I n o w v i e w w i t h e q u a n i m i t y , if w i t h d w i n d l i n g e x p e c t a t i o n ( B r e n t et al. 1 9 8 1 ; M c L a r e n et al. 1 9 8 1 ) , t h e prospect of Steele's theory being upheld, because I n o w realize that, in the d e e p e s t a n d fullest sense, it is a D a r w i n i a n t h e o r y ; a v a r i e t y of D a r w i n i a n theory m o r e o v e r w h i c h , like the theory of j u m p i n g genes, is p a r t i c u l a r l y c o n g e n i a l to t h e thesis of this b o o k , s i n c e it stresses s e l e c t i o n at a l e v e l o t h e r than t h a t o f t h e i n d i v i d u a l o r g a n i s m . T h o u g h p a r d o n a b l e , t h e c l a i m t h a t i t challenges D a r w i n i s m turns out to be j u s t a journalistic g l o a t ,

provided

D a r w i n i s m is understood in the w a y that I think it o u g h t to be understood. A s for S t e e l e ' s t h e o r y itself, e v e n i f the facts d o n o t u p h o l d it, i t w i l l h a v e done us the v a l u a b l e service of forcing us to shar pen o u r p e r c e p t i o n of D a r w i n i s m . I am not qualified to e v a l u a t e the t e c h n i c a l details of Steele's e x p e r i m e n t s a n d those o f his c r i t i c s ( a g o o d e v a l u a t i o n i s g i v e n b y H o w a r d

Selfish D N A , J u m p i n g G e n e s , and a L a m a r c k i a n Scare

166

1981), a n d w i l l c o n c e n t r a t e o n d i s c u s s i n g t h e i m p a c t o f his t h e o r y , s h o u l d t h e facts e v e n t u a l l y p r o v e t o s u p p o r t it. Steele

forges

threefold

union

of Burnet's

(1969)

theory

of clonal

s e l e c t i o n , T e m i n ' s ( 1 9 7 4 ) p r o v i r u s t h e o r y , a n d his o w n a t t a c k o n the s a n c t i t y o f W e i s m a n n ' s g e r m - l i n e . F r o m B u r n e t h e gets the idea o f somatic mutation l e a d i n g to g e n e t i c diversity a m o n g the cells of the b o d y . N a t u r a l selection w i t h i n t h e b o d y t h e n sees t o i t t h a t t h e b o d y b e c o m e s p o p u l a t e d b y successful v a r i e t i e s o f c e l l s a t t h e e x p e n s e o f u n s u c c e s s f u l v a r i e t i e s . B u r n e t limits the i d e a t o a s p e c i a l class o f c e l l s w i t h i n t h e i m m u n e s y s t e m , a n d ' s u c c e s s ' m e a n s success in n e u t r a l i z i n g i n v a d i n g antigens, but Steele w o u l d generalize it to other cells.

From Temin

he gets

the idea of R N A viruses serving as

i n t e r c e l l u l a r m e s s e n g e r s , t r a n s c r i b i n g g e n e s i n o n e c e l l , c a r r y i n g the i n f o r m a tion to a n o t h e r cell a n d reverse-transcribing it b a c k into D N A in the second cell using reverse transcriptase. S t e e l e uses t h e T e m i n t h e o r y , b u t w i t h a n i m p o r t a n t a d d i t i o n a l e m p h a s i s o n germ-line c e l l s a s r e c i p i e n t s o f r e v e r s e - t r a n s c r i b e d g e n e t i c i n f o r m a t i o n . H e w i s e l y l i m i t s m o s t o f his d i s c u s s i o n t o t h e i m m u n e s y s t e m , a l t h o u g h his a m b i t i o n s for his t h e o r y a r e l a r g e r . H e c i t e s f o u r s t u d i e s o n ' i d i o t y p y ' i n the rabbit.

If injected

with

a foreign substance,

different

individual

rabbits

c o m b a t it by m a k i n g different antibodies. E v e n if m e m b e r s of a genetically identical clone are subjected to the same antigen, each individual responds w i t h its o w n u n i q u e ' i d i o t y p e ' . N o w , i f t h e r a b b i t s r e a l l y a r e g e n e t i c a l l y identical, the difference in their idiotypes must be due to environmental or c h a n c e differences, a n d should not, a c c o r d i n g to o r t h o d o x y , be inherited. Of the four studies cited, o n e g a v e a surprising result. T h e i d i o t y p e of a rabbit t u r n e d o u t t o b e i n h e r i t e d b y its c h i l d r e n , a l t h o u g h n o t s h a r e d b y its c l o n e m a t e s . S t e e l e stresses t h e f a c t t h a t i n this s t u d y t h e p a r e n t r a b b i t s w e r e e x p o s e d t o t h e a n t i g e n before m a t i n g t o p r o d u c e t h e o f f s p r i n g . I n t h e o t h e r t h r e e s t u d i e s t h e p a r e n t s w e r e i n j e c t e d w i t h a n t i g e n after m a t i n g , a n d the offspring did not inherit their idiotypes. If i d i o t y p e w e r e inherited as a part of a n i n v i o l a t e g e r m - p l a s m , i t s h o u l d n o t h a v e m a d e a n y d i f f e r e n c e w h e t h e r the r a b b i t s m a t e d b e f o r e o r after i n j e c t i o n . Steele's interpretation begins w i t h the B u r n e t theory. S o m a t i c mutation generates

genetic

diversity

the

population

of i m m u n e

cells.

Clonal

s e l e c t i o n f a v o u r s t h o s e g e n e t i c v a r i e t i e s o f c e l l t h a t s a t i s f a c t o r i l y d e s t r o y the antigen, and they b e c o m e v e r y numerous. T h e r e is m o r e than one solution to a n y a n t i g e n i c p r o b l e m , a n d t h e e n d result o f t h e s e l e c t i o n p r o c e s s i s different i n e v e r y r a b b i t . N o w T e m i n ' s p r o v i r u s e s s t e p in. T h e y t r a n s c r i b e a r a n d o m s a m p l e o f t h e g e n e s i n t h e i m m u n e c e l l s . B e c a u s e c e l l s c a r r y i n g successful a n t i b o d y g e n e s o u t n u m b e r t h e o t h e r s , t h e s e successful g e n e s a r e s t a t i s t i c a l l y m o s t l i k e l y t o b e t r a n s c r i b e d . T h e p r o v i r u s e s c a r t t h e s e g e n e s off t o t h e g e r m cells,

burrow

into

the

germ-line

chromosomes

and

leave

them

there,

p r e s u m a b l y s n i p p i n g o u t t h e i n c u m b e n t o c c u p a n t s o f the l o c u s a s t h e y d o so.

Selfish D N A , J u m p i n g G e n e s , and a L a m a r c k i a n S c a r e

167

T h e next generation of rabbits is thereby a b l e to benefit directly from the i m m u n o l o g i c a l e x p e r i e n c e o f its p a r e n t s , w i t h o u t h a v i n g t o e x p e r i e n c e t h e relevant antigens themselves, a n d w i t h o u t the painfully slow a n d wasteful intervention of selective organism death. T h e r e a l l y i m p r e s s i v e e v i d e n c e o n l y b e c a m e a v a i l a b l e after S t e e l e ' s t h e o r y was cut and dried and published, a striking and rather surprising instance of science p r o c e e d i n g in the w a y philosophers think it p r o c e e d s . G o r c z y n s k i a n d Steele

(1980)

investigated

the

inheritance,

via

the

father,

of i m m u n e

tolerance in mice.

U s i n g an e x t r e m e l y h i g h - d o s a g e version of the classic

M e d a w a r method,

they e x p o s e d b a b y m i c e t o cells from a n o t h e r strain,

thereby r e n d e r i n g t h e m tolerant as adults to s u b s e q u e n t grafts from the s a m e d o n o r strain. T h e y then bred from these tolerant m a l e s , a n d c o n c l u d e d that their tolerance w a s inherited b y a b o u t h a l f their c h i l d r e n , w h o w e r e n o t e x p o s e d a s i n f a n t s t o t h e f o r e i g n a n t i g e n s . F u r t h e r m o r e , t h e effect s e e m e d t o carry over to the g r a n d c h i l d g e n e r a t i o n . Subject

inheritance

confirmation,

acquired

have

here

characteristics.

prima-facie

Gorczynski

and

case

for

Steele's

the brief

discussion o f their e x p e r i m e n t , a n d o f e x t e n d e d e x p e r i m e n t s r e p o r t e d m o r e recently ( G o r c z y n s k i & Steele 1 9 8 1 ) , resembles Steele's interpretation of the rabbit w o r k , p a r a p h r a s e d a b o v e . T h e m a i n differences b e t w e e n the t w o cases are firstly

that

the

rabbits

could

have

inherited

something

maternal

cytoplasm w h i l e the m i c e c o u l d not; a n d s e c o n d l y that the rabbits w e r e alleged to h a v e inherited an acquired i m m u n i t y , w h i l e the m i c e are supposed to have inherited

an acquired

tolerance.

T h e s e differences are p r o b a b l y

i m p o r t a n t ( R i d l e y 1 9 8 0 b ; B r e n t e t al. 1 9 8 1 ) , b u t I s h a l l n o t m a k e m u c h o f them,

since

themselves.

not

attempting

evaluate

the

experimental

results

I shall c o n c e n t r a t e on the question of w h e t h e r , in a n y case,

Steele is really offering 'a L a m a r c k i a n c h a l l e n g e to D a r w i n i s m ' . There

are

some

historical

points

get

out

of the

way

first.

The

i n h e r i t a n c e o f a c q u i r e d c h a r a c t e r i s t i c s i s n o t t h e a s p e c t o f his t h e o r y t h a t L a m a r c k h i m s e l f e m p h a s i z e d a n d , contra S t e e l e ( 1 9 7 9 , p . 6 ) , i t i s n o t t r u e t h a t the i d e a o r i g i n a t e d w i t h h i m : h e s i m p l y t o o k o v e r t h e c o n v e n t i o n a l w i s d o m o f his t i m e a n d g r a f t e d t o i t o t h e r p r i n c i p l e s l i k e ' s t r i v i n g ' a n d ' u s e a n d disuse'. Steele's viruses seem m o r e reminiscent of D a r w i n ' s o w n p a n g e n e t i c 'gemmules' than of a n y t h i n g postulated by L a m a r c k . B u t I mention history just to get it out of the w a y . We g i v e the n a m e D a r w i n i s m to the t h e o r y that undirected variation in an insulated germ-line is acted upon by selection of its p h e n o t y p i c c o n s e q u e n c e s . W e g i v e t h e n a m e L a m a r c k i s m t o t h e t h e o r y that the g e r m - l i n e is not insulated, improvements

may

directly

mould

and it.

that this

environmentally sense,

imprinted

Steele's

theory

Lamarckian and anti-Darwinian? By inheriting their parents' a c q u i r e d idiotypes, rabbits w o u l d u n d o u b t e d l y benefit. T h e y w o u l d b e g i n life w i t h a h e a d start i n t h e i m m u n o l o g i c a l b a t t l e

168

Selfish D N A , J u m p i n g G e n e s , and a L a m a r c k i a n Scare

against p l a g u e s that their parents met, a n d that they themselves are likely to meet. T h i s is a directed, a d a p t i v e c h a n g e , then. But is it really imprinted by the e n v i r o n m e n t ? If a n t i b o d y formation w o r k e d a c c o r d i n g to some kind of 'instructive' theory, the a n s w e r w o u l d be yes. T h e e n v i r o n m e n t , in the shape of

antigenic

protein

molecules,

would

than

directly

mould

antibody

m o l e c u l e s i n p a r e n t r a b b i t s . I f the o f f s p r i n g o f those r a b b i t s t u r n e d o u t t o i n h e r i t a p r e d i l e c t i o n t o m a k e t h e s a m e a n t i b o d i e s , w e w o u l d h a v e fullb l o o d e d L a m a r c k i s m . But the conformations o f the a n t i b o d y proteins w o u l d , o n this t h e o r y , s o m e h o w h a v e t o b e r e v e r s e - t r a n s l a t e d i n t o n u c l e o t i d e c o d e . Steele

(p.

36)

adamant

that

there is no suggestion of such

reverse

t r a n s l a t i o n , o n l y r e v e r s e transcription f r o m R N A t o D N A . H e i s not p r o p o s i n g any violation of C r i c k ' s central d o g m a , although of course others are at l i b e r t y t o d o s o ( I s h a l l r e t u r n t o this p o i n t i n a m o r e g e n e r a l c o n t e x t l a t e r ) . T h e v e r y e s s e n c e o f S t e e l e ' s h y p o t h e s i s i s t h a t the a d a p t i v e i m p r o v e m e n t comes a b o u t through selection of initially r a n d o m variation. It is about as D a r w i n i a n a theory as it is possible to be, p r o v i d e d we think of the replicator and not the organism as the unit of selection. N o r is it just v a g u e l y analogous t o D a r w i n i s m , i n t h e w a y of, s a y , t h e ' m e m e ' t h e o r y , o r P r i n g l e ' s ( 1 9 5 1 ) theory

that

frequencies

learning in

results

from

selection

among

neuronal

coupled

population

pool

of oscillation

oscillators.

Steele's

r e p l i c a t o r s a r e D N A m o l e c u l e s i n c e l l n u c l e i . T h e y a r e n o t j u s t analogous t o the replicators o f D a r w i n i s m . scheme

for

modification

natural to

selection

plug

T h e y are

the v e r y s a m e replicators. T h e

which

outlined

into

the

Steele

straight

Chapter

theory.

needs no

Steele's

kind

L a m a r c k i s m o n l y s e e m s l i k e t h e i m p r i n t i n g o f e n v i r o n m e n t a l f e a t u r e s o n the g e r m - l i n e if we think at the level of the i n d i v i d u a l o r g a n i s m . It is true that he i s c l a i m i n g t h a t c h a r a c t e r i s t i c s a c q u i r e d b y t h e organism a r e i n h e r i t e d . B u t i f we look at the l o w e r level of genetic replicators, it is clear that the a d a p t a t i o n c o m e s a b o u t t h r o u g h s e l e c t i o n n o t ' i n s t r u c t i o n ' (see b e l o w ) . I t j u s t h a p p e n s t o b e s e l e c t i o n w i t h i n t h e o r g a n i s m . S t e e l e ( 1 9 7 9 , p . 43) w o u l d not d i s a g r e e : ' . . . it

depends

very

much

essential

Darwinian

principles

of natural

selection'. Despite Steele's a v o w e d indebtedness to A r t h u r K o e s t l e r , there is naught h e r e for t h e c o m f o r t o f t h o s e , u s u a l l y n o n - b i o l o g i s t s , w h o s e a n t i p a t h y t o D a r w i n i s m i s f u n d a m e n t a l l y p r o v o k e d b y t h e b o g y o f ' b l i n d c h a n c e ' . O r , for that m a t t e r , the t w i n b o g y of a ruthlessly indifferent g r i m reaper, m o c k i n g us as the sole First C a u s e of o u r e x a l t e d persons, m o d i f y i n g 'all things by blindly s t a r v i n g a n d m u r d e r i n g e v e r y t h i n g t h a t i s n o t l u c k y e n o u g h t o s u r v i v e i n the u n i v e r s a l s t r u g g l e for h o g w a s h ' should

hear

triumphant

(Shaw 1921).

chuckles

from

the

If Steele proves right, we shade

of Bernard

Shaw!

S h a w ' s l i v e s p i r i t r e b e l l e d p a s s i o n a t e l y a g a i n s t the D a r w i n i a n ' c h a p t e r o f a c c i d e n t s ' . ' . . . i t s e e m s s i m p l e , b e c a u s e y o u d o n o t a t first r e a l i z e a l l t h a t i t i n v o l v e s . B u t w h e n its w h o l e s i g n i f i c a n c e d a w n s o n y o u , y o u r h e a r t sinks i n t o

Selfish D N A , J u m p i n g G e n e s , and a L a m a r c k i a n S c a r e

169

a h e a p o f s a n d w i t h i n y o u . T h e r e i s a h i d e o u s f a t a l i s m a b o u t it, a g h a s t l y a n d damnable reduction of beauty and intelligence, of strength and purpose, of honor and aspiration .. .'

I f w e must p l a c e e m o t i o n

before truth,

have

always found natural selection to h a v e an inspiring, if grim a n d austere, p o e t r y o f its o w n â&#x20AC;&#x201D; a ' g r a n d e u r i n this v i e w o f life' ( D a r w i n 1 8 5 9 ) . A l l I a m saying here is that if y o u are squeamish a b o u t 'blind c h a n c e ' , do not look to S t e e l e ' s t h e o r y for a n e s c a p e . B u t p e r h a p s i t i s n o t t o o m u c h t o h o p e t h a t a proper understanding of Steele's theory m a y help to show that 'blind c h a n c e ' is not

the

adequate epitome of Darwinism

that

Shaw,

Cannon

(1959),

K o e s t l e r ( 1 9 6 7 ) a n d o t h e r s t h i n k i t is. Steele's

theory,

then, is a version of D a r w i n i s m . T h e cells w h i c h are

s e l e c t e d , a c c o r d i n g t o t h e B u r n e t t h e o r y , a r e v e h i c l e s for a c t i v e r e p l i c a t o r s , n a m e l y the s o m a t i c a l l y m u t a t e d g e n e s w i t h i n t h e m . T h e y a r e a c t i v e , b u t a r e t h e y germ-line r e p l i c a t o r s ? T h e e s s e n c e o f w h a t I a m s a y i n g i s t h a t t h e a n s w e r is an e m p h a t i c yes, if Steele's addition to the B u r n e t theory is true. T h e y do not b e l o n g t o w h a t w e h a v e c o n v e n t i o n a l l y t h o u g h t o f a s t h e g e r m - l i n e , b u t it is a logical i m p l i c a t i o n of the theory that we h a v e simply b e e n m i s t a k e n as t o w h a t the g e r m - l i n e t r u l y is. A n y g e n e i n a ' s o m a t i c ' c e l l w h i c h i s a c a n d i d a t e for p r o v i r a l c o n v e y a n c e i n t o a g e r m c e l l is, by definition, a g e r m - l i n e replicator. being

S t e e l e ' s b o o k m i g h t be r e t i t l e d

uncomfortable

for

neo-Weismannists,

The Extended Germ-line! F a r f r o m it

turns

out

deeply

c o n g e n i a l to us. Perhaps, then, it is not really all that ironic that, a p p a r e n t l y u n k n o w n to S t e e l e , s o m e t h i n g b e a r i n g m o r e t h a n a p a s s i n g r e s e m b l a n c e t o his t h e o r y w a s a d o p t e d b y , o f all p e o p l e , W e i s m a n n himself, i n 1 8 9 4 . T h e f o l l o w i n g a c c o u n t i s t a k e n f r o m R i d l e y (in p r e s s ; M a y n a r d S m i t h , 1 9 8 0 , a l s o n o t e d t h e p r e c e d e n t ) . W e i s m a n n d e v e l o p e d a n idea from R o u x , w h i c h h e c a l l e d 'intras e l e c t i o n ' . I q u o t e from R i d l e y : ' R o u x h a d a r g u e d t h a t t h e r e i s a s t r u g g l e for food b e t w e e n t h e p a r t s o f a n o r g a n i s m j u s t l i k e t h e s t r u g g l e for e x i s t e n c e between organisms . . .

R o u x ' s theory w a s that the struggle o f the parts,

t o g e t h e r w i t h t h e i n h e r i t a n c e o f a c q u i r e d c h a r a c t e r s , w a s sufficient t o e x p l a i n a d a p t a t i o n . ' S u b s t i t u t e ' c l o n e s ' for ' p a r t s ' , a n d y o u h a v e S t e e l e ' s t h e o r y . B u t , a s m i g h t b e e x p e c t e d , W e i s m a n n did not g o all the w a y w i t h R o u x i n p o s t u l a t i n g the l i t e r a l i n h e r i t a n c e o f a c q u i r e d c h a r a c t e r i s t i c s . I n s t e a d , i n his theory of ' g e r m i n a l selection', he i n v o k e d the p s e u d o - L a m a r c k i a n p r i n c i p l e w h i c h later b e c a m e k n o w n as the ' B a l d w i n Effect' ( W e i s m a n n w a s not the o n l y o n e t o d i s c o v e r t h e i d e a b e f o r e B a l d w i n ) . W e i s m a n n ' s use o f t h e t h e o r y o f i n t r a - s e l e c t i o n i n e x p l a i n i n g c o a d a p t a t i o n w i l l b e d e a l t w i t h b e l o w , for i t closely parallels one of Steele's o w n p r e o c c u p a t i o n s . S t e e l e d o e s n o t v e n t u r e far f r o m his o w n field o f i m m u n o l o g y , b u t h e w o u l d like a v e r s i o n o f his t h e o r y t o a p p l y e l s e w h e r e , a n d p a r t i c u l a r l y t o t h e nervous

system

and

the

adaptive

improvement

mechanism

known

learning. ' I f [the hypothesis] is to h a v e a n y g e n e r a l a p p l i c a b i l i t y to the

Selfish D N A , J u m p i n g G e n e s , and a L a m a r c k i a n Scare

170

e v o l u t i o n a r y a d a p t a t i o n p r o c e s s , it must account for t h e a d a p t i v e p o t e n t i a l of the n e u r o n a l n e t w o r k s of the brain a n d central nervous system' (Steele 1979, p . 4 9 , his r a t h e r s u r p r i s i n g e m p h a s i s ) . H e s e e m s a little v a g u e a s t o e x a c t l y w h a t m i g h t be selected w i t h i n the brain, a n d , in case he c a n do something w i t h it, I offer h i m a free gift o f m y o w n t h e o r y o f ' s e l e c t i v e n e u r o n e d e a t h a s a possible m e m o r y m e c h a n i s m ' ( D a w k i n s 1971). But is the t h e o r y of c l o n a l selection really likely to a p p l y outside the domain

the

immune

system?

limited

the

very

special

c i r c u m s t a n c e s o f t h e i m m u n e s y s t e m , o r m i g h t i t b e l i n k e d u p w i t h the o l d L a m a r c k i a n p r i n c i p l e o f use a n d d i s u s e ? C o u l d c l o n a l s e l e c t i o n b e e m b r a c e d b y the b l a c k s m i t h ' s a r m s ? C o u l d the a d a p t i v e c h a n g e s b r o u g h t a b o u t b y m u s c u l a r exercise be i n h e r i t e d ? I d o u b t it very m u c h : the conditions are not r i g h t for n a t u r a l s e l e c t i o n t o w o r k w i t h i n the b l a c k s m i t h ' s a r m s i n f a v o u r of, say,

c e l l s t h a t flourish i n a n a e r o b i c e n v i r o n m e n t o v e r those p r e f e r r i n g

a n a e r o b i c b i o c h e m i s t r y , t h e successful g e n e s b e i n g r e v e r s e - t r a n s c r i b e d i n t o j u s t t h e r i g h t c h r o m o s o m a l l o c u s i n the g e r m - l i n e . B u t e v e n i f this k i n d o f t h i n g w e r e c o n c e i v a b l e for s o m e e x a m p l e o u t s i d e t h e i m m u n e s y s t e m , t h e r e i s a major theoretical difficulty. T h e p r o b l e m i s this. T h e q u a l i t i e s t h a t m a k e for s u c c e s s i n c l o n a l s e l e c t i o n w o u l d n e c e s s a r i l y b e t h o s e t h a t g i v e cells a n a d v a n t a g e o v e r r i v a l c e l l s i n the s a m e b o d y . T h e s e q u a l i t i e s n e e d h a v e n o c o n n e c t i o n w i t h w h a t i s g o o d for the b o d y as a w h o l e , a n d o u r discussion of o u t l a w s suggests that they might w e l l a c t i v e l y c o n f l i c t w i t h w h a t i s g o o d for t h e b o d y a s a w h o l e . I n d e e d , t o m e a s l i g h t l y u n s a t i s f a c t o r y a s p e c t o f t h e B u r n e t t h e o r y i t s e l f i s t h a t the s e l e c t i o n p r o c e s s at its h e a r t is c o n t r i v e d ad hoc. It is a s s u m e d t h a t those cells w h o s e a n t i b o d i e s n e u t r a l i z e i n v a d i n g antigens will p r o p a g a t e at the expense o f o t h e r c e l l s . B u t this p r o p a g a t i o n i s n o t d u e t o a n y i n t r i n s i c c e l l u l a r a d v a n t a g e : o n t h e c o n t r a r y , c e l l s t h a t d i d n o t risk t h e i r l i v e s s m o t h e r i n g a n t i g e n s b u t selfishly left t h e task t o t h e i r c o l l e a g u e s s h o u l d , o n t h e f a c e o f it, h a v e a built-in a d v a n t a g e . T h e theory has to introduce an arbitrary and u n p a r s i m o n i o u s s e l e c t i o n r u l e , i m p o s e d , a s i t w e r e , f r o m a b o v e , s o t h a t those cells w h i c h benefit the b o d y as a w h o l e b e c o m e m o r e n u m e r o u s . It is as t h o u g h a h u m a n d o g - b r e e d e r d e l i b e r a t e l y s e l e c t e d for a l t r u i s t i c h e r o i s m i n t h e f a c e o f d a n g e r . H e c o u l d p r o b a b l y a c h i e v e it, b u t natural s e l e c t i o n c o u l d not.

Unadulterated

clonal

selection

should

favour

selfish

cells

whose

b e h a v i o u r c o n f l i c t s w i t h t h e b e s t interests o f t h e b o d y a s a w h o l e . I n t h e t e r m s o f C h a p t e r 6 , w h a t I a m s a y i n g i s t h a t v e h i c l e s e l e c t i o n a t the cellular level is likely, u n d e r the B u r n e t theory, to c o m e into conflict with vehicle selection at the organism level. T h i s , of course, does not worry me, s i n c e I c a r r y n o b r i e f for t h e o r g a n i s m a s p r e - e m i n e n t v e h i c l e ; I s i m p l y a d d o n e m o r e e n t r y t o t h e list o f ' o u t l a w s I h a v e k n o w n ' ; o n e m o r e i n g e n i o u s b y w a y o f r e p l i c a t o r p r o p a g a t i o n , a l o n g w i t h j u m p i n g g e n e s a n d selfish D N A .

Selfish D N A , J u m p i n g G e n e s , a n d a L a m a r c k i a n S c a r e

171

B u t i t s h o u l d w o r r y a n y b o d y , s u c h a s S t e e l e , w h o sees c l o n a l s e l e c t i o n a s a s u p p l e m e n t a r y m e a n s b y w h i c h bodily a d a p t a t i o n s c o m e a b o u t . T h e p r o b l e m goes d e e p e r than that. It is not just that c l o n a l l y selected g e n e s w o u l d t e n d t o b e o u t l a w s a s far a s t h e rest o f t h e b o d y i s c o n c e r n e d . Steele

looks

clonal

selection

speed

evolution.

Conventional

D a r w i n i s m p r o c e e d s b y d i f f e r e n t i a l i n d i v i d u a l s u c c e s s , a n d its s p e e d , o t h e r things b e i n g e q u a l , will be limited by i n d i v i d u a l g e n e r a t i o n time. C l o n a l selection w o u l d be limited by cellular g e n e r a t i o n time, w h i c h is p e r h a p s t w o orders of m a g n i t u d e shorter. T h i s is w h y it m i g h t be t h o u g h t to speed up e v o l u t i o n b u t , t o a n t i c i p a t e t h e a r g u m e n t o f m y f i n a l c h a p t e r , i t raises a d e e p difficulty. T h e success of a c o m p l e x , m u l t i c e l l u l a r o r g a n , like an e y e , c a n n o t be j u d g e d in a d v a n c e of the eye's starting to w o r k . C e l l u l a r selection c o u l d n o t i m p r o v e the d e s i g n o f a n e y e , b e c a u s e t h e s e l e c t i v e e v e n t s a l l t a k e p l a c e i n the p r e f u n c t i o n a l e y e o f a n e m b r y o . T h e e m b r y o ' s e y e i s c l o s e d , a n d n e v e r sees a n i m a g e u n t i l after c e l l u l a r s e l e c t i o n , i f i t e x i s t e d , w o u l d b e c o m p l e t e . T h e general point is that cellular selection c a n n o t a c h i e v e the s p e e d i n g up of e v o l u t i o n a t t r i b u t e d t o it, i f t h e a d a p t a t i o n o f i n t e r e s t h a s t o d e v e l o p o n t h e slow scale of m u l t i c e l l u l a r c o o p e r a t i o n . Steele has a point

to m a k e about coadaptation.

As R i d l e y

(in press)

c o m p r e h e n s i v e l y d o c u m e n t s , m u l t i d i m e n s i o n a l c o a d a p t a t i o n w a s o n e o f the b u g b e a r s of the early D a r w i n i a n s . F o r instance, to take the e y e a g a i n , J. J. M u r p h y said ' I t i s p r o b a b l y n o e x a g g e r a t i o n t h a t , i n o r d e r t o i m p r o v e s u c h a n o r g a n a s t h e e y e a t a l l , i t m u s t b e i m p r o v e d i n t e n different w a y s a t o n c e ' (1866, quoted by R i d l e y ) . e v o l u t i o n of w h a l e s ,

I t m a y b e r e m e m b e r e d that, s p e a k i n g o f the

u s e d a s i m i l a r p r e m i s e for a different p u r p o s e in

C h a p t e r 6 . F u n d a m e n t a l i s t o r a t o r s still find the e y e o n e o f t h e i r m o s t t e l l i n g s t a n d b y s . I n c i d e n t a l l y , The Sunday Times ( 1 3 J u l y 1980) a n d The Guardian (21 N o v e m b e r 1978) both raise the d e b a t i n g point of the e y e as t h o u g h it w e r e a n e w o n e , t h e l a t t e r p a p e r r e a s s u r i n g u s t h a t a n e m i n e n t p h i l o s o p h e r (!) w a s r u m o u r e d t o b e g i v i n g t h e p r o b l e m his best a t t e n t i o n . S t e e l e s e e m s t o h a v e been

initially

coadaptation,

attracted and

Lamarckism

believes

that

his

because

clonal

his

selection

unease

theory

about

could

principle alleviate the difficulty, if difficulty there be. L e t u s m a k e use o f t h a t o t h e r c h e s t n u t o f t h e s c h o o l r o o m , t h e giraffe's n e c k , d i s c u s s i n g i t i n c o n v e n t i o n a l D a r w i n i a n t e r m s first. A m u t a t i o n t o elongate the ancestral n e c k m i g h t w o r k on, say, the v e r t e b r a e , but it seems to a

naive

observer

too

much

hope

that

the

same

mutation

will

simultaneously e l o n g a t e the arteries, veins, nerves, etc. A c t u a l l y , w h e t h e r it i s too m u c h t o h o p e d e p e n d s o n d e t a i l s o f e m b r y o l o g y w h i c h w e s h o u l d l e a r n t o b e m o r e a w a r e of: a m u t a t i o n t h a t a c t s s u f f i c i e n t l y e a r l y i n d e v e l o p m e n t c o u l d e a s i l y h a v e a l l those p a r a l l e l effects s i m u l t a n e o u s l y . H o w e v e r , let u s p l a y a l o n g w i t h the a r g u m e n t . T h e n e x t s t e p i s t o s a y t h a t i t i s d i f f i c u l t t o

Selfish D N A , J u m p i n g G e n e s , and a L a m a r c k i a n Scare

172

i m a g i n e a m u t a n t giraffe w i t h e l o n g a t e d v e r t e b r a e b e i n g a b l e t o e x p l o i t its t r e e t o p b r o w s i n g a d v a n t a g e , b e c a u s e its n e r v e s , b l o o d vessels, e t c . a r e t o o s h o r t for its n e c k . C o n v e n t i o n a l D a r w i n i a n s e l e c t i o n , n a i v e l y u n d e r s t o o d , h a s to w a i t

for a n

individual

that

is fortunate

enough

t o c o m b i n e all

the

necessary c o a d a p t e d mutations simultaneously. T h i s is w h e r e clonal selection c o u l d c o m e t o t h e r e s c u e . O n e m a j o r m u t a t i o n , s a y t h e e l o n g a t i o n o f the v e r t e b r a e , sets u p c o n d i t i o n s i n t h e n e c k w h i c h s e l e c t for c l o n e s o f cells t h a t c a n flourish in that e n v i r o n m e n t . M a y b e the e l o n g a t e d v e r t e b r a e p r o v i d e an o v e r s t r e t c h e d , h i g h l y strung, tense e n v i r o n m e n t in the n e c k , w h e r e only e l o n g a t e d c e l l s f l o u r i s h . I f t h e r e i s g e n e t i c v a r i a t i o n a m o n g the c e l l s , g e n e s 'for' e l o n g a t e d cells s u r v i v e a n d are passed on to the giraffe's c h i l d r e n . I h a v e put the p o i n t facetiously, but a m o r e sophisticated version of it could, I suppose, follow from the clonal selection theory. I s a i d I w o u l d r e t u r n t o W e i s m a n n a t this p o i n t , for h e t o o s a w t h e u t i l i t y of w i t h i n - b o d y

selection

solution

the

coadaptation

problem.

W e i s m a n n t h o u g h t that ' i n t r a - s e l e c t i o n ' â&#x20AC;&#x201D; t h e selective struggle a m o n g parts w i t h i n t h e b o d y â&#x20AC;&#x201D; ' w o u l d e n s u r e t h a t all t h e p a r t s i n s i d e t h e o r g a n i s m w e r e o f t h e best m u t u a l p r o p o r t i o n s ' ( R i d l e y i n p r e s s ) . ' I f I a m n o t m i s t a k e n , the phenomenon

which

Darwin

c a l l e d correlation,

and justly

regarded

as an

i m p o r t a n t f a c t o r i n e v o l u t i o n , i s for t h e m o s t p a r t a n effect o f i n t r a - s e l e c t i o n ' ( W e i s m a n n , q u o t e d in R i d l e y ) . As already stated, W e i s m a n n , unlike R o u x , did not go on to i n v o k e the direct inheritance of intra-selected varieties. Rather,

' . . . in e a c h separate i n d i v i d u a l the necessary a d a p t a t i o n will be

t e m p o r a r i l y a c c o m p l i s h e d b y intra-selection . . . T i m e w o u l d thus b e g a i n e d till, i n t h e c o u r s e o f g e n e r a t i o n s , b y c o n s t a n t s e l e c t i o n o f those g e r m s the p r i m a r y c o n s t i t u e n t s o f w h i c h a r e best s u i t e d t o o n e a n o t h e r , t h e g r e a t e s t possible d e g r e e of h a r m o n y m a y be reached.' I think I find W e i s m a n n ' s 'Baldwin

Effect'

version

the

theory

plausible

than

Steele's

L a m a r c k i a n version, a n d just as satisfying an e x p l a n a t i o n of coadaptation. I u s e d t h e w o r d ' s c a r e ' i n t h e h e a d i n g o f this s e c t i o n , a n d w e n t s o far a s t o say that a true r e v i v a l of L a m a r c k i s m w o u l d devastate my w o r l d - v i e w . Y e t t h e r e a d e r m a y n o w feel t h a t t h e s t a t e m e n t w a s a h o l l o w o n e , like t h a t o f a m a n w h o d r a m a t i c a l l y t h r e a t e n s t o e a t his h a t , w h i l e k n o w i n g full w e l l that his h a t i s m a d e o f p l e a s a n t l y f l a v o u r e d r i c e p a p e r . A L a m a r c k i a n z e a l o t m a y c o m p l a i n t h a t t h e last r e s o r t o f a D a r w i n i a n ,

h a v i n g failed

to discredit

a w k w a r d e x p e r i m e n t a l r e s u l t s , i s t o c l a i m t h e m for his o w n ; t o m a k e his o w n t h e o r y so r e s i l i e n t t h a t t h e r e is no e x p e r i m e n t a l result t h a t c o u l d falsify it. I a m s e n s i t i v e t o this c r i t i c i s m , a n d m u s t r e p l y t o it. I m u s t s h o w t h a t t h e h a t that I t h r e a t e n e d to eat really is t o u g h a n d distasteful. S o , if Steele's kind of L a m a r c k i s m is really D a r w i n i s m in disguise, w h a t kind of L a m a r c k i s m w o u l d not be? T h e k e y issue i s t h e o r i g i n o f a d a p t e d n e s s . G o u l d ( 1 9 7 9 ) m a k e s a r e l a t e d

Selfish D N A , J u m p i n g G e n e s , a n d a L a m a r c k i a n S c a r e

173

p o i n t w h e n h e s a y s t h a t t h e i n h e r i t a n c e o f a c q u i r e d c h a r a c t e r s , per se, i s n o t L a m a r c k i a n : ' L a m a r c k i s m is a t h e o r y of directed v a r i a t i o n ' ( m y e m p h a s i s ) . I d i s t i n g u i s h t w o classes o f t h e o r y o f t h e o r i g i n o f a d a p t e d n e s s . F o r f e a r o f getting c a u g h t up in historical details of exactly w h a t L a m a r c k and D a r w i n said, I shall not a n y m o r e call them L a m a r c k i s m a n d D a r w i n i s m . Instead, I shall b o r r o w from i m m u n o l o g y a n d call t h e m the instruction t h e o r y a n d the selection

theory.

Young

(1957),

Lorenz

(1966),

and

others

have

emphasized, we recognize adaptedness as an informational match between organism

and

environment

environment. can

regarded

animal as

that

embodying

well

adapted

information

its

about

its

e n v i r o n m e n t , in the w a y that a k e y e m b o d i e s information a b o u t the lock that it is built to u n d o . A c a m o u f l a g e d a n i m a l has b e e n said to c a r r y a p i c t u r e of its e n v i r o n m e n t o n its b a c k . L o r e n z d i s t i n g u i s h e d t w o k i n d s o f t h e o r y for t h e o r i g i n o f this k i n d o f f i t b e t w e e n o r g a n i s m a n d e n v i r o n m e n t , b u t b o t h his t h e o r i e s ( n a t u r a l s e l e c t i o n and reinforcement

learning)

are subdivisions of w h a t

selection theory. An initial pool of variation taneous

behaviour)

is worked

upon

calling the

(genetic mutation or spon-

by some

kind

of selection

process

(natural selection or r e w a r d / p u n i s h m e n t ) , w i t h the end result that o n l y the variants f i t t i n g the e n v i r o n m e n t a l lock r e m a i n . T h u s a d a p t e d n e s s i m p r o v e s by selection. T h e instruction theory is q u i t e different. W h e r e a s the selective k e y - m a k e r b e g i n s w i t h a l a r g e r a n d o m p o o l o f k e y s , tries t h e m a l l i n t h e l o c k , and discards those that d o n ' t fit, the instructive k e y - m a k e r s i m p l y takes a wax

impression

o f the

lock,

instructively camouflaged

and

makes

good

key directly.

The

a n i m a l r e s e m b l e s its e n v i r o n m e n t b e c a u s e t h e

e n v i r o n m e n t d i r e c t l y i m p r i n t s its a p p e a r a n c e o n t h e a n i m a l , a s e l e p h a n t s m e r g e i n t o t h e b a c k g r o u n d b e c a u s e t h e y a r e c o v e r e d b y its d u s t . I t h a s b e e n alleged that French mouths eventually b e c o m e p e r m a n e n t l y deformed into a s h a p e s u i t a b l e for p r o n o u n c i n g F r e n c h v o w e l s . I f so, this w o u l d b e a n i n s t r u c tive a d a p t a t i o n . S o , perhaps, is b a c k g r o u n d r e s e m b l a n c e in c h a m e l e o n s , t h o u g h o f c o u r s e t h e capacity t o c h a n g e c o l o u r a d a p t i v e l y i s p r e s u m a b l y a selective adaptation. T h e a d a p t i v e changes in p h y s i o l o g y to w h i c h we g i v e n a m e s like a c c l i m a t i z a t i o n a n d t r a i n i n g , t h e effects o f e x e r c i s e , u s e a n d d i s u s e , are p r o b a b l y all instructive. C o m p l e x a n d e l a b o r a t e a d a p t i v e f i t s c a n b e a c h i e v e d b y i n s t r u c t i o n , a s i n the l e a r n i n g o f a p a r t i c u l a r h u m a n l a n g u a g e . As already explained, it is clear that in Steele's theory the adaptedness c o m e s not from instruction b u t from selection, a n d g e n e t i c r e p l i c a t o r selection at that.

My world-view will

genetic

inheritance,

be overturned if somebody demonstrates

not just

of an

'acquired

characteristic'

but

the

of an

instructively acquired adaptation. T h e reason is that the inheritance of an instructively embryology.

acquired

adaptation would

violate

the

'central

dogma'

174

Selfish D N A , J u m p i n g G e n e s , and a L a m a r c k i a n Scare

The poverty of preformationism O d d l y , my b e l i e f in the i n v i o l a b i l i t y of the central d o g m a is not a d o g m a t i c o n e ! I t i s b a s e d o n r e a s o n . I m u s t b e c a u t i o u s h e r e , a n d d i s t i n g u i s h t w o forms o f c e n t r a l d o g m a , the central d o g m a o f m o l e c u l a r genetics and the central dogma

of embryology.

The

first

the

one

stated

Crick:

genetic

i n f o r m a t i o n m a y b e t r a n s l a t e d f r o m n u c l e i c a c i d t o p r o t e i n , b u t n o t the o t h e r w a y . S t e e l e ' s t h e o r y , a s h e h i m s e l f i s c a r e f u l t o p o i n t o u t , d o e s n o t v i o l a t e this d o g m a . H e m a k e s use o f r e v e r s e t r a n s c r i p t i o n f r o m R N A t o D N A , b u t n o t reverse translation from protein to R N A . I am not a m o l e c u l a r biologist, and so c a n n o t j u d g e the extent to w h i c h the theoretical b o a t w o u l d be rocked if such reverse

translation were

ever discovered.

does

not seem

to me

o b v i o u s l y i m p o s s i b l e i n p r i n c i p l e , b e c a u s e the t r a n s l a t i o n f r o m n u c l e i c a c i d to protein, or from protein to nucleic acid, is a simple dictionary look-up procedure, only slightly more c o m p l e x than the D N A / R N A transcription. In b o t h cases there is a o n e - t o - o n e m a p p i n g b e t w e e n the t w o codes. If a h u m a n , or a c o m p u t e r , e q u i p p e d w i t h the d i c t i o n a r y , c a n translate from protein to R N A , I d o n ' t see w h y n a t u r e s h o u l d n o t . T h e r e m a y b e a g o o d t h e o r e t i c a l r e a s o n , o r i t m a y just b e a n e m p i r i c a l l a w t h a t has n o t y e t b e e n v i o l a t e d . T h e r e i s n o n e e d for m e t o p u r s u e t h e m a t t e r b e c a u s e , i n a n y c a s e , a v e r y g o o d t h e o r e t i c a l c a s e c a n b e m a d e a g a i n s t v i o l a t i n g t h e o t h e r c e n t r a l d o g m a , the c e n t r a l d o g m a o f e m b r y o l o g y . T h i s i s t h e d o g m a t h a t the m a c r o s c o p i c form a n d b e h a v i o u r o f a n o r g a n i s m m a y b e , i n s o m e sense, c o d e d i n t h e g e n e s , b u t t h e c o d e i s i r r e v e r s i b l e . I f C r i c k ' s c e n t r a l d o g m a states t h a t p r o t e i n m a y not b e t r a n s l a t e d b a c k i n t o D N A , t h e c e n t r a l d o g m a o f e m b r y o l o g y states t h a t bodily form and b e h a v i o u r m a y not be translated back into protein. If y o u sleep in the sun w i t h y o u r h a n d o v e r y o u r chest, a w h i t e i m a g e of your hand will be imprinted on your otherwise tanned body. This image is a n a c q u i r e d c h a r a c t e r i s t i c . I n o r d e r for i t t o b e i n h e r i t e d , g e m m u l e s o r R N A viruses, or w h a t e v e r a g e n t of reverse translation is postulated, w o u l d have to scan

t h e macroscopic o u t l i n e o f t h e

hand

m o l e c u l a r structure of D N A necessary

image

and

translate it

into

the

to p r o g r a m the d e v e l o p m e n t of a

s i m i l a r h a n d i m a g e . I t i s s u g g e s t i o n s o f this k i n d t h a t c o n s t i t u t e a v i o l a t i o n o f the central d o g m a o f e m b r y o l o g y . The

central

common

sense.

dogma

of embryology

Rather,

does

logical

not

implication

inevitably of

from

rejecting

the

preformationist v i e w of d e v e l o p m e n t . I suggest, i n d e e d , that there is a close l i n k b e t w e e n t h e e p i g e n e t i c v i e w o f d e v e l o p m e n t a n d the D a r w i n i a n v i e w o f adaptation,

and

between

preformationism

and

the

Lamarckian

view

a d a p t a t i o n . Y o u m a y b e l i e v e i n i n h e r i t a n c e o f L a m a r c k i a n (i.e. ' i n s t r u c t i v e ' ) adaptations,

but only if y o u are prepared to e m b r a c e a preformationistic

v i e w o f e m b r y o l o g y . I f d e v e l o p m e n t were preformationistic, i f D N A really were a ' b l u e p r i n t for a b o d y ' , r e a l l y w e r e a c o d i f i e d h o m u n c u l u s , r e v e r s e developmentâ&#x20AC;&#x201D;looking-glass embryologyâ&#x20AC;&#x201D;would be conceivable.

Selfish D N A , J u m p i n g G e n e s , a n d a L a m a r c k i a n S c a r e

175

B u t the b l u e p r i n t m e t a p h o r o f t h e t e x t b o o k s i s d r e a d f u l l y m i s l e a d i n g , for i t i m p l i e s a o n e - t o - o n e m a p p i n g b e t w e e n bits o f b o d y a n d bits o f g e n o m e . B y inspecting a house, we m a y reconstruct a blueprint from w h i c h s o m e b o d y else c o u l d b u i l d a n i d e n t i c a l h o u s e , u s i n g t h e s a m e b u i l d i n g t e c h n i q u e a s w a s used for t h e o r i g i n a l h o u s e . T h e i n f o r m a t i o n a l a r r o w s f r o m b l u e p r i n t t o h o u s e a r e r e v e r s i b l e . T h e r e l a t i v e p o s i t i o n s o f t h e i n k lines i n t h e b l u e p r i n t a n d o f t h e b r i c k w a l l s i n the h o u s e a r e t r a n s f o r m a b l e , o n e i n t o t h e o t h e r , b y a few s i m p l e s c a l i n g r u l e s . T o g o f r o m b l u e p r i n t t o h o u s e , y o u m u l t i p l y a l l m e a s u r e m e n t s b y , say t w e n t y . T o g o from house t o b l u e p r i n t , y o u d i v i d e all measurements by t w e n t y . If the house s o m e h o w a c q u i r e s a n e w feature, say a w e s t w i n g , a s i m p l e , a u t o m a t i c p r o c e d u r e c o u l d b e w r i t t e n d o w n for a d d i n g a s c a l e d - d o w n m a p of the west w i n g to the b l u e p r i n t . If the g e n o m e w e r e a blueprint with a one-to-one m a p p i n g from g e n o t y p e to p h e n o t y p e , it w o u l d n o t b e i n c o n c e i v a b l e t h a t the w h i t e i m p r i n t o f a h a n d o n a n o t h e r w i s e t a n n e d chest c o u l d b e m a p p e d o n t o a sort o f m i n i a t u r e g e n e t i c s h a d o w o f itself, a n d so i n h e r i t e d . B u t this i s u t t e r l y a l i e n t o e v e r y t h i n g w e n o w u n d e r s t a n d a b o u t t h e w a y d e v e l o p m e n t w o r k s . T h e g e n o m e i s n o t , i n a n y sense w h a t s o e v e r , a s c a l e m o d e l o f t h e b o d y . I t i s a set o f i n s t r u c t i o n s w h i c h , i f f a i t h f u l l y o b e y e d i n t h e right order and under the right conditions, will result in a b o d y . I h a v e p r e v i o u s l y u s e d t h e m e t a p h o r o f a c a k e ( D a w k i n s i n press a ) . W h e n y o u m a k e a c a k e y o u m a y , i n s o m e sense, s a y t h a t y o u a r e ' t r a n s l a t i n g ' f r o m recipe to cake. But it is an irreversible process. Y o u c a n n o t dissect a c a k e and

thereby

reconstruct

the

original

recipe.

There

one-to-one,

reversible m a p p i n g from w o r d s of recipe to c r u m b s of c a k e . T h i s is not to say that a skilled c o o k c o u l d not a c h i e v e a passable reversal, by t a k i n g a c a k e p r e s e n t e d t o h i m a n d m a t c h i n g its taste a n d p r o p e r t i e s a g a i n s t his o w n p a s t experience of cakes a n d recipes, a n d then r e c o n s t r u c t i n g the r e c i p e . B u t that w o u l d b e a k i n d o f m e n t a l s e l e c t i o n p r o c e d u r e , a n d w o u l d i n n o sense b e a translation from c a k e t o r e c i p e ( a g o o d d i s c u s s i o n o f t h e d i f f e r e n c e b e t w e e n reversible and irreversible codes, in the c o n t e x t of the n e r v o u s system, is given by Barlow 1961). A c a k e i s t h e c o n s e q u e n c e o f t h e o b e y i n g o f a series o f i n s t r u c t i o n s , w h e n t o m i x the v a r i o u s i n g r e d i e n t s , w h e n t o a p p l y h e a t , e t c . I t i s n o t t r u e t h a t t h e c a k e i s those i n s t r u c t i o n s r e n d e r e d i n t o a n o t h e r c o d i n g m e d i u m . I t i s n o t l i k e a t r a n s l a t i o n o f the r e c i p e f r o m F r e n c h i n t o E n g l i s h , w h i c h i s i n p r i n c i p l e r e v e r s i b l e ( g i v e or t a k e a f e w nuances). A b o d y , t o o , is t h e c o n s e q u e n c e of t h e o b e y i n g o f a series o f i n s t r u c t i o n s ; n o t s o m u c h w h e n t o a p p l y h e a t a s w h e n to apply e n z y m e s speeding up particular c h e m i c a l reactions. If the process of e m b r y o n i c d e v e l o p m e n t i s c o r r e c t l y set i n m o t i o n i n t h e r i g h t e n v i r o n m e n t , the e n d result w i l l b e a w e l l - f o r m e d a d u l t b o d y , m a n y o f w h o s e a t t r i b u t e s w i l l b e i n t e r p r e t a b l e a s c o n s e q u e n c e s o f its g e n e s . B u t y o u c a n n o t r e c o n s t r u c t a n i n d i v i d u a l ' s g e n o m e b y i n s p e c t i n g his b o d y , a n y m o r e t h a n y o u c o u l d

176

Selfish D N A , J u m p i n g G e n e s , and a L a m a r c k i a n Scare

r e c o n s t r u c t W i l l i a m S h a k e s p e a r e b y d e c o d i n g his c o l l e c t e d w o r k s . C a n n o n ' s a n d G o u l d ' s false a r g u m e n t o f p . 1 1 6 i s v a l i d l y a d a p t e d t o e m b r y o l o g y . L e t m e p u t t h e m a t t e r i n a n o t h e r w a y . I f a m a n i s p a r t i c u l a r l y fat, there a r e m a n y w a y s i n w h i c h this m i g h t h a v e c o m e a b o u t . H e m i g h t h a v e a g e n e t i c p r e d i s p o s i t i o n t o m e t a b o l i z e his food p a r t i c u l a r l y t h o r o u g h l y . O r h e might

have been

overfed.

T h e end

result o f a n

e x c e s s o f food

may be

i d e n t i c a l t o t h e e n d r e s u l t o f a p a r t i c u l a r g e n e . I n b o t h c a s e s the m a n i s fat. B u t t h e r o u t e s b y w h i c h t h e t w o c a u s a l a g e n t s p r o d u c e d t h e i r c o m m o n effects a r e t o t a l l y d i f f e r e n t . F o r a m a n w h o i s a r t i f i c i a l l y stuffed w i t h food t o pass o n his a c q u i r e d fatness t o his c h i l d r e n g e n e t i c a l l y , s o m e m e c h a n i s m w o u l d h a v e to e x i s t t h a t s e n s e d his fatness, t h e n l o c a t e d a 'fatness g e n e ' a n d c a u s e d it to m u t a t e . B u t h o w c o u l d s u c h a fatness g e n e b e l o c a t e d ? T h e r e i s n o t h i n g i n t r i n s i c i n t h e n a t u r e o f t h e g e n e t h a t m a k e s i t r e c o g n i z a b l e a s a fatness g e n e . I t h a s its o b e s e effect o n l y a s a result o f t h e l o n g a n d c o m p l e x u n f o l d i n g sequence that is epigenetic development. T h e only w a y , in principle, to r e c o g n i z e a 'fatness g e n e ' for w h a t it is, is to a l l o w it to e x e r t its effects on the normal

processes

of development,

and

this

means

development

the

normal, forward direction. T h i s is w h y b o d i l y a d a p t a t i o n s c a n c o m e a b o u t by selection. G e n e s are a l l o w e d t o e x e r t t h e i r n o r m a l effects o n d e v e l o p m e n t . T h e i r d e v e l o p m e n t a l consequencesâ&#x20AC;&#x201D;phenotypic

effectsâ&#x20AC;&#x201D;feed

back on

those g e n e s '

chances of

s u r v i v i n g , a n d as a result g e n e frequencies c h a n g e in s u c c e e d i n g generations in a d a p t i v e directions. S e l e c t i v e theories of a d a p t a t i o n , but not instructive t h e o r i e s , c a n c o p e w i t h t h e f a c t t h a t t h e r e l a t i o n s h i p b e t w e e n a g e n e a n d its p h e n o t y p i c effect i s n o t a n i n t r i n s i c p r o p e r t y o f t h e g e n e , b u t a p r o p e r t y o f t h e f o r w a r d d e v e l o p m e n t a l c o n s e q u e n c e s o f the g e n e w h e n i n t e r a c t i n g w i t h the c o n s e q u e n c e s o f m a n y other genes a n d m a n y e x t e r n a l factors. C o m p l e x a d a p t a t i o n t o a n e n v i r o n m e n t m a y arise i n i n d i v i d u a l o r g a n i s m s through happens.

instruction from But,

given

that environment. assumption

m a n y c a s e s this c e r t a i n l y

of epigenetic,

not

preformationistic

e m b r y o l o g y , to e x p e c t such c o m p l e x a d a p t a t i o n s to be translated into the m e d i u m o f the g e n e t i c c o d e , b y some m e a n s other than the selection o f u n d i r e c t e d v a r i a t i o n , is a gross v i o l a t i o n of a l l t h a t I h o l d r a t i o n a l . T h e r e are other e x a m p l e s o f w h a t looks like true L a m a r c k i a n 'instruction' from the e n v i r o n m e n t b e i n g inherited. N o n - g e n e t i c a n o m a l i e s that appear, or e v e n that are s u r g i c a l l y i n d u c e d , in the cortex of ciliates, m a y be directly inherited.

This

has

been

demonstrated

Sonneborn

and

others.

B o n n e r ' s a c c o u n t , t h e y c u t o u t a s m a l l p o r t i o n o f the c o r t e x o f Paramecium a n d r e v e r s e d it. ' T h e r e s u l t i s a Paramecium w i t h p a r t o f o n e r o w o f b a s a l b o d i e s i n w h i c h t h e fine s t r u c t u r e a n d d e t a i l s a r e all p o i n t e d 180Â° a w a y from t h e rest o f t h e s u r f a c e . T h i s a n o m a l o u s k i n e t y i s n o w i n h e r i t e d ; i t a p p e a r s t o b e a p e r m a n e n t f i x t u r e o f t h e p r o g e n y ( w h i c h h a v e b e e n c a r r i e d t h r o u g h 800 generations)'

(Bonner 1974, p.

180). T h e inheritance a p p e a r s to be non-

Selfish D N A , J u m p i n g G e n e s , and a L a m a r c k i a n Scare

genic

and

obviously

non-nuclear.

' . . . the

cortex

made

177

m a c r o m o l e c u l e s t h a t a s s e m b l e i n a p a r t i c u l a r p a t t e r n , a n d . . . this p a t t e r n , even in a disturbed state, is directly inherited. . . . we h a v e a l a r g e a n d e x c e e d i n g l y c o m p l e x cortex w h o s e pattern of fitting together is a p r o p e r t y of the m a c r o m o l e c u l e s a t t h e c o r t e x a n d i s n o t d i r e c t l y u n d e r n u c l e a r c o n t r o l . O v e r w h a t must h a v e been a long time and a vast n u m b e r of cell cycles, a s u r f a c e s t r u c t u r e e v o l v e d . T h e s t r u c t u r e i t s e l f h a d p r o p e r t i e s s u c h t h a t its i m m e d i a t e form is i n d e p e n d e n t of the n u c l e u s ; at the s a m e time, it is totally d e p e n d e n t o n t h e n u c l e u s , w e p r e s u m e , for t h e s y n t h e s i s o f its s p e c i f i c a l l y shaped building blocks' (Bonner 1974). A s i n the c a s e o f S t e e l e ' s w o r k , w h e t h e r w e r e g a r d this a s t h e i n h e r i t a n c e o f acquired characteristics d e p e n d s u p o n our definition o f the g e r m - l i n e . I f w e d i r e c t o u r a t t e n t i o n t o t h e i n d i v i d u a l b o d y , a s u r g i c a l m u t i l a t i o n o f its c o r t e x is clearly an acquired characteristic h a v i n g n o t h i n g to do with the nuclear g e r m - l i n e . If, o n the o t h e r h a n d , w e l o o k a t u n d e r l y i n g r e p l i c a t o r s , i n this case perhaps general

the

heading

basal

bodies of cilia,

of replicator

the

propagation.

p h e n o m e n o n falls Given

that

under

the

macromolecular

structures in the cortex are true replicators, s u r g i c a l l y r o t a t i n g a p o r t i o n of c o r t e x i s a n a l o g o u s t o c u t t i n g o u t a p o r t i o n o f c h r o m o s o m e , i n v e r t i n g it, a n d putting it b a c k . N a t u r a l l y the inversion is inherited, b e c a u s e it is part of the g e r m - l i n e . It a p p e a r s t h a t e l e m e n t s of the c o r t e x of Paramecium h a v e a g e r m line

of their

own,

although

particularly

remarkable

one

that

the

information transmitted does not seem to be e n c o d e d in nucleic acids. We s h o u l d d e f i n i t e l y p r e d i c t t h a t n a t u r a l s e l e c t i o n m i g h t a c t d i r e c t l y o n this n o n - g e n i c g e r m - l i n e , s h a p i n g s u r f a c e s t r u c t u r e for t h e a d a p t i v e b e n e f i t o f t h e r e p l i c a t i n g u n i t s i n t h e s u r f a c e itself. I f t h e r e i s a n y c o n f l i c t b e t w e e n t h e interests o f these s u r f a c e r e p l i c a t o r s a n d n u c l e a r g e n e s , t h e r e s o l u t i o n o f t h e conflict should m a k e a fascinating study. T h i s is by no means the only e x a m p l e of non-nuclear inheritance. It is b e c o m i n g increasingly clear that non-nuclear genes, either in organelles such a s m i t o c h o n d r i a o r l o o s e i n c y t o p l a s m , e x e r t n o t i c e a b l e effects o n p h e n o t y p e s (Grun

1976).

Plasmagene,

had

discussing

intended the

expected

include

section

consequences

called

of selection

The

Selfish

acting

c y t o p l a s m i c r e p l i c a t o r s , a n d t h e l i k e l y results o f c o n f l i c t s w i t h n u c l e a r g e n e s . However,

mitochondria'

had

got

further

(now in C h a p t e r

than

some

brief remarks

12), w h e n two papers arrived

'selfish

(Eberhard

1980; C o s m i d e s & T o o b y 1981) w h i c h , independently, say e v e r y t h i n g I m i g h t h a v e said a n d m u c h m o r e . T o g i v e j u s t o n e e x a m p l e , ' T h e m i g r a t i o n of e g g m i t o c h o n d r i a to cluster a r o u n d the e g g nucleus, so as to favor their i n c l u s i o n i n t h e " n e o c y t o p l a s m " o f t h e p r o e m b r y o i n t h e g y m n o s p e r m s Larix a n d Pseudotsuga . . . m a y result f r o m c o m p e t i t i o n for i n c l u s i o n in t h e e m b r y o ' (Eberhard, p. 238). R a t h e r than extensively duplicate w h a t is in them I w o u l d prefer simply to r e c o m m e n d readers to consult b o t h these e x c e l l e n t

178

Selfish D N A , J u m p i n g G e n e s , and a L a m a r c k i a n Scare

papers. I will o n l y a d d that both papers are g o o d e x a m p l e s of the kind of discussion

that I

believe will b e c o m e c o m m o n p l a c e , once the replicator

replaces the i n d i v i d u a l o r g a n i s m as the f u n d a m e n t a l c o n c e p t u a l unit in our thinking a b o u t natural selection. O n e does not h a v e to be clairvoyant to p r o p h e s y , for e x a m p l e , t h e rise o f a f l o u r i s h i n g n e w d i s c i p l i n e o f ' p r o k a r y o t i c sociobiology'. N e i t h e r E b e r h a r d nor C o s m i d e s and T o o b y explicitly justify o r d o c u m e n t t h e g e n e s ' - e y e v i e w o f l i f e : t h e y s i m p l y assume i t : ' T h e r e c e n t shift t o w a r d s v i e w i n g t h e g e n e a s t h e u n i t o f s e l e c t i o n , c o u p l e d w i t h a r e c o g n i t i o n o f the different

modes

symbiosis,

of genetic

inheritance

makes

the

concept

of parasitism,

conflict, cooperation, and c o e v o l u t i o n â&#x20AC;&#x201D; w h i c h w e r e developed

with reference to w h o l e organismsâ&#x20AC;&#x201D;relevant to genes within an organism' ( C o s m i d e s & T o o b y ) . T h e s e p a p e r s h a v e w h a t I c a n o n l y d e s c r i b e a s the flavour of post-revolutionary normal science ( K u h n 1970).

10 An Agony in Five Fits

T h e r e a d e r m a y r e m a r k t h a t w e h a v e c o m e t h u s far w i t h s c a r c e l y a m e n t i o n o f 'fitness'. T h i s w a s d e l i b e r a t e . I h a v e m i s g i v i n g s a b o u t t h e t e r m , but I h a v e been h o l d i n g my fire. S e v e r a l of the earlier c h a p t e r s h a v e b e e n a i m e d , in their different w a y s , at e x p o s i n g the w e a k n e s s e s in the i n d i v i d u a l o r g a n i s m ' s c a n d i d a c y for the title o f o p t i m o n , adaptations

may

be said

to work.

'Fitness',

the as

u n i t for w h o s e b e n e f i t is

normally

used

e c o l o g i s t s a n d e t h o l o g i s t s , is a v e r b a l t r i c k , a d e v i c e c o n t r i v e d to m a k e it possible t o t a l k i n t e r m s o f i n d i v i d u a l s , a s o p p o s e d t o t r u e r e p l i c a t o r s , a s beneficiaries of a d a p t a t i o n . T h e w o r d is therefore a kind of v e r b a l s y m b o l of the p o s i t i o n t h a t I a m t r y i n g t o a r g u e a g a i n s t . M o r e t h a n t h a t , t h e w o r d i s actively confusing because it has b e e n used in so m a n y different w a y s . It is therefore fitting to end the critical section of the b o o k w i t h a discussion of fitness. Herbert Spencer's

(1864)

term 'survival of the fittest' w a s a d o p t e d by

D a r w i n (1866) a t the u r g i n g o f W a l l a c e ( 1 8 6 6 ) . W a l l a c e ' s a r g u m e n t m a k e s f a s c i n a t i n g r e a d i n g t o d a y , a n d I c a n n o t resist q u o t i n g h i m a t s o m e l e n g t h : My dear Darwin,â&#x20AC;&#x201D;I

h a v e been so repeatedly struck by the utter

i n a b i l i t y o f n u m b e r s o f i n t e l l i g e n t p e r s o n s t o see c l e a r l y , o r a t a l l , t h e s e l f - a c t i n g a n d n e c e s s a r y effects o f N a t u r a l S e l e c t i o n , t h a t I a m led t o conclude

that

the

term

itself,

and

your

mode

of illustrating

it,

h o w e v e r c l e a r a n d b e a u t i f u l t o m a n y o f us, a r e y e t n o t t h e b e s t a d a p t e d to impress it on the g e n e r a l naturalist p u b l i c . . . in J a n e t ' s recent w o r k o n the ' M a t e r i a l i s m o f the Present D a y ' . . . h e considers y o u r w e a k p o i n t t o b e t h a t y o u d o n o t see t h a t ' t h o u g h t a n d d i r e c t i o n a r e essential t o t h e a c t i o n o f N a t u r a l S e l e c t i o n ' . T h e s a m e o b j e c t i o n has been m a d e a score of times by y o u r c h i e f o p p o n e n t s , a n d I h a v e h e a r d i t a s often s t a t e d m y s e l f i n c o n v e r s a t i o n . N o w , I t h i n k this arises almost entirely from y o u r c h o i c e of the term N a t u r a l S e l e c t i o n , a n d so c o n s t a n t l y c o m p a r i n g i t i n its effects t o m a n ' s s e l e c t i o n , a n d a l s o t o 179

180

An A g o n y in Five F i t s

y o u r so frequently personifying nature as 'selecting', as 'preferring', as ' s e e k i n g o n l y t h e g o o d o f t h e s p e c i e s ' , e t c . , e t c . T o the few this i s a s clear

daylight,

and

beautifully

suggestive,

but

many

e v i d e n t l y a s t u m b l i n g b l o c k . I w i s h , t h e r e f o r e , to s u g g e s t to y o u the p o s s i b i l i t y o f e n t i r e l y a v o i d i n g this s o u r c e o f m i s c o n c e p t i o n i n y o u r g r e a t w o r k (if n o w n o t t o o l a t e ) , a n d a l s o i n a n y f u t u r e e d i t i o n s o f the 'Origin',

and I

t h i n k i t m a y b e d o n e w i t h o u t difficulty a n d v e r y

e f f e c t u a l l y b y a d o p t i n g S p e n c e r ' s t e r m ( w h i c h h e g e n e r a l l y uses i n p r e f e r e n c e t o N a t u r a l S e l e c t i o n ) , v i z . ' S u r v i v a l o f the F i t t e s t ' . T h i s term is the p l a i n expression of the fact; m e t a p h o r i c a l e x p r e s s i o n of it,

and

' N a t u r a l S e l e c t i o n ' is a

to a c e r t a i n d e g r e e indirect a n d

incorrect, s i n c e , e v e n p e r s o n i f y i n g N a t u r e , she d o e s n o t s o m u c h select s p e c i a l v a r i a t i o n s as e x t e r m i n a t e t h e m o s t u n f a v o u r a b l e o n e s . . . [ T h e Wallace-Darwin Correspondence].

I t m a y s e e m h a r d t o b e l i e v e t h a t a n y o n e c o u l d h a v e b e e n m i s l e d i n the w a y that W a l l a c e indicates, but Y o u n g ( 1 9 7 1 )

provides ample evidence

c o n f i r m i n g t h a t D a r w i n ' s c o n t e m p o r a r i e s often w e r e s o m i s l e d . E v e n t o d a y t h e c o n f u s i o n i s n o t u n k n o w n , a n d a n a n a l o g o u s m u d d l e arises o v e r the catch-phrase There

'selfish g e n e ' :

reason

for

' T h i s is an ingenious theory but far-fetched.

imputing

the

complex

emotion

o f selfishness

m o l e c u l e s ' ( B e t h e l l 1 9 7 8 ) ; ' G e n e s c a n n o t b e selfish o r unselfish, a n y m o r e than

atoms

can

be jealous,

elephants

abstract

biscuits

teleological'

( M i d g l e y 1 9 7 9 ; see r e p l y i n D a w k i n s 1 9 8 1 ) . D a r w i n ( 1 8 6 6 ) w a s i m p r e s s e d b y W a l l a c e ' s l e t t e r , w h i c h h e f o u n d 'as c l e a r a s d a y l i g h t ' , a n d h e r e s o l v e d t o i n c o r p o r a t e ' s u r v i v a l o f t h e f i t t e s t ' i n t o his w r i t i n g s , a l t h o u g h h e c a u t i o n e d t h a t ' t h e t e r m N a t u r a l S e l e c t i o n has n o w b e e n so largely used a b r o a d a n d at h o m e that I d o u b t w h e t h e r it could be g i v e n u p , a n d w i t h a l l its faults I s h o u l d b e s o r r y t o see the a t t e m p t m a d e . Whether

will

rejected

must

now depend

the

" s u r v i v a l of the

fittest" . . . ' ( D a r w i n c l e a r l y understood the ' m e m e ' p r i n c i p l e ) . ' A s i n time t h e t e r m m u s t g r o w i n t e l l i g i b l e , t h e o b j e c t i o n s t o its use w i l l g r o w w e a k e r and weaker.

I d o u b t w h e t h e r t h e use o f a n y t e r m w o u l d h a v e m a d e the

s u b j e c t i n t e l l i g i b l e t o s o m e m i n d s . . . A s for M . J a n e t , h e i s a m e t a p h y s i c i a n , a n d such g e n t l e m e n are so a c u t e that

t h i n k t h e y often m i s u n d e r s t a n d

c o m m o n folk.' W h a t neither W a l l a c e nor D a r w i n could h a v e foreseen w a s that 'survival o f t h e fittest' w a s d e s t i n e d t o g e n e r a t e m o r e s e r i o u s c o n f u s i o n t h a n ' n a t u r a l selection' e v e r h a d . A familiar e x a m p l e is the a t t e m p t , rediscovered with almost pathetic eagerness by successive generations of a m a t e u r (and even professional)

philosophers

('so

acute

that

they

misunderstand

common

f o l k ' ? ) , to d e m o n s t r a t e that the theory of natural selection is a worthless t a u t o l o g y (an a m u s i n g v a r i a n t is t h a t it is u n f a l s i f i a b l e a n d t h e r e f o r e f a l s e ! ) .

An A g o n y in F i v e F i t s

181

I n fact the i l l u s i o n o f t a u t o l o g y s t e m s e n t i r e l y f r o m t h e p h r a s e ' s u r v i v a l o f t h e fittest', a n d n o t f r o m t h e t h e o r y i t s e l f a t a l l . T h e a r g u m e n t i s a r e m a r k a b l e e x a m p l e of the e l e v a t i o n of w o r d s a b o v e their station, in w h i c h respect it resembles St A n s e l m ' s ontological p r o o f of the existence of G o d . L i k e G o d , natural selection is too big a theory to be p r o v e d or d i s p r o v e d by w o r d games.

God

and

natural selection are,

after a l l ,

the only

two workable

theories w e h a v e o f w h y w e exist. B r i e f l y , t h e t a u t o l o g y i d e a i s this. survival of the fittest, a n d

N a t u r a l selection is defined as the

the fittest are defined

those

that survive.

T h e r e f o r e the w h o l e of D a r w i n i s m is an unfalsifiable t a u t o l o g y a n d we d o n ' t have

worry

our

heads

about

any

more.

Fortunately,

several

a u t h o r i t a t i v e r e p l i e s t o this w h i m s i c a l little c o n c e i t a r e a v a i l a b l e ( M a y n a r d Smith

1969; Stebbins 1 9 7 7 ; A l e x a n d e r 1980), and I n e e d not l a b o u r my

o w n . I w i l l , h o w e v e r , c h a l k u p t h e t a u t o l o g y i d e a o n m y list o f m u d d l e s a t t r i b u t a b l e t o t h e c o n c e p t o f fitness. It is, as I h a v e s a i d , a p u r p o s e of this c h a p t e r to s h o w t h a t fitness is a v e r y difficult c o n c e p t , a n d t h a t t h e r e m i g h t b e s o m e t h i n g t o b e s a i d for d o i n g w i t h o u t i t w h e n e v e r w e c a n . O n e w a y I s h a l l d o this i s t o s h o w t h a t t h e w o r d h a s b e e n u s e d b y b i o l o g i s t s i n a t l e a s t f i v e d i f f e r e n t senses. T h e first a n d o l d e s t m e a n i n g i s t h e o n e closest t o e v e r y d a y u s a g e . Fit the F i r s t W h e n S p e n c e r , W a l l a c e a n d D a r w i n o r i g i n a l l y used the t e r m 'fitness', the charge of t a u t o l o g y w o u l d not h a v e o c c u r r e d to a n y o n e .

I s h a l l c a l l this

original usage fitness[1]. It did not h a v e a precise technical m e a n i n g , and the f i t t e s t w e r e n o t defined a s

those that survive.

Fitness

meant,

roughly,

the

capacity to survive and reproduce, but it was not defined and measured as precisely s y n o n y m o u s w i t h r e p r o d u c t i v e success. It h a d a r a n g e of specific meanings,

depending

upon

the

particular

aspect

o f life

that

one

was

e x a m i n i n g . If the subject of attention w a s efficiency in g r i n d i n g v e g e t a b l e f o o d , the f i t t e s t i n d i v i d u a l s w e r e t h o s e w i t h t h e h a r d e s t t e e t h o r t h e m o s t powerful j a w muscles. I n different contexts the f i t t e s t i n d i v i d u a l s w o u l d b e t a k e n t o m e a n those w i t h t h e k e e n e s t e y e s , t h e s t r o n g e s t l e g m u s c l e s , t h e s h a r p e s t e a r s , t h e swiftest r e f l e x e s . T h e s e c a p a c i t i e s a n d a b i l i t i e s , a l o n g w i t h countless others, w e r e supposed to i m p r o v e o v e r the g e n e r a t i o n s , a n d n a t u r a l s e l e c t i o n effected t h a t i m p r o v e m e n t . ' S u r v i v a l o f t h e f i t t e s t ' w a s a g e n e r a l characterization

these

particular

improvements.

There

nothing

tautological a b o u t that. It w a s only later that fitness w a s a d o p t e d as a t e c h n i c a l term. Biologists t h o u g h t t h e y n e e d e d a w o r d for t h a t h y p o t h e t i c a l q u a n t i t y t h a t t e n d s t o b e m a x i m i z e d as a result of n a t u r a l selection. T h e y c o u l d h a v e c h o s e n 'selective potential', or 'survivability', or

'W'

b u t i n f a c t t h e y lit u p o n 'fitness'. T h e y

d i d the e q u i v a l e n t o f r e c o g n i z i n g t h a t t h e d e f i n i t i o n t h e y w e r e s e e k i n g m u s t

182

An A g o n y in Five F i t s

b e ' w h a t e v e r i t t a k e s t o m a k e t h e s u r v i v a l o f t h e fittest i n t o a t a u t o l o g y ' . T h e y r e d e f i n e d fitness a c c o r d i n g l y . B u t t h e t a u t o l o g y i s n o t a p r o p e r t y o f D a r w i n i s m itself, m e r e l y o f the c a t c h p h r a s e w e s o m e t i m e s use t o d e s c r i b e it. I f I s a y t h a t a t r a i n t r a v e l l i n g a t a n a v e r a g e v e l o c i t y o f 1 2 0 m . p . h . w i l l r e a c h its d e s t i n a t i o n i n h a l f t h e t i m e i t t a k e s a t r a i n t r a v e l l i n g at 60 m . p . h . , t h e f a c t t h a t I h a v e u t t e r e d a t a u t o l o g y does

not

prevent

the

trains

from

running,

nor

does

stop

asking

m e a n i n g f u l q u e s t i o n s a b o u t w h a t m a k e s o n e t r a i n faster t h a n t h e o t h e r : d o e s i t h a v e a l a r g e r e n g i n e , s u p e r i o r fuel, a m o r e s t r e a m l i n e d s h a p e , o r w h a t ? T h e c o n c e p t o f v e l o c i t y i s defined i n s u c h a w a y a s t o m a k e s t a t e m e n t s s u c h a s t h e o n e a b o v e t a u t o l o g i c a l l y t r u e . I t i s this t h a t m a k e s t h e c o n c e p t o f v e l o c i t y useful. A s M a y n a r d S m i t h (1969) w i t h e r i n g l y p u t it: ' O f course D a r w i n i s m c o n t a i n s t a u t o l o g i c a l f e a t u r e s : a n y s c i e n t i f i c t h e o r y c o n t a i n i n g t w o lines o f a l g e b r a d o e s s o . ' A n d w h e n H a m i l t o n ( 1 9 7 5 a ) , s p e a k i n g o f ' s u r v i v a l o f the fittest', s a i d

t h a t ' a c c u s a t i o n s o f t a u t o l o g y s e e m h a r d l y fair o n this s m a l l

p h r a s e i t s e l f , h e w a s p u t t i n g i t m i l d l y . G i v e n t h e p u r p o s e for w h i c h f i t n e s s w a s r e d e f i n e d , ' s u r v i v a l o f t h e f i t t e s t ' had t o b e c o m e a t a u t o l o g y . T o r e d e f i n e f i t n e s s i n a s p e c i a l t e c h n i c a l sense m i g h t h a v e d o n e n o h a r m , other than to g i v e some earnest philosophers a field day, but unfortunately its e x a c t t e c h n i c a l m e a n i n g h a s v a r i e d w i d e l y , a n d this h a s h a d the m o r e serious

effect

of confusing

unexceptionable

of the

some

various

biologists technical

too.

The

meanings

most that

precise adopted

and by

population geneticists.

Fit the Second F o r p o p u l a t i o n geneticists, fitness is an o p e r a t i o n a l measure, e x a c t l y defined in terms of a m e a s u r e m e n t p r o c e d u r e . T h e w o r d is a p p l i e d not really to a w h o l e i n d i v i d u a l o r g a n i s m b u t to a g e n o t y p e , usually at a single locus. T h e fitness W of a g e n o t y p e , s a y Aa, m a y be d e f i n e d as I â&#x20AC;&#x201D; S, w h e r e S is the coefficient of selection against the g e n o t y p e

(Falconer

1960).

It m a y be

r e g a r d e d as a m e a s u r e of the n u m b e r of offspring that a t y p i c a l i n d i v i d u a l of g e n o t y p e Aa is e x p e c t e d to b r i n g up to reproductive age, w h e n all other v a r i a t i o n is a v e r a g e d out. It is usually expressed relative to the correspondi n g f i t n e s s o f o n e p a r t i c u l a r g e n o t y p e a t the l o c u s , w h i c h i s a r b i t r a r i l y defined as I. T h e n there is said to be selection, at that locus, in favour of g e n o t y p e s w i t h h i g h e r fitness, relative to g e n o t y p e s w i t h l o w e r fitness. I shall c a l l this s p e c i a l p o p u l a t i o n g e n e t i c i s t s ' m e a n i n g o f t h e t e r m f i t n e s s [ 2 ] . W h e n we say that b r o w n - e y e d individuals are fitter than blue-eyed individuals we a r e t a l k i n g a b o u t f i t n e s s [ 2 ] . W e a s s u m e t h a t a l l o t h e r v a r i a t i o n a m o n g the i n d i v i d u a l s i s a v e r a g e d o u t , a n d w e a r e , i n effect, a p p l y i n g t h e w o r d fitness t o t w o g e n o t y p e s at a single locus.

An A g o n y in F i v e F i t s

183

Fit the T h i r d But

while

population

geneticists

are

interested

directly

changes

genotype frequencies and gene frequencies, ethologists and ecologists look at whole

organisms

integrated

systems

that

appear

maximizing

s o m e t h i n g . F i t n e s s [ 3 ] , o r ' c l a s s i c a l fitness', i s a p r o p e r t y o f a n i n d i v i d u a l o r g a n i s m , often e x p r e s s e d a s t h e p r o d u c t o f s u r v i v a l a n d f e c u n d i t y . I t i s a m e a s u r e o f t h e i n d i v i d u a l ' s r e p r o d u c t i v e s u c c e s s , o r its s u c c e s s i n p a s s i n g its genes on to future generations. F o r instance, as m e n t i o n e d in C h a p t e r 7, C l u t t o n - B r o c k et al. (in press) a r e c o n d u c t i n g a l o n g - t e r m s t u d y of a r e d d e e r population on the island of R h u m , a n d part of their a i m is to c o m p a r e the lifetime r e p r o d u c t i v e s u c c e s s e s o r fitness[3] o f i d e n t i f i e d i n d i v i d u a l s t a g s a n d hinds. N o t i c e the difference b e t w e e n

the fitness[3] of an i n d i v i d u a l a n d

the

fitness[2] o f a g e n o t y p e . T h e m e a s u r e d f i t n e s s [ 2 ] o f t h e b r o w n - e y e d g e n o t y p e will contribute t o the f i t n e s s [ 3 ] o f a n i n d i v i d u a l w h o h a p p e n s t o h a v e b r o w n e y e s , b u t s o w i l l t h e f i t n e s s [ 2 ] o f his g e n o t y p e a t a l l o t h e r l o c i . T h u s t h e fitness[2] of a g e n o t y p e at a locus c a n be r e g a r d e d as an a v e r a g e of the f i t n e s s [ 3 ] s o f a l l i n d i v i d u a l s p o s s e s s i n g t h a t g e n o t y p e . A n d t h e fitness[3] o f a n i n d i v i d u a l c a n b e r e g a r d e d a s i n f l u e n c e d b y t h e f i t n e s s [ 2 ] o f his g e n o t y p e , a v e r a g e d o v e r a l l his l o c i ( F a l c o n e r 1 9 6 0 ) . It is e a s y to m e a s u r e t h e fitness[2] of a g e n o t y p e at a l o c u s , b e c a u s e e a c h g e n o t y p e , AA, Aa, e t c . , o c c u r s a c o u n t a b l e n u m b e r o f t i m e s i n s u c c e s s i v e g e n e r a t i o n s i n a p o p u l a t i o n . B u t t h e s a m e i s n o t t r u e o f t h e fitness[3] o f a n organism.

You

c a n ' t c o u n t the n u m b e r o f times a n o r g a n i s m o c c u r s i n

successive generations, because h e o n l y occurs o n c e , ever. T h e f i t n e s s [ 3 ] o f a n o r g a n i s m i s often m e a s u r e d a s t h e n u m b e r o f his o f f s p r i n g r e a r e d t o a d u l t h o o d , b u t t h e r e i s s o m e d i s p u t e o v e r t h e usefulness o f this. O n e p r o b l e m i s raised b y W i l l i a m s ( 1 9 6 6 ) c r i t i c i z i n g M e d a w a r ( 1 9 6 0 ) w h o h a d s a i d : ' T h e genetical usage of "fitness" is an extreme attenuation of the ordinary u s a g e : i t is, i n effect, a s y s t e m o f p r i c i n g t h e e n d o w m e n t s o f o r g a n i s m s i n t h e c u r r e n c y o f o f f s p r i n g , i.e., i n t e r m s o f n e t r e p r o d u c t i v e p e r f o r m a n c e . I t i s a genetic valuation of goods, not a statement a b o u t their nature or q u a l i t y . ' W i l l i a m s is w o r r i e d

that

this

retrospective definition,

s u i t a b l e for

particular individuals w h o h a v e existed. It suggests a p o s t h u m o u s e v a l u a t i o n of particular a n i m a l s as ancestors, not a w a y of e v a l u a t i n g the qualities that c a n b e e x p e c t e d t o m a k e for s u c c e s s i n g e n e r a l .

' M y m a i n criticism of

M e d a w a r ' s s t a t e m e n t i s t h a t i t focuses a t t e n t i o n o n t h e r a t h e r t r i v i a l p r o b l e m o f the d e g r e e t o w h i c h a n o r g a n i s m a c t u a l l y a c h i e v e s r e p r o d u c t i v e s u r v i v a l . T h e central biological

p r o b l e m is not survival as such,

b u t d e s i g n for

s u r v i v a l ' ( W i l l i a m s 1 9 6 6 , p . 1 5 8 ) . W i l l i a m s is, i n a sense, h a n k e r i n g after t h e p r e - t a u t o l o g i c a l v i r t u e s o f f i t n e s s [ 1 ] , a n d t h e r e i s m u c h t o b e s a i d i n his f a v o u r . B u t the f a c t i s t h a t f i t n e s s [ 3 ] h a s b e c o m e w i d e l y u s e d b y b i o l o g i s t s i n

184

An A g o n y in F i v e F i t s

t h e sense d e s c r i b e d laymen

and

Medawar.

was surely

M e d a w a r ' s passage was addressed to

attempt

enable

them

standard

b i o l o g i c a l t e r m i n o l o g y w h i l e a v o i d i n g the otherwise i n e v i t a b l e confusion w i t h c o m m o n - u s a g e ' a t h l e t i c ' fitness. The

concept

o f fitness

has

the

power

confuse

even

distinguished

biologists. C o n s i d e r the f o l l o w i n g m i s u n d e r s t a n d i n g o f W a d d i n g t o n (1957) b y E m e r s o n ( 1 9 6 0 ) . W a d d i n g t o n h a d u s e d t h e w o r d ' s u r v i v a l ' i n the sense o f r e p r o d u c t i v e s u r v i v a l o r f i t n e s s [ 3 ] : ' . . . s u r v i v a l d o e s n o t , o f c o u r s e , m e a n the b o d i l y e n d u r a n c e o f a s i n g l e i n d i v i d u a l . . . t h a t i n d i v i d u a l " s u r v i v e s " best w h i c h l e a v e s m o s t o f f s p r i n g ' . E m e r s o n q u o t e s this, t h e n g o e s o n : ' C r i t i c a l d a t a o n this c o n t e n t i o n a r e d i f f i c u l t t o find, a n d i t i s l i k e l y t h a t m u c h n e w investigation is n e e d e d before the point is either verified or refuted.' F o r once,

the

ritual

lip-service

the

need

for

research

utterly

inappropriate. W h e n we are talking a b o u t matters of definition, empirical r e s e a r c h c a n n o t h e l p us. W a d d i n g t o n w a s c l e a r l y defining s u r v i v a l i n a s p e c i a l s e n s e ( t h e sense o f f i t n e s s [ 3 ] ) , n o t m a k i n g a p r o p o s i t i o n o f fact s u b j e c t t o empirical

verification

falsification.

Yet

Emerson

apparently

thought

W a d d i n g t o n w a s m a k i n g t h e p r o v o c a t i v e s t a t e m e n t t h a t those i n d i v i d u a l s w i t h t h e h i g h e s t c a p a c i t y t o s u r v i v e t e n d a l s o t o b e t h e i n d i v i d u a l s w i t h the l a r g e s t n u m b e r o f o f f s p r i n g . H i s f a i l u r e t o g r a s p the t e c h n i c a l c o n c e p t o f f i t n e s s [ 3 ] , i s i n d i c a t e d b y a n o t h e r q u o t a t i o n from t h e s a m e p a p e r : ' I t w o u l d be e x t r e m e l y difficult to e x p l a i n the e v o l u t i o n of the uterus a n d m a m m a r y glands

individual.'

m a m m a l s . . . as

the

result

of natural

In a c c o r d a n c e w i t h the influential

selection

of the fittest

C h i c a g o - b a s e d school of

t h o u g h t o f w h i c h h e w a s a l e a d e r ( A l l e e , E m e r s o n e l al. 1 9 4 9 ) , E m e r s o n used this a s a n a r g u m e n t i n f a v o u r o f g r o u p s e l e c t i o n . M a m m a r y g l a n d s a n d u t e r u s e s w e r e , for h i m , a d a p t a t i o n s for t h e c o n t i n u a t i o n o f t h e s p e c i e s . W o r k e r s w h o c o r r e c t l y use t h e c o n c e p t o f f i t n e s s [ 3 ] a d m i t t h a t i t c a n b e m e a s u r e d o n l y as a c r u d e a p p r o x i m a t i o n . If it is m e a s u r e d as the n u m b e r of c h i l d r e n b o r n i t n e g l e c t s j u v e n i l e m o r t a l i t y a n d fails t o a c c o u n t for p a r e n t a l c a r e . If it is m e a s u r e d as n u m b e r of offspring r e a c h i n g r e p r o d u c t i v e age it neglects v a r i a t i o n in r e p r o d u c t i v e success of the g r o w n offspring. If it is m e a s u r e d a s n u m b e r o f g r a n d c h i l d r e n i t n e g l e c t s . . . a n d s o o n a d infinitum. I d e a l l y w e m i g h t c o u n t t h e r e l a t i v e n u m b e r o f d e s c e n d a n t s a l i v e after s o m e very

large

number of generations.

But such

'ideal'

m e a s u r e h a s the

c u r i o u s p r o p e r t y t h a t , i f c a r r i e d t o its l o g i c a l c o n c l u s i o n , i t c a n t a k e o n l y t w o v a l u e s ; i t i s a n a l l - o r - n o n e m e a s u r e . I f w e l o o k far e n o u g h i n t o t h e future, either I shall h a v e no d e s c e n d a n t s at all, or all persons a l i v e will be my d e s c e n d a n t s ( F i s h e r 1 9 3 0 a ) . I f I a m d e s c e n d e d from a p a r t i c u l a r i n d i v i d u a l m a l e w h o lived a million years a g o , it is virtually certain that y o u are d e s c e n d e d from him too. T h e f i t n e s s o f any particular long-dead individual, as measured in present-day descendants, is either zero or total. Williams w o u l d p r e s u m a b l y s a y t h a t if this is a p r o b l e m it is so o n l y for p e o p l e t h a t

An A g o n y in Five F i t s

185

w i s h t o m e a s u r e t h e actual r e p r o d u c t i v e s u c c e s s o f p a r t i c u l a r i n d i v i d u a l s . If, o n the o t h e r h a n d , w e a r e i n t e r e s t e d i n q u a l i t i e s t h a t t e n d , o n a v e r a g e , t o m a k e i n d i v i d u a l s likely t o e n d u p i n t h e set o f a n c e s t o r s , t h e p r o b l e m d o e s n o t arise. I n a n y c a s e a m o r e b i o l o g i c a l l y i n t e r e s t i n g s h o r t c o m i n g o f t h e c o n c e p t o f f i t n e s s [ 3 ] h a s led t o t h e d e v e l o p m e n t o f t w o n e w e r u s a g e s o f t h e t e c h n i c a l term fitness.

Fit the F o u r t h Hamilton

(1964a,b),

in a pair of p a p e r s w h i c h we c a n n o w see to h a v e

m a r k e d a turning point in the history of e v o l u t i o n a r y theory, m a d e us a w a r e of an important deficiency in classical fitness[3], the m e a s u r e based on the reproductive

success

of an

organism.

The

reason

reproductive

success

matters, as opposed to m e r e i n d i v i d u a l survival, is that r e p r o d u c t i v e success i s a m e a s u r e o f s u c c e s s i n p a s s i n g o n g e n e s . T h e o r g a n i s m s w e see a r o u n d u s are d e s c e n d e d from ancestors, and they h a v e inherited s o m e of the attributes that m a d e those individuals ancestors as o p p o s e d to non-ancestors.

If an

o r g a n i s m exists i t c o n t a i n s t h e g e n e s o f a l o n g l i n e o f s u c c e s s f u l a n c e s t o r s . T h e f i t n e s s [ 3 ] o f a n o r g a n i s m i s its s u c c e s s a s a n a n c e s t o r , o r , a c c o r d i n g t o taste, its c a p a c i t y for s u c c e s s a s a n a n c e s t o r . B u t H a m i l t o n g r a s p e d t h e c e n t r a l importance of w h a t , previously, h a d been only g l a n c i n g l y referred to in stray sentences

of Fisher

(1930a)

and

Haldane

(1955).

This

that

natural

selection will favour organs a n d b e h a v i o u r that cause the i n d i v i d u a l ' s genes t o b e p a s s e d o n , w h e t h e r o r n o t t h e i n d i v i d u a l is, h i m s e l f , a n a n c e s t o r . A n i n d i v i d u a l t h a t assists his b r o t h e r t o b e a n a n c e s t o r m a y t h e r e b y e n s u r e t h e survival in the g e n e - p o o l of the genes 'for' brotherly assistance. H a m i l t o n s a w t h a t p a r e n t a l c a r e i s r e a l l y o n l y a s p e c i a l c a s e o f c a r i n g for c l o s e r e l a t i v e s w i t h a h i g h p r o b a b i l i t y o f c o n t a i n i n g t h e g e n e s for c a r i n g . C l a s s i c a l f i t n e s s [ 3 ] , r e p r o d u c t i v e s u c c e s s , w a s t o o n a r r o w . I t h a d t o b e b r o a d e n e d t o inclusive fitness, w h i c h will here be called fitness[4]. I t i s s o m e t i m e s s u p p o s e d t h a t t h e i n c l u s i v e fitness o f a n i n d i v i d u a l i s his o w n fitness[3] plus h a l f the fitnesses[3] of e a c h b r o t h er plus o n e - e i g h t h of the fitness[3] of e a c h cousin,

etc.

(e.g.

B y g o t t e t al.

1979).

Barash

(1980)

e x p l i c i t l y defines i t a s ' t h e s u m o f i n d i v i d u a l f i t n e s s ( r e p r o d u c t i v e s u c c e s s ) a n d the r e p r o d u c t i v e s u c c e s s o f a n i n d i v i d u a l ' s r e l a t i v e s , w i t h e a c h r e l a t i v e d e v a l u e d in proportion as it is m o r e distantly related'. T h i s w o u l d not be a sensible m e a s u r e t o try t o u s e , a n d , a s W e s t - E b e r h a r d ( 1 9 7 5 ) e m p h a s i z e s , i t i s n o t the m e a s u r e H a m i l t o n offered us. T h e r e a s o n i t w o u l d n o t b e s e n s i b l e can be stated in various w a y s . O n e w a y of p u t t i n g it is that it a l l o w s children to be counted m a n y times, as though they h a d m a n y existences (Grafen 1 9 7 9 ) . T h e n a g a i n , i f a c h i l d i s b o r n t o o n e o f a set o f b r o t h e r s , t h e i n c l u s i v e f i t n e s s o f a l l the o t h e r b r o t h e r s w o u l d , a c c o r d i n g t o this v i e w , i m m e d i a t e l y rise a n e q u a l n o t c h , r e g a r d l e s s w h e t h e r a n y o f t h e m lifted a f i n g e r t o f e e d t h e

186

An A g o n y in F i v e F i t s

infant.

Indeed the inclusive fitness of another brother yet unborn would

t h e o r e t i c a l l y b e i n c r e a s e d b y t h e b i r t h o f his e l d e r n e p h e w . F u r t h e r , this l a t e r b r o t h e r c o u l d b e a b o r t e d s h o r t l y after c o n c e p t i o n a n d still, a c c o r d i n g t o this erroneous v i e w , enjoy a massive 'inclusive fitness' t h r o u g h the descendants of his e l d e r b r o t h e r s . T o p u s h t o t h e reductio a d absurdum, h e n e e d n ' t e v e n b o t h e r t o b e c o n c e i v e d , y e t still h a v e a h i g h ' i n c l u s i v e f i t n e s s ' ! H a m i l t o n c l e a r l y s a w this f a l l a c y , a n d t h e r e f o r e his c o n c e p t o f i n c l u s i v e fitness w a s m o r e subtle. T h e inclusive fitness of an organism is not a property of himself,

but

a p r o p e r t y o f his a c t i o n s o r effects.

Inclusive fitness is

c a l c u l a t e d f r o m a n i n d i v i d u a l ' s o w n r e p r o d u c t i v e s u c c e s s p l u s his effects o n the

reproductive

success

his

relatives,

each

one

weighed

the

a p p r o p r i a t e c o e f f i c i e n t o f r e l a t e d n e s s . T h e r e f o r e , for i n s t a n c e , i f m y b r o t h e r e m i g r a t e s t o A u s t r a l i a , s o I c a n h a v e n o effect, o n e w a y o r t h e o t h e r , o n his r e p r o d u c t i v e s u c c e s s , m y i n c l u s i v e fitness d o e s n o t g o u p e a c h t i m e h e h a s a child! N o w 'effects' o f p u t a t i v e causes c a n o n l y b e m e a s u r e d b y c o m p a r i s o n w i t h other putative causes, or by c o m p a r i s o n with their absence. We cannot, then, t h i n k o f t h e effects o f i n d i v i d u a l A o n t h e s u r v i v a l a n d r e p r o d u c t i o n o f his r e l a t i v e s i n a n y a b s o l u t e s e n s e . W e c o u l d c o m p a r e t h e effects o f his c h o o s i n g t o p e r f o r m a c t X r a t h e r t h a n a c t Y . O r w e c o u l d t a k e t h e effects o f his l i f e t i m e ' s set o f d e e d s a n d c o m p a r e t h e m w i t h a h y p o t h e t i c a l l i f e t i m e o f t o t a l i n a c t i o n â&#x20AC;&#x201D; a s t h o u g h h e h a d n e v e r b e e n c o n c e i v e d . I t i s this l a t t e r u s a g e t h a t is n o r m a l l y m e a n t by the inclusive fitness of an individual organism. T h e point is

that inclusive fitness is not an

absolute property of an

organism in the same w a y as classical fitness[3] could in theory be, if m e a s u r e d i n c e r t a i n w a y s . I n c l u s i v e fitness i s a p r o p e r t y o f a t r i p l e c o n s i s t i n g o f a n o r g a n i s m o f i n t e r e s t , a n a c t o r set o f a c t s o f i n t e r e s t , a n d a n a l t e r n a t i v e set o f a c t s for c o m p a r i s o n . W e a s p i r e t o m e a s u r e , t h e n , n o t t h e a b s o l u t e i n c l u s i v e f i t n e s s o f t h e o r g a n i s m I , b u t t h e effect o n I ' s i n c l u s i v e f i t n e s s o f his d o i n g a c t X i n c o m p a r i s o n w i t h his d o i n g a c t Y . I f ' a c t ' X i s t a k e n t o b e I's e n t i r e life s t o r y , Y m a y b e t a k e n a s e q u i v a l e n t t o a h y p o t h e t i c a l w o r l d i n w h i c h I did not exist. An organism's inclusive fitness, then, is defined so that it is not affected by the r e p r o d u c t i v e success of relatives on another continent w h o m h e n e v e r meets a n d w h o m h e has n o w a y o f affecting. T h e m i s t a k e n v i e w that the inclusive fitness of an o r g a n i s m is a w e i g h t e d s u m o f t h e r e p r o d u c t i v e s u c c e s s e s o f a l l its r e l a t i v e s e v e r y w h e r e , w h o h a v e ever lived, and w h o will ever live, is extremely c o m m o n . A l t h o u g h Hamilton i s n o t r e s p o n s i b l e for t h e e r r o r s o f his f o l l o w e r s , this m a y b e o n e r e a s o n w h y m a n y p e o p l e h a v e s o m u c h difficulty d e a l i n g w i t h the c o n c e p t o f inclusive f i t n e s s , a n d i t m a y p r o v i d e a r e a s o n for a b a n d o n i n g t h e c o n c e p t a t s o m e t i m e in the future. T h e r e is y e t a fifth m e a n i n g of fitness, w h i c h was designed to a v o i d this p a r t i c u l a r d i f f i c u l t y o f i n c l u s i v e f i t n e s s , b u t w h i c h h a s difficulties o f its o w n .

An A g o n y in F i v e F i t s

187

Fit the Fifth F i t n e s s [ 5 ] i s ' p e r s o n a l fitness' i n t h e sense o f O r l o v e ( 1 9 7 5 , 1 9 7 9 ) . I t c a n b e t h o u g h t o f a s a k i n d o f b a c k w a r d s w a y o f l o o k i n g a t i n c l u s i v e fitness. W h e r e i n c l u s i v e f i t n e s s [ 4 ] f o c u s e s o n t h e effects t h e i n d i v i d u a l o f i n t e r e s t h a s o n t h e fitness[3] o f his r e l a t i v e s , p e r s o n a l fitness[5] f o c u s e s o n t h e effects t h a t t h e i n d i v i d u a l ' s r e l a t i v e s h a v e o n his f i t n e s s [ 3 ] . T h e fitness[3] o f a n i n d i v i d u a l i s s o m e m e a s u r e o f t h e n u m b e r o f his o f f s p r i n g o r d e s c e n d a n t s . B u t H a m i l t o n ' s logic has s h o w n us that we m a y e x p e c t an i n d i v i d u a l to end up w i t h m o r e offspring t h e n h e c o u l d r e a r himself, b e c a u s e his r e l a t i v e s c o n t r i b u t e t o w a r d s rearing

some

o f his

offspring.

animal's

fitness[5]

may

briefly

c h a r a c t e r i z e d a s ' t h e s a m e a s his fitness[3] b u t d o n ' t f o r g e t t h a t this m u s t i n c l u d e the e x t r a o f f s p r i n g h e g e t s a s a r e s u l t o f h e l p f r o m his r e l a t i v e s ' T h e advantage, in practice, of using personal fitness[5] over inclusive fitness[4] i s t h a t w e e n d u p s i m p l y c o u n t i n g o f f s p r i n g , a n d t h e r e i s n o risk o f a given child's being mistakenly counted m a n y times over. A g i v e n child is a p a r t o f t h e f i t n e s s [ 5 ] o f his p a r e n t s o n l y . H e p o t e n t i a l l y c o r r e s p o n d s t o a t e r m i n t h e i n c l u s i v e fitness[4] o f a n i n d e f i n i t e n u m b e r o f u n c l e s , a u n t s , c o u s i n s , etc., l e a d i n g t o a d a n g e r o f his b e i n g c o u n t e d s e v e r a l t i m e s ( G r a f e n 1 9 7 9 ; Hines & M a y n a r d Smith 1979). Inclusive fitness[4] w h e n

properly

used,

and

personal fitness[5], give

e q u i v a l e n t results. B o t h a r e m a j o r t h e o r e t i c a l a c h i e v e m e n t s a n d t h e i n v e n t o r of either of them w o u l d deserve lasting honour. It is entirely characteristic that H a m i l t o n himself q u i e t l y i n v e n t e d b o t h in the s a m e p a p e r , s w i t c h i n g from o n e t o a n o t h e r w i t h a swiftness t h a t b e w i l d e r e d a t l e a s t o n e l a t e r a u t h o r (Cassidy

1978,

581).

Hamilton's

(1964a)

name

for

fitness[5]

was

' n e i g h b o u r - m o d u l a t e d f i t n e s s ' . H e c o n s i d e r e d t h a t its u s e , t h o u g h c o r r e c t , w o u l d b e u n w i e l d y , a n d for this r e a s o n h e i n t r o d u c e d i n c l u s i v e f i t n e s s [ 4 ] a s a more manageable alternative approach. M a y n a r d Smith

(in press)

agrees

t h a t i n c l u s i v e f i t n e s s [ 4 ] i s o f t e n e a s i e r t o use t h a n n e i g h b o u r - m o d u l a t e d fitness[5], and

illustrates

the

point

working

through

particular

hypothetical e x a m p l e using both methods in turn. N o t i c e t h a t b o t h these f i t n e s s e s , l i k e ' c l a s s i c a l ' f i t n e s s [ 3 ] , a r e f i r m l y t i e d t o the i d e a o f t h e i n d i v i d u a l o r g a n i s m a s ' m a x i m i z i n g a g e n t ' . I t i s o n l y p a r t l y facetiously that I h a v e characterized inclusive fitness as 'that property of an individual organism w h i c h will a p p e a r to be m a x i m i z e d w h e n w h a t is really being maximized is gene survival' (Dawkins 1978a). ( O n e might generalize this p r i n c i p l e t o o t h e r ' v e h i c l e s ' . A g r o u p s e l e c t i o n i s t m i g h t d e f i n e his o w n v e r s i o n o f i n c l u s i v e f i t n e s s a s ' t h a t p r o p e r t y o f a group w h i c h w i l l a p p e a r t o b e maximized w h e n w h a t is really being m a x i m i z e d is gene survival'!) H i s t o r i c a l l y , i n d e e d , I see t h e c o n c e p t o f i n c l u s i v e f i t n e s s a s t h e i n s t r u m e n t of a brilliant last-ditch rescue attempt, an attempt to save the i n d i v i d u a l organism

the

level

at which

u n d e r l y i n g spirit o f H a m i l t o n ' s ( 1 9 6 4 )

think

about

natural

selection.

The

p a p e r s o n i n c l u s i v e fitness i s g e n e

An A g o n y in Five F i t s

188

selectionist. T h e brief note of 1963 w h i c h preceded them is explicitly so: ' D e s p i t e t h e p r i n c i p l e o f " s u r v i v a l o f t h e f i t t e s t " t h e u l t i m a t e c r i t e r i o n that d e t e r m i n e s w h e t h e r G will spread is not w h e t h e r the b e h a v i o r is to the b e n e f i t of t h e b e h a v e r b u t w h e t h e r it is to t h e b e n e f i t of t h e g e n e G . . .' T o g e t h e r w i t h W i l l i a m s ( 1 9 6 6 ) , H a m i l t o n could fairly be regarded as one of the

fathers

of gene

selectionism

modern

behavioural

and

ecological

studies: A g e n e i s b e i n g f a v o r e d i n n a t u r a l s e l e c t i o n i f t h e a g g r e g a t e o f its replicas forms an increasing fraction of the total g e n e pool. We are going

be concerned

with genes supposed

t o affect

the social

b e h a v i o r o f t h e i r b e a r e r s , s o let u s try t o m a k e t h e a r g u m e n t m o r e v i v i d by a t t r i b u t i n g to the genes, t e m p o r a r i l y , intelligence and a certain freedom of choice.

I m a g i n e t h a t a g e n e i s c o n s i d e r i n g the

p r o b l e m o f i n c r e a s i n g t h e n u m b e r o f its r e p l i c a s a n d i m a g i n e that i t c a n c h o o s e b e t w e e n c a u s i n g p u r e l y s e l f - i n t e r e s t e d b e h a v i o r b y its bearer

(leading

'disinterested'

behavior

more that

reproduction benefits

some

A) way

and a

causing

relative,

[Hamilton 1972]. H a v i n g m a d e use o f his i n t e l l i g e n t g e n e m o d e l , H a m i l t o n l a t e r e x p l i c i t l y a b a n d o n s i t i n f a v o u r o f the i n c l u s i v e f i t n e s s effect o f a n individual o n the p r o p a g a t i o n o f c o p i e s o f his g e n e s . I t i s p a r t o f t h e thesis o f this b o o k t h a t h e m i g h t h a v e d o n e b e t t e r t o h a v e s t u c k b y his ' i n t e l l i g e n t g e n e ' m o d e l . I f i n d i v i d u a l o r g a n i s m s c a n b e a s s u m e d t o w o r k for t h e a g g r e g a t e benefit o f all their genes, it doesn't m a t t e r w h e t h e r we think in terms of genes w o r k i n g to ensure their s u r v i v a l , or of individuals w o r k i n g to m a x i m i z e their inclusive f i t n e s s . I s u s p e c t t h a t H a m i l t o n felt m o r e c o m f o r t a b l e w i t h t h e i n d i v i d u a l a s t h e a g e n t o f b i o l o g i c a l s t r i v i n g , o r p e r h a p s h e s u r m i s e d t h a t m o s t o f his c o l l e a g u e s w e r e n o t y e t r e a d y t o a b a n d o n t h e i n d i v i d u a l a s a g e n t . B u t , o f all t h e b r i l l i a n t t h e o r e t i c a l a c h i e v e m e n t s o f H a m i l t o n a n d his f o l l o w e r s , w h i c h h a v e b e e n e x p r e s s e d i n t e r m s o f i n c l u s i v e f i t n e s s [ 4 ] (or p e r s o n a l f i t n e s s [ 5 ] ) , I c a n n o t think of a n y that could not h a v e b e e n m o r e simply derived in terms of Hamilton's (Charnov

'intelligent

gene',

manipulating

bodies

for

its

own

ends

1977).

Individual-level thinking is superficially attractive because individuals, unlike genes, h a v e nervous systems and limbs w h i c h render them capable of w o r k i n g in o b v i o u s w a y s to m a x i m i z e something. It is therefore natural to ask w h a t q u a n t i t y , in theory, they m i g h t be e x p e c t e d to m a x i m i z e , a n d i n c l u s i v e f i t n e s s i s t h e a n s w e r . B u t w h a t m a k e s this s o d a n g e r o u s i s t h a t it, too, is really a m e t a p h o r . I n d i v i d u a l s do not consciously strive to m a x i m i z e a n y t h i n g ; t h e y b e h a v e as if m a x i m i z i n g s o m e t h i n g . It is e x a c t l y the same 'as i f logic that w e a p p l y t o 'intelligent genes'. G e n e s m a n i p u l a t e the w o r l d a s i f

189

An Agony in Five Fits

striving to m a x i m i z e their o w n survival. T h e y do not really 'strive', but my p o i n t i s t h a t i n this r e s p e c t t h e y d o n o t differ f r o m i n d i v i d u a l s . N e i t h e r individuals

nor

genes

really

strive

maximize

anything.

Or,

rather,

i n d i v i d u a l s m a y s t r i v e for s o m e t h i n g , b u t i t w i l l b e a m o r s e l o f f o o d , a n attractive female, or a desirable territory, not inclusive fitness. To the extent t h a t i t i s useful for u s t o t h i n k o f i n d i v i d u a l s w o r k i n g a s i f t o m a x i m i z e fitness, we m a y , with precisely the same licence, think of genes as if they w e r e striving to m a x i m i z e their survival. T h e difference is that the q u a n t i t y the genes m a y be thought of as m a x i m i z i n g (survival of replicas) is a great deal simpler and easier to deal w i t h in models than the q u a n t i t y i n d i v i d u a l s m a y be thought of as m a x i m i z i n g

(fitness).

repeat that if we think about

individual animals m a x i m i z i n g something, there is a serious d a n g e r of our confusing ourselves,

since

m a y forget w h e t h e r w e

are

using

'as

l a n g u a g e o r w h e t h e r w e are t a l k i n g a b o u t the a n i m a l s consciously striving for s o m e g o a l .

Since no sane

biologist

could

imagine

DNA

molecules

c o n s c i o u s l y s t r i v i n g for a n y t h i n g , t h e d a n g e r o f this c o n f u s i o n o u g h t n o t t o exist w h e n w e t a l k o f g e n e s a s m a x i m i z i n g a g e n t s . It is my belief that thinking in terms of individuals striving to m a x i m i z e s o m e t h i n g has led to o u t r i g h t error, in a w a y that t h i n k i n g in terms of genes striving to m a x i m i z e something w o u l d conclusions

that

not.

their perpetrators w o u l d

admit

outright are

error,

w r o n g after

mean further

reflection. I h a v e d o c u m e n t e d these errors in the section l a b e l l e d ' C o n f u s i o n ' of Dawkins (1978a), and in Dawkins (1979a, especially Misunderstandings 5, 6, 7 and

1 1 ) . T h e s e papers g i v e detailed e x a m p l e s , from the published

literature, of errors w h i c h , I b e l i e v e , result from ' i n d i v i d u a l - l e v e l ' t h i n k i n g . T h e r e is no need to harp on them again here, and I will just give one e x a m p l e of the kind of thing I m e a n , w i t h o u t m e n t i o n i n g n a m e s , u n d e r the title o f the ' A c e o f S p a d e s F a l l a c y ' . T h e coefficient o f relationship b e t w e e n t w o relatives, say g r a n d f a t h e r a n d grandson, c a n be taken to be e q u i v a l e n t to t w o distinct q u a n t i t i e s . It is often e x p r e s s e d a s t h e m e a n fraction o f a g r a n d f a t h e r ' s g e n o m e t h a t i s e x p e c t e d t o b e i d e n t i c a l b y d e s c e n t w i t h t h a t o f the g r a n d s o n . I t i s a l s o t h e probability t h a t a n a m e d g e n e of the g r a n d f a t h e r will be identical by descent w i t h a g e n e in the g r a n d s o n . S i n c e t h e t w o a r e n u m e r i c a l l y t h e s a m e , i t m i g h t s e e m n o t t o m a t t e r w h i c h w e t h i n k i n t e r m s of. E v e n t h o u g h t h e p r o b a b i l i t y m e a s u r e i s logically m o r e a p p r o p r i a t e , it m i g h t seem that either m e a s u r e c o u l d be used for t h i n k i n g a b o u t h o w m u c h ' a l t r u i s m ' a g r a n d f a t h e r ' o u g h t ' t o d i s p e n s e t o his g r a n d s o n . I t d o e s m a t t e r , h o w e v e r , w h e n w e s t a r t t h i n k i n g a b o u t t h e v a r i a n c e as well as the m e a n . Several people h a v e pointed out that the fraction of g e n o m e o v e r l a p between parent and child is e x a c t l y e q u a l to the coefficient of relationship, w h e r e a s for a l l o t h e r r e l a t i v e s t h e c o e f f i c i e n t o f r e l a t i o n s h i p g i v e s o n l y t h e m e a n f i g u r e ; t h e a c t u a l f r a c t i o n s h a r e d m i g h t b e m o r e a n d i t m i g h t b e less.

An Agony in Five Fits

I t h a s b e e n s a i d , t h e r e f o r e , t h a t t h e c o e f f i c i e n t o f r e l a t i o n s h i p i s ' e x a c t ' for the

parent/child

relationship,

but

'probabilistic'

for

all

others.

But

this

u n i q u e n e s s of the p a r e n t / c h i l d relationship applies o n l y if we think in terms of fractions of g e n o m e s s h a r e d . If, i n s t e a d , we t h i n k in t e r m s of probabilities of sharing

particular

genes,

the

parent/child

relationship

is just

'prob-

abilistic' as a n y other. T h i s still m i g h t b e t h o u g h t n o t t o m a t t e r , a n d i n d e e d i t d o e s n o t m a t t e r u n t i l w e a r e t e m p t e d t o d r a w false c o n c l u s i o n s . O n e false c o n c l u s i o n t h a t has been d r a w n in the literature is that a parent, faced w i t h a c h o i c e b e t w e e n f e e d i n g its o w n c h i l d a n d f e e d i n g a full s i b l i n g e x a c t l y t h e s a m e a g e a s its o w n child

(and

w i t h e x a c t l y the same m e a n coefficient o f relationship),

s h o u l d f a v o u r its o w n c h i l d p u r e l y o n t h e g r o u n d s t h a t its g e n e t i c r e l a t e d n e s s is a ' s u r e t h i n g ' r a t h e r t h a n a ' g a m b l e ' . B u t it is o n l y the fraction of g e n o m e s h a r e d t h a t is a s u r e t h i n g . T h e probability t h a t a p a r t i c u l a r g e n e , in this c a s e a g e n e for a l t r u i s m , is i d e n t i c a l by d e s c e n t w i t h o n e in t h e o f f s p r i n g is j u s t as c h a n c y a s i n t h e c a s e o f t h e full s i b l i n g . I t i s n e x t t e m p t i n g t o t h i n k t h a t a n a n i m a l m i g h t try t o use c u e s t o estimate w h e t h e r a particular relative happens to share m a n y genes with itself or

not.

The

reasoning

conveniently

expressed

the

currently

fashionable style of subjective m e t a p h o r : ' A l l my brothers share, on average, h a l f m y g e n o m e , b u t s o m e o f m y brothers share m o r e than half a n d others less t h a n half. I f I c o u l d w o r k o u t w h i c h o n e s s h a r e m o r e t h a n half, I c o u l d s h o w favouritism towards them, a n d thereby benefit my genes. Brother A resembles me in hair colour, eye c o l o u r and several other features, whereas b r o t h e r B h a r d l y resembles me at all. T h e r e f o r e A p r o b a b l y shares more g e n e s w i t h m e . T h e r e f o r e I s h a l l feed A i n p r e f e r e n c e t o B . ' T h a t soliloquy was supposed to be spoken by an individual animal. T h e f a l l a c y i s q u i c k l y s e e n w h e n w e c o m p o s e a s i m i l a r s o l i l o q u y , this t i m e t o b e s p o k e n b y o n e o f H a m i l t o n ' s ' i n t e l l i g e n t ' genes, a g e n e ' f o r ' f e e d i n g b r o t h e r s : ' B r o t h e r A has c l e a r l y inherited my g e n e c o l l e a g u e s from the hair-colour d e p a r t m e n t a n d from the eye-colour department, but w h a t do I care about t h e m ? T h e g r e a t q u e s t i o n is, h a s A o r B i n h e r i t e d a c o p y o f me? H a i r c o l o u r a n d e y e c o l o u r tell m e n o t h i n g a b o u t t h a t u n l e s s I h a p p e n t o b e l i n k e d t o t h o s e o t h e r g e n e s . ' L i n k a g e is, t h e n , i m p o r t a n t h e r e , b u t i t i s j u s t a s i m p o r t a n t for t h e ' d e t e r m i n i s t i c ' p a r e n t / o f f s p r i n g r e l a t i o n s h i p a s for a n y ' p r o b a b i l i s t i c ' relationship. T h e fallacy i s c a l l e d the A c e o f S p a d e s F a l l a c y b e c a u s e o f the following analogy. Suppose it is important to me to know whether your hand of thirteen cards contains the ace of spades. If I am given no information, I k n o w that the o d d s are thirteen in fifty-two, or one in four, that y o u h a v e the a c e . T h i s is my first guess as to the p r o b a b i l i t y . If s o m e b o d y whispers to me that y o u h a v e a v e r y strong h a n d in spades, I w o u l d be justified in revising u p w a r d s my initial estimate of the p r o b a b i l i t y that y o u h a v e the a c e . If I am

An A g o n y in F i v e Fit:

191

told t h a t y o u h a v e t h e k i n g , q u e e n , j a c k , 1 0 , 8 , 6 , 5 , 4 , 3 a n d 2 , I w o u l d b e correct in c o n c l u d i n g that y o u h a v e a very strong h a n d in spades. But, so l o n g as the d e a l w a s honest, I w o u l d be a m u g if I therefore p l a c e d a bet on your h a v i n g the a c e ! ( A c t u a l l y the a n a l o g y is a bit unfair here, b e c a u s e the odds of y o u r h a v i n g the a c e are n o w three in f o r t y - t w o , substantially l o w e r t h a n t h e p r i o r o d d s o f o n e i n four.) I n t h e b i o l o g i c a l c a s e w e m a y a s s u m e t h a t , l i n k a g e a s i d e , k n o w l e d g e o f a b r o t h e r ' s e y e c o l o u r tells u s n o t h i n g , o n e w a y o r t h e o t h e r , a b o u t w h e t h e r h e s h a r e s a p a r t i c u l a r g e n e for b r o t h e r l y altruism. T h e r e is no reason to suppose that the theorists w h o h a v e p e r p e t r a t e d the biological versions o f the A c e o f S p a d e s F a l l a c y are b a d g a m b l e r s . I t w a s n ' t their p r o b a b i l i t y theory they g o t w r o n g , but their b i o l o g i c a l a s s u m p t i o n s . In particular, they assumed that an individual o r g a n i s m , as a coherent entity, w o r k s o n b e h a l f o f c o p i e s o f a l l t h e g e n e s i n s i d e it. I t w a s a s i f a n a n i m a l ' c a r e d ' a b o u t t h e s u r v i v a l o f c o p i e s o f its e y e - c o l o u r g e n e s , h a i r - c o l o u r g e n e s , e t c . I t i s b e t t e r t o a s s u m e t h a t o n l y g e n e s 'for c a r i n g ' c a r e , a n d t h e y o n l y c a r e about copies of themselves. I m u s t stress t h a t I

a m n o t s u g g e s t i n g t h a t e r r o r s o f this k i n d f o l l o w

i n e v i t a b l y from t h e i n c l u s i v e fitness a p p r o a c h . W h a t I d o s u g g e s t i s t h a t t h e y a r e t r a p s for the u n w a r y t h i n k e r a b o u t i n d i v i d u a l - l e v e l m a x i m i z a t i o n , w h i l e they

present

danger

the

thinker about

gene-level

maximization,

h o w e v e r u n w a r y . E v e n H a m i l t o n has m a d e a n error, afterwards pointed out b y himself, w h i c h I a t t r i b u t e t o i n d i v i d u a l - l e v e l t h i n k i n g . T h e p r o b l e m arises i n H a m i l t o n ' s c a l c u l a t i o n o f c o e f f i c i e n t s o f r e l a t i o n ship, r, in h y m e n o p t e r a n families. As is n o w well k n o w n , he m a d e brilliant use o f t h e o d d r v a l u e s r e s u l t i n g f r o m the h a p l o d i p l o i d s e x - d e t e r m i n i n g s y s t e m o f H y m e n o p t e r a , n o t a b l y t h e c u r i o u s f a c t t h a t r b e t w e e n sisters i s ¾ . But consider the relationship b e t w e e n a female a n d her father. O n e h a l f of the f e m a l e ' s g e n o m e i s i d e n t i c a l b y d e s c e n t w i t h t h a t o f h e r f a t h e r : t h e ' o v e r l a p ' o f h e r g e n o m e w i t h his i s ½ , a n d H a m i l t o n c o r r e c t l y g a v e ½ a s t h e coefficient o f r e l a t i o n s h i p b e t w e e n a f e m a l e a n d h e r f a t h e r . T h e t r o u b l e comes w h e n we look at the same relationship the other w a y r o u n d . W h a t is the

coefficient

of relationship

between

male

and

his

daughter?

One

n a t u r a l l y e x p e c t s it to be r e f l e x i v e , ½ a g a i n , b u t t h e r e is a d i f f i c u l t y . S i n c e a m a l e i s h a p l o i d , h e h a s h a l f a s m a n y g e n e s a s his d a u g h t e r i n t o t a l . H o w , then, c a n w e c a l c u l a t e the ' o v e r l a p ' , the fraction o f genes s h a r e d ? D o w e say that

the m a l e ' s g e n o m e o v e r l a p s w i t h

h a l f his d a u g h t e r ' s g e n o m e ,

and

therefore that r is ½? Or do we say that e v e r y single o n e of the m a l e ' s genes w i l l be f o u n d in his d a u g h t e r , a n d t h e r e f o r e r is 1 ? H a m i l t o n o r i g i n a l l y g a v e ½ a s t h e f i g u r e , t h e n i n 1 9 7 1 c h a n g e d his m i n d and g a v e 1. In 1964 he h a d tried to solve the difficulty of h o w to c a l c u l a t e an o v e r l a p b e t w e e n a h a p l o i d a n d a diploid g e n o t y p e by arbitrarily treating the male as a kind of h o n o r a r y diploid. ' T h e relationships c o n c e r n i n g males are

192 An

Agony

Five

Fits

w o r k e d o u t b y a s s u m i n g e a c h m a l e t o c a r r y a " c i p h e r " g e n e t o m a k e u p his diploid pair, one " c i p h e r " never being considered identical by descent with a n o t h e r ' ( H a m i l t o n 1 9 6 4 b ) . A t t h e t i m e , h e r e c o g n i z e d t h a t this p r o c e d u r e was

'arbitrary

the

sense

that

some

other

value

for

the

fundamental

m o t h e r - s o n a n d f a t h e r - d a u g h t e r link w o u l d h a v e g i v e n a n e q u a l l y coherent s y s t e m ' . H e l a t e r p r o n o u n c e d this m e t h o d o f c a l c u l a t i o n p o s i t i v e l y e r r o n e o u s a n d , i n a n a p p e n d i x a d d e d t o a r e p r i n t i n g o f his c l a s s i c p a p e r , g a v e the c o r r e c t r u l e s for c a l c u l a t i n g r i n h a p l o d i p l o i d s y s t e m s ( H a m i l t o n 1 9 7 1 b ) . H i s r e v i s e d m e t h o d o f c a l c u l a t i o n g i v e s r b e t w e e n a m a l e a n d his d a u g h t e r a s 1 ( n o t ½), a n d r b e t w e e n a m a l e a n d his b r o t h e r as ½ (not ¼). C r o z i e r ( 1 9 7 0 ) i n d e p e n d e n t l y c o r r e c t e d the error. T h e p r o b l e m w o u l d never h a v e arisen, and n o arbitrary 'honorary diploid' m e t h o d w o u l d h a v e b e e n c a l l e d for, h a d w e a l l a l o n g t h o u g h t i n t e r m s o f selfish

genes

maximizing

their

survival

rather

than

terms

o f selfish

i n d i v i d u a l s m a x i m i z i n g t h e i r i n c l u s i v e fitness. C o n s i d e r a n ' i n t e l l i g e n t g e n e ' sitting in

the b o d y of a m a l e h y m e n o p t e r a n ,

'contemplating'

an act of

a l t r u i s m t o w a r d s a d a u g h t e r . I t k n o w s for c e r t a i n t h a t t h e d a u g h t e r ' s b o d y c o n t a i n s a c o p y o f itself. I t d o e s n o t ' c a r e ' t h a t h e r g e n o m e c o n t a i n s t w i c e a s m a n y g e n e s a s its p r e s e n t , m a l e , b o d y .

It ignores the other half of her

genome,

when

secure

the

knowledge

that

the

daughter

reproduces,

m a k i n g g r a n d c h i l d r e n for t h e p r e s e n t m a l e , it, t h e i n t e l l i g e n t g e n e itself, h a s a 50 per cent c h a n c e of getting into e a c h grandchild. To the intelligent gene in a h a p l o i d m a l e , a g r a n d c h i l d is as v a l u a b l e as an o r d i n a r y offspring w o u l d be in a n o r m a l d i p l o i d system. By the s a m e token, a d a u g h t e r is twice as v a l u a b l e a s a d a u g h t e r w o u l d b e i n a n o r m a l d i p l o i d s y s t e m . F r o m the intelligent g e n e ' s p o i n t of v i e w , the coefficient of relationship b e t w e e n father and d a u g h t e r is i n d e e d 1, not ½. N o w look a t the relationship the other w a y r o u n d . T h e intelligent gene a g r e e s w i t h H a m i l t o n ' s o r i g i n a l f i g u r e o f ½ for t h e c o e f f i c i e n t o f r e l a t i o n s h i p b e t w e e n a f e m a l e h y m e n o p t e r a n a n d h e r f a t h e r . A g e n e sits in a f e m a l e a n d c o n t e m p l a t e s an act of altruism t o w a r d s the father of that female. It k n o w s t h a t i t h a s a n e q u a l c h a n c e o f h a v i n g c o m e from t h e f a t h e r o r from t h e m o t h e r o f t h e f e m a l e i n w h i c h i t sits. F r o m its p o i n t o f v i e w , t h e n , t h e c o e f f i c i e n t o f r e l a t i o n s h i p b e t w e e n its p r e s e n t b o d y a n d e i t h e r o f t h e t w o p a r e n t b o d i e s is A, T h e s a m e k i n d o f r e a s o n i n g l e a d s t o a n a n a l o g o u s n o n - r e f l e x i v e n e s s i n the b r o t h e r - s i s t e r r e l a t i o n s h i p . A g e n e in a f e m a l e sees a sister as h a v i n g ¾ of a c h a n c e o f c o n t a i n i n g itself, a n d a b r o t h e r a s h a v i n g ¼ o f a c h a n c e o f c o n t a i n i n g itself. A g e n e i n a m a l e , h o w e v e r , l o o k s a t t h e sister o f t h a t m a l e a n d sees t h a t s h e h a s ½ a c h a n c e of c o n t a i n i n g a c o p y of itself, n o t ¼ as Hamilton's original cipher gene ('honorary diploid') method gave. I b e l i e v e i t w i l l b e a d m i t t e d t h a t h a d H a m i l t o n u s e d his o w n ' i n t e l l i g e n t g e n e ' t h o u g h t e x p e r i m e n t w h e n c a l c u l a t i n g these c o e f f i c i e n t s o f r e l a t i o n s h i p ,

An Agony in Five Fits

193

i n s t e a d o f t h i n k i n g i n t e r m s o f individuals a s a g e n t s m a x i m i z i n g s o m e t h i n g , h e w o u l d h a v e g o t t h e r i g h t a n s w e r t h e first t i m e .

If these errors h a d b e e n

simple miscalculations it w o u l d obviously be p e d a n t i c to discuss t h e m , o n c e their original a u t h o r h a d p o i n t e d t h e m out. B u t they w e r e n o t m i s c a l c u lations, they w e r e based on a h i g h l y instructive c o n c e p t u a l error. T h e s a m e is true o f the n u m b e r e d ' M i s u n d e r s t a n d i n g s o f K i n S e l e c t i o n ' t h a t I q u o t e d before. I h a v e tried

to s h o w in

this c h a p t e r t h a t t h e c o n c e p t of fitness as a

technical term is a confusing o n e . It is confusing b e c a u s e it c a n l e a d to admitted

error,

the

case

of Hamilton's

original

calculation

h a p l o d i p l o i d coefficients o f r e l a t i o n s h i p , a n d a s i n t h e c a s e o f s e v e r a l o f m y '12 Misunderstandings of K i n Selection'. It is confusing because it can lead philosophers to think the w h o l e theory of n a t u r a l selection is a t a u t o l o g y . A n d i t i s c o n f u s i n g e v e n t o b i o l o g i s t s b e c a u s e i t h a s b e e n u s e d i n a t least five different senses, m a n y o f w h i c h h a v e b e e n m i s t a k e n for a t l e a s t o n e o f t h e others. Emerson, as we h a v e seen, confused fitness[3] w i t h fitness[1]. I n o w g i v e an

example

of a

confusion

o f fitness[3]

with

fitness[2].

Wilson

(1975)

p r o v i d e s a useful g l o s s a r y o f t e r m s n e e d e d b y s o c i o b i o l o g i s t s . U n d e r 'fitness' h e refers u s t o ' g e n e t i c f i t n e s s ' . W e t u r n t o ' g e n e t i c f i t n e s s ' a n d find i t d e f i n e d as ' T h e contribution to the next g e n e r a t i o n of o n e g e n o t y p e in a p o p u l a t i o n relative to the contributions of other g e n o t y p e s . ' E v i d e n t l y 'fitness' is b e i n g used i n the sense o f t h e p o p u l a t i o n g e n e t i c i s t ' s f i t n e s s [ 2 ] . B u t t h e n , i f w e l o o k u p ' i n c l u s i v e f i t n e s s ' i n the g l o s s a r y w e f i n d : ' T h e s u m o f a n i n d i v i d u a l ' s o w n f i t n e s s p l u s a l l its i n f l u e n c e o n f i t n e s s i n its r e l a t i v e s o t h e r t h a n d i r e c t descendants . . . '

Here,

f i t n e s s [ 3 ] (since

'the

individual's

applied

o w n fitness' must

individuals),

not

the

'classical'

g e n o t y p i c fitness

(fitness[2]) w h i c h i s t h e o n l y 'fitness' d e f i n e d i n t h e g l o s s a r y . T h e g l o s s a r y is, then, i n c o m p l e t e , a p p a r e n t l y because of a confusion b e t w e e n fitness of a g e n o t y p e a t a l o c u s (fitness[2])

and r e p r o d u c t i v e success of an i n d i v i d u a l

(fitness [ 3 ] ) . A s i f m y f i v e f o l d list w e r e n o t c o n f u s i n g e n o u g h a l r e a d y , i t m a y n e e d extending. For reasons concerned w i t h an interest in b i o l o g i c a l 'progress', Thoday

(1953)

seeks t h e 'fitness' o f a l o n g - t e r m l i n e a g e , d e f i n e d a s t h e

p r o b a b i l i t y t h a t t h e l i n e a g e w i l l c o n t i n u e for a v e r y l o n g t i m e s u c h a s 1 0

generations, and contributed to by such 'biotic' factors ( W i l l i a m s 1966) as ' g e n e t i c f l e x i b i l i t y ' . T h o d a y ' s f i t n e s s d o e s n o t c o r r e s p o n d t o a n y o f m y list o f five. T h e n a g a i n , the fitness[2] of p o p u l a t i o n geneticists is a d m i r a b l y c l e a r a n d useful, b u t m a n y p o p u l a t i o n g e n e t i c i s t s a r e , for r e a s o n s b e s t k n o w n t o themselves, very interested in another q u a n t i t y w h i c h is called the m e a n f i t n e s s o f a p o p u l a t i o n . W i t h i n the g e n e r a l c o n c e p t o f ' i n d i v i d u a l f i t n e s s ' , Brown ( 1 9 7 5 ; B r o w n & B r o w n 1981) wishes to m a k e a distinction b e t w e e n 'direct fitness' and 'indirect fitness'. D i r e c t fitness is the same as w h a t I am

194

An A g o n y in F i v e F i t s

c a l l i n g fitness[3].

I n d i r e c t fitness c a n b e c h a r a c t e r i z e d a s s o m e t h i n g like

f i t n e s s [ 4 ] m i n u s fitness[3], i.e. t h e c o m p o n e n t o f i n c l u s i v e fitness t h a t results from the r e p r o d u c t i o n of collateral relatives as opposed to direct descendants (I

presume

grandchildren

count

the

direct

component,

though

the

decision is a r b i t r a r y ) . B r o w n himself is clear a b o u t the m e a n i n g of the terms, b u t I believe they h a v e considerable p o w e r to confuse. For instance, they a p p e a r to lend w e i g h t to the v i e w (not held by B r o w n , but held by a distressing n u m b e r of other authors, e.g. G r a n t 1978, and several writers on 'helpers at the nest' in birds) that there is s o m e t h i n g u n p a r s i m o n i o u s about 'kin selection' selection'

(the

'indirect component')

'direct

component'),

as compared with view

which

'individual

have

criticized

sufficiently before ( D a w k i n s 1 9 7 6 a , 1978a, 1 9 7 9 a ) . T h e r e a d e r m a y h a v e b e e n b e w i l d e r e d a n d i r r i t a t e d a t m y d r a w n o u t list o f f i v e o r m o r e s e p a r a t e m e a n i n g s o f f i t n e s s . I h a v e f o u n d this a p a i n f u l c h a p t e r to write, a n d I am a w a r e that it will not h a v e been easy to read. It m a y b e t h e last r e s o r t o f a p o o r w r i t e r t o b l a m e his s u b j e c t m a t t e r , b u t I r e a l l y d o b e l i e v e i t i s t h e c o n c e p t o f f i t n e s s i t s e l f w h i c h i s r e s p o n s i b l e for the a g o n y i n this c a s e . T h e p o p u l a t i o n g e n e t i c i s t s ' f i t n e s s [ 2 ] a s i d e , the c o n c e p t o f fitness as a p p l i e d to i n d i v i d u a l organisms has b e c o m e forced and contrived. Before

Hamilton's

revolution,

our

world

was

peopled

individual

organisms w o r k i n g single-mindedly to keep themselves alive and to have c h i l d r e n . I n t h o s e d a y s i t w a s n a t u r a l t o m e a s u r e s u c c e s s i n this u n d e r t a k i n g at the level of the individual organism.

H a m i l t o n c h a n g e d all t h a t b u t

unfortunately,

ideas

conclusion

instead

and

of following

sweeping

the

his

individual

through

organism

from

to its

their

logical

pedestal

n o t i o n a l a g e n t o f m a x i m i z a t i o n , h e e x e r t e d his g e n i u s i n d e v i s i n g a m e a n s o f r e s c u i n g the i n d i v i d u a l . He c o u l d h a v e persisted in s a y i n g : g e n e survival is w h a t m a t t e r s ; let us e x a m i n e w h a t a g e n e w o u l d h a v e to do in order to p r o p a g a t e c o p i e s o f itself. I n s t e a d h e , i n effect, s a i d : g e n e s u r v i v a l i s w h a t matters; w h a t is the m i n i m u m c h a n g e we h a v e to m a k e to our old v i e w of w h a t i n d i v i d u a l s m u s t d o , i n o r d e r t h a t w e m a y c l i n g o n t o o u r i d e a o f the individual

the

unit

action?

The

resultâ&#x20AC;&#x201D;inclusive fitnessâ&#x20AC;&#x201D;was

t e c h n i c a l l y correct, but c o m p l i c a t e d a n d easy to misunderstand. I shall avoid m e n t i o n i n g f i t n e s s a g a i n i n this b o o k , w h i c h I trust w i l l m a k e for easier reading.

The

p h e n o t y p e itself.

three

chapters

develop

the

theory

o f the

extended

11 T h e Genetical Evolution of A n i m a l Artefacts

W h a t do we really m e a n by the p h e n o t y p i c

effect o f a g e n e ?

smattering of molecular biology m a y suggest one kind of answer. E a c h gene c o d e s for t h e s y n t h e s i s o f o n e p r o t e i n c h a i n . I n a p r o x i m a l sense t h a t p r o t e i n i s its p h e n o t y p i c effect. M o r e d i s t a l effects l i k e e y e c o l o u r o r b e h a v i o u r a r e , i n t h e i r t u r n , effects o f t h e p r o t e i n f u n c t i o n i n g a s a n e n z y m e . S u c h a s i m p l e a c c o u n t does not, h o w e v e r , b e a r m u c h s e a r c h i n g analysis. T h e 'effect' o f a n y would-be cause can be g i v e n m e a n i n g only in terms of a c o m p a r i s o n , e v e n if o n l y a n i m p l i e d c o m p a r i s o n , w i t h a t least o n e a l t e r n a t i v e c a u s e . I t i s s t r i c t l y i n c o m p l e t e t o s p e a k o f b l u e e y e s a s ' t h e effect' o f a g i v e n g e n e G 1 . I f w e s a y such

thing,

really

imply

the

potential

existence

of at

least

one

a l t e r n a t i v e a l l e l e , c a l l i t G2, a n d a t least o n e a l t e r n a t i v e p h e n o t y p e , P 2 , i n this c a s e , s a y , b r o w n e y e s . I m p l i c i t l y w e a r e m a k i n g a s t a t e m e n t a b o u t a r e l a t i o n b e t w e e n a p a i r of g e n e s {G1, G2} a n d a p a i r of d i s t i n g u i s h a b l e phenotypes { P 1 , P2}, in an environment w h i c h either is constant or varies in a

non-systematic

way

that

its

contribution

randomizes

out.

' E n v i r o n m e n t ' , i n t h a t last c l a u s e , i s t a k e n t o i n c l u d e a l l t h e g e n e s a t o t h e r loci t h a t m u s t

b e p r e s e n t i n o r d e r for

be expressed.

Our

s t a t e m e n t is t h a t t h e r e is a s t a t i s t i c a l t e n d e n c y for i n d i v i d u a l s w i t h G1 to be more likely than individuals with G2 to show P1 (rather than P 2 ) . Of course t h e r e is no n e e d to d e m a n d t h a t P1 s h o u l d always be a s s o c i a t e d w i t h G1, n o r that G1 should a l w a y s lead to P1: in the real w o r l d outside l o g i c textbooks, the s i m p l e c o n c e p t s o f ' n e c e s s a r y ' a n d ' s u f f i c i e n t ' m u s t u s u a l l y b e r e p l a c e d b y statistical e q u i v a l e n t s . S u c h an insistence that p h e n o t y p e s are not caused by g e n e s , b u t o n l y p h e n o t y p i c differences c a u s e d b y g e n e d i f f e r e n c e s ( J e n s e n 1 9 6 1 ; H i n d e 1 9 7 5 ) m a y seem to w e a k e n the c o n c e p t of genetic d e t e r m i n a t i o n to the point w h e r e i t ceases t o b e i n t e r e s t i n g . T h i s i s far f r o m t h e c a s e , a t l e a s t i f t h e s u b j e c t o f o u r interest i s n a t u r a l s e l e c t i o n , b e c a u s e n a t u r a l s e l e c t i o n t o o i s c o n c e r n e d w i t h differences ( C h a p t e r 2 ) . N a t u r a l s e l e c t i o n i s t h e p r o c e s s b y w h i c h s o m e alleles o u t - p r o p a g a t e t h e i r a l t e r n a t i v e s , a n d t h e i n s t r u m e n t s b y w h i c h t h e y 195

196

T h e Genetical Evolution of A n i m a l Artefacts

a c h i e v e this a r e t h e i r p h e n o t y p i c effects. I t f o l l o w s t h a t p h e n o t y p i c effects c a n a l w a y s b e t h o u g h t o f a s relative t o a l t e r n a t i v e p h e n o t y p i c effects. It is c u s t o m a r y to speak as if differences a l w a y s m e a n differences b e t w e e n i n d i v i d u a l bodies or other discrete 'vehicles'. T h e purpose of the next three chapters is to s h o w that we c a n e m a n c i p a t e the c o n c e p t of the p h e n o t y p i c d i f f e r e n c e f r o m t h a t o f t h e d i s c r e t e v e h i c l e a l t o g e t h e r , a n d this i s t h e m e a n i n g o f t h e title ' e x t e n d e d p h e n o t y p e ' . I s h a l l s h o w t h a t t h e o r d i n a r y l o g i c o f g e n e t i c t e r m i n o l o g y leads i n e v i t a b l y to the c o n c l u s i o n that genes c a n be said t o h a v e extended p h e n o t y p i c effects, effects w h i c h n e e d n o t b e e x p r e s s e d a t the level of a n y particular v e h i c l e . F o l l o w i n g an earlier paper ( D a w k i n s 1978a) I shall take a step-by-step a p p r o a c h to the e x t e n d e d p h e n o t y p e , b e g i n n i n g w i t h c o n v e n t i o n a l e x a m p l e s o f ' o r d i n a r y ' p h e n o t y p i c effects a n d g r a d u a l l y e x t e n d i n g t h e c o n c e p t o f t h e p h e n o t y p e o u t w a r d s s o t h a t the c o n t i n u i t y i s easy to a c c e p t . T h e i d e a of the genetic d e t e r m i n a t i o n of a n i m a l artefacts is a d i d a c t i c a l l y useful i n t e r m e d i a t e e x a m p l e , a n d this w i l l b e t h e m a i n t o p i c o f this c h a p t e r . B u t first, c o n s i d e r a g e n e A w h o s e i m m e d i a t e m o l e c u l a r effect is the s y n t h e s i s o f a b l a c k p r o t e i n w h i c h d i r e c t l y c o l o u r s t h e skin o f a n a n i m a l b l a c k . T h e n t h e g e n e ' s o n l y p r o x i m a l effect, i n t h e m o l e c u l a r b i o l o g i s t ' s s i m p l e s e n s e , is t h e s y n t h e s i s of this o n e b l a c k p r o t e i n . B u t is A a g e n e 'for b e i n g b l a c k ' ? T h e point I w a n t to m a k e is that, as a matter of definition, that d e p e n d s o n h o w t h e p o p u l a t i o n v a r i e s . A s s u m e t h a t A h a s a n a l l e l e A', w h i c h fails t o s y n t h e s i z e t h e b l a c k p i g m e n t , s o t h a t i n d i v i d u a l s h o m o z y g o u s for A ' t e n d t o b e w h i t e . I n this c a s e A i s t r u l y a g e n e ' f o r ' b e i n g b l a c k , i n t h e sense i n w h i c h I w i s h t o use t h e p h r a s e . B u t i t m a y a l t e r n a t i v e l y b e t h a t a l l the v a r i a t i o n in skin c o l o u r that a c t u a l l y occurs in the p o p u l a t i o n is d u e to v a r i a t i o n at a q u i t e d i f f e r e n t l o c u s , B. B's i m m e d i a t e b i o c h e m i c a l effect is t h e synthesis of a protein w h i c h is not a b l a c k p i g m e n t , but w h i c h acts as an e n z y m e , o n e o f w h o s e i n d i r e c t effects (in c o m p a r i s o n w i t h its a l l e l e B'), a t s o m e distant r e m o v e , is the facilitation of the synthesis by A of the black p i g m e n t in skin cells. To be sure, A, the g e n e w h o s e protein p r o d u c t is the b l a c k pigment, is n e c e s s a r y i n o r d e r for a n i n d i v i d u a l t o b e b l a c k : s o a r e t h o u s a n d s o f o t h e r g e n e s , i f o n l y b e c a u s e t h e y a r e n e c e s s a r y t o m a k e t h e i n d i v i d u a l exist a t a l l . B u t I s h a l l n o t c a l l A a g e n e for b l a c k n e s s u n l e s s s o m e of t h e v a r i a t i o n in the p o p u l a t i o n i s d u e t o l a c k o f A . I f a l l i n d i v i d u a l s , w i t h o u t fail, h a v e A , a n d t h e o n l y reason individuals are not b l a c k is that they h a v e B' rather than B, we s h a l l s a y t h a t B, b u t n o t A, is a g e n e for b l a c k n e s s . If t h e r e is v a r i a t i o n at b o t h l o c i a f f e c t i n g b l a c k n e s s , w e s h a l l refer t o b o t h A a n d B a s g e n e s for blackness. T h e point that is r e l e v a n t here is that both A a n d B are potentially e n t i t l e d t o b e c a l l e d g e n e s for b l a c k n e s s , d e p e n d i n g o n t h e a l t e r n a t i v e s t h a t exist in the p o p u l a t i o n . T h e fact that the causal c h a i n linking A to the p r o d u c t i o n o f t h e b l a c k p i g m e n t m o l e c u l e i s s h o r t , w h i l e t h a t for B i s l o n g

The Genetical Evolution of A n i m a l Artefacts

197

a n d t o r t u o u s , i s i r r e l e v a n t . M o s t g e n e effects s e e n b y w h o l e a n i m a l b i o l o g i s t s , a n d all t h o s e s e e n b y e t h o l o g i s t s , a r e l o n g a n d t o r t u o u s . A geneticist c o l l e a g u e has a r g u e d that there are virtually no b e h a v i o u r g e n e t i c traits, b e c a u s e a l l t h o s e so-far d i s c o v e r e d h a v e t u r n e d o u t t o b e ' b y p r o d u c t s ' o f m o r e f u n d a m e n t a l m o r p h o l o g i c a l o r p h y s i o l o g i c a l effects. But

what

physiological

earth or

does

think

behavioural,

any

if not

genetic

trait

'byproduct'

is,

morphological,

of something

f u n d a m e n t a l ? I f w e t h i n k t h e m a t t e r t h r o u g h w e find t h a t a l l g e n e t i c effects are ' b y p r o d u c t s ' e x c e p t protein molecules. R e t u r n i n g t o the b l a c k skin e x a m p l e , i t i s e v e n p o s s i b l e t h a t the c h a i n o f c a u s a t i o n l i n k i n g a g e n e s u c h a s B t o its b l a c k - s k i n n e d p h e n o t y p e m i g h t involve a b e h a v i o u r a l link. S u p p o s e that A c a n synthesize b l a c k p i g m e n t only in

the presence of sunlight,

and suppose

that B works

making

i n d i v i d u a l s seek s u n l i g h t , i n c o m p a r i s o n w i t h B ' w h i c h m a k e s t h e m s e e k shade. B individuals will then tend to be b l a c k e r than B' individuals, b e c a u s e they spend m o r e time in

t h e s u n . B i s still,

by existing t e r m i n o l o g i c a l

c o n v e n t i o n , a g e n e 'for b l a c k n e s s ' , n o less t h a n i t w o u l d b e i f its c a u s a l c h a i n involved internal biochemistry only, rather than an 'external' behavioural loop. I n d e e d , a geneticist in the p u r e sense of the w o r d n e e d not c a r e a b o u t the d e t a i l e d p a t h w a y f r o m g e n e t o p h e n o t y p i c effect. S t r i c t l y s p e a k i n g , a geneticist w h o concerns h i m s e l f w i t h these interesting matters is t e m p o r a r i l y w e a r i n g the h a t o f a n e m b r y o l o g i s t . T h e p u r e g e n e t i c i s t i s c o n c e r n e d w i t h e n d p r o d u c t s , a n d i n p a r t i c u l a r w i t h d i f f e r e n c e s b e t w e e n a l l e l e s i n t h e i r effects o n e n d p r o d u c t s . N a t u r a l s e l e c t i o n ' s c o n c e r n s a r e p r e c i s e l y t h e s a m e , for natural

selection

'works

outcomes'

(Lehrman

1970).

The

interim

c o n c l u s i o n i s t h a t w e a r e a l r e a d y a c c u s t o m e d t o p h e n o t y p i c effects b e i n g attached to their genes by long and devious chains of causal connection, therefore

further

extensions

overstretch our credulity. further

extension,

the

concept

phenotype

should

not

T h i s c h a p t e r t a k e s t h e first s t e p t o w a r d s s u c h

looking

animal

artefacts

examples

of the

phenotypic expression of genes. T h e fascinating subject of a n i m a l artefacts is r e v i e w e d by Hansell press).

shows

that

artefacts

provide

useful

case

studies

for

(in

several

p r i n c i p l e s o f g e n e r a l e t h o l o g i c a l i m p o r t a n c e . T h i s c h a p t e r uses t h e e x a m p l e o f artefacts in the service of e x p l a i n i n g a n o t h e r p r i n c i p l e , that of the e x t e n d e d phenotype. C o n s i d e r a h y p o t h e t i c a l species of caddis-fly w h o s e larvae build houses out of stones w h i c h t h e y select from those a v a i l a b l e on the b o t t o m of the s t r e a m . distinct

colours

might

observe

of house,

dark

that

the

and

light.

population By

contains

breeding

two

rather

experiments

establish that the c h a r a c t e r s 'dark house' a n d 'light h o u s e ' b r e e d true in some simple house.

M e n d e l i a n fashion, say w i t h d a r k house d o m i n a n t to light

principle

recombination

data,

ought where

to the

possible

genes

for

discover,

house

colour

by sit

analysing on

the

198

T h e Genetical Evolution of A n i m a l Artefacts

c h r o m o s o m e s . T h i s is, o f c o u r s e , h y p o t h e t i c a l . I d o n o t k n o w o f a n y g e n e t i c w o r k o n c a d d i s h o u s e s , a n d i t w o u l d b e difficult t o d o b e c a u s e a d u l t s a r e difficult t o b r e e d i n c a p t i v i t y ( M . H . H a n s e l l , personal c o m m u n i c a t i o n ) . But m y p o i n t i s t h a t , i f t h e p r a c t i c a l difficulties c o u l d b e o v e r c o m e , n o b o d y would

very

surprised

if house

colour did

turn

out

simple

Mendelian character in accordance with my thought experiment. (Actually, c o l o u r is a slightly unfortunate e x a m p l e to h a v e chosen, since c a d d i s vision is p o o r a n d they a l m o s t c e r t a i n l y ignore visual cues in c h o o s i n g stones. R a t h e r t h a n use a m o r e r e a l i s t i c e x a m p l e l i k e s t o n e s h a p e ( H a n s e l l ) , I s t a y w i t h c o l o u r for t h e s a k e o f t h e a n a l o g y w i t h t h e b l a c k p i g m e n t d i s c u s s e d a b o v e . ) T h e i n t e r e s t i n g s e q u e l i s this. H o u s e c o l o u r i s d e t e r m i n e d b y t h e c o l o u r o f the stones c h o s e n from the stream bed by the l a r v a , not by the b i o c h e m i c a l synthesis of a b l a c k p i g m e n t . T h e genes d e t e r m i n i n g house colour must work v i a t h e b e h a v i o u r a l m e c h a n i s m t h a t c h o o s e s s t o n e s , p e r h a p s v i a the e y e s . S o m u c h w o u l d b e a g r e e d b y a n y e t h o l o g i s t . A l l t h a t this c h a p t e r a d d s i s a logical

point:

once we have accepted

that

t h e r e a r e g e n e s for b u i l d i n g

b e h a v i o u r , t h e r u l e s o f e x i s t i n g t e r m i n o l o g y i m p l y t h a t t h e a r t e f a c t itself should be treated as part of the p h e n o t y p i c expression of genes in the a n i m a l . T h e stones are outside the b o d y of the o r g a n i s m , yet l o g i c a l l y such a g e n e is a g e n e ' f o r ' h o u s e c o l o u r , i n e x a c t l y a s s t r o n g a sense a s t h e h y p o t h e t i c a l g e n e B w a s for s k i n c o l o u r . A n d B w a s i n d e e d a g e n e for skin c o l o u r , e v e n t h o u g h i t w o r k e d b y m e d i a t i n g s u n - s e e k i n g b e h a v i o u r , i n e x a c t l y a s s t r o n g a sense a s a g e n e ' f o r ' a l b i n i s m i s c a l l e d a g e n e for s k i n c o l o u r . T h e l o g i c i s i d e n t i c a l i n all three cases. We h a v e taken the first step in e x t e n d i n g the c o n c e p t of a g e n e ' s p h e n o t y p i c effect o u t s i d e t h e i n d i v i d u a l b o d y . I t w a s n o t a difficult step to t a k e , b e c a u s e we h a d a l r e a d y softened up o u r resistance by realizing t h a t e v e n n o r m a l ' i n t e r n a l ' p h e n o t y p i c effects m a y lie a t t h e e n d o f l o n g , r a m i f i e d , a n d i n d i r e c t , c a u s a l c h a i n s . L e t u s n o w s t e p o u t a little f u r t h e r . T h e h o u s e o f a c a d d i s i s s t r i c t l y n o t a p a r t o f its c e l l u l a r b o d y , b u t i t d o e s fit s n u g l y r o u n d the b o d y .

I f the b o d y i s r e g a r d e d a s a g e n e v e h i c l e , o r

s u r v i v a l m a c h i n e , i t i s e a s y t o see t h e s t o n e h o u s e a s a k i n d o f e x t r a p r o t e c t i v e w a l l , i n a f u n c t i o n a l s e n s e t h e o u t e r p a r t o f the v e h i c l e . I t j u s t h a p p e n s t o b e m a d e of stone rather than chitin. N o w consider a spider sitting at the centre of her w e b . If she is r e g a r d e d as a g e n e v e h i c l e , her w e b is not a part of that v e h i c l e i n q u i t e t h e s a m e o b v i o u s sense a s a c a d d i s h o u s e , s i n c e w h e n she t u r n s r o u n d t h e w e b d o e s n o t t u r n w i t h h e r . B u t the d i s t i n c t i o n i s c l e a r l y a frivolous one.

a v e r y real

sense h e r w e b i s a t e m p o r a r y f u n c t i o n a l

extension of her b o d y , a h u g e extension of the effective c a t c h m e n t area of her predatory organs. O n c e a g a i n , I k n o w of no genetic analysis of spider w e b m o r p h o l o g y , but there is n o t h i n g difficult in p r i n c i p l e a b o u t i m a g i n i n g such an analysis. It is known

that

individual

spiders

have

consistent

idiosyncrasies

which

are

r e p e a t e d i n w e b after w e b . O n e f e m a l e Zygiella-x-notata, for i n s t a n c e , w a s

The Genetical Evolution of A n i m a l Artefacts

199

seen t o b u i l d m o r e t h a n 100 w e b s , a l l l a c k i n g a p a r t i c u l a r c o n c e n t r i c r i n g (Witt,

Read

Peakall

1968).

N o b o d y familiar with

the

literature

behaviour genetics (e.g. M a n n i n g 1971) w o u l d be surprised if the observed idiosyncrasies of individual

spiders

Indeed, our belief that spiders'

turned

out

have

webs have evolved

genetic

basis.

t h e i r efficient s h a p e

through natural selection necessarily c o m m i t s us to a b e l i e f that, at least in the p a s t , w e b v a r i a t i o n m u s t h a v e b e e n u n d e r g e n e t i c i n f l u e n c e ( C h a p t e r 2 ) . A s i n the c a s e o f t h e c a d d i s h o u s e s , t h e g e n e s m u s t h a v e w o r k e d v i a b u i l d i n g behaviour,

before

neuroanatomy,

that

before

embryonic

that perhaps v i a cell

development

perhaps

membrane biochemistry.

via By

w h a t e v e r e m b r y o l o g i c a l routes the genes m a y w o r k in detail, the s m a l l e x t r a step from b e h a v i o u r t o w e b i s n o t a n y m o r e d i f f i c u l t t o c o n c e i v e o f t h a n t h e m a n y c a u s a l steps w h i c h p r e c e d e d t h e b e h a v i o u r a l effect, a n d w h i c h lie b u r i e d i n the l a b y r i n t h o f n e u r o e m b r y o l o g y . N o b o d y has a n y t r o u b l e u n d e r s t a n d i n g the i d e a o f g e n e t i c c o n t r o l o f m o r p h o l o g i c a l differences. N o w a d a y s few people h a v e trouble u n d e r s t a n d i n g that

there

is,

principle,

difference

between

genetic

control

morphology and genetic control of behaviour, and we are unlikely to be misled by unfortunate statements such as 'Strictly s p e a k i n g , it is the brain (rather than the b e h a v i o u r ) that is g e n e t i c a l l y i n h e r i t e d '

( P u g h in press).

T h e p o i n t h e r e is, o f c o u r s e , t h a t i f t h e r e i s a n y sense i n w h i c h t h e b r a i n i s inherited, b e h a v i o u r m a y b e inherited i n e x a c t l y the s a m e sense. I f w e object to calling behaviour inherited, as some do on tenable grounds, then we must, to be consistent, object to c a l l i n g brains inherited too. A n d if we do d e c i d e to allow that both m o r p h o l o g y and b e h a v i o u r m a y b e inherited, w e c a n n o t reasonably at the s a m e time object to c a l l i n g caddis house c o l o u r a n d spider w e b shape inherited. T h e extra step from b e h a v i o u r t o e x t e n d e d p h e n o t y p e , i n this c a s e t h e s t o n e h o u s e o r t h e w e b , i s a s c o n c e p t u a l l y n e g l i g i b l e a s t h e step f r o m m o r p h o l o g y t o b e h a v i o u r . From

the

viewpoint

o f this

book an

animal

artefact,

any other

phenotypic product whose variation is influenced by a gene, can be regarded as a p h e n o t y p i c tool by w h i c h that g e n e c o u l d p o t e n t i a l l y l e v e r itself into the next generation. A g e n e m a y so lever itself by a d o r n i n g the tail of a m a l e bird of paradise w i t h a sexually attractive blue feather, or by c a u s i n g a m a l e b o w e r b i r d t o p a i n t his b o w e r w i t h p i g m e n t c r u s h e d i n his b i l l o u t o f b l u e b e r r i e s . T h e d e t a i l s m a y b e d i f f e r e n t i n t h e t w o c a s e s b u t t h e effect, f r o m t h e gene's point of v i e w , is the same. G e n e s that a c h i e v e sexually attractive p h e n o t y p i c effects w h e n c o m p a r e d w i t h t h e i r a l l e l e s a r e f a v o u r e d , a n d i t i s t r i v i a l w h e t h e r t h o s e p h e n o t y p i c effects a r e ' c o n v e n t i o n a l ' o r

'extended'.

T h i s is underlined by the interesting o b s e r v a t i o n that b o w e r bird species w i t h especially splendid b o w e r s tend to h a v e relatively d r a b p l u m a g e , w h i l e those species w i t h r e l a t i v e l y b r i g h t p l u m a g e

tend

to build

less e l a b o r a t e a n d

s p e c t a c u l a r b o w e r s ( G i l l i a r d 1 9 6 3 ) . I t i s a s t h o u g h s o m e s p e c i e s h a v e shifted

T h e Genetical Evolution of Animal Artefacts

200

part

of the

burden

of adaptation

from

bodily

phenotype

extended

phenotype. S o far t h e p h e n o t y p i c effects w e h a v e b e e n c o n s i d e r i n g h a v e e x t e n d e d o n l y a few y a r d s a w a y from the initiating genes, but in principle there is no reason w h y t h e p h e n o t y p i c l e v e r s o f g e n e p o w e r s h o u l d n o t r e a c h o u t for m i l e s . A b e a v e r d a m i s b u i l t c l o s e t o t h e l o d g e , b u t t h e effect o f t h e d a m m a y b e t o flood an a r e a thousands of square metres in extent. As to the a d v a n t a g e of t h e p o n d f r o m t h e b e a v e r ' s p o i n t o f v i e w , t h e best g u e s s s e e m s t o b e t h a t i t i n c r e a s e s t h e d i s t a n c e t h e b e a v e r c a n t r a v e l b y w a t e r , w h i c h i s safer t h a n t r a v e l l i n g b y l a n d , a n d e a s i e r for t r a n s p o r t i n g w o o d . A b e a v e r t h a t lives b y a s t r e a m q u i c k l y e x h a u s t s t h e s u p p l y o f food trees l y i n g a l o n g t h e s t r e a m b a n k w i t h i n a r e a s o n a b l e d i s t a n c e . B y b u i l d i n g a d a m a c r o s s t h e s t r e a m the b e a v e r c r e a t e s a l a r g e s h o r e l i n e w h i c h i s a v a i l a b l e for safe a n d e a s y f o r a g i n g w i t h o u t t h e b e a v e r h a v i n g t o m a k e l o n g a n d difficult j o u r n e y s o v e r l a n d . interpretation

right,

the

lake

may

be regarded

huge

I f this

extended

p h e n o t y p e , e x t e n d i n g the f o r a g i n g r a n g e of the b e a v e r in a w a y w h i c h is s o m e w h a t a n a l o g o u s to the w e b of the spider. As in the case of the spider w e b , n o b o d y h a s d o n e a g e n e t i c s t u d y o f b e a v e r d a m s , b u t w e r e a l l y d o not need to in o r d e r to c o n v i n c e ourselves of the rightness of r e g a r d i n g the d a m , a n d the lake, as part of the p h e n o t y p i c expression of b e a v e r genes. It is e n o u g h that we a c c e p t that b e a v e r dams must h a v e evolved by D a r w i n i a n n a t u r a l s e l e c t i o n : this c a n o n l y h a v e c o m e a b o u t i f d a m s h a v e v a r i e d u n d e r the control of genes ( C h a p t e r 2). Just by t a l k i n g a b o u t a few e x a m p l e s of a n i m a l artefacts, then, we h a v e p u s h e d the c o n c e p t u a l r a n g e of the g e n e ' s p h e n o t y p e out to m a n y miles. But n o w we c o m e up a g a i n s t a c o m p l i c a t i o n . A b e a v e r d a m is usually the w o r k of more

than

one

individual.

Mated

pairs

routinely

work

together,

and

s u c c e s s i v e g e n e r a t i o n s o f a f a m i l y m a y i n h e r i t r e s p o n s i b i l i t y for t h e u p k e e p a n d extension of a ' t r a d i t i o n a l ' d a m - c o m p l e x c o m p r i s i n g a staircase of half a d o z e n d a m s stepping d o w n s t r e a m , and m a y b e several 'canals' as well. N o w it w a s easy to a r g u e that a c a d d i s house, or a spider w e b , w a s the extended p h e n o t y p e o f t h e g e n e s o f t h e s i n g l e i n d i v i d u a l t h a t b u i l t it. B u t w h a t a r e w e to m a k e of an artefact that is the j o i n t production of a pair of animals or a f a m i l y ? W o r s e , consider the m o u n d built by a c o l o n y of c o m p a s s termites, a tombstone-shaped

slab,

one of a vista of similar

m o n o l i t h s all oriented

p r e c i s e l y n o r t h - s o u t h , a n d r i s i n g to a h e i g h t t h a t d w a r f s its b u i l d e r s as a mile-high skyscraper w o u l d d w a r f a m a n (von Frisch 1 9 7 5 ) . It is built by p e r h a p s a m i l l i o n t e r m i t e s , s e p a r a t e d b y t i m e i n t o c o h o r t s , like m e d i e v a l m a s o n s w h o c o u l d w o r k a lifetime on one c a t h e d r a l a n d n e v e r meet their c o l l e a g u e s t h a t w o u l d c o m p l e t e it. A p a r t i s a n o f t h e i n d i v i d u a l a s t h e u n i t o f s e l e c t i o n m i g h t p a r d o n a b l y ask e x a c t l y whose e x t e n d e d p h e n o t y p e t h e t e r m i t e m o u n d is supposed to be. I f this

consideration

seems

complicate

the

idea

of the

extended

T h e Genetical Evolution of A n i m a l Artefacts

20I

p h e n o t y p e b e y o n d all reason, I c a n o n l y point o u t that e x a c t l y the s a m e problem

has

always

arisen

with

'conventional'

phenotypes.

are

thoroughly a c c u s t o m e d to the i d e a that a g i v e n p h e n o t y p i c entity, an o r g a n say, or a b e h a v i o u r pattern, is influenced by a large n u m b e r of g e n e s w h o s e effects i n t e r a c t i n a d d i t i v e o r m o r e c o m p l e x w a y s . H u m a n h e i g h t a t a g i v e n a g e i s affected b y g e n e s a t m a n y l o c i , i n t e r a c t i n g w i t h e a c h o t h e r a n d w i t h d i e t a r y a n d o t h e r e n v i r o n m e n t a l effects. T h e h e i g h t o f a t e r m i t e m o u n d a t a given mound-age

is,

no doubt,

also controlled

many

environmental

factors a n d m a n y g e n e s , a d d i n g t o o r m o d i f y i n g e a c h o t h e r s ' effects. I t i s incidental

that in

the case of the

termite m o u n d

t h e proximal

theatre of

w i t h i n - b o d y g e n e effects h a p p e n s t o b e d i s t r i b u t e d a m o n g t h e c e l l s o f a l a r g e number of worker bodies. I f w e a r e g o i n g t o w o r r y a b o u t p r o x i m a l effects, t h e g e n e s i n f l u e n c i n g m y height act i n w a y s that are distributed a m o n g m a n y separate cells. M y b o d y i s full o f g e n e s , w h i c h h a p p e n t o b e i d e n t i c a l l y d i s t r i b u t e d a m o n g m y m a n y s o m a t i c c e l l s . E a c h g e n e e x e r t s its effects a t t h e c e l l u l a r l e v e l , o n l y a m i n o r i t y o f g e n e s e x p r e s s i n g t h e m s e l v e s i n a n y o n e c e l l . T h e s u m m e d effects o f a l l these effects o n c e l l s , t o g e t h e r w i t h s i m i l a r effects f r o m t h e e n v i r o n m e n t , m a y b e m e a s u r e d a s m y t o t a l h e i g h t . S i m i l a r l y , a t e r m i t e m o u n d i s full o f g e n e s . T h e s e genes, too, are distributed a m o n g the nuclei of a l a r g e n u m b e r of cells. It h a p p e n s that the cells are not c o n t a i n e d in q u i t e s u c h a c o m p a c t single u n i t a s the cells i n m y b o d y , b u t e v e n h e r e t h e d i f f e r e n c e i s n o t v e r y g r e a t . Termites m o v e around relative to each other more than h u m a n organs do, b u t i t i s n o t u n k n o w n for h u m a n c e l l s t o t r a v e l r a p i d l y a b o u t t h e b o d y i n pursuance

o f their

errands,

for

instance

phagocytes

hunting

down

and

e n g u l f i n g m i c r o s c o p i c p a r a s i t e s . A m o r e i m p o r t a n t d i f f e r e n c e (in t h e c a s e o f a termite m o u n d , t h o u g h not in the case of a c o r a l r e e f built by a c l o n e of individuals)

that

the

cells

the

termite

mound

are

gathered

into

genetically heterogeneous p a c k a g e s : each individual termite is a clone of cells b u t a different c l o n e f r o m a l l o t h e r i n d i v i d u a l s i n t h e nest. T h i s , h o w ever, is only a relative c o m p l i c a t i o n . F u n d a m e n t a l l y w h a t is g o i n g on is that genes, c o m p a r e d with their alleles, exert quantitative, m u t u a l l y interacting, m u t u a l l y m o d i f y i n g , effects o n a s h a r e d p h e n o t y p e , t h e m o u n d . T h e y d o this p r o x i m a l l y b y c o n t r o l l i n g the c h e m i s t r y o f cells i n w o r k e r bodies, a n d h e n c e worker b e h a v i o u r . T h e principle is the same, w h e t h e r the cells h a p p e n to be o r g a n i z e d into one large h o m o g e n e o u s c l o n e , as in the h u m a n b o d y , or into a heterogeneous collection of clones, as in the termite m o u n d . I postpone until l a t e r t h e c o m p l i c a t i n g p o i n t t h a t a t e r m i t e b o d y i t s e l f is a ' c o l o n y ' , w i t h a s u b s t a n t i a l f r a c t i o n o f its g e n e t i c r e p l i c a t o r s c o n t a i n e d i n s y m b i o t i c p r o t o z o a or bacteria. W h a t , then, w o u l d a genetics of termite m o u n d s look like? S u p p o s e we were to do a population survey of compass m o u n d s in the A u s t r a l i a n steppe, s c o r i n g a trait s u c h a s c o l o u r , b a s a l l e n g t h / w i d t h r a t i o , o r s o m e i n t e r n a l

The Genetical Evolution of A n i m a l Artefacts

202

structural 'organ'

featureâ&#x20AC;&#x201D;for

structure.

termite

How

could

mounds we

are a

bodies

genetic

with

study

complex

of such

group-

m a n u f a c t u r e d p h e n o t y p e s ? We need not hope to find normal M e n d e l i a n inheritance with simple dominance. An obvious complication, as already m e n t i o n e d , is that the g e n o t y p e s of the i n d i v i d u a l s w o r k i n g on a n y one m o u n d a r e n o t i d e n t i c a l . F o r m o s t o f t h e life o f a n a v e r a g e c o l o n y , h o w e v e r , a l l t h e w o r k e r s a r e full s i b l i n g s , t h e c h i l d r e n o f t h e p r i m a r y r o y a l p a i r o f alates w h o f o u n d e d the c o l o n y . L i k e their parents the w o r k e r s are diploid. W e m a y p r e s u m e t h a t t h e k i n g ' s t w o sets o f g e n e s a n d t h e q u e e n ' s t w o sets o f genes

are

permuted

throughout

the several

million

worker

bodies.

The

' g e n o t y p e ' o f t h e a g g r e g a t e o f w o r k e r s m a y t h e r e f o r e b e r e g a r d e d , i n a sense, a s a s i n g l e tetraploid g e n o t y p e c o n s i s t i n g o f a l l t h e g e n e s w h i c h t h e o r i g i n a l founding pair contributed.

I t i s n o t q u i t e a s s i m p l e a s t h a t , for v a r i o u s

r e a s o n s , for i n s t a n c e s e c o n d a r y r e p r o d u c t i v e s often arise i n o l d e r c o l o n i e s a n d t h e s e m a y t a k e o n t h e full r e p r o d u c t i v e r o l e i f o n e o f t h e o r i g i n a l r o y a l p a i r dies. T h i s m e a n s that the w o r k e r s b u i l d i n g the later parts of a m o u n d m a y n o t b e full s i b l i n g s o f t h o s e t h a t b e g a n t h e task, b u t t h e i r n e p h e w s a n d n i e c e s (probably inbred and rather uniform, incidentallyâ&#x20AC;&#x201D;Hamilton

1972; Bartz

1 9 7 9 ) . T h e s e l a t e r r e p r o d u c t i v e s still d r a w t h e i r g e n e s f r o m t h e ' t e t r a p l o i d ' set i n t r o d u c e d b y t h e o r i g i n a l r o y a l p a i r , b u t t h e i r p r o g e n y w i l l p e r m u t e a particular subset

of those

original

genes.

One

of the

things

'mound-

g e n e t i c i s t ' m i g h t l o o k o u t for, t h e n , i s a s u d d e n c h a n g e i n d e t a i l s o f m o u n d building

after

replacement

of a

primary

reproductive

secondary

reproductive. Ignoring

the

problem

introduced

secondary

reproductives,

let

confine our hypothetical genetic study to y o u n g e r colonies whose workers c o n s i s t e n t i r e l y o f full s i b l i n g s . S o m e c h a r a c t e r s i n w h i c h m o u n d s v a r y m a y turn

out

largely

controlled

one

locus,

while

others

will

p o l y g e n i c a l l y c o n t r o l l e d a t m a n y l o c i . T h i s i s n o different f r o m o r d i n a r y diploid genetics, but our n e w quasi-tetraploid genetics n o w introduces some c o m p l i c a t i o n s . S u p p o s e the b e h a v i o u r a l m e c h a n i s m i n v o l v e d in choosing the c o l o u r of the m u d used in b u i l d i n g varies g e n e t i c a l l y .

(Again, colour is

c h o s e n for c o n t i n u i t y w i t h e a r l i e r t h o u g h t e x p e r i m e n t s , a l t h o u g h a g a i n i t w o u l d b e m o r e r e a l i s t i c t o a v o i d a v i s u a l trait, s i n c e t e r m i t e s m a k e little use of vision. If necessary, we m a y suppose the choice to be m a d e chemically, m u d c o l o u r b e i n g i n c i d e n t a l l y correlated w i t h the c h e m i c a l cues. T h i s is i n s t r u c t i v e , for i t a g a i n e m p h a s i z e s t h e fact t h a t o u r w a y o f l a b e l l i n g a p h e n o t y p i c trait is a m a t t e r of a r b i t r a r y c o n v e n i e n c e . ) F o r simplicity, assume that m u d c h o i c e is influenced by the diploid g e n o t y p e of the individual w o r k e r d o i n g the c h o o s i n g , in a simple one locus M e n d e l i a n fashion with c h o i c e of d a r k m u d d o m i n a n t o v e r c h o i c e of light m u d . T h e n a m o u n d built by

colony

containing

some

dark-preferring

workers

and

some

light

preferring w o r k e r s will consist of a m i x t u r e of d a r k a n d light m u d s and will

T h e G e n e t i c a l E v o l u t i o n of A n i m a l A r t e f a c t s

203

presumably be intermediate in overall colour. Of course such simple genetic assumptions are highly i m p r o b a b l e . T h e y are e q u i v a l e n t to the simplifying assumptions we ordinarily m a k e w h e n explaining elementary conventional genetics, a n d I m a k e t h e m here to e x p l a i n a n a l o g o u s l y the principles of h o w a science of 'extended genetics' might work. U s i n g these a s s u m p t i o n s , t h e n , w e c a n w r i t e d o w n t h e e x p e c t e d e x t e n d e d p h e n o t y p e s , c o n s i d e r i n g m u d c o l o u r o n l y , r e s u l t i n g f r o m crosses b e t w e e n t h e various possible f o u n d i n g pair g e n o t y p e s . F o r instance, all colonies f o u n d e d by a heterozygous king and a heterozygous q u e e n will contain d a r k - b u i l d i n g and

light-building

workers

the

ratio

3:1.

The

resulting

extended

p h e n o t y p e will be a m o u n d built of three parts d a r k m u d a n d one part light m u d , therefore nearly, but not c o m p l e t e l y , dark in c o l o u r . If c h o i c e of m u d colour is influenced by polygenes at m a n y loci, the 'tetraploid g e n o t y p e ' of the c o l o n y m a y b e e x p e c t e d t o i n f l u e n c e t h e e x t e n d e d p h e n o t y p e , p e r h a p s i n a n a d d i t i v e w a y . T h e c o l o n y ' s i m m e n s e s i z e w i l l l e a d t o its a c t i n g a s a statistical a v e r a g i n g d e v i c e ,

m a k i n g the m o u n d

as a w h o l e

b e c o m e the

extended p h e n o t y p i c expression of the genes of the r o y a l pair, manifested v i a the b e h a v i o u r o f s e v e r a l m i l l i o n w o r k e r s e a c h c o n t a i n i n g a d i f f e r e n t d i p l o i d s a m p l e o f those g e n e s . M u d c o l o u r w a s a n e a s y c h a r a c t e r for u s t o c h o o s e , b e c a u s e m u d i t s e l f blends in a simple additive m a n n e r : m i x dark a n d light m u d , a n d y o u get k h a k i m u d . I t w a s t h e r e f o r e e a s y for u s t o d e d u c e t h e r e s u l t o f a s s u m i n g t h a t e a c h w o r k e r g o e s its o w n w a y , c h o o s i n g m u d o f its o w n p r e f e r r e d c o l o u r (or c h e m i c a l a s s o c i a t e d w i t h c o l o u r ) , a s d e t e r m i n e d b y its o w n d i p l o i d g e n o t y p e . But w h a t can we say a b o u t a characteristic of overall m o u n d m o r p h o l o g y , say b a s a l w i d t h / l e n g t h r a t i o ? I n itself, this i s n o t a c h a r a c t e r t h a t a n y s i n g l e worker can determine.

E a c h single w o r k e r must be o b e y i n g b e h a v i o u r a l

rules, t h e result o f w h i c h , s u m m e d o v e r t h o u s a n d s o f i n d i v i d u a l s , i s t h e production of a m o u n d of regular shape a n d stated dimensions. O n c e a g a i n , the difficulty i s o n e w e h a v e m e t b e f o r e , i n t h e e m b r y o n i c d e v e l o p m e n t o f a n o r d i n a r y d i p l o i d m u l t i c e l l u l a r b o d y . E m b r y o l o g i s t s a r e still w r e s t l i n g w i t h p r o b l e m s o f this k i n d , a n d v e r y f o r m i d a b l e t h e y a r e . T h e r e d o a p p e a r t o b e some

analogies

with

termite

mound

development.

For

instance,

conventional embryologists frequently a p p e a l to the c o n c e p t of the c h e m i c a l g r a d i e n t , w h i l e i n Macrotermes t h e r e i s e v i d e n c e t h a t t h e s h a p e a n d s i z e o f t h e royal cell is d e t e r m i n e d by a p h e r o m o n a l g r a d i e n t a r o u n d the b o d y of the queen

(Bruinsma & Leuthold

1 9 7 7 ) . E a c h cell in a d e v e l o p i n g e m b r y o

behaves as if it ' k n o w s ' w h e r e it is in the b o d y , a n d it g r o w s to h a v e a form and

physiology

appropriate

that

part

of the

body

(Wolpert

1970).

S o m e t i m e s t h e effects o f a m u t a t i o n a r e e a s y t o i n t e r p r e t a t t h e c e l l u l a r l e v e l . F o r i n s t a n c e , a m u t a t i o n t h a t affects skin p i g m e n t a t i o n h a s a r a t h e r o b v i o u s l o c a l effect o n e a c h skin c e l l . B u t o t h e r m u t a t i o n s affect c o m p l e x c h a r a c t e r s in

drastic

ways.

Well-known

examples

are

the

'homeotic'

mutants

T h e Genetical Evolution of A n i m a l Artefacts

204

Drosophila, s u c h a s t h e o n e t h a t g r o w s a c o m p l e t e a n d w e l l - f o r m e d l e g i n the socket w h e r e an a n t e n n a o u g h t to be. F o r a c h a n g e in one single g e n e to w r e a k s u c h a m a j o r , y e t o r d e r l y , c h a n g e i n t h e p h e n o t y p e , i t m u s t m a k e its lesion rather h i g h in a h i e r a r c h i c a l c h a i n of c o m m a n d . By a n a l o g y , if a single i n f a n t r y m a n g o e s off his h e a d h e a l o n e r u n s a m o k ; b u t i f a g e n e r a l loses his reason an entire a r m y behaves crazily on a grand scaleâ&#x20AC;&#x201D;invades an ally instead of an e n e m y , s a y â&#x20AC;&#x201D; w h i l e each individual soldier in that army is o b e y i n g o r d e r s n o r m a l l y a n d s e n s i b l y , a n d his i n d i v i d u a l b e h a v i o u r a s h e p u t s o n e foot i n front o f t h e o t h e r w i l l b e i n d i s t i n g u i s h a b l e f r o m t h a t o f a soldier in an a r m y w i t h a sane general. P r e s u m a b l y an individual

t e r m i t e w o r k i n g o n a little c o r n e r o f a b i g

m o u n d is in a s i m i l a r p o s i t i o n to a c e l l in a d e v e l o p i n g e m b r y o , or a s i n g l e soldier tirelessly o b e y i n g orders w h o s e purpose in the larger s c h e m e of things he does not u n d e r s t a n d . N o w h e r e in the single termite's nervous system is t h e r e a n y t h i n g r e m o t e l y e q u i v a l e n t t o a c o m p l e t e i m a g e o f w h a t t h e finished m o u n d will look like ( W i l s o n 1 9 7 1 , p. 228). E a c h w o r k e r is e q u i p p e d with a small toolkit of b e h a v i o u r a l rules, choose an already

and he/she is probably stimulated to

i t e m o f b e h a v i o u r b y local stimuli e m a n a t i n g from

accomplished,

matter

whether

he/she

other

the w o r k workers

a c c o m p l i s h e d i t â&#x20AC;&#x201D; s t i m u l i e m a n a t i n g f r o m t h e p r e s e n t s t a t e o f t h e nest i n the worker's i m m e d i a t e vicinity ('stigmergie', Grasse 1959). For my purposes it d o e s n ' t m a t t e r e x a c t l y w h a t t h e b e h a v i o u r a l rules a r e , b u t t h e y w o u l d b e something like: ' I f you c o m e upon a heap of mud with a certain pheromone o n it, p u t a n o t h e r d o l l o p o f m u d o n t h e t o p . ' T h e i m p o r t a n t p o i n t a b o u t s u c h r u l e s i s t h a t t h e y h a v e a p u r e l y l o c a l effect. T h e g r a n d d e s i g n o f t h e w h o l e m o u n d e m e r g e s o n l y a s the s u m m e d c o n s e q u e n c e s o f thousands o f o b e y i n g s of micro-rules

( H a n s e l l in press). P a r t i c u l a r interest attaches to the local

r u l e s t h a t a r e r e s p o n s i b l e for d e t e r m i n i n g g l o b a l p r o p e r t i e s s u c h a s t h e b a s e l e n g t h o f the c o m p a s s m o u n d . H o w d o the i n d i v i d u a l w o r k e r s o n the g r o u n d ' k n o w ' that they h a v e r e a c h e d the b o u n d a r y o f the g r o u n d p l a n ? Perhaps i n s o m e t h i n g like the s a m e w a y as the cells at the b o u n d a r y of a liver ' k n o w ' that they are not in the m i d d l e of the liver. In a n y case, w h a t e v e r the local b e h a v i o u r a l r u l e s m a y b e t h a t d e t e r m i n e t h e o v e r a l l s h a p e a n d size o f a termite m o u n d ,

they are presumably subject to genetic variation in

the

population at large. It is entirely plausible, indeed almost inevitable, that b o t h the s h a p e a n d size o f c o m p a s s termite m o u n d s h a v e e v o l v e d b y natural selection, just like a n y feature of bodily m o r p h o l o g y . T h i s can only have c o m e a b o u t t h r o u g h t h e s e l e c t i o n o f m u t a t i o n s a c t i n g a t t h e l o c a l l e v e l o n the building b e h a v i o u r of individual worker termites. N o w o u r s p e c i a l p r o b l e m arises, w h i c h w o u l d n o t arise i n t h e o r d i n a r y e m b r y o g e n e s i s of a m u l t i c e l l u l a r b o d y , nor in the e x a m p l e of m i x i n g light a n d d a r k m u d s . U n l i k e the cells of a m u l t i c e l l u l a r b o d y , the w o r k e r s are not

T h e Genetical Evolution of A n i m a l Artefacts

205

g e n e t i c a l l y identical. In the e x a m p l e of the d a r k a n d light m u d , it w a s easy to

suppose

that

genetically

heterogeneous

work-force

would

simply

construct a m o u n d of m i x e d m u d . But a work-force w h i c h w a s genetically heterogeneous w i t h respect to o n e of the b e h a v i o u r a l rules that affected overall m o u n d s h a p e m i g h t p r o d u c e curious results. B y a n a l o g y w i t h o u r simple M e n d e l i a n m o d e l of m u d selection, a c o l o n y m i g h t contain workers f a v o u r i n g t w o d i f f e r e n t r u l e s for d e t e r m i n i n g t h e b o u n d a r y o f t h e m o u n d , s a y in the ratio three to one. It is p l e a s i n g to i m a g i n e that such a b i m o d a l c o l o n y might produce a m o u n d with a strange double wall and a m o a t b e t w e e n ! M o r e p r o b a b l y , t h e r u l e s o b e y e d b y i n d i v i d u a l s w o u l d i n c l u d e p r o v i s i o n for the m i n o r i t y t o a l l o w t h e m s e l v e s t o b e o v e r r u l e d b y m a j o r i t y d e c i s i o n s , s o that only one clean-cut w a l l w o u l d e m e r g e . T h i s c o u l d w o r k in a similar w a y t o t h e ' d e m o c r a t i c ' c h o i c e o f a n e w nest site i n h o n e y b e e s w a r m s , o b s e r v e d by Lindauer (1961). S c o u t b e e s l e a v e t h e s w a r m h a n g i n g i n a t r e e , a n d p r o s p e c t for s u i t a b l e n e w p e r m a n e n t sites s u c h a s h o l l o w trees. E a c h s c o u t r e t u r n s a n d d a n c e s o n the s u r f a c e o f t h e s w a r m , u s i n g t h e w e l l - k n o w n v o n F r i s c h c o d e t o i n d i c a t e the

direction

investigated.

and The

distance 'vigour'

the

prospective

of the d a n c e

indicates

site the

that

she

has

individual

just

scout's

assessment o f t h e v i r t u e s o f t h e site. N e w b e e s a r e r e c r u i t e d t o g o o u t a n d e x a m i n e i t for t h e m s e l v e s , a n d i f t h e y ' a p p r o v e ' t h e y t o o d a n c e ' i n its f a v o u r ' on returning. After some hours, then, the scouts h a v e formed themselves into a few ' p a r t i e s ' , e a c h o n e ' a d v o c a t i n g ' a d i f f e r e n t n e s t site. F i n a l l y , m i n o r i t y 'opinions' b e c o m e even smaller minorities, as allegiances are transferred to m a j o r i t y d a n c e s . W h e n a n o v e r w h e l m i n g m a j o r i t y h a s b e e n a c h i e v e d for o n e site, t h e w h o l e s w a r m t a k e s o f f a n d flies t h e r e t o set u p h o m e . L i n d a u e r o b s e r v e d this p r o c e d u r e for n i n e t e e n d i f f e r e n t s w a r m s , a n d i n o n l y t w o o f t h e s e c a s e s w a s a c o n s e n s u s n o t s o o n r e a c h e d . I q u o t e his a c c o u n t of one of these: I n the first c a s e t w o g r o u p s o f m e s s e n g e r s h a d g o t i n t o c o m p e t i t i o n ; one g r o u p a n n o u n c e d a nesting place to the northwest, the other to the northeast. N e i t h e r o f the t w o w i s h e d t o y i e l d . T h e s w a r m then f i n a l l y f l e w off a n d I c o u l d s c a r c e l y b e l i e v e m y e y e s â&#x20AC;&#x201D; i t s o u g h t t o d i v i d e itself. T h e o n e h a l f w a n t e d t o f l y t o t h e n o r t h w e s t , t h e o t h e r t o the northeast.

A p p a r e n t l y each g r o u p of scouting bees w a n t e d

a b d u c t t h e s w a r m t o t h e n e s t i n g p l a c e o f its o w n c h o i c e . B u t t h a t w a s n a t u r a l l y n o t p o s s i b l e , for o n e g r o u p w a s a l w a y s w i t h o u t t h e q u e e n , a n d t h e r e r e s u l t e d a r e m a r k a b l e t u g o f w a r i n t h e a i r , o n c e 100 m e t e r s to the northwest, then a g a i n 150 meters to the northeast, until finally after h a l f a n h o u r t h e s w a r m g a t h e r e d t o g e t h e r a t t h e o l d l o c a t i o n . I m m e d i a t e l y both groups b e g a n again with their soliciting dances,

206

The Genetical Evolution of Animal Artefacts

a n d i t w a s n o t u n t i l t h e n e x t d a y t h a t t h e n o r t h e a s t g r o u p finally y i e l d e d ; they e n d e d their d a n c e and thus an a g r e e m e n t w a s reached on the nesting p l a c e in the northwest [ L i n d a u e r 1 9 6 1 , p. 4 3 ] . T h e r e is no suggestion here that the t w o s u b g r o u p s of bees w e r e genetically d i f f e r e n t , t h o u g h t h e y m a y h a v e b e e n . W h a t m a t t e r s for the p o i n t I a m m a k i n g is that e a c h i n d i v i d u a l follows local b e h a v i o u r a l rules, the c o m b i n e d effect o f w h i c h n o r m a l l y g i v e s rise t o c o o r d i n a t e d s w a r m b e h a v i o u r . T h e s e e v i d e n t l y i n c l u d e r u l e s for r e s o l v i n g ' d i s p u t e s ' i n f a v o u r o f the m a j o r i t y . D i s a g r e e m e n t s o v e r t h e p r e f e r r e d l o c a t i o n for t h e o u t e r w a l l o f a t e r m i t e m o u n d m i g h t b e j u s t a s s e r i o u s for c o l o n y s u r v i v a l a s d i s a g r e e m e n t o v e r n e s t i n g sites a m o n g L i n d a u e r ' s b e e s ( c o l o n y s u r v i v a l m a t t e r s , b e c a u s e o f its effects o n t h e s u r v i v a l o f t h e g e n e s c a u s i n g i n d i v i d u a l s t o r e s o l v e d i s p u t e s ) . A s a w o r k i n g h y p o t h e s i s we m i g h t e x p e c t that disputes resulting from genetic h e t e r o g e n e i t y i n t e r m i t e s w o u l d b e r e s o l v e d b y s i m i l a r r u l e s . I n this w a y the e x t e n d e d p h e n o t y p e c o u l d take up a discrete a n d regular shape, despite being built by genetically heterogeneous workers. The

analysis

of artefacts g i v e n

this

chapter seems,

at first sight,

v u l n e r a b l e to reductio ad absurdum. I s n ' t t h e r e a sense, it m a y be a s k e d , in w h i c h e v e r y effect

that an a n i m a l has upon

the w o r l d is an extended

p h e n o t y p e ? W h a t a b o u t t h e f o o t p r i n t s left i n t h e m u d b y a n o y s t e r c a t c h e r , the paths w o r n t h r o u g h the grass by sheep, the l u x u r i a n t tussock that marks t h e site of a last y e a r ' s c o w p a t ? A p i g e o n ' s nest is an a r t e f a c t w i t h o u t a d o u b t , b u t in g a t h e r i n g the sticks the bird also c h a n g e s the a p p e a r a n c e of the g r o u n d w h e r e t h e y h a d l a i n . I f t h e nest i s c a l l e d e x t e n d e d p h e n o t y p e , w h y s h o u l d n ' t w e s o c a l l t h e b a r e p a t c h o f g r o u n d w h e r e t h e sticks u s e d t o l i e ? To

answer

this

must

recall

the fundamental

reason

why

we are

i n t e r e s t e d i n t h e p h e n o t y p i c e x p r e s s i o n o f g e n e s i n the f i r s t p l a c e . O f a l l the m a n y p o s s i b l e r e a s o n s , t h e o n e w h i c h c o n c e r n s u s i n this b o o k i s a s f o l l o w s . We

are

fundamentally

interested

natural

selection,

therefore

the

differential s u r v i v a l of r e p l i c a t i n g entities such as genes. G e n e s are favoured or disfavoured relative to their alleles as a c o n s e q u e n c e of their p h e n o t y p i c effects u p o n t h e w o r l d . S o m e o f t h e s e p h e n o t y p i c effects m a y b e i n c i d e n t a l c o n s e q u e n c e s o f others, a n d h a v e n o b e a r i n g o n the survival c h a n c e s , one w a y or the other, of the genes c o n c e r n e d . A genetic m u t a t i o n that changes t h e s h a p e o f a n o y s t e r c a t c h e r ' s foot w i l l d o u b t l e s s t h e r e b y i n f l u e n c e t h e o y s t e r c a t c h e r ' s s u c c e s s i n p r o p a g a t i n g it. I t m a y , for i n s t a n c e , s l i g h t l y r e d u c e t h e b i r d ' s risk o f s i n k i n g i n t o m u d , w h i l e a t t h e s a m e t i m e i t s l i g h t l y s l o w s h i m d o w n w h e n h e i s r u n n i n g o n firm g r o u n d . S u c h effects a r e l i k e l y t o b e o f d i r e c t r e l e v a n c e to n a t u r a l selection. B u t the m u t a t i o n will also h a v e an effect o n t h e s h a p e o f t h e f o o t p r i n t s left b e h i n d i n the m u d â&#x20AC;&#x201D; a r g u a b l y a n e x t e n d e d p h e n o t y p i c effect. If, a s i s p e r f e c t l y l i k e l y , this h a s n o i n f l u e n c e o n the success of the g e n e c o n c e r n e d (Williams 1966, p p . 1 2 - 1 3 ) , it is of no

The Genetical Evolution of A n i m a l Artefacts

207

interest t o t h e s t u d e n t o f n a t u r a l s e l e c t i o n , a n d t h e r e i s n o p o i n t i n b o t h e r i n g t o discuss i t u n d e r t h e h e a d i n g o f t h e e x t e n d e d p h e n o t y p e , t h o u g h i t w o u l d b e f o r m a l l y c o r r e c t t o d o s o . If, o n t h e o t h e r h a n d , t h e c h a n g e d f o o t p r i n t d i d i n f l u e n c e s u r v i v a l o f t h e o y s t e r c a t c h e r , s a y b y m a k i n g i t h a r d e r for p r e d a t o r s to

track the

bird,

would

w a n t to regard

part

of the

extended

p h e n o t y p e o f t h e g e n e . P h e n o t y p i c effects o f g e n e s , w h e t h e r a t t h e l e v e l o f intracellular b i o c h e m i s t r y , gross b o d i l y m o r p h o l o g y or e x t e n d e d p h e n o t y p e , are

potentially

generation,

devices

or barriers

which

genes

lever

t o t h e i r d o i n g so.

themselves

into

the

I n c i d e n t a l side-effects are not

a l w a y s effective as tools or barriers, a n d we do not b o t h e r to r e g a r d t h e m as

phenotypic

expressions

of genes,

either

the

conventional

the

extended phenotype level. I t i s u n f o r t u n a t e t h a t this c h a p t e r h a s h a d t o b e r a t h e r h y p o t h e t i c a l . T h e r e h a v e been o n l y a few studies of the genetics of b u i l d i n g b e h a v i o u r in a n y animal

(e.g. D i l g e r

genetics'

will

1962), but there is no reason to think that 'artefact

any

different,

principle,

from

behaviour

genetics

g e n e r a l l y ( H a n s e l l i n p r e s s ) . T h e i d e a o f t h e e x t e n d e d p h e n o t y p e i s still sufficiently u n f a m i l i a r t h a t i t m i g h t n o t i m m e d i a t e l y o c c u r t o a g e n e t i c i s t t o study termite m o u n d s as a p h e n o t y p e , even if it w e r e p r a c t i c a l l y easy to do soâ&#x20AC;&#x201D;and

wouldn't

easy.

Yet

must

acknowledge

least

the

theoretical validity of such a b r a n c h of genetics if we are to c o u n t e n a n c e the Darwinian evolution of beaver dams and termite mounds. A n d w h o can d o u b t t h a t , i f t e r m i t e m o u n d s fossilized p l e n t i f u l l y , w e w o u l d see g r a d e d e v o l u t i o n a r y series w i t h t r e n d s a s s m o o t h (or a s p u n c t u a t e d ! ) a s a n y t h a t w e find in vertebrate skeletal palaeontology (Schmidt 1 9 5 5 ; Hansell in press)? Permit me one further speculation to lead us into the next c h a p t e r . I h a v e spoken as if the genes inside a termite m o u n d w e r e all enclosed in the nuclei o f cells o f t e r m i t e b o d i e s . T h e ' e m b r y o l o g i c a l ' f o r c e s b e a r i n g o n t h e e x t e n d e d phenotype have been assumed termites.

Yet

the

chapter on

to originate from the genes of individual arms races and manipulation should h a v e

a l e r t e d u s t o a n o t h e r w a y o f l o o k i n g a t it. I f a l l t h e D N A c o u l d b e d i s t i l l e d out of a termite m o u n d , perhaps as m u c h as one-quarter of it w o u l d not h a v e originated from termite nuclei at all. S o m e such p r o p o r t i o n of the b o d y weight of each individual termite is typically m a d e up of symbiotic cellulosedigesting m i c r o o r g a n i s m s in the g u t â&#x20AC;&#x201D; f l a g e l l a t e s or b a c t e r i a . T h e s y m b i o n t s are o b l i g a t e l y d e p e n d e n t o n the termites, a n d the termites o n t h e m . T h e proximal p h e n o t y p i c p o w e r of the s y m b i o n t genes is exerted v i a protein synthesis i n s y m b i o n t c y t o p l a s m . B u t j u s t a s t e r m i t e g e n e s r e a c h o u t b e y o n d the cells t h a t e n c l o s e t h e m a n d m a n i p u l a t e t h e d e v e l o p m e n t o f w h o l e t e r m i t e bodies a n d h e n c e of the m o u n d , is it not almost i n e v i t a b l e that the s y m b i o n t genes

will

have

surroundings? termite cells

And and

been will hence

selected this

exert

phenotypic

power

not include exerting p h e n o t y p i c

bodies,

termite

behaviour

and

their

power on

even

termite

208

T h e Genetical Evolution of Animal Artefacts

m o u n d s ? A l o n g t h e s e l i n e s , c o u l d t h e e v o l u t i o n o f e u s o c i a l i t y i n the I s o p t e r a be e x p l a i n e d as an a d a p t a t i o n of the m i c r o s c o p i c s y m b i o n t s rather than of the termites themselves? T h i s c h a p t e r h a s e x p l o r e d t h e i d e a o f t h e e x t e n d e d p h e n o t y p e , first o f g e n e s in a single i n d i v i d u a l , then of genes from different but closely related i n d i v i d u a l s , m e m b e r s of a k i n - g r o u p . T h e logic of the a r g u m e n t n o w seems to c o m p e l us to c o n t e m p l a t e the possibility of an extended phenotype's being j o i n t l y m a n i p u l a t e d , not necessarily c o o p e r a t i v e l y , b y genes from distantly related i n d i v i d u a l s , i n d i v i d u a l s of different species, e v e n different k i n g d o m s . T h i s i s t h e d i r e c t i o n i n w h i c h o u r n e x t o u t w a r d s t e p m u s t t a k e us.

1 2 Host Phenotypes of Parasite Genes

L e t us briefly take stock of w h e r e we h a v e r e a c h e d in o u r o u t w a r d march. T h e phenotypic expression of a gene can extend outside the cell in w h i c h t h e g e n e s e x e r t t h e i r i m m e d i a t e b i o c h e m i c a l i n f l u e n c e , t o affect g r o s s features o f a w h o l e m u l t i c e l l u l a r b o d y . T h i s i s c o m m o n p l a c e , a n d w e a r e c o n v e n t i o n a l l y used to the i d e a of a g e n e ' s p h e n o t y p i c expression b e i n g e x t e n d e d this far. In the previous c h a p t e r we took the small further step of e x t e n d i n g the phenotype to artefacts, built by individual b e h a v i o u r w h i c h is subject to g e n e t i c v a r i a t i o n , for i n s t a n c e c a d d i s h o u s e s . N e x t w e s a w t h a t a n e x t e n d e d phenotype can be built under the joint influence of genes in m o r e than one individual body. B e a v e r d a m s and termite m o u n d s are collectively built by the b e h a v i o u r a l efforts o f m o r e t h a n o n e i n d i v i d u a l . A g e n e t i c m u t a t i o n i n one i n d i v i d u a l b e a v e r c o u l d s h o w itself in p h e n o t y p i c c h a n g e in the shared artefact. If the p h e n o t y p i c c h a n g e in the artefact h a d an influence on the success o f r e p l i c a t i o n o f t h e n e w g e n e , n a t u r a l s e l e c t i o n w o u l d a c t , p o s i t i v e l y or negatively, to c h a n g e the probability of similar artefacts existing in the future. T h e g e n e ' s e x t e n d e d p h e n o t y p i c effect, s a y a n i n c r e a s e i n t h e h e i g h t o f the d a m , affects its c h a n c e s o f s u r v i v a l i n p r e c i s e l y t h e s a m e s e n s e a s i n t h e c a s e o f a g e n e w i t h a n o r m a l p h e n o t y p i c effect, s u c h a s a n i n c r e a s e i n t h e l e n g t h o f the t a i l . T h e f a c t t h a t t h e d a m i s t h e s h a r e d p r o d u c t o f t h e b u i l d i n g behaviour of several beavers does not alter the principle: genes that tend to m a k e beavers build h i g h d a m s will themselves, on a v e r a g e , tend to r e a p the benefits (or costs) o f h i g h d a m s , e v e n t h o u g h e v e r y d a m m a y b e j o i n t l y b u i l t b y several beavers. I f t w o b e a v e r s w o r k i n g o n the s a m e d a m h a v e different g e n e s for d a m h e i g h t , interaction interactions.

between

the resulting e x t e n d e d p h e n o t y p e will reflect the

the genes,

There could

in the s a m e w a y as

be extended genetic

bodies reflect g e n e

a n a l o g u e s o f epistasis,

modifier genes, even of d o m i n a n c e a n d recessiveness. Finally, at the end of the c h a p t e r , we s a w that genes ' s h a r i n g ' a g i v e n e x t e n d e d p h e n o t y p i c trait m i g h t c o m e from different species, e v e n different 209

Host Phenotypes of Parasite Genes

2IO

p h y l a a n d different k i n g d o m s . T h i s c h a p t e r will d e v e l o p t w o further ideas. O n e is that p h e n o t y p e s that extend outside the body do not h a v e to be i n a n i m a t e a r t e f a c t s : t h e y c a n t h e m s e l v e s b e b u i l t o f l i v i n g tissue. T h e o t h e r idea is that w h e r e v e r there are 'shared' genetic influences on an extended p h e n o t y p e , the shared influences m a y be in conflict with e a c h other rather t h a n c o o p e r a t i v e . T h e r e l a t i o n s h i p s w e s h a l l b e c o n c e r n e d w i t h a r e those o f parasites a n d their hosts. I shall s h o w that it is l o g i c a l l y sensible to regard parasite g e n e s as h a v i n g p h e n o t y p i c expression in host bodies a n d b e h a v i o u r . T h e c a d d i s l a r v a rides inside the stone house that it built. It therefore s e e m s a p p r o p r i a t e t o r e g a r d t h e h o u s e a s t h e o u t e r w a l l o f the g e n e v e h i c l e , t h e c a s i n g o f t h e s u r v i v a l m a c h i n e . I t i s e v e n e a s i e r t o r e g a r d the shell o f a s n a i l a s p a r t o f t h e p h e n o t y p i c e x p r e s s i o n o f s n a i l g e n e s s i n c e , a l t h o u g h the s h e l l i s i n o r g a n i c a n d ' d e a d ' , its c h e m i c a l s u b s t a n c e w a s d i r e c t l y s e c r e t e d b y s n a i l c e l l s . V a r i a t i o n s i n , s a y , shell t h i c k n e s s w o u l d b e c a l l e d g e n e t i c i f g e n e s in snail

cells

affected

'environmental'.

shell

thickness.

Otherwise

they

B u t there are reports o f snails w i t h

would

called

t r e m a t o d e parasites

h a v i n g t h i c k e r shells t h a n u n p a r a s i t i z e d snails ( C h e n g 1 9 7 3 ) . F r o m t h e p o i n t o f v i e w o f s n a i l g e n e t i c s , this a s p e c t o f shell v a r i a t i o n i s u n d e r ' e n v i r o n m e n t a l ' c o n t r o l â&#x20AC;&#x201D; t h e f l u k e i s p a r t o f t h e e n v i r o n m e n t o f t h e s n a i l â&#x20AC;&#x201D; b u t from the p o i n t of v i e w of fluke genetics it m i g h t w e l l be u n d e r genetic control: it m i g h t , i n d e e d , be an e v o l v e d a d a p t a t i o n of the fluke. It is a d m i t t e d l y also p o s s i b l e t h a t t h e t h i c k e n e d s h e l l is a p a t h o l o g i c a l r e s p o n s e of t h e s n a i l , a d u l l b y p r o d u c t o f i n f e c t i o n . B u t let m e e x p l o r e t h e p o s s i b i l i t y t h a t i t i s a fluke a d a p t a t i o n , b e c a u s e i t i s a n i n t e r e s t i n g i d e a t o use i n f u r t h e r d i s c u s s i o n . I f w e c o n s i d e r s n a i l s h e l l v a r i a t i o n as, i n p a r t , p h e n o t y p i c e x p r e s s i o n o f s n a i l g e n e s , w e m i g h t r e c o g n i z e a n o p t i m u m s h e l l t h i c k n e s s i n the f o l l o w i n g s e n s e . S e l e c t i o n p r e s u m a b l y p e n a l i z e s s n a i l g e n e s t h a t m a k e shells t o o t h i c k , a s w e l l a s t h o s e t h a t m a k e shells t o o t h i n . T h i n shells p r o v i d e i n a d e q u a t e protection.

Genes

for

too-thin

shells

therefore

endanger

their

germ-line

copies, w h i c h are thus not favoured by natural selection. Shells that are too t h i c k p r e s u m a b l y p r o t e c t t h e i r s n a i l s ( a n d t h e e n c l o s e d g e r m - l i n e g e n e s for extra thickness)

s u p e r l a t i v e l y , b u t t h e e x t r a c o s t o f m a k i n g a t h i c k shell

d e t r a c t s f r o m t h e s n a i l ' s s u c c e s s i n s o m e o t h e r w a y . I n t h e e c o n o m y o f the body,

r e s o u r c e s t h a t a r e c o n s u m e d i n m a k i n g e x t r a - t h i c k shells,

c a r r y i n g the e x t r a w e i g h t a r o u n d , making, say,

larger gonads.

and in

m i g h t better h a v e b e e n diverted into

C o n t i n u i n g with the hypothetical example,

t h e r e f o r e , g e n e s for e x t r a - t h i c k shells w i l l t e n d t o i n d u c e i n t h e i r b o d i e s s o m e compensating disadvantage such as relatively small gonads, and they will therefore not be passed on to the next generation so effectively. E v e n if there is, i n f a c t , n o t r a d e - o f f b e t w e e n s h e l l t h i c k n e s s a n d g o n a d s i z e , t h e r e i s b o u n d t o b e s o m e k i n d o f a n a l o g o u s trade-off, a n d a c o m p r o m i s e w i l l b e r e a c h e d a t a n i n t e r m e d i a t e t h i c k n e s s . G e n e s t h a t t e n d t o m a k e s n a i l shells e i t h e r t o o thick or too thin w i l l not prosper in the snail g e n e p o o l .

Host Phenotypes of Parasite Genes

2 1 1

B u t this w h o l e a r g u m e n t p r e s u p p o s e s t h a t t h e o n l y g e n e s t h a t h a v e p o w e r over variation in shell thickness are snail genes. W h a t if s o m e of the c a u s a l factors t h a t a r e , b y d e f i n i t i o n , e n v i r o n m e n t a l f r o m t h e s n a i l ' s p o i n t o f v i e w , turn o u t to be g e n e t i c from s o m e o t h e r p o i n t of v i e w , say t h a t of the fluke? Suppose we a d o p t the suggestion m a d e a b o v e that some fluke genes are c a p a b l e , t h r o u g h a n i n f l u e n c e o n s n a i l p h y s i o l o g y , o f e x e r t i n g a n effect o n snail shell t h i c k n e s s . I f shell t h i c k n e s s i n f l u e n c e s t h e r e p l i c a t i o n s u c c e s s o f such fluke genes, n a t u r a l selection is b o u n d to w o r k on their frequencies relative to their alleles in the fluke g e n e - p o o l . C h a n g e s in snail shell thickness m a y b e r e g a r d e d , t h e n , a t l e a s t i n p a r t , a s p o t e n t i a l a d a p t a t i o n s for t h e benefit o f f l u k e g e n e s . N o w , the o p t i m u m shell thickness from the point of v i e w of the fluke genes is h a r d l y likely to be the s a m e as the o p t i m u m from the p o i n t of v i e w of snail g e n e s . F o r i n s t a n c e , s n a i l g e n e s w i l l b e s e l e c t e d for t h e i r b e n e f i c i a l effects o n snail

reproduction

well

as snail survival,

but

(except

under special

c i r c u m s t a n c e s w h i c h w e s h a l l c o m e o n to) f l u k e g e n e s m a y v a l u e s n a i l survival b u t they will not v a l u e snail r e p r o d u c t i o n at all. In the i n e v i t a b l e trade-off b e t w e e n

the d e m a n d s

of snail

survival

and

snail

reproduction,

therefore, snail genes w i l l be selected to p r o d u c e an o p t i m a l c o m p r o m i s e , while fluke genes will

be selected

to d e v a l u e snail r e p r o d u c t i o n to the

a d v a n t a g e of snail s u r v i v a l , a n d h e n c e to t h i c k e n the shell. A t h i c k e n i n g of the shell

parasitized

snails

is,

it will

remembered,

the

observed

phenomenon with which we began. It m a y be objected here that, a l t h o u g h a fluke has no direct stake in the r e p r o d u c t i o n o f its o w n s n a i l h o s t , i t d o e s h a v e a s t a k e i n t h e r e b e i n g a n e w g e n e r a t i o n o f snails a t l a r g e . T h i s i s t r u e , b u t w e m u s t b e v e r y c a r e f u l b e f o r e w e use t h e f a c t t o p r e d i c t t h a t s e l e c t i o n w o u l d f a v o u r f l u k e a d a p t a t i o n s t o e n h a n c e s n a i l r e p r o d u c t i o n . T h e q u e s t i o n w e h a v e t o ask i s t h i s . G i v e n t h a t the f l u k e g e n e - p o o l w a s d o m i n a t e d b y g e n e s t h a t a i d e d s n a i l r e p r o d u c t i o n a t the e x p e n s e o f s n a i l s u r v i v a l , w o u l d s e l e c t i o n f a v o u r a selfish f l u k e g e n e t h a t s a c r i f i c e d t h e r e p r o d u c t i o n o f its p a r t i c u l a r s n a i l h o s t ,

even

parasitically

c a s t r a t e d t h e s n a i l , i n t h e i n t e r e s t o f p r o l o n g i n g t h e life o f t h a t h o s t , a n d h e n c e o f p r o m o t i n g its o w n s u r v i v a l a n d r e p r o d u c t i o n ? E x c e p t u n d e r s p e c i a l circumstances the a n s w e r is surely y e s ; such a rare g e n e w o u l d i n v a d e the fluke gene-pool,

since

could

exploit

the

free

supply

of n e w

snails

encouraged by the public-spirited majority of the fluke p o p u l a t i o n . In other words, f a v o u r i n g snail r e p r o d u c t i o n at the e x p e n s e of snail s u r v i v a l w o u l d n o t b e a f l u k e E S S . F l u k e g e n e s t h a t m a n a g e t o shift t h e s n a i l ' s i n v e s t m e n t o f resources a w a y from r e p r o d u c t i o n a n d into s u r v i v a l w i l l tend to be f a v o u r e d in the fluke g e n e - p o o l .

It is entirely plausible, therefore, that the extra

t h i c k n e s s of shells o b s e r v e d in p a r a s i t i z e d s n a i l s is a fluke a d a p t a t i o n . O n this h y p o t h e s i s , t h e s h e l l p h e n o t y p e i s a s h a r e d p h e n o t y p e , i n f l u e n c e d by fluke genes as w e l l as by snail genes, j u s t as the b e a v e r d a m is a p h e n o t y p e

2 1 2

shared

Host Phenotypes o f Parasite Genes

by genes in more than one individual beaver.

A c c o r d i n g t o the

hypothesis, there are t w o o p t i m u m thicknesses of snail shells: a relatively thick fluke o p t i m u m , a n d a s o m e w h a t thinner snail o p t i m u m . T h e observed t h i c k n e s s i n p a r a s i t i z e d snails w i l l p r o b a b l y b e s o m e w h e r e b e t w e e n the t w o o p t i m a , since snail genes a n d fluke genes are both in a position to exert p o w e r , a n d they are e x e r t i n g their p o w e r in opposite directions. A s for p a r a s i t e - f r e e s n a i l s , i t m i g h t b e e x p e c t e d t h a t t h e i r shells w o u l d h a v e the s n a i l - o p t i m a l thickness, since there are no fluke genes to exert p o w e r . T h i s is too simple, h o w e v e r . If the population at large has a high incidence of fluke infestation,

the g e n e - p o o l will p r o b a b l y contain genes that tend to

c o m p e n s a t e for t h e t h i c k e n i n g effect o f f l u k e g e n e s . T h i s w o u l d l e a d t o uninfected thinner

snails

even

thicknesses

having

than

the

fluke-free

over-compensating snail

optimum.

areas should

phenotypes,

therefore

shells

predict

intermediate

that that

between

are shell

those o f

i n f e c t e d s n a i l s a n d u n i n f e c t e d snails i n f l u k e - i n f e s t e d a r e a s . I d o n o t k n o w o f a n y e v i d e n c e b e a r i n g o n this p r e d i c t i o n , b u t i t w o u l d b e i n t e r e s t i n g t o l o o k . N o t e t h a t this p r e d i c t i o n d o e s n o t d e p e n d o n a n y a d hoc a s s u m p t i o n a b o u t snails ' w i n n i n g ' o r f l u k e s ' w i n n i n g ' . I t a s s u m e s t h a t b o t h s n a i l g e n e s a n d f l u k e g e n e s e x e r t some p o w e r o v e r t h e s n a i l p h e n o t y p e . T h e p r e d i c t i o n w i l l follow regardless of the q u a n t i t a t i v e details of that p o w e r . F l u k e s l i v e i n s i d e s n a i l shells in a sense t h a t is n o t t o o far r e m o v e d from the sense i n w h i c h s n a i l s l i v e i n s i d e s n a i l shells, a n d c a d d i s l a r v a e l i v e i n s i d e t h e i r stone houses. H a v i n g a c c e p t e d the idea that the form a n d c o l o u r of a caddis house

might

constitute

phenotypic

expression

of caddis genes,

it is not

d i f f i c u l t t o a c c e p t t h e i d e a o f t h e f o r m a n d c o l o u r o f a s n a i l shell b e i n g phenotypic

expression of genes in a fluke inside the snail.

If we could

fancifully i m a g i n e a fluke g e n e a n d a snail g e n e intelligently discussing with a c a d d i s g e n e t h e p r o b l e m s o f m a k i n g a h a r d o u t e r w a l l for p r o t e c t i o n , I d o u b t i f t h e c o n v e r s a t i o n w o u l d m a k e a n y r e f e r e n c e t o t h e fact t h a t the f l u k e w a s a parasite w h i l e the c a d d i s a n d the snail w e r e not. T h e rival merits of s e c r e t i n g c a l c i u m c a r b o n a t e , r e c o m m e n d e d b y the f l u k e a n d t h e s n a i l g e n e s , versus p i c k i n g up stones, preferred by the caddis g e n e , w o u l d be discussed. T h e r e m i g h t be s o m e reference to the fact that a c o n v e n i e n t a n d e c o n o m i c a l w a y o f s e c r e t i n g c a l c i u m c a r b o n a t e i n v o l v e s t h e use o f a s n a i l . B u t , from the gene's-eye viewpoint,

suspect that the c o n c e p t of parasitism w o u l d be

treated as irrelevant. A l l three genes m i g h t regard themselves as parasitic, or alternatively

using

comparable

levers

of power

influence

their

respective w o r l d s so as to s u r v i v e . T h e l i v i n g cells of the snail w o u l d be regarded

by the snail gene and

t h e f l u k e g e n e a s useful o b j e c t s t o b e

m a n i p u l a t e d i n t h e o u t s i d e w o r l d , i n e x a c t l y t h e s a m e sense a s t h e stones o n the b o t t o m o f the stream w o u l d b e r e g a r d e d b y the c a d d i s g e n e . B y d i s c u s s i n g i n o r g a n i c s n a i l shells, I h a v e r e t a i n e d c o n t i n u i t y w i t h the caddis houses a n d o t h e r n o n - l i v i n g artefacts of the previous c h a p t e r , thereby

Host Phenotypes of Parasite Genes

213

pursuing my policy of sustaining credulity by e x t e n d i n g the c o n c e p t of the p h e n o t y p e g r a d u a l l y by insensible degrees. B u t n o w it is time to grasp the l i v i n g s n a i l f i r m l y b y t h e h o r n s . F l u k e s o f t h e g e n u s Leucochloridium i n v a d e t h e h o r n s o f snails w h e r e t h e y c a n b e s e e n t h r o u g h t h e s k i n ,

conspicuously

p u l s a t i n g . T h i s t e n d s t o m a k e b i r d s , w h o a r e t h e n e x t h o s t i n t h e life c y c l e o f the f l u k e , b i t e off t h e t e n t a c l e s m i s t a k i n g t h e m , W i c k l e r ( 1 9 6 8 ) s u g g e s t s , for insects. W h a t i s i n t e r e s t i n g h e r e i s t h a t t h e f l u k e s s e e m a l s o t o m a n i p u l a t e t h e behaviour o f t h e s n a i l s . W h e t h e r i t i s b e c a u s e t h e s n a i l ' s e y e s a r e a t t h e e n d s o f the h o r n s , o r w h e t h e r t h r o u g h s o m e m o r e i n d i r e c t p h y s i o l o g i c a l r o u t e , t h e fluke m a n a g e s to c h a n g e the snail's b e h a v i o u r w i t h respect to light. T h e n o r m a l n e g a t i v e p h o t o t a x i s i s r e p l a c e d i n i n f e c t e d snails b y p o s i t i v e l i g h t s e e k i n g . T h i s c a r r i e s t h e m u p t o o p e n sites w h e r e t h e y a r e p r e s u m a b l y m o r e l i k e l y t o b e e a t e n b y b i r d s , a n d this b e n e f i t s t h e f l u k e . O n c e a g a i n , i f this i s t o b e r e g a r d e d a s a p a r a s i t i c a d a p t a t i o n , a n d i n d e e d it is widely so regarded (Wickler 1968; H o l m e s & Bethel 1 9 7 2 ) , we are forced to postulate the s o m e t i m e existence of genes in the parasite g e n e - p o o l that influenced

the

b e h a v i o u r o f hosts,

since all D a r w i n i a n adaptations

e v o l v e d by the selection of genes. By definition such genes w e r e genes 'for' snail b e h a v i o u r , a n d t h e s n a i l b e h a v i o u r h a s t o b e r e g a r d e d a s p a r t o f t h e phenotypic expression of fluke genes. T h e genes in one organism's cells, then, c a n h a v e e x t e n d e d p h e n o t y p i c i n f l u e n c e o n t h e l i v i n g b o d y o f a n o t h e r o r g a n i s m ; i n this c a s e a p a r a s i t e ' s genes

find

phenotypic

expression

the

behaviour

o f its

host.

The

p a r a s i t o l o g y l i t e r a t u r e i s full o f i n t e r e s t i n g e x a m p l e s w h i c h a r e n o w u s u a l l y i n t e r p r e t e d a s a d a p t i v e m a n i p u l a t i o n o f hosts b y p a r a s i t e s ( e . g . H o l m e s & Bethel 1 9 7 2 ; L o v e 1980). It has not, to be sure, a l w a y s b e e n f a s h i o n a b l e a m o n g parasitologists to m a k e such interpretations explicit. For instance, an important review of parasitic castration in C r u s t a c e a

(Reinhard

1956)

packed with detailed information and speculation on the precise physiologic a l r o u t e s b y w h i c h p a r a s i t e s c a s t r a t e t h e i r hosts, b u t i s a l m o s t d e v o i d o f discussion o n w h y t h e y m i g h t h a v e b e e n selected t o d o so, o r w h e t h e r , instead, castration is s i m p l y a fortuitous b y p r o d u c t of parasitization. It m a y be an interesting indication of c h a n g i n g scientific fashions that a m o r e recent review (Baudoin 1975) extensively considers the functional significance of parasitic castration from the i n d i v i d u a l parasite's point o f v i e w . B a u d o i n c o n c l u d e s : ' T h e m a i n theses o f this p a p e r a r e ( 1 ) t h a t p a r a s i t i c c a s t r a t i o n c a n b e v i e w e d a s a p a r a s i t e ' s a d a p t a t i o n a n d (2) t h a t a d v a n t a g e s d e r i v e d f r o m this a d a p t a t i o n a r e a r e s u l t o f r e d u c t i o n i n h o s t r e p r o d u c t i v e effort; w h i c h i n t u r n g i v e s rise t o i n c r e a s e d h o s t s u r v i v o r s h i p , i n c r e a s e d h o s t g r o w t h and/or increased e n e r g y a v a i l a b l e to the parasite t h e r e b y i n c r e a s i n g the p a r a s i t e ' s D a r w i n i a n f i t n e s s . ' T h i s is, o f c o u r s e , v e r y m u c h t h e a r g u m e n t I h a v e just followed in discussing parasite-induced t h i c k e n i n g of snail shells. A g a i n , a b e l i e f that parasitic castration is a parasite a d a p t a t i o n l o g i c a l l y

Host Phenotypes of Parasite Genes

214

i m p l i e s t h a t t h e r e m u s t b e , o r a t least m u s t h a v e b e e n , p a r a s i t e g e n e s 'for' changes

host

physiology.

T h e symptoms of parasitic

castration,

sex-

c h a n g e , increased size, or w h a t e v e r they m a y be, are properly regarded as extended phenotypic manifestations of parasite genes. The

alternative

physiology

and

pathological

Baudoin's

interpretation

that

changes

b e h a v i o u r are not parasite adaptations,

byproducts

infection.

Consider

the

host

but simply dull

parasitic

barnacle

( t h o u g h in its a d u l t s t a g e it l o o k s m o r e l i k e a f u n g u s ) Sacculina. It m i g h t be said t h a t Sacculina d o e s n o t d i r e c t l y b e n e f i t f r o m t h e c a s t r a t i o n o f its c r a b host, but s i m p l y sucks n u t r i m e n t from all t h r o u g h the host's b o d y , and as a side-effect o f its d e v o u r i n g t h e tissues o f t h e g o n a d s t h e c r a b s h o w s t h e s y m p t o m s o f castration. I n support o f the a d a p t a t i o n hypothesis, h o w e v e r , B a u d o i n points to those cases in w h i c h parasites a c h i e v e the castration by synthesis of host h o r m o n e s , surely a specific a d a p t a t i o n rather than a b o r i n g b y p r o d u c t . E v e n in those cases w h e r e the castration is initially caused as a b y p r o d u c t o f t h e d e v o u r i n g o f g o n a d a l tissue, m y s u s p i c i o n i s t h a t s e l e c t i o n would

subsequently

act

parasites

modify

the

details

their

p h y s i o l o g i c a l effects o n hosts, m o d i f y t h e m i n a w a y f a v o u r a b l e t o t h e p a r a s i t e ' s w e l l - b e i n g . Sacculina p r e s u m a b l y h a s s o m e o p t i o n s o v e r w h i c h p a r t s o f t h e c r a b ' s b o d y its r o o t s y s t e m i n v a d e s f i r s t . N a t u r a l s e l e c t i o n i s s u r e l y l i k e l y t o f a v o u r g e n e s i n Sacculina t h a t c a u s e i t t o i n v a d e g o n a d a l tissue before i n v a d i n g v i t a l o r g a n s o n w h i c h t h e c r a b ' s s u r v i v a l d e p e n d s . A p p l y i n g this k i n d o f a r g u m e n t a t a m o r e d e t a i l e d l e v e l , s i n c e g o n a d a l d e s t r u c t i o n has m u l t i p l e a n d c o m p l e x effects o n c r a b p h y s i o l o g y , a n a t o m y a n d b e h a v i o u r , i t is entirely reasonable to guess that selection w o u l d act on parasites to finetune

their

initially

castration

fortuitous

t e c h n i q u e so

consequences

as to increase

of castration.

p a r a s i t o l o g i s t s w o u l d a g r e e w i t h this f e e l i n g

their benefit from

(P.

believe O.

many

Lawrence,

the

modern personal

c o m m u n i c a t i o n ) . A l l that I am a d d i n g , then, is the l o g i c a l point that the c o m m o n b e l i e f t h a t p a r a s i t i c c a s t r a t i o n i s a n a d a p t a t i o n i m p l i e s t h a t the m o d i f i e d host p h e n o t y p e i s p a r t o f t h e e x t e n d e d p h e n o t y p e o f p a r a s i t e g e n e s . P a r a s i t e s often s t u n t t h e g r o w t h of t h e i r hosts, a n d it is e a s y to see this as a b o r i n g b y p r o d u c t o f i n f e c t i o n . M o r e i n t e r e s t t h e r e f o r e a t t a c h e s t o those r a r e r c a s e s i n w h i c h p a r a s i t e s e n h a n c e host g r o w t h , a n d I h a v e a l r e a d y m e n t i o n e d t h e c a s e o f t h e t h i c k e n e d s n a i l s h e l l s . C h e n g ( 1 9 7 3 , p . 22) b e g i n s his a c c o u n t of such cases w i t h a r e v e a l i n g sentence: ' A l t h o u g h one generally considers p a r a s i t e s t o b e d e t r i m e n t a l t o t h e i r hosts a n d c a u s e t h e loss o f e n e r g y a n d poor health, instances are k n o w n w h e r e the o c c u r r e n c e of parasites actually i n d u c e s e n h a n c e d g r o w t h o f t h e h o s t . ' B u t C h e n g i s h e r e s o u n d i n g like a medical doctor rather than

like a

Darwinian

biologist.

If 'detriment'

defined in terms of r e p r o d u c t i v e success rather than survival a n d 'health', it i s p r o b a b l e t h a t g r o w t h - e n h a n c e m e n t i s i n d e e d d e t r i m e n t a l t o t h e host, for t h e r e a s o n s g i v e n i n m y d i s c u s s i o n o f s n a i l shells.

N a t u r a l s e l e c t i o n has

Host P h e n o t y p e s o f P a r a s i t e G e n e s

215

p r e s u m a b l y f a v o u r e d an o p t i m a l host size, a n d if a parasite causes the host to d e v i a t e f r o m this size in either direction it is p r o b a b l y h a r m i n g t h e h o s t ' s r e p r o d u c t i v e success, e v e n if it is at the s a m e time p r o m o t i n g host s u r v i v a l . A l l the e x a m p l e s o f g r o w t h - e n h a n c e m e n t g i v e n b y C h e n g c a n b e easily understood as parasite-induced switches of resources a w a y from investment i n host r e p r o d u c t i o n , w h i c h i s o f n o i n t e r e s t t o t h e p a r a s i t e , t o t h e g r o w t h and survival of the host's o w n b o d y , w h i c h is of g r e a t interest to the parasite (again we must b e w a r e of the group-selectionist p l e a that the existence of a n e w g e n e r a t i o n o f hosts i s o f i m p o r t a n c e t o t h e p a r a s i t e species). M i c e i n f e c t e d b y l a r v a e o f t h e t a p e w o r m Spirometra mansanoides g r o w faster t h a n u n i n f e c t e d m i c e . I t h a s b e e n s h o w n t h a t t h e t a p e w o r m s a c h i e v e this b y secreting a substance resembling a mouse g r o w t h h o r m o n e . M o r e d r a m a t i c a l l y , b e e t l e l a r v a e o f t h e g e n u s Tribolium, w h e n i n f e c t e d b y t h e s p o r o z o a n Nosema, u s u a l l y fail t o m e t a m o r p h o s e i n t o a d u l t s . I n s t e a d t h e y c o n t i n u e t o g r o w t h r o u g h a s m a n y a s six e x t r a l a r v a l m o u l t s , e n d i n g u p a s g i a n t l a r v a e weighing more than twice as m u c h as non-parasitized controls. Evidence suggests

that

this

m a j o r shift

beetle

priorities,

from

reproduction

i n d i v i d u a l g r o w t h , i s d u e t o t h e s y n t h e s i s o f j u v e n i l e h o r m o n e , o r its c l o s e a n a l o g u e , b y t h e p r o t o z o a n p a r a s i t e . A g a i n this i s o f i n t e r e s t b e c a u s e , a s a l r e a d y s u g g e s t e d for t h e c a s e o f p a r a s i t i c c a s t r a t i o n o f Crustacea, i t m a k e s the

boring

special

byproduct

molecules

theory

ordinarily

all

but

untenable. Juvenile

synthesized

insects,

not

hormones protozoa.

are The

synthesis o f a n i n s e c t h o r m o n e b y a p r o t o z o a n p a r a s i t e h a s t o b e r e g a r d e d a s a specific a n d r a t h e r e l a b o r a t e a d a p t a t i o n . T h e e v o l u t i o n o f t h e c a p a c i t y t o s y n t h e s i z e j u v e n i l e h o r m o n e b y Nosema m u s t h a v e c o m e a b o u t t h r o u g h t h e s e l e c t i o n o f g e n e s i n t h e Nosema g e n e - p o o l . T h e p h e n o t y p i c effect o f t h e s e g e n e s , w h i c h led t o t h e i r s u r v i v a l i n t h e Nosema g e n e - p o o l , w a s a n e x t e n d e d p h e n o t y p i c effect, a n effect w h i c h m a n i f e s t e d i t s e l f i n b e e t l e b o d i e s . O n c e a g a i n t h e p r o b l e m o f i n d i v i d u a l b e n e f i t v e r s u s g r o u p b e n e f i t arises, and in an a c u t e form. A p r o t o z o a n is so small in c o m p a r i s o n w i t h a beetle l a r v a t h a t a s i n g l e p r o t o z o a n , o n its o w n , c o u l d n o t m u s t e r a s u f f i c i e n t d o s e o f h o r m o n e t o affect the b e e t l e . H o r m o n e m a n u f a c t u r e m u s t b e a g r o u p effort by large n u m b e r s of i n d i v i d u a l p r o t o z o a . It benefits all i n d i v i d u a l parasites i n the b e e t l e , b u t i t m u s t a l s o cost e a c h i n d i v i d u a l s o m e t h i n g t o a d d his t i n y c o n t r i b u t i o n t o t h e g r o u p c h e m i c a l effort. I f t h e i n d i v i d u a l p r o t o z o a w e r e genetically heterogeneous, consider w h a t would happen. A s s u m e a majority of protozoa cooperating in synthesizing hormone. An individual with a rare g e n e t h a t m a d e h i m o p t o u t o f t h e g r o u p effort w o u l d s a v e h i m s e l f t h e c o s t o f synthesis. S u c h a s a v i n g w o u l d be of i m m e d i a t e benefit to h i m , a n d to the selfish g e n e t h a t m a d e h i m o p t o u t . T h e loss o f his c o n t r i b u t i o n t o t h e g r o u p synthesis w o u l d h u r t his r i v a l s j u s t a s m u c h a s i t h u r t h i m . I n a n y c a s e t h e loss t o t h e g r o u p ' s

productivity would

be very small,

though

it w o u l d

represent a major s a v i n g to him. T h e r e f o r e , e x c e p t u n d e r special conditions,

216

Host Phenotypes of Parasite Genes

taking part in a c o o p e r a t i v e g r o u p synthesis together w i t h genetic rivals is n o t a n e v o l u t i o n a r i l y s t a b l e s t r a t e g y . W e m u s t t h e r e f o r e p r e d i c t t h a t all the Nosema i n a g i v e n b e e t l e w i l l b e f o u n d t o b e c l o s e r e l a t i v e s , p r o b a b l y a n identical c l o n e . I d o n ' t k n o w of a n y direct e v i d e n c e here, but the expectation i s i n l i n e w i t h t h e t y p i c a l s p o r o z o a n life c y c l e . Baudoin

properly

emphasizes

the

analogous

point

connection with

p a r a s i t i c c a s t r a t i o n . H e h a s a s e c t i o n e n t i t l e d ' K i n s h i p o f c a s t r a t o r s i n the same

individual

invariably

host',

produced

offspring . . . parasitic

which

either

single

castration

says

'Parasitic

parasites

usually

castration by

produced

their either

almost

immediate by

single

g e n o t y p e s or by v e r y closely related g e n o t y p e s . M e t a c e r c a r i a l infections in snails a r e e x c e p t i o n s . . . I n t h e s e c a s e s , h o w e v e r , p a r a s i t i c c a s t r a t i o n m a y b e i n c i d e n t a l . ' B a u d o i n i s f u l l y a w a r e o f t h e s i g n i f i c a n c e o f these f a c t s : ' . . . the g e n e t i c r e l a t i o n s h i p o f c a s t r a t o r s w i t h i n i n d i v i d u a l hosts i s s u c h t h a t n a t u r a l s e l e c t i o n a t t h e l e v e l o f i n d i v i d u a l g e n o t y p e s c a n a c c o u n t for t h e o b s e r v e d effects'. M a n y f a s c i n a t i n g e x a m p l e s o f p a r a s i t e s m a n i p u l a t i n g the b e h a v i o u r o f t h e i r hosts c a n b e g i v e n . F o r n e m a t o m o r p h l a r v a e w h o n e e d t o b r e a k o u t o f t h e i r i n s e c t hosts a n d g e t i n t o w a t e r w h e r e t h e y l i v e a s a d u l t s , ' . . . a m a j o r d i f f i c u l t y i n t h e p a r a s i t e ' s life i s t h e r e t u r n t o w a t e r .

I t is, t h e r e f o r e , o f

p a r t i c u l a r i n t e r e s t t h a t t h e p a r a s i t e a p p e a r s t o affect t h e b e h a v i o u r o f its h o s t , a n d " e n c o u r a g e s " i t t o r e t u r n t o w a t e r . T h e m e c h a n i s m b y w h i c h this i s a c h i e v e d i s o b s c u r e , b u t t h e r e a r e sufficient i s o l a t e d r e p o r t s t o certify t h a t t h e p a r a s i t e d o e s i n f l u e n c e its h o s t , a n d often s u i c i d a l l y for t h e host . . . O n e of the m o r e d r a m a t i c reports describes an infected bee flying o v e r a pool and, w h e n a b o u t s i x feet o v e r it, d i v i n g s t r a i g h t i n t o t h e w a t e r . I m m e d i a t e l y o n i m p a c t the g o r d i a n w o r m burst out and s w a m into the w a t e r , the m a i m e d b e e b e i n g left t o d i e ' ( C r o l l 1 9 6 6 ) . P a r a s i t e s t h a t h a v e a life c y c l e i n v o l v i n g a n i n t e r m e d i a t e host, from w h i c h t h e y h a v e t o m o v e t o a d e f i n i t i v e h o s t , o f t e n m a n i p u l a t e t h e b e h a v i o u r o f the i n t e r m e d i a t e h o s t t o m a k e i t m o r e l i k e l y t o b e e a t e n b y t h e d e f i n i t i v e host. W e h a v e a l r e a d y s e e n a n e x a m p l e o f this, t h e c a s e o f Leucochloridium i n snail tentacles. H o l m e s and Bethel

(1972)

have reviewed many examples, and

they h a v e t h e m s e l v e s p r o v i d e d us w i t h o n e of the most t h o r o u g h l y researched cases (Bethel & H o l m e s 1 9 7 3 ) . T h e y studied t w o species of a c a n t h o c e p h a l a n w o r m s , Polymorphus paradoxus a n d P. marilis.

Both

use a f r e s h w a t e r

'shrimp'

( r e a l l y a n a m p h i p o d ) , Gammarus lacustris, a s a n i n t e r m e d i a t e host, a n d b o t h use d u c k s as t h e d e f i n i t i v e h o s t . P. paradoxus, h o w e v e r , s p e c i a l i z e s in the m a l l a r d , w h i c h is a s u r f a c e - d a b b l i n g d u c k , w h i l e P. marilis s p e c i a l i z e s in d i v i n g d u c k s . I d e a l l y t h e n , P . paradoxus m i g h t b e n e f i t b y m a k i n g its s h r i m p s s w i m to the surface, w h e r e they are likely to be eaten by m a l l a r d s , w h i l e P. marilis m i g h t b e n e f i t b y m a k i n g its s h r i m p s a v o i d t h e s u r f a c e . U n i n f e c t e d Gammarus lacustris t e n d to a v o i d l i g h t , a n d s t a y c l o s e to the l a k e

Host Phenotypes of Parasite Genes

217

bottom. Bethel and H o l m e s noticed striking differences in the b e h a v i o u r of s h r i m p s i n f e c t e d w i t h c y s t a c a n t h s o f P . paradoxus. T h e y s t a y e d c l o s e t o t h e surface, and c l u n g tenaciously to surface plants a n d e v e n to the hairs on the researchers' legs. T h i s s u r f a c e - h u g g i n g b e h a v i o u r w o u l d p r e s u m a b l y m a k e them v u l n e r a b l e to predation by d a b b l i n g m a l l a r d s , a n d also by muskrats w h i c h a r e a n a l t e r n a t i v e d e f i n i t i v e host o f P . paradoxus. B e t h e l a n d H o l m e s believe

that

the

habit

clinging

weeds

makes

infected

shrimps

particularly vulnerable to muskrats, w h o gather floating vegetation and take it h o m e to feed off it. L a b o r a t o r y tests c o n f i r m e d t h a t s h r i m p s i n f e c t e d w i t h c y s t a c a n t h s o f P . paradoxus seek t h e l i g h t e d h a l f o f a t a n k , a n d a l s o p o s i t i v e l y a p p r o a c h t h e source of light. T h i s is the opposite of the b e h a v i o u r s h o w n by uninfected s h r i m p s . I n c i d e n t a l l y , i t i s n o t t h a t t h e i n f e c t e d s h r i m p s w e r e g e n e r a l l y sick and floated passively to the surface, as in the c o m p a r a b l e case of C r o w d e n a n d B r o o m ' s ( 1 9 8 0 ) fish. T h e s e s h r i m p s fed a c t i v e l y , o f t e n l e a v i n g t h e s u r f a c e l a y e r t o d o so, b u t w h e n t h e y c a p t u r e d a m o r s e l o f f o o d t h e y p r o m p t l y t o o k i t to the surface to eat it w h e r e a s a n o r m a l s h i m p w o u l d h a v e t a k e n it to the bottom. A n d w h e n startled in mid water, instead of d i v i n g to the b o t t o m as a n o r m a l s h r i m p w o u l d , t h e y h e a d e d for t h e s u r f a c e . S h r i m p s i n f e c t e d b y c y s t a c a n t h s o f t h e o t h e r s p e c i e s , P . marilis, h o w e v e r , d o n o t h u g t h e s u r f a c e . I n l a b o r a t o r y tests t h e y a d m i t t e d l y s o u g h t t h e l i g h t e d h a l f o f a n a q u a r i u m i n p r e f e r e n c e t o t h e d a r k half, b u t t h e y d i d n o t o r i e n t positively t o w a r d s the source of l i g h t : they distributed themselves r a n d o m l y i n the l i g h t e d half, r a t h e r t h a n a t t h e s u r f a c e . W h e n s t a r t l e d , t h e y w e n t t o the b o t t o m r a t h e r t h a n t o t h e s u r f a c e . B e t h e l a n d H o l m e s s u g g e s t t h a t t h e t w o s p e c i e s o f p a r a s i t e m o d i f y t h e b e h a v i o u r o f t h e i r i n t e r m e d i a t e host i n different w a y s , c a l c u l a t e d t o m a k e t h e s h r i m p s m o r e v u l n e r a b l e t o p r e d a t i o n b y t h e i r d e f i n i t i v e hosts, s u r f a c e - f e e d i n g a n d d i v i n g p r e d a t o r s r e s p e c t i v e l y . A later p a p e r (Bethel & H o l m e s 1977) p r o v i d e s partial c o n f i r m a t i o n of this

hypothesis.

Captive

mallards

and

muskrats

the

laboratory

took

s h r i m p s i n f e c t e d w i t h P. paradoxus at a h i g h e r r a t e t h a n t h e y t o o k u n i n f e c t e d s h r i m p s . S h r i m p s i n f e c t e d w i t h P . marilis, h o w e v e r , w e r e n o t t a k e n a n y m o r e often t h a n u n i n f e c t e d o n e s , e i t h e r b y m a l l a r d s o r b y m u s k r a t s .

It would

obviously

predator,

desirable

predicting

that

the

shrimps

reciprocal infected

experiment

with

cystacanths

of P.

diving marilis

w o u l d , i n this c a s e , b e r e l a t i v e l y m o r e v u l n e r a b l e . T h i s e x p e r i m e n t d o e s n o t appear to have been done. Let us provisionally accept Bethel and Holmes's hypothesis, and rephrase i t i n the l a n g u a g e o f t h e e x t e n d e d p h e n o t y p e . T h e a l t e r e d b e h a v i o u r o f t h e shrimp is r e g a r d e d as an a d a p t a t i o n on the part of the a c a n t h o c e p h a l a n p a r a s i t e . I f this h a s c o m e a b o u t t h r o u g h n a t u r a l s e l e c t i o n , t h e r e m u s t h a v e been

genetic

variation

'for'

shrimp

behaviour

the

worm

gene-pool,

o t h e r w i s e t h e r e w o u l d h a v e b e e n n o t h i n g for n a t u r a l s e l e c t i o n t o w o r k o n .

2l8

Host Phenotypes of Parasite Genes

We m a y , therefore, talk of w o r m genes h a v i n g phenotypic expression in s h r i m p b o d i e s , i n j u s t t h e s a m e sense a s w e a r e a c c u s t o m e d t o t a l k i n g o f h u m a n genes h a v i n g phenotypic expression in h u m a n bodies. T h e c a s e o f t h e f l u k e ( ' b r a i n w o r m ' ) Dicrocoelium dendriticum i s often q u o t e d a s a n o t h e r e l e g a n t e x a m p l e o f a p a r a s i t e m a n i p u l a t i n g a n i n t e r m e d i a t e host t o i n c r e a s e its c h a n c e s o f e n d i n g u p i n its d e f i n i t i v e h o s t ( W i c k l e r 1 9 7 6 ; L o v e 1980).

The

definitive

host

ungulate

such

sheep,

and

the

i n t e r m e d i a t e hosts a r e f i r s t a s n a i l a n d t h a n a n a n t . T h e n o r m a l life c y c l e c a l l s for t h e a n t t o b e a c c i d e n t a l l y e a t e n b y t h e s h e e p . I t s e e m s t h a t t h e f l u k e cercaria

achieves

this

a way

analogous

t h a t o f the Leucochloridium

m e n t i o n e d a b o v e . B y b u r r o w i n g i n t o t h e s u b o e s o p h a g e a l g a n g l i o n , the a p t l y n a m e d ' b r a i n w o r m ' c h a n g e s the ant's behaviour. W h e r e a s an uninfected a n t w o u l d n o r m a l l y r e t r e a t i n t o its nest w h e n i t b e c a m e c o l d , i n f e c t e d ants c l i m b to the top of grass stems, c l a m p their j a w s in the plant and remain i m m o b i l e as if asleep. H e r e they are v u l n e r a b l e to b e i n g eaten by the w o r m ' s d e f i n i t i v e h o s t . T h e i n f e c t e d a n t , l i k e a n o r m a l a n t , d o e s r e t r e a t d o w n the g r a s s s t e m t o a v o i d d e a t h f r o m t h e m i d d a y h e a t â&#x20AC;&#x201D; w h i c h w o u l d b e b a d for t h e p a r a s i t e â&#x20AC;&#x201D; b u t i t r e t u r n s t o its a e r i a l r e s t i n g p o s i t i o n i n t h e c o o l o f the afternoon ( L o v e 1980). W i c k l e r (1976) says that of the a p p r o x i m a t e l y fifty c e r c a r i a e t h a t i n f e c t a g i v e n a n t , o n l y o n e b u r r o w s i n t o t h e b r a i n a n d i t dies in the process:

' I t s a c r i f i c e s i t s e l f for t h e b e n e f i t o f t h e o t h e r c e r c a r i a e . '

U n d e r s t a n d a b l y , W i c k l e r therefore predicts that the g r o u p of cercariae in an ant will be found to be a p o l y e m b r y o n i c clone. A n e v e n m o r e e l a b o r a t e e x a m p l e i s t h e c a s e o f c r o w n g a l l , o n e o f t h e few k n o w n p l a n t c a n c e r s ( K e r r 1 9 7 8 ; S c h e l l e t al. 1 9 7 9 ) . E x c e p t i o n a l l y for a c a n c e r i t i s i n d u c e d b y a b a c t e r i u m , Agrobacterium. T h e s e b a c t e r i a i n d u c e t h e c a n c e r in the p l a n t o n l y if they themselves c o n t a i n a Ti plasmid, a small ring of extrachromosomal

DNA.

The

plasmid

may

regarded

a u t o n o m o u s r e p l i c a t o r ( C h a p t e r 9 ) a l t h o u g h , like a n y other D N A replicator, i t c a n n o t s u c c e e d a p a r t f r o m t h e c e l l u l a r m a c h i n e r y p u t t o g e t h e r u n d e r the i n f l u e n c e o f o t h e r D N A r e p l i c a t o r s , i n this c a s e t h o s e o f t h e host. T i g e n e s a r e t r a n s f e r r e d f r o m b a c t e r i a l t o p l a n t c e l l s , a n d t h e i n f e c t e d p l a n t cells a r e i n d u c e d to m u l t i p l y u n c o n t r o l l a b l y , w h i c h is w h y the c o n d i t i o n is called a c a n c e r . T h e T i genes also c a u s e the p l a n t cells t o synthesize large quantities of substances called opines, w h i c h the plants w o u l d not normally make, and w h i c h they c a n n o t use. T h e interesting point is that, in an e n v i r o n m e n t rich in opines, Ti-infected bacteria survive and reproduce m u c h better than noninfected b a c t e r i a . T h i s is b e c a u s e the Ti p l a s m i d provides the b a c t e r i u m with a set o f g e n e s w h i c h e n a b l e t h e b a c t e r i u m t o use t h e o p i n e s a s a s o u r c e o f energy

and

chemicals.

The

plasmids

could

almost

regarded

practising artificial selection in favour of infected bacteria, hence in favour of copies of themselves. T h e opines also function as bacterial 'aphrodisiacs', as K e r r p u t s it, p r o m o t i n g b a c t e r i a l c o n j u g a t i o n a n d t h e r e f o r e p l a s m i d transfer.

Host Phenotypes of Parasite Genes

Kerr

(1978)

concludes:

'It

very

elegant

example

219

of biological

e v o l u t i o n ; it e v e n d e m o n s t r a t e s a p p a r e n t altruism in b a c t e r i a l g e n e s . . . T h e D N A w h i c h is transferred from b a c t e r i u m to p l a n t has no future; it dies w h e n the p l a n t c e l l d i e s . H o w e v e r , b y a l t e r i n g t h e p l a n t c e l l t o p r o d u c e a n o p i n e , i t e n s u r e s (a) p r e f e r e n t i a l s e l e c t i o n o f t h e s a m e D N A i n b a c t e r i a l c e l l s and

(b)

transfer o f t h a t

DNA

to other bacterial

cells.

It demonstrates

evolution a t the level o f genes, not organisms, w h i c h m a y o n l y b e g e n e carriers.' (Such statements are, of course, music to my ears, b u t I h o p e K e r r will forgive my p u b l i c l y w o n d e r i n g at the gratuitous c a u t i o n of ' m a y o n l y b e ' g e n e carriers. It is a bit like s a y i n g ' T h e eyes m a y be the w i n d o w s of the soul' or ' O , my L u v e m a y be like a red red rose'. It m a y h a v e b e e n the w o r k of an editorial hand!) K e r r continues: 'In n a t u r a l l y - i n d u c e d c r o w n galls o n m a n y ( b u t n o t all) hosts, v e r y f e w b a c t e r i a s u r v i v e i n t h e g a l l . . . A t f i r s t s i g h t , i t w o u l d appear that pathogenicity is conferring no biological a d v a n t a g e . It is o n l y w h e n o n e c o n s i d e r s o p i n e p r o d u c t i o n b y t h e h o s t a n d its effect o n bacteria living at the surface of the g a l l , that the strong selective a d v a n t a g e o f g e n e s for p a t h o g e n i c i t y b e c o m e s c l e a r . ' M a y r (1963, pp.

1 9 6 - 1 9 7 ) discusses t h e p h e n o m e n o n o f p l a n t s m a k i n g

g a l l s t o h o u s e i n s e c t s , i n t e r m s s o f a v o u r a b l e t o m y thesis t h a t I c a n q u o t e him verbatim almost without c o m m e n t : W h y . . . s h o u l d a p l a n t m a k e t h e g a l l s u c h a p e r f e c t d o m i c i l e for a n i n s e c t t h a t i s its e n e m y ? A c t u a l l y w e a r e d e a l i n g h e r e w i t h t w o selection pressures. On the o n e h a n d , selection w o r k s on a p o p u l a t i o n of gall

insects

and

favors

those

whose

gall-inducing

chemicals

stimulate the p r o d u c t i o n of galls g i v i n g m a x i m u m p r o t e c t i o n to the y o u n g l a r v a . T h i s , o b v i o u s l y , i s a m a t t e r o f life o r d e a t h for t h e g a l l insect

and

thus

constitutes

very

high

selection

pressure.

The

o p p o s i n g selection pressure on the p l a n t is in most cases quite small b e c a u s e h a v i n g a few galls will depress v i a b i l i t y of the plant host only v e r y s l i g h t l y . T h e ' c o m p r o m i s e ' i n this c a s e i s a l l i n f a v o r o f t h e g a l l insect. T o o h i g h a density of the g a l l insect is u s u a l l y p r e v e n t e d by d e n s i t y - d e p e n d e n t factors not related to the p l a n t host.

M a y r is here i n v o k i n g the e q u i v a l e n t of the i i f e / d i n n e r p r i n c i p l e ' to e x p l a i n w h y the p l a n t d o e s n o t f i g h t b a c k a g a i n s t t h e r e m a r k a b l e m a n i p u l a t i o n b y the i n s e c t . I t i s n e c e s s a r y for m e t o a d d o n l y t h i s . I f M a y r i s r i g h t t h a t t h e g a l l i s a n a d a p t a t i o n for t h e b e n e f i t o f t h e i n s e c t a n d n o t t h e p l a n t , i t c a n h a v e e v o l v e d o n l y t h r o u g h the n a t u r a l selection of genes in the insect g e n e pool. L o g i c a l l y , we h a v e to r e g a r d these as genes w i t h p h e n o t y p i c expression i n p l a n t tissue, i n t h e s a m e sense a s s o m e o t h e r g e n e o f t h e i n s e c t , s a y o n e for e y e c o l o u r , c a n b e s a i d t o h a v e p h e n o t y p i c e x p r e s s i o n i n i n s e c t tissue. C o l l e a g u e s w i t h w h o m I discuss the d o c t r i n e of the e x t e n d e d p h e n o t y p e

220

Host Phenotypes of Parasite Genes

repeatedly c o m e up with the same entertaining speculations. Is it just an a c c i d e n t t h a t w e s n e e z e w h e n g e t t i n g a c o l d , o r c o u l d i t b e a result o f m a n i p u l a t i o n by viruses to increase their c h a n c e s of infecting another host? Do a n y v e n e r e a l diseases increase the libido, e v e n if o n l y b y i n d u c i n g an itch, like e x t r a c t o f S p a n i s h f l y ? D o the b e h a v i o u r a l s y m p t o m s o f rabies infection increase the c h a n c e of the virus b e i n g passed on

(Bacon &

Macdonald

1 9 8 0 ) ? ' W h e n a d o g g e t s r a b i e s , its t e m p e r c h a n g e s q u i c k l y . I t i s often m o r e a f f e c t i o n a t e for a d a y o r t w o , a n d g i v e n t o l i c k i n g its h u m a n c o n t a c t s , a d a n g e r o u s p r a c t i c e , for t h e v i r u s i s a l r e a d y i n its s a l i v a . S o o n i t g r o w s restless a n d w a n d e r s off, r e a d y t o b i t e a n y o n e t h a t g e t s i n its w a y ' Britannica

1977).

E v e n non-carnivorous animals are driven

(Encyclopaedia by the rabies

virus to v i c i o u s biting, and there are recorded cases of h u m a n s contracting t h e d i s e a s e f r o m t h e b i t e s o f n o r m a l l y h a r m l e s s f r u i t - e a t i n g b a t s . A p a r t from the

obvious

wandering'

power

of biting

might very well serve

(Hamilton &

May

spread

saliva-borne

to spread

virus,

'restless

the virus m o r e effectively

1 9 7 7 ) . T h a t the w i d e s p r e a d a v a i l a b i l i t y o f c h e a p air

t r a v e l h a s h a d a d r a m a t i c i m p a c t o n the s p r e a d o f h u m a n d i s e a s e i s o b v i o u s : dare we w o n d e r w h e t h e r the phrase 'travel b u g ' might have a more than metaphorical significance? T h e reader will p r o b a b l y , like me, f i n d such speculations far-fetched. T h e y a r e i n t e n d e d o n l y a s l i g h t - h e a r t e d i l l u s t r a t i o n s o f t h e kind o f t h i n g t h a t m i g h t g o o n (see a l s o E w a l d , 1 9 8 0 , w h o d r a w s a t t e n t i o n t o t h e m e d i c a l s i g n i f i c a n c e o f this k i n d o f t h i n k i n g ) . A l l I r e a l l y n e e d t o e s t a b l i s h i s t h a t i n some e x a m p l e s h o s t s y m p t o m s c a n p r o p e r l y b e r e g a r d e d a s p a r a s i t i c a d a p t a t i o n ; s a y , for instance,

the

Peter

Pan

syndrome

Tribolium

induced

protozoan-

synthesized j u v e n i l e h o r m o n e . G i v e n such an admitted parasite adaptation, t h e c o n c l u s i o n I w i s h t o d r a w i s n o t r e a l l y d i s p u t a b l e . I f host b e h a v i o u r o r p h y s i o l o g y is a parasite a d a p t a t i o n , there must be (have been) parasite genes ' f o r ' m o d i f y i n g t h e h o s t , a n d t h e h o s t m o d i f i c a t i o n s a r e t h e r e f o r e p a r t o f the phenotypic

expression

of those

parasite genes.

The

extended

phenotype

r e a c h e s o u t o f t h e b o d y i n w h o s e c e l l s the g e n e s lie, r e a c h e s o u t t o t h e l i v i n g tissues o f o t h e r o r g a n i s m s . T h e r e l a t i o n s h i p o f Sacculina g e n e t o c r a b b o d y i s n o t i n p r i n c i p l e different f r o m t h e r e l a t i o n s h i p o f c a d d i s g e n e t o s t o n e , n o r i n d e e d different from the r e l a t i o n s h i p o f h u m a n g e n e t o h u m a n s k i n . T h i s i s the f i r s t o f the p o i n t s t h a t I i n t e n d e d t o e s t a b l i s h i n this c h a p t e r . I t h a s t h e c o r o l l a r y , w h i c h I h a v e a l r e a d y e m p h a s i z e d in other terms in C h a p t e r 4, that the b e h a v i o u r of an i n d i v i d u a l m a y n o t a l w a y s b e i n t e r p r e t a b l e a s d e s i g n e d t o m a x i m i z e its o w n g e n e t i c w e l f a r e : i t m a y b e m a x i m i z i n g s o m e b o d y else's g e n e t i c w e l f a r e , i n this c a s e t h a t o f a p a r a s i t e i n s i d e it. I n t h e n e x t c h a p t e r w e s h a l l g o further, a n d see t h a t s o m e o f t h e a t t r i b u t e s o f a n i n d i v i d u a l m a y b e r e g a r d e d a s p h e n o t y p i c expression of genes in other individuals w h o need not necessarily be parasites inside.

Host Phenotypes o f Parasite Genes

2 2 1

T h e s e c o n d p o i n t o f this p r e s e n t c h a p t e r i s t h a t t h e g e n e s t h a t b e a r u p o n any given

extended

phenotypic

trait m a y

conflict

rather

than

concert with one another. I could talk in terms of a n y of the e x a m p l e s g i v e n a b o v e , b u t I shall stick to one, the case of the snail shell t h i c k e n e d by the influence of a fluke. To r e c a p i t u l a t e that story in slightly different terms, a student of snail genetics a n d a student of fluke g e n e t i c s m i g h t e a c h look at the s a m e p h e n o t y p i c v a r i a t i o n , v a r i a t i o n i n s n a i l s h e l l t h i c k n e s s . T h e s n a i l g e n e t i c i s t w o u l d p a r t i t i o n t h e v a r i a n c e between a g e n e t i c a n d a n e n v i r o n mental c o m p o n e n t , by c o r r e l a t i n g the thickness of shells in p a r e n t snails a n d their offspring. T h e f l u k e geneticist w o u l d i n d e p e n d e n t l y p a r t i t i o n the s a m e o b s e r v e d v a r i a n c e i n t o a g e n e t i c a n d a n e n v i r o n m e n t a l c o m p o n e n t , i n his c a s e b y c o r r e l a t i n g t h e shell t h i c k n e s s o f s n a i l s c o n t a i n i n g p a r t i c u l a r f l u k e s w i t h t h e shell t h i c k n e s s o f s n a i l s c o n t a i n i n g t h e o f f s p r i n g o f t h o s e s a m e f l u k e s . As far as the snail g e n e t i c i s t is c o n c e r n e d , t h e fluke c o n t r i b u t i o n is p a r t of w h a t he calls the ' e n v i r o n m e n t a l ' variation.

R e c i p r o c a l l y , for t h e f l u k e

geneticist, v a r i a t i o n d u e to snail genes is ' e n v i r o n m e n t a l ' v a r i a t i o n . An

'extended

geneticist'

would

acknowledge

both

sources

of genetic

variation. He w o u l d h a v e to w o r r y a b o u t the form of their i n t e r a c t i o n â&#x20AC;&#x201D; i s it additive, multiplicative, 'epistatic', etc.?â&#x20AC;&#x201D;but in principle such worries are a l r e a d y familiar to b o t h the snail geneticist a n d the fluke geneticist. W i t h i n a n y o r g a n i s m , different g e n e s i n f l u e n c e t h e s a m e p h e n o t y p i c t r a i t s , a n d t h e f o r m o f the i n t e r a c t i o n i s a p r o b l e m w i t h r e s p e c t t o g e n e s w i t h i n o n e n o r m a l g e n o m e j u s t a s m u c h a s i t i s for g e n e s i n a n ' e x t e n d e d ' g e n o m e . I n t e r a c t i o n s b e t w e e n t h e effects o f s n a i l g e n e a n d f l u k e g e n e a r e , i n p r i n c i p l e , n o d i f f e r e n t f r o m i n t e r a c t i o n s b e t w e e n t h e effects o f o n e s n a i l g e n e a n d a n o t h e r s n a i l gene. A n d yet, it m a y be said, is there not a rather i m p o r t a n t difference? S n a i l gene m a y interact w i t h snail g e n e in a d d i t i v e , m u l t i p l i c a t i v e , or a n y other w a y s , b u t d o they not b o t h h a v e the s a m e interests a t h e a r t ? B o t h h a v e b e e n s e l e c t e d i n t h e p a s t b e c a u s e t h e y w o r k e d for t h e s a m e e n d , t h e s u r v i v a l a n d r e p r o d u c t i o n o f t h e snails t h a t b o r e t h e m . F l u k e g e n e a n d f l u k e g e n e , t o o , a r e w o r k i n g for t h e s a m e e n d , t h e r e p r o d u c t i v e s u c c e s s o f t h e f l u k e . B u t s n a i l gene and fluke g e n e do not h a v e the s a m e interests at heart. O n e is selected to p r o m o t e snail r e p r o d u c t i o n , the other to p r o m o t e fluke r e p r o d u c t i o n . T h e r e i s t r u t h i n t h e p r o t e s t a t i o n s o f the last p a r a g r a p h , b u t i t i s i m p o r t a n t t o b e c l e a r a b o u t e x a c t l y w h e r e t h a t t r u t h lies. I t i s n o t t h a t t h e r e i s s o m e o b v i o u s t r a d e - u n i o n spirit u n i t i n g f l u k e g e n e s a g a i n s t a r i v a l u n i o n o f s n a i l g e n e s . T o persist w i t h this h a r m l e s s a n t h r o p o m o r p h i s m , e a c h g e n e i s f i g h t i n g o n l y its a l l e l e s a t t h e s a m e l o c u s , a n d i t w i l l ' u n i t e ' w i t h g e n e s a t o t h e r l o c i o n l y insofar as d o i n g so assists it in its selfish w a r a g a i n s t its o w n a l l e l e s . A f l u k e g e n e m a y ' u n i t e ' w i t h o t h e r f l u k e g e n e s i n this w a y b u t , e q u a l l y , i f i t w a s c o n v e n i e n t t o d o so, i t m i g h t u n i t e w i t h p a r t i c u l a r s n a i l g e n e s . A n d i f i t remains true that snail genes are in p r a c t i c e selected to w o r k t o g e t h e r w i t h

Host Phenotypes of Parasite Genes

222

e a c h other a n d against an o p p o s i n g g a n g of fluke genes, the reason is only that snail g e n e s tend to g a i n from the s a m e events in the w o r l d as do other snail g e n e s . F l u k e genes stand to g a i n from other events. A n d the real reason w h y snail genes stand to g a i n from the s a m e events as e a c h other, w h i l e fluke g e n e s s t a n d t o g a i n f r o m a different set o f e v e n t s , i s s i m p l y t h i s : a l l s n a i l g e n e s share

the same

route into

the

next generationâ&#x20AC;&#x201D;snail

gametes.

All fluke

g e n e s , o n t h e o t h e r h a n d , m u s t use a different r o u t e , f l u k e c e r c a r i a e , t o g e t i n t o t h e n e x t g e n e r a t i o n . I t i s this f a c t a l o n e t h a t ' u n i t e s ' s n a i l g e n e s against fluke genes and v i c e versa. If it w e r e the case that the parasite genes passed out of the host's b o d y inside the host's g a m e t e s , things m i g h t be v e r y d i f f e r e n t . T h e i n t e r e s t s o f host g e n e s a n d p a r a s i t e g e n e s m i g h t n o t b e q u i t e identical, but they w o u l d then be v e r y m u c h closer than in the case of fluke a n d snail. I t f o l l o w s f r o m t h e e x t e n d e d p h e n o t y p e v i e w o f life, t h e n , t h a t c r u c i a l i m p o r t a n c e a t t a c h e s t o the m e a n s b y w h i c h parasites p r o p a g a t e their genes out of a g i v e n host into a n e w host. If the parasite's m e a n s of genetic exit f r o m t h e h o s t ' s b o d y i s t h e s a m e a s t h e h o s t ' s , n a m e l y t h e host's g a m e t e s o r s p o r e s , t h e r e w i l l b e r e l a t i v e l y little c o n f l i c t b e t w e e n t h e ' i n t e r e s t s ' o f p a r a s i t e and

host

genes.

For

example,

both

would

'agree'

about

the

optimum

t h i c k n e s s o f t h e h o s t ' s s h e l l . B o t h w i l l b e s e l e c t e d t o w o r k n o t o n l y for host s u r v i v a l b u t for host r e p r o d u c t i o n a s w e l l , w i t h a l l t h a t t h a t e n t a i l s . T h i s m i g h t i n c l u d e host s u c c e s s i n c o u r t s h i p a n d e v e n , i f t h e p a r a s i t e s a s p i r e t o b e ' i n h e r i t e d ' b y t h e h o s t ' s o w n o f f s p r i n g , host s u c c e s s i n p a r e n t a l c a r e . U n d e r s u c h c i r c u m s t a n c e s t h e i n t e r e s t s o f p a r a s i t e a n d host w o u l d

be likely to

c o i n c i d e t o s u c h a n e x t e n t t h a t i t m i g h t b e c o m e difficult for u s t o d e t e c t t h a t a

separate

parasite

existed

all.

clearly

of g r e a t

interest

for

parasitologists a n d 'symbiologists' to study such v e r y intimate parasites or s y m b i o n t s , s y m b i o n t s w i t h an interest in the success of their host's g a m e t e s as w e l l as in the s u r v i v a l of their host's b o d y . S o m e lichens m i g h t be promisi n g e x a m p l e s , a n d s o m i g h t b a c t e r i a l e n d o s y m b i o n t s o f insects w h i c h a r e t r a n s m i t t e d t r a n s o v a r i a l l y a n d i n s o m e c a s e s s e e m t o i n f l u e n c e t h e host sex ratio (Peleg & Norris 1972). Mitochondria,

chloroplasts,

and

other

cell

organelles

with

their o w n

r e p l i c a t i n g D N A m i g h t a l s o b e g o o d c a n d i d a t e s for s t u d y i n this c o n n e c t i o n . A f a s c i n a t i n g a c c o u n t o f c e l l o r g a n e l l e s a n d m i c r o o r g a n i s m s seen a s s e m i autonomous

symbionts

proceedings

of a

inhabiting

symposium

Richmond and Smith

entitled

cellular The

ecology

Cell

given

Habitat,

the

edited

(1979). T h e closing words of Smith's introductory

chapter are particularly m e m o r a b l e and apposite: 'In non-living habitats, an organism

either

exists

or it does

not.

the

cell

habitat,

invading

o r g a n i s m c a n p r o g r e s s i v e l y lose p i e c e s o f itself, s l o w l y b l e n d i n g i n t o t h e general

background,

Indeed,

one is

its

reminded

former

existence

of Alice

betrayed

Wonderland's

only

some

relic.

encounter with

the

Host P h e n o t y p e s o f P a r a s i t e G e n e s

223

C h e s h i r e C a t . A s she w a t c h e d it, " i t v a n i s h e d q u i t e s l o w l y , b e g i n n i n g w i t h the tail, a n d e n d i n g w i t h t h e g r i n , w h i c h r e m a i n e d s o m e t i m e after t h e rest o f it had g o n e " ' (Smith 1979). M a r g u l i s (1976) gives an interesting survey of all t h e d e g r e e s o f v a n i s h i n g o f t h e g r i n . R i c h m o n d ' s (1979) chapter, too, is very c o n g e n i a l to the present thesis: 'It is c o n v e n t i o n a l to regard cells as units of b i o l o g i c a l function. A n o t h e r v i e w , p a r t i c u l a r l y a p p o s i t e t o this s y m p o s i u m , i s t h a t t h e c e l l i s t h e m i n i m a l u n i t capable o f replicating D N A . . . S u c h a c o n c e p t places D N A a t the centre o f biology. T h u s D N A is not r e g a r d e d s i m p l y as a h e r e d i t a r y m e a n s of ensuring the l o n g t e r m s u r v i v a l o f t h e o r g a n i s m s o f w h i c h i t f o r m s p a r t . R a t h e r , i t stresses t h a t t h e p r i m a r y r o l e o f cells i s t o m a x i m i z e t h e a m o u n t a n d d i v e r s i t y o f D N A i n t h e b i o s p h e r e . . . ' T h i s last r e m a r k , i n c i d e n t a l l y , i s u n f o r t u n a t e . M a x i m i z i n g the a m o u n t and diversity of D N A in the biosphere is the concern of nobody and nothing. Rather, each small piece of D N A is selected for its p o w e r t o m a x i m i z e its own s u r v i v a l a n d r e p l i c a t i o n . R i c h m o n d g o e s o n : ' I f t h e c e l l i s c o n s i d e r e d a s a u n i t for t h e r e p l i c a t i o n o f D N A , i t f o l l o w s t h a t D N A a d d i t i o n a l t o t h a t r e q u i r e d for t h e d u p l i c a t i o n o f t h e c e l l m a y a l s o be carried; m o l e c u l a r parasitism, symbiosis and m u t u a l i s m m a y o c c u r at the D N A level, as it does at higher organizational levels in b i o l o g y . ' We h a v e arrived

back

the

c o n c e p t o f 'selfish

DNA'

which

was

a subject of

C h a p t e r 9. It is interesting to speculate on whether mitochondria, chloroplasts, and other

DNA-bearing

(Margulis 1970,

organelles

originated

from

parasitic

prokaryotes

1981). But, important as that question is as a m a t t e r of

history, it does not bear, o n e w a y or the other, on my present c o n c e r n . I am h e r e i n t e r e s t e d i n w h e t h e r m i t o c h o n d r i a l D N A i s l i k e l y t o w o r k for t h e s a m e phenotypic ends as nuclear D N A , or whether it is likely to be in conflict with it. T h i s s h o u l d d e p e n d n o t o n t h e h i s t o r i c o r i g i n s o f m i t o c h o n d r i a b u t o n their p r e s e n t m e t h o d o f p r o p a g a t i n g t h e i r D N A . M i t o c h o n d r i a l g e n e s a r e passed o u t o f o n e m e t a z o a n b o d y i n t o a b o d y o f t h e n e x t g e n e r a t i o n i n e g g c y t o p l a s m . A n o p t i m a l female p h e n o t y p e from the p o i n t o f v i e w o f the female's o w n nuclear genes is likely to be v e r y m u c h the s a m e as an o p t i m a l female p h e n o t y p e from the point o f v i e w o f her m i t o c h o n d r i a l D N A . B o t h h a v e an interest in her successfully s u r v i v i n g ,

reproducing, and rearing

offspring. A t least, t h a t i s t r u e a s far a s f e m a l e o f f s p r i n g a r e c o n c e r n e d . M i t o c h o n d r i a p r e s u m a b l y h a v e n o ' w i s h ' for t h e i r b o d i e s t o h a v e s o n s : a m a l e b o d y r e p r e s e n t s t h e e n d o f t h e l i n e a s far a s m i t o c h o n d r i a l d e s c e n t i s concerned. A l l mitochondria in existence h a v e spent the vast majority of their a n c e s t r a l c a r e e r s i n f e m a l e b o d i e s , a n d t h e y m i g h t t e n d t o h a v e w h a t i t takes t o persist i n i n h a b i t i n g f e m a l e b o d i e s .

In birds the interests of

mitochondrial D N A will b e closely similar t o those o f Y - c h r o m o s o m a l D N A , and slightly d i v e r g e n t from those o f a u t o s o m a l a n d X - c h r o m o s o m a l D N A . A n d i f m i t o c h o n d r i a l D N A c o u l d exert p h e n o t y p i c p o w e r i n the e g g o f a

224

Host Phenotypes of Parasite Genes

m a m m a l , i t i s p e r h a p s n o t t o o f a n c i f u l t o i m a g i n e i t f r a n t i c a l l y f i g h t i n g off t h e kiss o f d e a t h o f Y - b e a r i n g s p e r m s ( E b e r h a r d 1 9 8 0 ; C o s m i d e s & T o o b y 1981). B u t i n a n y case, i f the interests o f m i t o c h o n d r i a l D N A a n d n u c l e a r D N A a r e n o t a l w a y s i d e n t i c a l , t h e y a r e v e r y c l o s e , c e r t a i n l y m u c h closer than the interests o f fluke D N A a n d snail D N A . T h e m e s s a g e o f t h e p r e s e n t s e c t i o n i s this. T h e f a c t t h a t s n a i l g e n e s c o n f l i c t w i t h f l u k e g e n e s m o r e t h a n t h e y c o n f l i c t w i t h o t h e r s n a i l g e n e s a t different l o c i i s n o t t h e o b v i o u s f o r e g o n e c o n c l u s i o n i t m i g h t a p p e a r t o b e . I t results s i m p l y f r o m t h e f a c t t h a t a n y t w o g e n e s i n a s n a i l n u c l e u s a r e o b l i g e d t o use the s a m e exit route from the present b o d y into the future. B o t h h a v e the s a m e stake in the success of the present snail in m a n u f a c t u r i n g gametes, g e t t i n g t h e m f e r t i l i z e d , a n d s e c u r i n g t h e s u r v i v a l a n d r e p r o d u c t i o n o f the offspring so formed. F l u k e genes conflict w i t h snail genes in their influence on t h e s h a r e d p h e n o t y p e , s i m p l y b e c a u s e t h e i r d e s t i n y i s s h a r e d for o n l y a short p a r t o f t h e f u t u r e : t h e i r c o m m o n c a u s e i s l i m i t e d t o t h e life o f t h e p r e s e n t host b o d y , a n d d o e s n o t c a r r y o v e r i n t o t h e g a m e t e s a n d o f f s p r i n g o f the present host. T h e role of m i t o c h o n d r i a in the a r g u m e n t is to e x e m p l i f y cases w h e r e p a r a s i t e a n d h o s t g e n e s s h a r e t h e s a m e g a m e t i c d e s t i n y , a t least i n p a r t . I f n u c l e a r genes do not conflict with nuclear genes at other loci, it is only b e c a u s e meiosis is e v e n - h a n d e d : meiosis does not n o r m a l l y favour some loci o v e r others, nor some alleles over others, but scrupulously puts one gene at r a n d o m from

each

diploid

pair

every gamete.

Of course

there are

i n s t r u c t i v e e x c e p t i o n s , a n d for m y thesis t h e y a r e s u f f i c i e n t l y i m p o r t a n t t o h a v e d o m i n a t e d t h e t w o c h a p t e r s o n ' o u t l a w s ' a n d 'selfish D N A ' . T h e r e , a s here, an i m p o r t a n t message is that replicating entities will tend to w o r k a g a i n s t e a c h o t h e r t o t h e e x t e n t t h a t t h e y e m p l o y different m e t h o d s o f egress from v e h i c l e to v e h i c l e . Returning symbiotic

the

main

relationships

can

subject be

of the

classified

present in

chapter,

various

ways

parasitic for

and

different

purposes. T h e classifications d e v e l o p e d by parasitologists and doctors are no doubt

useful

for

their

purposes,

but

want

develop

particular

classification based on the concept of gene p o w e r . It should be r e m e m b e r e d t h a t , f r o m this p o i n t o f v i e w , t h e n o r m a l r e l a t i o n s h i p b e t w e e n different g e n e s in the same nucleus, e v e n on the same c h r o m o s o m e , is just one extreme on the c o n t i n u u m of parasitic or symbiotic relationships. T h e first d i m e n s i o n o f m y c l a s s i f i c a t i o n h a s a l r e a d y b e e n stressed.

c o n c e r n s t h e d e g r e e o f s i m i l a r i t y o r d i f f e r e n c e i n t h e m e t h o d s o f egress from hosts, a n d p r o p a g a t i o n o f host genes a n d parasite genes. A t one e x t r e m e will b e p a r a s i t e s t h a t use t h e h o s t ' s p r o p a g u l e s for their o w n r e p r o d u c t i o n . F o r s u c h p a r a s i t e s a n o p t i m u m host p h e n o t y p e f r o m t h e p a r a s i t e ' s p o i n t o f v i e w i s l i k e l y t o c o i n c i d e w i t h t h e o p t i m u m f r o m t h e p o i n t o f v i e w o f t h e host's o w n g e n e s . T h i s i s n o t t o s a y t h a t t h e host g e n e s w o u l d n o t ' p r e f e r ' t o b e rid

Host Phenotypes of Parasite Genes

225

o f the p a r a s i t e a l t o g e t h e r . B u t b o t h h a v e a n i n t e r e s t i n m a s s - p r o d u c i n g t h e same propagules, a n d both h a v e an interest in d e v e l o p i n g a p h e n o t y p e that i s g o o d for m a s s - p r o d u c i n g t h o s e s a m e p r o p a g u l e s : t h e r i g h t b e a k l e n g t h , w i n g shape, courtship b e h a v i o u r , clutch size, etc., d o w n to m i n u t e details of all a s p e c t s o f t h e p h e n o t y p e . A t the o t h e r e x t r e m e w i l l b e p a r a s i t e s w h o s e g e n e s a r e p a s s e d o n n o t i n t h e host's r e p r o d u c t i v e p r o p a g u l e s b u t , s a y , i n t h e h o s t ' s e x h a l e d b r e a t h , o r i n the host's d e a d b o d y . I n t h e s e c a s e s t h e o p t i m u m h o s t p h e n o t y p e f r o m t h e parasite genes' point of v i e w is likely to be v e r y different from the o p t i m u m host p h e n o t y p e f r o m t h e host g e n e s ' p o i n t o f v i e w . T h e p h e n o t y p e w h i c h emerges will be a c o m p r o m i s e . T h i s , then, is one dimension of classification of host-parasite relationships.

I shall call it the d i m e n s i o n of ' p r o p a g u l e

overlap'. A second dimension of classification concerns the time of action of parasite g e n e s d u r i n g host d e v e l o p m e n t . A g e n e , w h e t h e r a h o s t g e n e o r a p a r a s i t e gene, c a n exert a m o r e f u n d a m e n t a l influence on the final host p h e n o t y p e if i t a c t s e a r l y i n t h e d e v e l o p m e n t o f t h e host e m b r y o t h a n i f i t a c t s l a t e . A radical c h a n g e such as the d e v e l o p m e n t of two heads c o u l d be a c h i e v e d by a s i n g l e m u t a t i o n (in host o r p a r a s i t e g e n o m e ) p r o v i d e d t h e m u t a t i o n a c t e d sufficiently e a r l y i n t h e e m b r y o n i c d e v e l o p m e n t o f t h e h o s t . A l a t e - a c t i n g m u t a n t ( a g a i n , i n host o r p a r a s i t e g e n o m e ) â&#x20AC;&#x201D; a m u t a n t t h a t d o e s n o t b e g i n t o a c t u n t i l t h e host b o d y h a s r e a c h e d a d u l t h o o d â&#x20AC;&#x201D; i s l i k e l y t o h a v e o n l y a s m a l l effect, s i n c e t h e g e n e r a l a r c h i t e c t u r e o f t h e b o d y w i l l , b y t h e n , h a v e b e e n l a i d d o w n . T h e r e f o r e a p a r a s i t e t h a t e n t e r s its h o s t after t h e h o s t h a s r e a c h e d a d u l t h o o d is less l i k e l y to h a v e a r a d i c a l effect on t h e h o s t ' s p h e n o t y p e t h a n a parasite that gets in early. T h e r e are n o t a b l e e x c e p t i o n s , h o w e v e r , such as the p a r a s i t i c c a s t r a t i o n o f C r u s t a c e a a l r e a d y m e n t i o n e d . M y third d i m e n s i o n o f classification o f h o s t - p a r a s i t e relations c o n c e r n s the c o n t i n u u m from w h a t m a y be c a l l e d close i n t i m a c y to a c t i o n at a d i s t a n c e . A l l g e n e s e x e r t p o w e r p r i m a r i l y b y s e r v i n g a s t e m p l a t e s for t h e s y n t h e s i s o f p r o t e i n s . T h e l o c u s o f p r i m a r y g e n e p o w e r is, t h e r e f o r e , t h e c e l l , i n p a r t i c u l a r the c y t o p l a s m s u r r o u n d i n g t h e n u c l e u s i n w h i c h t h e g e n e sits. M e s s e n g e r R N A streams t h r o u g h the n u c l e a r m e m b r a n e a n d m e d i a t e s g e n e t i c control over cytoplasmic biochemistry. T h e phenotypic expression of a gene is then, i n the f i r s t p l a c e , its i n f l u e n c e o n c y t o p l a s m i c b i o c h e m i s t r y . I n its t u r n , this i n f l u e n c e s t h e f o r m a n d s t r u c t u r e o f t h e w h o l e c e l l , a n d t h e n a t u r e o f its c h e m i c a l a n d p h y s i c a l i n t e r a c t i o n s w i t h n e i g h b o u r i n g c e l l s . T h i s affects t h e b u i l d - u p o f m u l t i c e l l u l a r tissues, a n d i n t u r n t h e d i f f e r e n t i a t i o n o f a v a r i e t y o f tissues i n t h e d e v e l o p i n g b o d y . F i n a l l y e m e r g e t h e a t t r i b u t e s o f t h e w h o l e organism

t h a t gross a n a t o m i s t s a n d

ethologists identify at

their level as

phenotypic expressions of genes. W h e r e p a r a s i t e g e n e s e x e r t s h a r e d p o w e r w i t h host g e n e s o v e r t h e s a m e host p h e n o t y p i c c h a r a c t e r i s t i c , t h e c o n f l u e n c e o f t h e t w o p o w e r s m a y o c c u r

226

Host Phenotypes of Parasite Genes

a t a n y s t a g e i n t h e c h a i n j u s t d e s c r i b e d . S n a i l g e n e s , a n d t h e g e n e s o f the fluke that parasitizes the snail, exert their p o w e r s e p a r a t e l y from e a c h other a t t h e c e l l u l a r a n d e v e n t h e tissue l e v e l . T h e y i n f l u e n c e t h e c y t o p l a s m i c c h e m i s t r y of their r e s p e c t i v e cells separately, b e c a u s e they do not share cells. T h e y i n f l u e n c e tissue f o r m a t i o n s e p a r a t e l y ,

b e c a u s e s n a i l tissues a r e n o t

i n t i m a t e l y i n f i l t r a t e d b y f l u k e tissues i n t h e w a y t h a t , s a y , t h e a l g a l a n d f u n g a l tissues o f a l i c h e n a r e i n t i m a t e . S n a i l g e n e s a n d f l u k e g e n e s i n f l u e n c e the d e v e l o p m e n t of o r g a n systems, indeed of w h o l e organisms, separately, b e c a u s e all the fluke cells are g a t h e r e d t o g e t h e r in one mass rather than being interspersed

a m o n g snail cells.

I f f l u k e g e n e s i n f l u e n c e s n a i l shell

t h i c k n e s s , t h e y d o s o b y first c o l l a b o r a t i n g w i t h o t h e r f l u k e g e n e s t o m a k e a whole fluke. O t h e r p a r a s i t e s a n d s y m b i o n t s m o r e i n t i m a t e l y i n f i l t r a t e t h e s y s t e m s o f the host. A t t h e e x t r e m e a r e t h e p l a s m i d s a n d o t h e r f r a g m e n t s o f D N A w h i c h , a s w e s a w i n C h a p t e r 9 , l i t e r a l l y i n s e r t t h e m s e l v e s i n t h e host c h r o m o s o m e s . I t i s i m p o s s i b l e t o i m a g i n e a m o r e i n t i m a t e p a r a s i t e . ' S e l f i s h D N A ' itself i s n o t more intimate, and indeed we m a y never k n o w h o w m a n y of our genes, w h e t h e r 'junk' or 'useful', originated as inserted plasmids. It seems to follow f r o m t h e thesis o f this b o o k t h a t t h e r e i s n o i m p o r t a n t d i s t i n c t i o n b e t w e e n o u r ' o w n ' genes a n d parasitic or symbiotic insertion sequences. W h e t h e r they c o n f l i c t o r c o o p e r a t e w i l l d e p e n d n o t o n t h e i r h i s t o r i c a l o r i g i n s b u t o n the circumstances from w h i c h they stand to gain now. V i r u s e s h a v e t h e i r o w n p r o t e i n j a c k e t , b u t t h e y i n s e r t t h e i r D N A i n t o the host's cell. T h e y are therefore in a position to influence the cellular chemistry of the host at an intimate level, if not quite such an intimate level as an insertion s e q u e n c e in the host c h r o m o s o m e .

I n t r a c e l l u l a r p a r a s i t e s i n the

c y t o p l a s m , too, m a y be presumed to be in a position to exert considerable p o w e r o v e r host p h e n o t y p e s . S o m e p a r a s i t e s d o n o t i n f i l t r a t e t h e host a t t h e c e l l u l a r l e v e l , b u t a t t h e tissue l e v e l . E x a m p l e s a r e Sacculina, a n d m a n y f u n g a l a n d p l a n t p a r a s i t e s , w h e r e parasite cells and host cells are distinct, but w h e r e the parasite invades t h e h o s t ' s tissues b y m e a n s o f a n i n t r i c a t e a n d finely d i v i d e d r o o t s y s t e m . T h e s e p a r a t e c e l l s o f p a r a s i t i c b a c t e r i a a n d p r o t o z o a m a y i n f i l t r a t e t h e h o s t tissues w i t h s i m i l a r l y c o m p r e h e n s i v e i n t i m a c y . T o a s l i g h t l y lesser e x t e n t t h a n a c e l l p a r a s i t e , s u c h a 'tissue p a r a s i t e ' is in a s t r o n g p o s i t i o n to i n f l u e n c e o r g a n development

and

gross

p h e n o t y p i c form

and

behaviour.

O t h e r internal

p a r a s i t e s , s u c h a s t h e f l u k e s w e h a v e b e e n d i s c u s s i n g , d o n o t m i x t h e i r tissues w i t h t h o s e o f t h e h o s t , b u t k e e p t h e i r tissues t o t h e m s e l v e s a n d e x e r t p o w e r only at the level of the w h o l e organism. B u t w e h a v e not yet r e a c h e d the end o f our c o n t i n u u m o f p r o x i m i t y . N o t a l l p a r a s i t e s l i v e p h y s i c a l l y i n s i d e t h e i r hosts. T h e y m a y e v e n s e l d o m c o m e into c o n t a c t w i t h their hosts. A c u c k o o is a parasite in v e r y m u c h the same w a y a s a f l u k e . B o t h a r e w h o l e - o r g a n i s m p a r a s i t e s r a t h e r t h a n tissue p a r a s i t e s

H o s t P h e n o t y p e s of P a r a s i t e G e n e s

227

o r c e l l p a r a s i t e s . I f fluke g e n e s c a n b e s a i d t o h a v e p h e n o t y p i c e x p r e s s i o n i n a snail's b o d y , there is no sensible reason w h y c u c k o o g e n e s should not be said to h a v e p h e n o t y p i c expression in a reed w a r b l e r ' s b o d y . T h e difference is a practical one, a n d a rather smaller one than the difference b e t w e e n , say, a c e l l u l a r p a r a s i t e a n d a tissue p a r a s i t e . T h e p r a c t i c a l d i f f e r e n c e i s t h a t t h e c u c k o o d o e s n o t l i v e i n s i d e t h e r e e d w a r b l e r ' s b o d y , s o h a s less o p p o r t u n i t y for m a n i p u l a t i n g t h e h o s t ' s i n t e r n a l b i o c h e m i s t r y .

It has to rely on other

m e d i a for its m a n i p u l a t i o n , for i n s t a n c e s o u n d w a v e s a n d l i g h t w a v e s . A s d i s c u s s e d in C h a p t e r 4, it uses a s u p e r n o r m a l l y b r i g h t g a p e to i n j e c t its control into the reed w a r b l e r ' s n e r v o u s system v i a the

eyes.

I t uses a n

especially loud b e g g i n g c r y to control the reed w a r b l e r ' s n e r v o u s system v i a the ears. C u c k o o genes, i n e x e r t i n g their d e v e l o p m e n t a l p o w e r o v e r host phenotypes, h a v e to rely on action at a distance. T h e concept of genetic action at a distance pushes our idea of the extended p h e n o t y p e o u t t o its l o g i c a l c u l m i n a t i o n . T h a t i s w h e r e w e m u s t g o i n t h e next chapter.

13 Action at a Distance

Snail

shells

coil

either

the

right

the

left.

Usually

all

i n d i v i d u a l s i n o n e s p e c i e s c o i l t h e s a m e w a y , b u t a f e w p o l y m o r p h i c species are to be found. In the Pacific island l a n d snail

Partula

suturalis s o m e l o c a l

populations are right-handed, others are left-handed, and others are mixed in various proportions.

It is therefore possible to study the genetics of

d i r e c t i o n a l i t y o f c o i l i n g ( M u r r a y & C l a r k e 1 9 6 6 ) . W h e n snails from r i g h t h a n d e d p o p u l a t i o n s w e r e c r o s s e d w i t h snails f r o m l e f t - h a n d e d p o p u l a t i o n s , e v e r y o f f s p r i n g c o i l e d t h e s a m e w a y a s its ' m o t h e r ' (the p a r e n t t h a t p r o v i d e d the e g g : the snails are h e r m a p h r o d i t e s ) . T h i s m i g h t be thought to indicate a n o n - g e n e t i c m a t e r n a l i n f l u e n c e . B u t w h e n M u r r a y a n d C l a r k e crossed F 1 snails w i t h e a c h o t h e r t h e y o b t a i n e d a c u r i o u s r e s u l t . A l l t h e p r o g e n y w e r e left-handed,

regardless of the direction of c o i l i n g of either parent. T h e i r

i n t e r p r e t a t i o n o f t h e results i s t h a t c o i l i n g i s g e n e t i c a l l y d e t e r m i n e d , w i t h left-handedness phenotype

dominant controlled

to not

right-handedness, by

its

own

but

genotype

that but

an its

animal's mother's

g e n o t y p e . T h u s the F1 i n d i v i d u a l s d i s p l a y e d the p h e n o t y p e s dictated by their m o t h e r s '

genotypes,

although

all

contained

the same h e t e r o z y g o u s

g e n o t y p e s since t h e y w e r e p r o d u c e d b y m a t i n g t w o p u r e strains. S i m i l a r l y , the F2 p r o g e n y of F1 m a t i n g s all d i s p l a y e d the p h e n o t y p e a p p r o p r i a t e to an F1 g e n o t y p e â&#x20AC;&#x201D; l e f t - h a n d e d since that is d o m i n a n t a n d the F1 g e n o t y p e w a s h e t e r o z y g o u s . T h e u n d e r l y i n g g e n o t y p e s o f the F 2 g e n e r a t i o n p r e s u m a b l y s e g r e g a t e d i n c l a s s i c 3 : 1 M e n d e l i a n f a s h i o n , b u t this d i d n o t s h o w itself i n their p h e n o t y p e s .

It w o u l d h a v e s h o w n itself in the p h e n o t y p e s of their

progeny. N o t e that it is the m o t h e r ' s g e n o t y p e , not her p h e n o t y p e , w h i c h controls her offspring's p h e n o t y p e . T h e F1 individuals themselves w e r e left-handed or right-handed

equal

proportion,

yet

all

had

the

same

heterozygous

g e n o t y p e , a n d a l l t h e r e f o r e p r o d u c e d l e f t - h a n d e d o f f s p r i n g . A s i m i l a r effect h a d b e e n o b t a i n e d e a r l i e r i n t h e f r e s h w a t e r s n a i l Limnaea peregra, t h o u g h i n t h a t c a s e r i g h t - h a n d e d n e s s w a s d o m i n a n t . O t h e r s u c h ' m a t e r n a l effects' h a v e 228

A c t i o n at a D i s t a n c e

229

l o n g b e e n k n o w n t o g e n e t i c i s t s . A s F o r d ( 1 9 7 5 ) p u t it, ' W e h a v e h e r e s i m p l e M e n d e l i a n inheritance the expression of w h i c h is constantly d e l a y e d one g e n e r a t i o n . ' T h e p h e n o m e n o n p e r h a p s arises w h e n t h e e m b r y o l o g i c a l e v e n t d e t e r m i n i n g t h e p h e n o t y p i c trait o c c u r s s o e a r l y i n d e v e l o p m e n t a s t o b e influenced b y m a t e r n a l messenger R N A from the e g g c y t o p l a s m , before the z y g o t e h a s b e g u n t o m a n u f a c t u r e its o w n m e s s e n g e r R N A . T h e d i r e c t i o n o f coiling in snails is d e t e r m i n e d by the initial d i r e c t i o n of spiral c l e a v a g e , w h i c h occurs before the e m b r y o ' s o w n D N A has b e g u n t o w o r k ( C o h e n 1977)T h i s k i n d o f effect p r o v i d e s a s p e c i a l o p p o r t u n i t y for t h e k i n d o f m a t e r n a l m a n i p u l a t i o n of offspring that we discussed in C h a p t e r 4. M o r e g e n e r a l l y , it is a s p e c i a l e x a m p l e of g e n e t i c ' a c t i o n at a d i s t a n c e ' .

It i l l u s t r a t e s , in a

particularly clear a n d simple m a n n e r , that the p o w e r of a g e n e m a y e x t e n d b e y o n d t h e b o u n d a r i e s o f t h e b o d y i n w h o s e c e l l s i t sits ( H a l d a n e 1 9 3 2 b ) . W e c a n n o t h o p e that all g e n e t i c a c t i o n at a distance w i l l r e v e a l itself in so elegant

Mendelian

manner

the

case

of the

snails. Just

as,

c o n v e n t i o n a l genetics, the M e n d e l i a n m a j o r genes of the s c h o o l r o o m are the tip o f t h e i c e b e r g o f r e a l i t y , s o w e m a y m a k e c o n j e c t u r e s a b o u t a p o l y g e n i c ' e x t e n d e d g e n e t i c s ' , a g e n e t i c s in w h i c h a c t i o n at a d i s t a n c e is rife b u t in w h i c h t h e effects o f t h e g e n e s a r e c o m p l e x a n d i n t e r a c t i n g , a n d t h e r e f o r e difficult t o sort o u t . A g a i n a s i n c o n v e n t i o n a l g e n e t i c s , w e d o n o t n e c e s s a r i l y h a v e to do g e n e t i c e x p e r i m e n t s in o r d e r to infer the p r e s e n c e of g e n e t i c influence

variation.

Once

have

satisfied

c h a r a c t e r i s t i c is a D a r w i n i a n a d a p t a t i o n this,

ourselves

that

given

in itself, is t a n t a m o u n t to

satisfying ourselves that v a r i a t i o n in that c h a r a c t e r m u s t at o n e t i m e h a v e had a genetic basis. If it h a d not, selection c o u l d not h a v e preserved the a d v a n t a g e o u s a d a p t a t i o n in the p o p u l a t i o n . O n e p h e n o m e n o n t h a t l o o k s l i k e a n a d a p t a t i o n a n d w h i c h , i n s o m e sense, involves action at a distance, is the ' B r u c e Effect'. A f e m a l e m o u s e w h o has just been inseminated by one m a l e has her p r e g n a n c y b l o c k e d by exposure to c h e m i c a l i n f l u e n c e f r o m a s e c o n d m a l e . T h e effect s e e m s a l s o t o o c c u r i n a variety of species of m i c e a n d voles in nature. S c h w a g m e y e r (1980) considers three m a i n hypotheses of the a d a p t i v e significance of the B r u c e Effect, b u t for t h e s a k e o f a r g u m e n t

I shall not, here, a d v o c a t e the hypothesis that

S c h w a g m e y e r attributes to m e â&#x20AC;&#x201D; t h a t the B r u c e Effect represents a k i n d of female a d a p t a t i o n . Instead I shall look at it from the m a l e point of v i e w , a n d simply

assume

that

the

second

male

benefits

himself by

p r e v e n t i n g the

female's p r e g n a n c y , t h e r e b y e l i m i n a t i n g the offspring of a m a l e r i v a l , w h i l e a t t h e s a m e t i m e b r i n g i n g the f e m a l e q u i c k l y i n t o o e s t r u s s o t h a t h e c a n m a t e with her himself. I h a v e expressed the hypothesis in the l a n g u a g e of C h a p t e r 4, the l a n g u a g e of individual m a n i p u l a t i o n . But it c a n e q u a l l y well be expressed in the l a n g u a g e of the e x t e n d e d p h e n o t y p e a n d genetic a c t i o n at a d i s t a n c e . G e n e s

230

A c t i o n at a D i s t a n c e

i n m a l e m i c e h a v e p h e n o t y p i c e x p r e s s i o n i n f e m a l e b o d i e s , i n j u s t the s a m e sense a s g e n e s i n m o t h e r s n a i l s h a v e p h e n o t y p i c e x p r e s s i o n i n t h e b o d i e s o f their c h i l d r e n . In the snail case, the m e d i u m of the action at a distance w a s assumed to be m a t e r n a l messenger R N A . In the mouse case it is apparently a m a l e p h e r o m o n e . M y thesis i s t h a t t h e d i f f e r e n c e b e t w e e n t h e t w o cases i s n o t a fundamental one. Consider how an

'extended geneticist'

m i g h t talk a b o u t

the genetical

e v o l u t i o n of the B r u c e Effect. A m u t a n t g e n e arose w h i c h , w h e n present in the b o d y of a m a l e m o u s e , h a d p h e n o t y p i c expression in the bodies of female m i c e w i t h w h o m h e c a m e i n c o n t a c t . T h e r o u t e o f a c t i o n o f the g e n e o n its final p h e n o t y p e w a s l o n g a n d c o m p l e x , b u t n o t n o t i c e a b l y m o r e s o t h a n routes of genetic action w i t h i n

bodies

customarily are.

conventional

w i t h i n - b o d y g e n e t i c s , the c h a i n of c a u s a t i o n l e a d i n g from g e n e to observed p h e n o t y p e m a y h a v e m a n y links. T h e f i r s t link i s a l w a y s R N A , the second i s p r o t e i n . A b i o c h e m i s t m a y d e t e c t t h e p h e n o t y p e t h a t interests h i m a t this second link stage. Physiologists or anatomists w i l l not pick up the p h e n o t y p e that interests

them

until m o r e stages h a v e

been

passed.

T h e y will

not

c o n c e r n t h e m s e l v e s w i t h t h e d e t a i l s o f these e a r l i e r l i n k s i n t h e c h a i n , b u t w i l l t a k e t h e m for g r a n t e d . W h o l e - o r g a n i s m g e n e t i c i s t s f i n d i t sufficient t o d o b r e e d i n g e x p e r i m e n t s l o o k i n g o n l y a t w h a t , for t h e m , i s t h e f i n a l l i n k i n the c h a i n , e y e c o l o u r , c r i n k l i n e s s o f h a i r , o r w h a t e v e r i t is. T h e b e h a v i o u r geneticist looks at an even more distant l i n k â&#x20AC;&#x201D; w a l t z i n g in mice, creepingthrough m a n i a in sticklebacks, h y g i e n e in h o n e y b e e s , etc. He arbitrarily chooses to r e g a r d a b e h a v i o u r pattern as the end link in the c h a i n , but he k n o w s that the a b n o r m a l b e h a v i o u r of a m u t a n t is caused by, say, a b n o r m a l n e u r o a n a t o m y , or a b n o r m a l endocrine physiology. He knows that he could h a v e l o o k e d w i t h a m i c r o s c o p e a t t h e n e r v o u s s y s t e m i n o r d e r t o d e t e c t his mutants, but he preferred to look at b e h a v i o u r instead (Brenner 1974). He m a d e a n a r b i t r a r y d e c i s i o n t o r e g a r d o b s e r v e d b e h a v i o u r a s t h e e n d link i n the c h a i n o f c a u s a t i o n . Whichever

link

the

chain

geneticist

chooses

regard

the

' p h e n o t y p e ' of interest, he k n o w s that the decision w a s an arbitrary one. He m i g h t h a v e chosen an earlier stage, and he m i g h t h a v e chosen a later one. S o , a student of the g e n e t i c s of the B r u c e Effect c o u l d assay m a l e p h e r o m o n e s b i o c h e m i c a l l y i n o r d e r t o d e t e c t t h e v a r i a t i o n u p o n w h i c h t o b a s e his g e n e t i c study.

could

look

further

back

the

chain,

ultimately

the

i m m e d i a t e p o l y p e p t i d e products o f the genes c o n c e r n e d . O r h e could look later in the c h a i n . W h a t i s t h e n e x t l a t e r l i n k i n t h e c h a i n after t h e m a l e p h e r o m o n e ? I t i s o u t s i d e t h e m a l e b o d y . T h e c h a i n o f c a u s a t i o n e x t e n d s a c r o s s a g a p i n t o the female b o d y . It goes t h r o u g h a n u m b e r of stages in the female b o d y , a n d o n c e a g a i n o u r geneticist does not h a v e to b o t h e r himself w i t h the details. He

A c t i o n at a D i s t a n c e

231

c h o o s e s , for c o n v e n i e n c e , t o e n d his c o n c e p t u a l c h a i n a t t h e p o i n t w h e r e t h e g e n e causes p r e g n a n c y b l o c k a g e in females. T h a t is the p h e n o t y p i c g e n e p r o d u c t w h i c h h e finds m o s t e a s y t o a s s a y , a n d i t i s t h e p h e n o t y p e w h i c h i s o f direct interest to h i m as a student of a d a p t a t i o n in nature.

A b o r t i o n in

f e m a l e m i c e , a c c o r d i n g t o this h y p o t h e s i s , i s a p h e n o t y p i c effect o f a g e n e i n male mice. H o w , then, w o u l d the ' e x t e n d e d geneticist' visualize the e v o l u t i o n o f the Bruce Effect? T h e m u t a n t gene w h i c h ,

w h e n present in males,

has

the

p h e n o t y p i c effect i n f e m a l e b o d i e s o f c a u s i n g t h e m t o a b o r t , i s f a v o u r e d b y n a t u r a l s e l e c t i o n o v e r its a l l e l e s . I t i s f a v o u r e d b e c a u s e i t t e n d s t o b e c a r r i e d i n t h e b o d i e s o f t h e o f f s p r i n g w h i c h t h e f e m a l e b e a r s after b l o c k i n g h e r previous p r e g n a n c y . But, following the h a b i t of C h a p t e r 4, we n o w guess that females w o u l d be u n l i k e l y to s u b m i t to such m a n i p u l a t i o n w i t h o u t resistance, and that a kind of arms r a c e m i g h t d e v e l o p . In the l a n g u a g e of i n d i v i d u a l advantage,

selection

would

favour

mutant

females

that

resisted

the

p h e r o m o n a l m a n i p u l a t i o n o f the males. H o w w o u l d the ' e x t e n d e d geneticist' t h i n k a b o u t this r e s i s t a n c e ? B y i n v o k i n g t h e c o n c e p t o f t h e m o d i f i e r g e n e . O n c e again, we turn first to conventional w i t h i n - b o d y genetics to remind ourselves of a principle, then carry that principle o v e r into the r e a l m of extended genetics. In w i t h i n - b o d y genetics we are quite used to the idea of more than one g e n e affecting variation in a n y g i v e n p h e n o t y p i c character. S o m e t i m e s i t i s c o n v e n i e n t t o d e s i g n a t e o n e l o c u s a s h a v i n g t h e ' m a j o r ' effect o n t h e c h a r a c t e r , t h e o t h e r s h a v i n g ' m o d i f y i n g ' effects. A t o t h e r t i m e s n o o n e locus p r e d o m i n a t e s o v e r the others sufficiently to be c a l l e d major. A l l the g e n e s m a y b e t h o u g h t o f a s m o d i f y i n g t h e effects o f e a c h o t h e r .

In the

chapter o n ' O u t l a w s a n d M o d i f i e r s ' , w e s a w that t w o loci b e a r i n g o n the same phenotypic c h a r a c t e r m a y be subject to conflicting selection pressures. T h e e n d result m a y b e s t a l e m a t e , c o m p r o m i s e , o r o u t r i g h t v i c t o r y for o n e side o r t h e o t h e r . T h e p o i n t i s t h a t c o n v e n t i o n a l w i t h i n - b o d y g e n e t i c s i s already a c c u s t o m e d to t h i n k i n g of the n a t u r a l selection of genes at different loci b e a r i n g u p o n t h e s a m e p h e n o t y p i c c h a r a c t e r b u t i n o p p o s i t e d i r e c t i o n s . A p p l y t h e lesson i n t h e e x t e n d e d g e n e t i c s d o m a i n . T h e p h e n o t y p i c t r a i t o f interest i s a b o r t i o n i n f e m a l e m i c e . T h e g e n e s b e a r i n g u p o n i t n o d o u b t i n c l u d e a set o f g e n e s i n t h e f e m a l e ' s o w n b o d y , a n d a l s o a n o t h e r set o f g e n e s i n the m a l e ' s b o d y . I n t h e c a s e o f t h e m a l e g e n e s t h e l i n k s i n t h e c h a i n o f c a u s a t i o n i n c l u d e p h e r o m o n a l a c t i o n a t a d i s t a n c e , a n d this m a y m a k e t h e influence of the m a l e genes seem v e r y indirect. B u t the causal links in the c a s e o f the f e m a l e g e n e s a r e l i k e l y t o b e n e a r l y a s i n d i r e c t , a l b e i t t h e y a r e confined

inside

her body.

P r o b a b l y t h e y m a k e use

of various chemical

secretions flowing in her b l o o d s t r e a m , w h e r e a s the m a l e g e n e s m a k e use, in a d d i t i o n , o f c h e m i c a l s e c r e t i o n s f l o w i n g i n t h e a i r . T h e p o i n t i s t h a t b o t h sets of genes, by l o n g a n d indirect causal links, b e a r u p o n the s a m e p h e n o t y p i c

232

A c t i o n at a D i s t a n c e

c h a r a c t e r , a b o r t i o n i n t h e f e m a l e , a n d e i t h e r set o f g e n e s m a y b e r e g a r d e d a s m o d i f i e r s o f t h e o t h e r set, j u s t a s s o m e g e n e s w i t h i n e a c h set m a y b e r e g a r d e d a s m o d i f i e r s o f o t h e r s w i t h i n t h e s a m e set. M a l e genes influence the female p h e n o t y p e . F e m a l e genes influence the female p h e n o t y p e , a n d also modify the influence o f m a l e genes. F o r all w e k n o w , female genes influence the m a l e p h e n o t y p e in counter-manipulation, in w h i c h case we e x p e c t the selection of modifiers a m o n g genes in males. T h i s w h o l e s t o r y c o u l d h a v e b e e n t o l d i n t h e l a n g u a g e o f C h a p t e r 4 , the l a n g u a g e of individual manipulation. T h e l a n g u a g e of extended genetics is not d e m o n s t r a b l y m o r e c o r r e c t . It is a different w a y of s a y i n g the same thing. T h e N e c k e r C u b e h a s f l i p p e d . R e a d e r s m u s t d e c i d e for t h e m s e l v e s w h e t h e r they like the n e w v i e w better than the old.

I suggest that the w a y the

e x t e n d e d g e n e t i c i s t tells t h e s t o r y o f t h e B r u c e Effect i s m o r e e l e g a n t a n d p a r s i m o n i o u s t h a n t h e w a y t h e c o n v e n t i o n a l g e n e t i c i s t w o u l d h a v e told it. Both geneticists potentially h a v e to contend with a formidably long and c o m p l e x c h a i n of causation, l e a d i n g from g e n e to p h e n o t y p e . B o t h admit that their c h o i c e of w h i c h link in the c h a i n to d e s i g n a t e as the p h e n o t y p i c c h a r a c t e r of interestâ&#x20AC;&#x201D;earlier links b e i n g consigned to the e m b r y o l o g i s t â&#x20AC;&#x201D; i s arbitrary. T h e c o n v e n t i o n a l geneticist m a k e s the further arbitrary decision to cut off all c h a i n s at the p o i n t w h e r e they r e a c h the outer w a l l of the b o d y . G e n e s affect p r o t e i n s , a n d p r o t e i n s affect X w h i c h affects Y w h i c h affects Z w h i c h . . . affects t h e p h e n o t y p i c c h a r a c t e r o f i n t e r e s t . B u t t h e c o n v e n t i o n a l g e n e t i c i s t d e f i n e s ' p h e n o t y p i c effect' i n s u c h a w a y t h a t X , Y a n d Z m u s t all be

confined

inside

one

individual

body

wall.

The

extended

geneticist

r e c o g n i z e s t h a t this c u t - o f f i s a r b i t r a r y , a n d h e i s q u i t e h a p p y t o a l l o w his X , Y a n d Z to leap the g a p b e t w e e n one individual b o d y and another. T h e c o n v e n t i o n a l g e n e t i c i s t t a k e s i n his s t r i d e t h e b r i d g i n g o f g a p s b e t w e e n cells w i t h i n b o d i e s . H u m a n r e d b l o o d c e l l s , for i n s t a n c e , h a v e n o n u c l e i , a n d m u s t express the p h e n o t y p e s of genes in other cells. So w h y should we not, w h e n t h e o c c a s i o n w a r r a n t s it, c o n c e i v e o f t h e b r i d g i n g o f g a p s b e t w e e n cells i n d i f f e r e n t b o d i e s ? A n d w h e n w i l l t h e o c c a s i o n w a r r a n t i t ? W h e n e v e r w e find i t c o n v e n i e n t , a n d this w i l l t e n d t o b e i n a n y o f t h o s e c a s e s w h e r e , i n conventional l a n g u a g e , one organism appears to be manipulating another. T h e e x t e n d e d geneticist w o u l d , i n fact, b e quite h a p p y t o rewrite the w h o l e o f C h a p t e r 4 , f i x i n g his g a z e o n t h e n e w f a c e o f t h e N e c k e r C u b e . I s h a l l s p a r e t h e r e a d e r a n y s u c h r e w r i t i n g , a l t h o u g h i t w o u l d b e a n i n t e r e s t i n g task to u n d e r t a k e . I shall not pile e x a m p l e on e x a m p l e of genetic action at a d i s t a n c e , b u t i n s t e a d w i l l d i s c u s s t h e c o n c e p t , a n d p r o b l e m s t h a t i t raises, more generally. In the c h a p t e r on a r m s races a n d m a n i p u l a t i o n I said that an o r g a n i s m ' s l i m b s m i g h t b e a d a p t e d t o w o r k for t h e g e n e s o f a n o t h e r o r g a n i s m , a n d I a d d e d t h a t this i d e a c o u l d n o t b e m a d e f u l l y m e a n i n g f u l u n t i l l a t e r i n the book. I m e a n t that it could be m a d e meaningful in terms of genetic action at

A c t i o n at a D i s t a n c e

233

a d i s t a n c e . S o , w h a t d o e s it m e a n to s a y t h a t a f e m a l e ' s m u s c l e s w o r k for a m a l e ' s g e n e s , or t h a t a p a r e n t ' s l i m b s w o r k for its o f f s p r i n g ' s g e n e s , or t h a t a reed w a r b l e r ' s l i m b s w o r k for a c u c k o o ' s g e n e s ? I t w i l l b e r e m e m b e r e d t h a t the

'central

theorem'

of the

selfish

organism

claims

that

animal's

b e h a v i o u r t e n d s t o m a x i m i z e its o w n ( i n c l u s i v e ) fitness. W e s a w t h a t t o t a l k o f a n i n d i v i d u a l b e h a v i n g s o a s t o m a x i m i z e its i n c l u s i v e fitness i s e q u i v a l e n t to talking of the g e n e or genes 'for' that b e h a v i o u r p a t t e r n m a x i m i z i n g their s u r v i v a l . W e h a v e n o w a l s o s e e n t h a t , i n p r e c i s e l y t h e s a m e sense a s i t i s e v e r p o s s i b l e to t a l k of a g e n e ' f o r ' a b e h a v i o u r p a t t e r n , it is p o s s i b l e to t a l k of a

gene,

one

organism,

'for'

behaviour

pattern

(or

other

pheno-

typic characteristic) in a n o t h e r o r g a n i s m . P u t t i n g these three things together we

arrive

animal's

our

own

behaviour

'central

tends

theorem'

maximize

the

survival

extended of the

phenotype:

genes

'for'

that

behaviour, whether or not those genes happen to be in the body of the particular animal performing

it.

A n d h o w far afield c a n t h e p h e n o t y p e e x t e n d ? I s t h e r e a n y l i m i t t o a c t i o n a t a d i s t a n c e , a s h a r p cut-off, a n i n v e r s e s q u a r e l a w ? T h e f a r t h e s t a c t i o n a t a distance I c a n think of is a m a t t e r of several miles, the distance s e p a r a t i n g the e x t r e m e m a r g i n s o f a b e a v e r l a k e f r o m t h e g e n e s for w h o s e s u r v i v a l i t i s a n a d a p t a t i o n . I f b e a v e r l a k e s c o u l d fossilize, w e w o u l d p r e s u m a b l y see a t r e n d t o w a r d s i n c r e a s e d l a k e s i z e i f w e a r r a n g e d t h e fossils i n c h r o n o l o g i c a l order. T h e increase i n size w a s doubtless a n a d a p t a t i o n p r o d u c e d b y n a t u r a l s e l e c t i o n , i n w h i c h c a s e w e h a v e t o infer t h a t t h e e v o l u t i o n a r y t r e n d c a m e about by allele r e p l a c e m e n t . In the terms of the e x t e n d e d p h e n o t y p e , alleles for l a r g e r l a k e s r e p l a c e d a l l e l e s for s m a l l e r l a k e s . I n t h e s a m e t e r m s , b e a v e r s c a n b e said t o c a r r y w i t h i n t h e m s e l v e s g e n e s w h o s e p h e n o t y p i c e x p r e s s i o n extends m a n y miles a w a y from the genes themselves. W h y not hundreds of miles, thousands of miles? C o u l d an ectoparasite w h i c h stayed b e h i n d in E n g l a n d inject a s w a l l o w w i t h a d r u g w h i c h affected t h a t s w a l l o w ' s b e h a v i o u r o n its a r r i v a l i n A f r i c a , a n d c o u l d t h e c o n s e q u e n c e i n A f r i c a b e u s e f u l l y r e g a r d e d a s the p h e n o t y p i c e x p r e s s i o n o f p a r a s i t e g e n e s in E n g l a n d ? T h e logic of the e x t e n d e d p h e n o t y p e m i g h t s e e m to f a v o u r the idea, but I think in p r a c t i c e it is unlikely, at least if we are t a l k i n g a b o u t p h e n o t y p i c e x p r e s s i o n as adaptation. I see a c r u c i a l p r a c t i c a l d i f f e r e n c e f r o m the c a s e o f the b e a v e r d a m . A g e n e i n a b e a v e r w h i c h , w h e n c o m p a r e d w i t h its a l l e l e s , c a u s e s a l a r g e r l a k e t o c o m e i n t o e x i s t e n c e , c a n d i r e c t l y b e n e f i t itself b y m e a n s o f its l a k e . A l l e l e s c a u s i n g s m a l l e r l a k e s a r e less l i k e l y t o s u r v i v e , a s a d i r e c t c o n s e q u e n c e o f t h e i r s m a l l e r p h e n o t y p e s . I t is, h o w e v e r , h a r d t o see h o w a g e n e i n a n E n g l i s h e c t o p a r a s i t e c o u l d b e n e f i t itself, a t t h e e x p e n s e o f its a l l e l e s i n E n g l a n d , a s a d i r e c t r e s u l t o f its A f r i c a n p h e n o t y p i c e x p r e s s i o n . A f r i c a i s p r o b a b l y t o o far a w a y for t h e c o n s e q u e n c e s o f t h e g e n e ' s a c t i o n t o feed b a c k a n d affect t h e w e l f a r e o f t h e g e n e itself. By the s a m e token, b e y o n d a certain size of b e a v e r lakes, it w o u l d b e c o m e

234

A c t i o n at a D i s t a n c e

h a r d to r e g a r d further increases in size as a d a p t a t i o n s . T h e reason is that, b e y o n d a c e r t a i n s i z e , o t h e r b e a v e r s t h a n the b u i l d e r s o f t h e d a m a r e j u s t a s likely to benefit from e a c h increase in size as the d a m - b u i l d e r s themselves. A b i g lake benefits all the beavers in the area, w h e t h e r they created it or w h e t h e r t h e y j u s t f o u n d i t a n d e x p l o i t e d it. S i m i l a r l y , e v e n i f a g e n e i n a n E n g l i s h a n i m a l c o u l d e x e r t s o m e p h e n o t y p i c effect o n A f r i c a w h i c h d i r e c t l y benefited the survival of the gene's ' o w n ' a n i m a l , other English animals of the s a m e kind w o u l d almost certainly benefit just as m u c h . We must not f o r g e t t h a t n a t u r a l s e l e c t i o n i s a l l a b o u t relative s u c c e s s . It is a d m i t t e d l y p o s s i b l e

to s p e a k of

a g e n e as h a v i n g a p a r t i c u l a r

p h e n o t y p i c e x p r e s s i o n , e v e n w h e n its o w n s u r v i v a l i s n o t i n f l u e n c e d b y t h a t p h e n o t y p i c e x p r e s s i o n . I n this sense, t h e n , a g e n e i n E n g l a n d m i g h t i n d e e d h a v e p h e n o t y p i c e x p r e s s i o n i n a r e m o t e c o n t i n e n t w h e r e its c o n s e q u e n c e s d o n o t f e e d b a c k u p o n its o w n s u c c e s s i n t h e E n g l i s h g e n e - p o o l . B u t I h a v e a l r e a d y a r g u e d t h a t i n t h e w o r l d o f t h e e x t e n d e d p h e n o t y p e this i s n o t a profitable w a y of speaking.

used the e x a m p l e of footprints in m u d as

p h e n o t y p i c e x p r e s s i o n o f g e n e s for foot s h a p e , a n d I g a v e m y i n t e n t i o n o f using extended

p h e n o t y p e l a n g u a g e only w h e n the character concerned

m i g h t c o n c e i v a b l y i n f l u e n c e , p o s i t i v e l y o r n e g a t i v e l y , t h e r e p l i c a t i o n success of the g e n e or genes c o n c e r n e d . It is n o t p l a u s i b l e , b u t it h e l p s to m a k e t h e p o i n t if I c o n s t r u c t a t h o u g h t e x p e r i m e n t i n w h i c h i t w o u l d i n d e e d b e useful t o s p e a k o f a g e n e a s h a v i n g p h e n o t y p i c expression e x t e n d i n g to another continent. S w a l l o w s return, each year,

to e x a c t l y the s a m e nest.

It follows that an ectoparasite, waiting

d o r m a n t i n a s w a l l o w ' s nest i n E n g l a n d , c a n e x p e c t t o see t h e v e r y s a m e s w a l l o w b o t h b e f o r e a n d after t h e s w a l l o w ' s j o u r n e y t o A f r i c a . I f t h e p a r a s i t e c o u l d engineer some c h a n g e in the s w a l l o w ' s b e h a v i o u r in Africa, it might indeed r e a p the c o n s e q u e n c e s on the s w a l l o w ' s return to E n g l a n d . Suppose, for i n s t a n c e , t h a t t h e p a r a s i t e n e e d s a r a r e t r a c e e l e m e n t w h i c h i s n o t f o u n d i n E n g l a n d , b u t w h i c h o c c u r s i n t h e fat o f a p a r t i c u l a r A f r i c a n fly. S w a l l o w s n o r m a l l y h a v e n o p r e f e r e n c e for this f l y , b u t t h e p a r a s i t e , b y i n j e c t i n g a d r u g i n t o t h e s w a l l o w b e f o r e i t l e a v e s for A f r i c a , s o c h a n g e s its d i e t a r y p r e f e r e n c e s a s t o i n c r e a s e t h e l i k e l i h o o d o f its e a t i n g s p e c i m e n s o f this f l y . W h e n the s w a l l o w r e t u r n s t o E n g l a n d , its b o d y c o n t a i n s e n o u g h o f t h e t r a c e e l e m e n t t o b e n e f i t t h e i n d i v i d u a l p a r a s i t e (or its c h i l d r e n ) w a i t i n g i n t h e o r i g i n a l nest, benefit t h e m at the e x p e n s e of rivals w i t h i n the parasite species. O n l y in c i r c u m s t a n c e s such as these w o u l d I wish to speak of a g e n e in one continent as h a v i n g phenotypic expression in another continent. T h e r e i s a risk, w h i c h I h a d b e t t e r f o r e s t a l l , t h a t s u c h t a l k o f a d a p t a t i o n o n a g l o b a l s c a l e m a y c a l l t o t h e r e a d e r ' s m i n d t h e f a s h i o n a b l e i m a g e o f the e c o l o g i c a l ' w e b ' , of w h i c h the most e x t r e m e manifestation is the ' G a i a ' hypothesis of L o v e l o c k (1979). My w e b of interlocking extended phenotypic i n f l u e n c e s b e a r s a superficial r e s e m b l a n c e t o the w e b s o f m u t u a l d e p e n d e n c e

A c t i o n at a D i s t a n c e

235

and symbiosis that bulk so largely in the p o p - e c o l o g y literature (e.g.

The

Ecologist) a n d i n L o v e l o c k ' s b o o k . T h e c o m p a r i s o n c o u l d h a r d l y b e m o r e misleading.

Since Lovelock's G a i a

hypothesis

has

been

enthusiastically

e s p o u s e d b y n o less a scientist t h e n M a r g u l i s ( 1 9 8 1 ) , a n d e x t r a v a g a n t l y praised by M e l l a n b y (1979) as the w o r k of a genius, it c a n n o t be i g n o r e d , and I must digress in order c a t e g o r i c a l l y to d i s c l a i m a n y c o n n e c t i o n w i t h the extended phenotype. Lovelock

rightly

regards

homeostatic

self-regulation

one

the

c h a r a c t e r i s t i c a c t i v i t i e s o f l i v i n g o r g a n i s m s , a n d this l e a d s h i m t o t h e d a r i n g hypothesis that the w h o l e E a r t h is e q u i v a l e n t to a single l i v i n g o r g a n i s m . W h e r e a s T h o m a s ' s ( 1 9 7 4 ) l i k e n i n g of the w o r l d to a l i v i n g cell c a n be accepted

throwaway

poetic

line,

Lovelock

clearly

takes

his

E a r t h / o r g a n i s m c o m p a r i s o n s e r i o u s l y e n o u g h t o d e v o t e a w h o l e b o o k t o it. H e r e a l l y m e a n s it. H i s e x p l a n a t i o n s o f t h e n a t u r e o f t h e a t m o s p h e r e a r e r e p r e s e n t a t i v e o f his i d e a s . T h e E a r t h h a s m u c h m o r e o x y g e n t h a n i s t y p i c a l of c o m p a r a b l e planets. It has l o n g been w i d e l y suggested that g r e e n plants are p r o b a b l y a l m o s t e n t i r e l y r e s p o n s i b l e for this h i g h o x y g e n c o n t e n t . M o s t people would regard o x y g e n production as a byproduct of plant activity, and a f o r t u n a t e o n e for t h o s e o f u s w h o n e e d t o b r e a t h e o x y g e n ( p r e s u m a b l y , t o o , we have been selected to breathe o x y g e n partly because there is so m u c h of it a b o u t ) . L o v e l o c k goes further, a n d regards o x y g e n p r o d u c t i o n by plants as a n a d a p t a t i o n o n t h e p a r t o f t h e E a r t h / o r g a n i s m o r ' G a i a ' ( n a m e d after t h e G r e e k E a r t h g o d d e s s ) : p l a n t s p r o d u c e o x y g e n because i t b e n e f i t s life a s a whole. H e uses the s a m e k i n d o f a r g u m e n t for o t h e r g a s e s t h a t o c c u r i n s m a l l amounts: W h a t , then, is the purpose of m e t h a n e a n d h o w does it relate to o x y g e n ? O n e obvious function is to m a i n t a i n the integrity of the a n a e r o b i c z o n e s o f its o r i g i n [ p . 7 3 ] . A n o t h e r p u z z l i n g atmospheric gas is nitrous o x i d e . .. We m a y be sure that

the

efficient

biosphere

unlikely

squander

the

energy

r e q u i r e d i n m a k i n g this o d d g a s u n l e s s i t h a s s o m e useful f u n c t i o n . T w o p o s s i b l e uses c o m e t o m i n d . . . [ p . 7 4 ] . A n o t h e r n i t r o g e n o u s g a s m a d e i n l a r g e v o l u m e s i n t h e soil a n d t h e s e a and released to the air is a m m o n i a . . . As w i t h m e t h a n e , the b i o s p h e r e uses a g r e a t d e a l o f e n e r g y i n p r o d u c i n g a m m o n i a , w h i c h i s n o w e n t i r e l y o f b i o l o g i c a l o r i g i n . Its f u n c t i o n i s a l m o s t c e r t a i n l y t o c o n t r o l the acidity o f the e n v i r o n m e n t . . . [p. 7 7 ] . T h e fatal f l a w i n L o v e l o c k ' s h y p o t h e s i s w o u l d h a v e i n s t a n t l y o c c u r r e d t o h i m i f h e h a d w o n d e r e d a b o u t the l e v e l o f n a t u r a l s e l e c t i o n p r o c e s s w h i c h

A c t i o n at a D i s t a n c e

236

w o u l d be r e q u i r e d in order to p r o d u c e the E a r t h ' s supposed adaptations. Homeostatic adaptations in individual bodies evolve because individuals w i t h i m p r o v e d h o m e o s t a t i c a p p a r a t u s pass o n t h e i r g e n e s m o r e e f f e c t i v e l y than i n d i v i d u a l s w i t h inferior homeostatic apparatuses. F o r the a n a l o g y to a p p l y s t r i c t l y , t h e r e w o u l d h a v e t o h a v e b e e n a set o f r i v a l G a i a s , p r e s u m a b l y o n d i f f e r e n t p l a n e t s . B i o s p h e r e s w h i c h d i d n o t d e v e l o p efficient h o m e o s t a t i c regulation of their p l a n e t a r y atmospheres tended to go extinct. T h e Universe w o u l d h a v e t o b e full o f d e a d p l a n e t s w h o s e h o m e o s t a t i c r e g u l a t i o n s y s t e m s had

failed,

with,

dotted

around,

handful of successful,

well-regulated

p l a n e t s o f w h i c h E a r t h i s o n e . E v e n this i m p r o b a b l e s c e n a r i o i s n o t sufficient to lead

to the

e v o l u t i o n of p l a n e t a r y a d a p t a t i o n s of the kind L o v e l o c k

proposes. In addition we w o u l d h a v e to postulate some kind of reproduction, w h e r e b y s u c c e s s f u l p l a n e t s s p a w n e d c o p i e s o f t h e i r life f o r m s o n n e w p l a n e t s . I a m n o t , o f c o u r s e , s u g g e s t i n g t h a t L o v e l o c k b e l i e v e s i t h a p p e n e d like that.

would

surely

consider

the

idea

of interplanetary

selection

l u d i c r o u s a s I d o . O b v i o u s l y h e s i m p l y d i d n o t see his h y p o t h e s i s a s e n t a i l i n g the h i d d e n assumptions that I think it entails. He m i g h t dispute that it does entail those assumptions, a n d m a i n t a i n that G a i a could e v o l v e her global a d a p t a t i o n s b y the o r d i n a r y processes o f D a r w i n i a n selection a c t i n g within the o n e p l a n e t . I v e r y m u c h d o u b t that a m o d e l of s u c h a selection process c o u l d b e m a d e t o w o r k : i t w o u l d h a v e a l l t h e n o t o r i o u s difficulties o f ' g r o u p s e l e c t i o n ' . F o r i n s t a n c e , i f p l a n t s a r e s u p p o s e d t o m a k e o x y g e n for t h e g o o d o f t h e b i o s p h e r e , i m a g i n e a m u t a n t p l a n t w h i c h s a v e d i t s e l f the costs o f o x y g e n manufacture.

Obviously

would

outreproduce

its

public-spirited

c o l l e a g u e s , a n d g e n e s for p u b l i c - s p i r i t e d n e s s w o u l d s o o n d i s a p p e a r . I t i s n o use p r o t e s t i n g t h a t o x y g e n m a n u f a c t u r e n e e d n o t h a v e c o s t s : i f i t d i d n o t h a v e costs,

the most p a r s i m o n i o u s e x p l a n a t i o n of o x y g e n production in plants

w o u l d be the o n e the scientific w o r l d accepts a n y w a y , that o x y g e n is a b y p r o d u c t o f s o m e t h i n g t h e p l a n t s d o for t h e i r o w n selfish g o o d . I d o not d e n y that s o m e b o d y m a y , one d a y , p r o d u c e a w o r k a b l e m o d e l of the evolution of G a i a ( p o s s i b l y a l o n g t h e lines o f ' M o d e l 2 ' b e l o w ) , a l t h o u g h I p e r s o n a l l y d o u b t it. B u t i f L o v e l o c k h a s s u c h a m o d e l i n m i n d h e d o e s n o t m e n t i o n it. I n d e e d , h e g i v e s n o i n d i c a t i o n t h a t t h e r e i s a difficult p r o b l e m h e r e . T h e G a i a h y p o t h e s i s i s a n e x t r e m e f o r m o f w h a t , for o l d t i m e s ' s a k e a l t h o u g h it is n o w rather unfair, I shall c o n t i n u e to call the ' B B C T h e o r e m ' . T h e B r i t i s h B r o a d c a s t i n g C o r p o r a t i o n i s r i g h t l y p r a i s e d for t h e e x c e l l e n c e o f its n a t u r e p h o t o g r a p h y , a n d i t u s u a l l y s t r i n g s t h e s e a d m i r a b l e v i s u a l i m a g e s t o g e t h e r w i t h a s e r i o u s c o m m e n t a r y . T h i n g s a r e c h a n g i n g n o w , b u t for y e a r s the d o m i n a n t message of these c o m m e n t a r i e s w a s o n e that h a d been elevated almost to the status of a religion by p o p ' e c o l o g y ' . T h e r e w a s something called the ' b a l a n c e of n a t u r e ' , an exquisitely fashioned m a c h i n e in w h i c h plants, h e r b i v o r e s , c a r n i v o r e s , parasites, and s c a v e n g e r s e a c h p l a y e d their a p p o i n t e d r o l e for t h e g o o d o f a l l . T h e o n l y t h i n g t h a t t h r e a t e n e d this d e l i c a t e

A c t i o n at a D i s t a n c e

ecological

china

shop

was

the

insensitive

bull

of h u m a n

progress,

237

the

bulldozer o f . . . , etc. T h e w o r l d needs the patient, toiling d u n g beetles a n d o t h e r s c a v e n g e r s , b u t for w h o s e selfless efforts a s t h e s a n i t a r y w o r k e r s o f t h e world . . . ,

etc.

Herbivores

need

their

predators,

but

for

whom

their

populations w o u l d soar out of control and threaten t h e m with extinction, just a s m a n ' s p o p u l a t i o n will unless . . . , etc. T h e B B C T h e o r e m i s often expressed i n t e r m s o f t h e p o e t r y o f w e b s a n d n e t w o r k s . T h e w h o l e w o r l d i s a finemeshed network of interrelationships, a w e b of connections w h i c h it has taken thousands of years to build up, and w o e betide m a n k i n d if we tear it d o w n . . . , etc. T h e r e is, n o d o u b t , m u c h m e r i t i n t h e m o r a l i s t i c e x h o r t a t i o n s t h a t s e e m t o f l o w f r o m t h e B B C T h e o r e m , b u t t h a t d o e s n o t m e a n its t h e o r e t i c a l b a s i s i s s o u n d . Its w e a k n e s s i s t h e o n e I h a v e a l r e a d y e x p o s e d i n t h e G a i a h y p o t h e s i s . A n e t w o r k o f r e l a t i o n s h i p s t h e r e m a y b e , b u t i t i s m a d e u p o f s m a l l , selfinterested c o m p o n e n t s .

E n t i t i e s t h a t p a y t h e costs o f f u r t h e r i n g t h e w e l l -

b e i n g o f the e c o s y s t e m a s a w h o l e w i l l t e n d t o r e p r o d u c e t h e m s e l v e s less successfully than contribute

rivals

nothing

that exploit their public-spirited the

general

welfare.

Hardin

colleagues,

(1968)

summed

and the

p r o b l e m u p i n his m e m o r a b l e p h r a s e ' T h e t r a g e d y o f t h e c o m m o n s ' , a n d m o r e r e c e n t l y ( H a r d i n 1 9 7 8 ) i n t h e a p h o r i s m , ' N i c e g u y s finish l a s t ' . I h a v e dealt w i t h the B B C T h e o r e m a n d the G a i a h y p o t h e s i s , b e c a u s e o f the d a n g e r t h a t m y o w n l a n g u a g e o f t h e e x t e n d e d p h e n o t y p e a n d a c t i o n a t a distance m a y sound like some o f the m o r e e x u b e r a n t l y e x t e n d e d n e t w o r k s a n d w e b s o f the T V ' e c o l o g i s t s ' . T o e m p h a s i z e t h e d i f f e r e n c e , t h e n , let m e b o r r o w t h e r h e t o r i c o f w e b s a n d n e t w o r k s , b u t use i t i n a v e r y d i f f e r e n t w a y , to explain the i d e a of the e x t e n d e d p h e n o t y p e a n d of g e n e t i c a c t i o n at a distance. L o c i in germ-line c h r o m o s o m e s are hotly contested pieces of p r o p e r t y . T h e contestants are a l l e l o m o r p h i c replicators. M o s t of the replicators in the w o r l d h a v e w o n their p l a c e i n i t b y d e f e a t i n g all a v a i l a b l e a l t e r n a t i v e alleles. T h e w e a p o n s w i t h w h i c h t h e y w o n , a n d t h e w e a p o n s w i t h w h i c h t h e i r r i v a l s lost, are

their

respective

phenotypic

consequences.

These

phenotypic

con-

s e q u e n c e s a r e c o n v e n t i o n a l l y t h o u g h t o f a s b e i n g r e s t r i c t e d t o a s m a l l field a r o u n d the r e p l i c a t o r itself, its b o u n d a r i e s b e i n g d e f i n e d b y t h e b o d y w a l l o f the i n d i v i d u a l o r g a n i s m i n w h o s e c e l l s t h e r e p l i c a t o r sits. B u t t h e n a t u r e o f the c a u s a l i n f l u e n c e o f g e n e o n p h e n o t y p e i s s u c h t h a t i t m a k e s n o s e n s e t o t h i n k o f the field o f i n f l u e n c e a s b e i n g l i m i t e d i n this a r b i t r a r y w a y , a n y m o r e t h a n i t m a k e s sense t o t h i n k o f i t a s l i m i t e d t o i n t r a c e l l u l a r b i o c h e m i s t r y . W e m u s t t h i n k o f e a c h r e p l i c a t o r a s t h e c e n t r e o f a field o f i n f l u e n c e o n t h e w o r l d a t l a r g e . C a u s a l i n f l u e n c e r a d i a t e s o u t f r o m t h e r e p l i c a t o r , b u t its p o w e r d o e s not d e c a y w i t h d i s t a n c e a c c o r d i n g t o a n y s i m p l e m a t h e m a t i c a l l a w . I t t r a v e l s w h e r e v e r i t c a n , far o r n e a r , a l o n g a v a i l a b l e a v e n u e s , a v e n u e s o f i n t r a c e l l u l a r biochemistry, of intercellular chemical and

physical interaction,

o f gross

238

A c t i o n at a D i s t a n c e

bodily form and physiology. T h r o u g h a variety Of physical and chemical m e d i a i t r a d i a t e s o u t b e y o n d the i n d i v i d u a l b o d y t o t o u c h o b j e c t s i n the w o r l d outside, i n a n i m a t e artefacts and even other living organisms. J u s t a s e v e r y g e n e i s t h e c e n t r e o f a r a d i a t i n g field o f i n f l u e n c e o n the w o r l d , so e v e r y p h e n o t y p i c c h a r a c t e r is the centre of c o n v e r g i n g influences from

many

genes,

both

within

and

outside

the

body

o f the

individual

o r g a n i s m . T h e w h o l e b i o s p h e r e â&#x20AC;&#x201D; r e c o g n i z e t h e s u p e r f i c i a l affinity w i t h the B B C T h e o r e m â&#x20AC;&#x201D; t h e w h o l e w o r l d o f p l a n t a n d a n i m a l m a t t e r i s criss-crossed w i t h a n i n t r i c a t e n e t w o r k o f fields o f g e n e t i c i n f l u e n c e , a w e b o f p h e n o t y p i c p o w e r . I c a n a l m o s t h e a r the t e l e v i s i o n c o m m e n t a r y : ' I m a g i n e b e i n g s h r u n k to the size of a

mitochondrion stationed

at a c o n v e n i e n t v a n t a g e point

outside the n u c l e a r m e m b r a n e of a h u m a n z y g o t e . W a t c h the molecules of messenger R N A a s they stream, b y the millions, out into the c y t o p l a s m o n t h e i r e r r a n d s o f p h e n o t y p i c p o w e r - p l a y . N o w g r o w t o t h e s i z e o f a c e l l i n the d e v e l o p i n g l i m b - b u d of a c h i c k e m b r y o . F e e l the wafts of c h e m i c a l inducers as they roll d o w n the gentle slopes of their axial g r a d i e n t s ! N o w g r o w again t o y o u r full s i z e , a n d s t a n d i n the m i d d l e o f a w o o d , a t d a w n i n s p r i n g . B i r d s o n g s u r g e s r o u n d y o u . M a l e s y r i n x e s p o u r o u t s o u n d , a n d a l l r o u n d the w o o d f e m a l e ovaries s w e l l . H e r e the influence travels in the form of pressure w a v e s i n t h e o p e n a i r , r a t h e r t h a n m o l e c u l e s i n c y t o p l a s m , b u t the p r i n c i p l e is the s a m e . At all three levels of the L i l l i p u t i a n / B r o b d i n g n a g i a n t h o u g h t experiment,

you

are

privileged

stand

the

midst

of uncountable

i n t e r l o c k i n g fields o f r e p l i c a t o r p o w e r . ' T h e r e a d e r w i l l g a t h e r t h a t i t w a s t h e message o f t h e B B C T h e o r e m t h a t I w a n t e d t o c r i t i c i z e , n o t its r h e t o r i c ! N e v e r t h e l e s s , a m o r e r e s t r a i n e d b r a n d o f eloquence

often

effective.

master of restrained

eloquence

b i o l o g i c a l w r i t i n g i s Ernst M a y r . H i s c h a p t e r o n ' T h e u n i t y o f the g e n o t y p e ' ( M a y r 1963) is often h e l d up to me in c o n v e r s a t i o n as d e e p l y antithetical to my

replicator-based

enthusiastically

viewpoint.

endorsing

almost

Since, every

the

word

contrary,

of that

find

chapter,

myself

something

must have been misunderstood, somewhere. M u c h the s a m e c o u l d b e said o f W r i g h t ' s (1980) e q u a l l y e l o q u e n t article on ' G e n i c and organismic selection', w h i c h purports to be a repudiation of t h e g e n i c s e l e c t i o n v i e w t h a t I h o l d , y e t a l m o s t n o n e o f w h i c h I find m y s e l f d i s a g r e e i n g w i t h . I t h i n k this is a v a l u a b l e p a p e r , e v e n t h o u g h its o s t e n s i b l e purpose is to a t t a c k the v i e w that ' w i t h respect to natural selection . . . it is the g e n e , not the i n d i v i d u a l or g r o u p , that is the unit'. W r i g h t c o n c l u d e s that ' T h e l i k e l i h o o d o f o r g a n i s m i c , i n s t e a d o f m e r e l y g e n i c , s e l e c t i o n g o e s far t o w a r d m e e t i n g o n e of the most serious objections to the theory of natural selection e n c o u n t e r e d by D a r w i n . ' He attributes the 'genie selection' v i e w to W i l l i a m s , M a y n a r d S m i t h a n d m e , a n d t r a c e s i t b a c k t o R . A . F i s h e r , I think c o r r e c t l y . A l l o f w h i c h m i g h t l e a d h i m t o b e s o m e w h a t b e m u s e d b y the following

accolade

from

Medawar

(1981):

'The

most

i m p o r t a n t single

A c t i o n at a D i s t a n c e

239

innovation in the m o d e r n synthesis w a s h o w e v e r the n e w c o n c e p t i o n that a population that was d e e m e d to u n d e r g o evolution c o u l d best be t h o u g h t of as a population of f u n d a m e n t a l r e p l i c a t i n g u n i t s — o f g e n e s — r a t h e r than as a population

of individual

animals

of cells.

Sewall

Wright . . . was

p r i n c i p a l i n n o v a t o r i n this n e w w a y o f t h i n k i n g — a p r i o r i t y for w h i c h R . A . F i s h e r , a n i m p o r t a n t b u t lesser f i g u r e , n e v e r f o r g a v e h i m I n t h e rest o f this c h a p t e r ,

hope to show that the version of 'genic

selectionism' that can be attacked as naively atomistic and reductionistic is a straw m a n ; that it is not the v i e w that I am a d v o c a t i n g ; a n d that if genes are c o r r e c t l y u n d e r s t o o d as b e i n g s e l e c t e d for their capacity to cooperate w i t h o t h e r genes in the g e n e - p o o l , we arrive at a theory of g e n i c selection w h i c h W r i g h t and M a y r will r e c o g n i z e a s fully c o m p a t i b l e w i t h their o w n v i e w s . N o t o n l y compatible but,

I w o u l d c l a i m , a truer a n d a clearer expression of their

v i e w s . I shall q u o t e k e y p a s s a g e s f r o m t h e s u m m a r y o f M a y r ' s c h a p t e r ( p p . 2 9 5 - 2 9 6 ) , s h o w i n g h o w they m a y b e a d a p t e d t o the w o r l d o f the e x t e n d e d phenotype. T h e p h e n o t y p e is the p r o d u c t of the h a r m o n i o u s i n t e r a c t i o n of all genes. T h e g e n o t y p e is a 'physiological t e a m ' in w h i c h a g e n e c a n m a k e a m a x i m u m c o n t r i b u t i o n t o fitness b y e l a b o r a t i n g its c h e m i c a l ' g e n e p r o d u c t ' in the n e e d e d q u a n t i t y a n d at the time w h e n it is needed in development [ M a y r 1963]. A n extended p h e n o t y p i c c h a r a c t e r i s t h e p r o d u c t o f t h e i n t e r a c t i o n o f m a n y genes w h o s e influence i m p i n g e s from b o t h inside a n d outside the o r g a n i s m . The

interaction

not

necessarily

harmonious—but

then

nor

are

gene

interactions within bodies necessarily harmonious, as we saw in C h a p t e r 8. T h e genes whose influences converge on a particular p h e n o t y p i c character a r e a ' p h y s i o l o g i c a l t e a m ' o n l y in a s p e c i a l a n d s u b t l e sense, a n d this is t r u e o f the c o n v e n t i o n a l w i t h i n - b o d y i n t e r a c t i o n s t o w h i c h M a y r refers, a s w e l l a s of extended interactions. I h a v e p r e v i o u s l y tried t o c o n v e y t h a t s p e c i a l sense w i t h t h e m e t a p h o r o f a rowing crew

(Dawkins

1976a,

pp.

91-92),

and

with

the

metaphor of

c o o p e r a t i o n b e t w e e n m y o p i c a n d n o r m a l - s i g h t e d p e o p l e ( D a w k i n s 1980, p p . 2 2 - 2 4 ) . T h e p r i n c i p l e m i g h t also b e l a b e l l e d t h e J a c k S p r a t p r i n c i p l e . T w o individuals with c o m p l e m e n t a r y appetites,

s a y for fat a n d

lean, or with

c o m p l e m e n t a r y skills, s a y i n g r o w i n g w h e a t a n d m i l l i n g it, f o r m n a t u r a l l y h a r m o n i o u s p a r t n e r s h i p s , a n d it is p o s s i b l e to r e g a r d a p a r t n e r s h i p as a higher-order unit. T h e interesting question is h o w such h a r m o n i o u s units come about. I w a n t to m a k e a general distinction b e t w e e n two models of selective processes,

both of w h i c h could,

in theory,

lead

to harmonious

cooperation and complementarity. T h e first m o d e l i n v o k e s s e l e c t i o n a t t h e l e v e l o f t h e h i g h e r - o r d e r u n i t s : i n a

240

A c t i o n at a D i s t a n c e

m e t a p o p u l a t i o n of h i g h e r - o r d e r units, h a r m o n i o u s units are favoured against d i s h a r m o n i o u s u n i t s . I t w a s a v e r s i o n o f this first m o d e l t h a t I s u g g e s t e d w a s implicit

the

Gaia

hypothesisâ&#x20AC;&#x201D;selection

among

planets

that case.

C o m i n g d o w n t o e a r t h , t h e first m o d e l m i g h t s u g g e s t t h a t g r o u p s o f a n i m a l s w h o s e m e m b e r s c o m p l e m e n t o n e a n o t h e r s ' skills, s a y g r o u p s c o n t a i n i n g b o t h farmers a n d millers, survive better than groups of farmers alone, or groups of m i l l e r s a l o n e . T h e s e c o n d m o d e l i s t h e o n e t h a t I find m o r e p l a u s i b l e . I t d o e s not need to postulate a m e t a p o p u l a t i o n of groups.

It is related to w h a t

p o p u l a t i o n geneticists call frequency-dependent selection. Selection goes on at the l o w e r level, the level of the c o m p o n e n t parts of a harmonious c o m p l e x . C o m p o n e n t s within a population are favoured by selection if they happen to interact h a r m o n i o u s l y w i t h the other c o m p o n e n t s that h a p p e n to be frequent in the p o p u l a t i o n . In a p o p u l a t i o n d o m i n a t e d by millers, i n d i v i d u a l farmers prosper, w h i l e in a p o p u l a t i o n d o m i n a t e d by farmers it p a y s to be a miller. B o t h kinds o f m o d e l l e a d t o a result w h i c h M a y r w o u l d call h a r m o n i o u s a n d c o o p e r a t i v e . B u t I am afraid that the c o n t e m p l a t i o n of h a r m o n y too o f t e n l e a d s b i o l o g i s t s t o t h i n k a u t o m a t i c a l l y i n t e r m s o f the first o f the t w o m o d e l s , a n d to forget the plausibility of the second. T h i s is true of genes w i t h i n a b o d y j u s t as it is true of farmers a n d millers in a c o m m u n i t y . T h e g e n o t y p e m a y be a ' p h y s i o l o g i c a l t e a m ' , b u t we do not h a v e to believe that that t e a m w a s necessarily selected as a harmonious unit in comparison with less h a r m o n i o u s r i v a l

units.

Rather,

each gene was selected

because it

p r o s p e r e d i n its e n v i r o n m e n t , a n d its e n v i r o n m e n t n e c e s s a r i l y i n c l u d e d t h e other genes w h i c h w e r e s i m u l t a n e o u s l y p r o s p e r i n g in the g e n e - p o o l . G e n e s w i t h c o m p l e m e n t a r y 'skills' prosper in e a c h others' presence. W h a t d o e s c o m p l e m e n t a r i n e s s m e a n for g e n e s ? T w o g e n e s m a y b e said t o b e c o m p l e m e n t a r y i f t h e s u r v i v a l o f e a c h , r e l a t i v e t o its a l l e l e s , i s e n h a n c e d w h e n t h e o t h e r i s a b u n d a n t i n t h e p o p u l a t i o n . T h e m o s t o b v i o u s r e a s o n for such m u t u a l assistance stems from the t w o genes performing a mutually c o m p l e m e n t a r y function w i t h i n individual bodies that they h a p p e n to share. T h e s y n t h e s i s o f c h e m i c a l s u b s t a n c e s o f b i o l o g i c a l i m p o r t a n c e often d e p e n d s u p o n a c h a i n of steps in a b i o c h e m i c a l p a t h w a y , e a c h o n e m e d i a t e d by a p a r t i c u l a r e n z y m e . T h e usefulness o f a n y o n e o f t h e s e e n z y m e s i s c o n d i t i o n a l u p o n the p r e s e n c e of the other e n z y m e s in the c h a i n . A g e n e - p o o l w h i c h is r i c h i n g e n e s for a l l e n z y m e s i n a g i v e n c h a i n e x c e p t o n e m a y set u p a s e l e c t i o n p r e s s u r e i n f a v o u r o f t h e g e n e for t h e m i s s i n g l i n k i n the c h a i n . I f there

are

alternative

pathways

the

same

biochemical

end

product,

selection m a y f a v o u r either p a t h w a y (but not both) d e p e n d i n g u p o n initial conditions. R a t h e r than r e g a r d the alternative p a t h w a y s as units b e t w e e n w h i c h selection chooses ( M o d e l 1), it is better to think as follows ( M o d e l 2 ) : selection will f a v o u r a g e n e that m a k e s a g i v e n e n z y m e , to the extent that g e n e s for m a k i n g t h e o t h e r e n z y m e s i n its p a t h w a y a r e a l r e a d y a b u n d a n t i n the g e n e - p o o l .

A c t i o n at a D i s t a n c e

241

But we do not h a v e to stay at a b i o c h e m i c a l level. I m a g i n e a species of m o t h w i t h stripes o n t h e w i n g s w h i c h r e s e m b l e g r o o v e s i n t r e e b a r k . S o m e i n d i v i d u a l s h a v e t r a n s v e r s e stripes w h i l e o t h e r s , i n a d i f f e r e n t a r e a , h a v e longitudinal stripes, the difference b e i n g d e t e r m i n e d at a single g e n e t i c locus. C l e a r l y a moth will be well c a m o u f l a g e d only if it points itself in the right d i r e c t i o n w h e n s i t t i n g o n t r e e b a r k ( S a r g e n t 1 9 6 9 b ) . S u p p o s e s o m e m o t h s sit vertically

and

others

horizontally,

the

behavioural

difference

being

c o n t r o l l e d a t a s e c o n d l o c u s . A n o b s e r v e r finds t h a t , f o r t u n a t e l y , a l l t h e m o t h s i n o n e a r e a h a v e l o n g i t u d i n a l stripes a n d sit v e r t i c a l l y ,

while in

a n o t h e r a r e a all t h e m o t h s h a v e t r a n s v e r s e stripes a n d sit h o r i z o n t a l l y . W e might

say,

between

then,

that

both

areas

there

t h e g e n e s for s t r i p e o r i e n t a t i o n

and

'harmonious

cooperation'

the genes d e t e r m i n i n g the

o r i e n t a t i o n o f s i t t i n g . H o w h a s this h a r m o n y c o m e a b o u t ? A g a i n w e i n v o k e o u r t w o m o d e l s . M o d e l 1 says that d i s h a r m o n i o u s g e n e c o m b i n a t i o n s â&#x20AC;&#x201D; t r a n s v e r s e stripes w i t h v e r t i c a l r e s t i n g b e h a v i o u r , o r l o n g i t u dinal

stripes

with

horizontal

resting

harmonious gene combinations.

behaviourâ&#x20AC;&#x201D;died

Model

out,

leaving

only

i n v o k e s s e l e c t i o n a m o n g combi-

nations o f g e n e s . M o d e l 2 , o n t h e o t h e r h a n d , i n v o k e s s e l e c t i o n a t t h e l o w e r l e v e l o f t h e g e n e . If, for w h a t e v e r r e a s o n , t h e g e n e - p o o l i n a g i v e n a r e a h a p p e n s t o b e a l r e a d y d o m i n a t e d b y g e n e s for t r a n s v e r s e s t r i p e s , this w i l l a u t o m a t i c a l l y set u p a s e l e c t i o n p r e s s u r e a t t h e b e h a v i o u r a l l o c u s i n f a v o u r o f g e n e s for s i t t i n g h o r i z o n t a l l y . T h i s i n t u r n w i l l set u p a s e l e c t i o n p r e s s u r e t o increase the p r e d o m i n a n c e of transverse stripe genes at the striping locus w h i c h will, in turn, reinforce the selection in favour of sitting h o r i z o n t a l l y . T h e population will therefore rapidly c o n v e r g e on the e v o l u t i o n a r i l y stable c o m b i n a t i o n , t r a n s v e r s e stripes/sit h o r i z o n t a l l y . C o n v e r s e l y , a d i f f e r e n t set o f starting conditions w o u l d evolutionarily

stable

lead

state,

the p o p u l a t i o n

longitudinal

to converge

stripes/sit

vertically.

combination of starting frequencies at the t w o loci

the other

Any

given

will converge,

after

selection, on o n e or other of the t w o stable states. M o d e l 1 i s a p p l i c a b l e o n l y i f t h e p a i r s o r sets o f c o o p e r a t i n g g e n e s a r e e s p e c i a l l y l i k e l y t o find t h e m s e l v e s t o g e t h e r i n b o d i e s , for i n s t a n c e i f t h e y a r e closely linked into a ' s u p e r g e n e ' on one c h r o m o s o m e . T h e y m i g h t indeed be so linked (Ford 1 9 7 5 ) , b u t M o d e l 2 is particularly interesting b e c a u s e it enables us to visualize the evolution of harmonious gene c o m p l e x e s w i t h o u t such

linkage.

Model

the

cooperating genes

may

c h r o m o s o m e s , a n d f r e q u e n c y - d e p e n d e n t s e l e c t i o n w i l l still l e a d

different to popu-

lations b e i n g d o m i n a t e d by genes that interact h a r m o n i o u s l y w i t h the other genes

the

population,

result

of evolution

one

another

evolutionarily stable state ( L a w l o r & M a y n a r d S m i t h 1 9 7 6 ) . In p r i n c i p l e the s a m e k i n d o f r e a s o n i n g i s a p p l i c a b l e t o sets o f t h r e e l o c i ( s u p p o s e s t r i p e s o n the

hindwing

were

controlled

different

locus

from

stripes

the

f o r e w i n g ) , four loci . . . n l o c i . I f w e t r y t o m o d e l t h e i n t e r a c t i o n s i n d e t a i l t h e

242

A c t i o n at a D i s t a n c e

m a t h e m a t i c s b e c o m e d i f f i c u l t , b u t t h a t d o e s n o t m a t t e r for t h e p o i n t I w a n t to m a k e . A l l I am saying is that there are two general w a y s in w h i c h harmonious

cooperation

can

come

about.

One

way

for

harmonious

c o m p l e x e s to be favoured by selection over dis-harmonious complexes. T h e o t h e r i s for t h e s e p a r a t e parts o f c o m p l e x e s t o b e f a v o u r e d i n the p r e s e n c e , i n the p o p u l a t i o n , of other parts w i t h w h i c h they h a p p e n to h a r m o n i z e . H a v i n g u s e d M o d e l 2 for t h e k i n d o f w i t h i n - b o d y g e n e h a r m o n y t h a t M a y r had in mind, we now generalize it to between-body, 'extended', gene interactions.

We are going to be

talking about

genetic

interaction

at a

distance, rather t h a n the p h e n o t y p i c action at a distance w h i c h w a s the subject of the

e a r l i e r p a r t o f this c h a p t e r .

T h i s is

easy

to do,

because

frequency-dependent selection has classically been applied to between-body interactions,

from

Fisher's

(1930a)

t h e o r y o f t h e sex r a t i o o n .

p o p u l a t i o n s h a v e a b a l a n c e d sex ratio? M o d e l

W h y do

1 w o u l d suggest that it is

b e c a u s e p o p u l a t i o n s w i t h a n u n b a l a n c e d sex r a t i o h a v e g o n e e x t i n c t . F i s h e r ' s o w n h y p o t h e s i s is, o f c o u r s e , a v e r s i o n o f M o d e l 2 . I f a p o p u l a t i o n h a p p e n s t o h a v e a n u n b a l a n c e d s e x r a t i o , s e l e c t i o n within t h a t p o p u l a t i o n f a v o u r s g e n e s that tend to restore the b a l a n c e . T h e r e is no need to postulate a metap o p u l a t i o n of p o p u l a t i o n s , as in the case of M o d e l 1. Other examples geneticists

(e.g.

of frequency-dependent advantage Clarke

1979),

and

have

are well

previously

known to

discussed

their

r e l e v a n c e t o t h e c o n t r o v e r s y o v e r ' h a r m o n i o u s c o o p e r a t i o n ' ( D a w k i n s 1980, p p . 2 2 - 2 4 ) . T h e p o i n t I w a n t t o stress h e r e i s t h a t , f r o m t h e p o i n t o f v i e w o f each

replicating

entity,

complementariness relationships

within

between

its

relationships

genomes

genes

are

of harmony,

not,

different

cooperation

principle,

genomes.

The

different

gene

for

and from

sitting

vertically on tree-trunks is favoured in a gene-pool w h i c h h a p p e n s to be rich i n g e n e s for l o n g i t u d i n a l s t r i p e s , a n d v i c e v e r s a . H e r e , a s i n t h e b i o c h e m i c a l e x a m p l e o f the c h a i n o f e n z y m e s , the c o o p e r a t i o n takes p l a c e w i t h i n bodies: the s i g n i f i c a n c e o f t h e f a c t t h a t t h e g e n e - p o o l i s r i c h i n g e n e s for l o n g i t u d i n a l stripes i s t h a t a n y g i v e n g e n e a t t h e l o c u s d e t e r m i n i n g s i t t i n g b e h a v i o u r i s t h e r e f o r e s t a t i s t i c a l l y l i k e l y to be in a l o n g i t u d i n a l l y s t r i p e d b o d y . I s u g g e s t that

should

think

primarily

of genes

being selected

against

the

b a c k g r o u n d of the other genes that h a p p e n to be frequent in the gene-pool, and

only

secondarily

make

distinction

between

whether

the

salient

between-gene interactions h a p p e n to occur within bodies or between them. W i c k l e r ( 1 9 6 8 ) , i n his f a s c i n a t i n g r e v i e w o f a n i m a l m i m i c r y , p o i n t s o u t that

individuals

sometimes

appear

cooperate

achieving

mimetic

resemblance. He recounts an observation by K o e n i g of what appeared to be a sea a n e m o n e in an a q u a r i u m tank. T h e following d a y there w e r e t w o a n e m o n e s , e a c h h a l f t h e s i z e o f t h e o r i g i n a l o n e , a n d t h e d a y after t h a t the o r i g i n a l l a r g e a n e m o n e h a d a p p a r e n t l y r e c o n s t i t u t e d itself. T h e i m p o s s i b i l i t y

A c t i o n at a D i s t a n c e

243

o f this f i n a l l y led K o e n i g t o i n v e s t i g a t e i n d e t a i l , a n d h e d i s c o v e r e d t h a t t h e ' a n e m o n e ' w a s i n fact a f a k e , p u t t o g e t h e r b y n u m e r o u s c o o p e r a t i n g a n n e l i d worms. E a c h w o r m represented one tentacle, and they grouped themselves into a circle in the sand. Fish s e e m e d to be fooled by the d e c e p t i o n just as K o e n i g o r i g i n a l l y w a s , for t h e y g a v e t h e f a k e a n e m o n e t h e s a m e k i n d o f w i d e berth they w o u l d

a real one.

Each individual worm

presumably gained

p r o t e c t i o n f r o m fish p r e d a t o r s , b y j o i n i n g i n t h e c o o p e r a t i v e m i m i c r y r i n g . I s u g g e s t t h a t i t i s n o t h e l p f u l t o s p e a k o f groups o f w o r m s t h a t f o r m r i n g s a s being selected over groups that do not. R a t h e r , ring-joining i n d i v i d u a l s are favoured in populations of ring-joiners. In various insect species, e a c h i n d i v i d u a l m i m i c s o n e flower of a m a n y flowered inflorescence, and therefore a c o o p e r a t i n g c r o w d of t h e m is needed before a w h o l e inflorescence c a n be c o n v i n c i n g l y m i m i c k e d . ' I n East A f r i c a it

possible

find

particular

plant

with

extremely

beautiful

i n f l o r e s c e n c e s . . . t h e i n d i v i d u a l flowers a r e a b o u t h a l f a c e n t i m e t r e in h e i g h t , l o o k r a t h e r like b r o o m f l o w e r s , a n d a r e a r r a n g e d a r o u n d a v e r t i c a l s t e m l i k e the f l o w e r s o f t h e l u p i n .

E x p e r i e n c e d b o t a n i s t s h a v e t a k e n this p l a n t for

Tinnaea or Sesamopteris a n d f o u n d t h e m s e l v e s s u d d e n l y h o l d i n g a b a r e s t e m after p l u c k i n g the " f l o w e r " . T h e f l o w e r h a d n o t f a l l e n o f f â&#x20AC;&#x201D; i t h a d f l o w n away!

The

nigritarsus In

"flower"

consists o f c i c a d a s ,

e i t h e r Ityraea gregorii o r

Oyarina

( W i c k l e r 1968, p. 6 1 ) .

order

develop

argument

need

make

certain

detailed

assumptions. S i n c e the details of the selection pressures b e a r i n g on these particular c i c a d a species are not k n o w n ,

it will

b e safest i f I

invent a

hypothetical c i c a d a w h i c h basically practises the same g r o u p - m i m i c r y trick as Ityraea a n d Oyarina. I a s s u m e t h a t my s p e c i e s o c c u r s in t w o c o l o u r m o r p h s , p i n k a n d b l u e , a n d t h a t the t w o m o r p h s m i m i c t w o d i f f e r e n t c o l o u r v a r i e t i e s of lupin. Pink a n d blue lupins are assumed to be e q u a l l y a b u n d a n t o v e r the w h o l e r a n g e of the c i c a d a species, b u t in a n y o n e l o c a l a r e a all the c i c a d a s are either pink or blue. together

near

the

' C o o p e r a t i o n ' occurs, in that individuals cluster

tips

plant

stems

and

together

resemble

lupin

inflorescences. It is ' h a r m o n i o u s ' in that m i x e d colour clusters do not o c c u r : I assume that a m i x e d c o l o u r cluster is especially likely to be spotted by predators as a fake, since real lupins do not h a v e t w o - t o n e inflorescences. H e r e i s h o w t h e h a r m o n y m i g h t h a v e c o m e a b o u t t h r o u g h M o d e l 2's frequency-dependent

selection.

any

given

area,

historical

accident

determined that there w a s an initial majority in f a v o u r of o n e c o l o u r t y p e or the o t h e r . I n a n a r e a t h a t h a p p e n e d t o b e d o m i n a t e d b y p i n k c i c a d a s , b l u e ones w e r e p e n a l i z e d .

In an area that h a p p e n e d to be d o m i n a t e d by blue

cicadas, pink one w e r e p e n a l i z e d . In both cases, simply b e i n g in the m i n o r i t y was disfavoured, b e c a u s e a m e m b e r of the m i n o r i t y t y p e w a s , by the l a w s of chance,

likely

than

m e m b e r of the

majority type

find

itself

244

A c t i o n at a D i s t a n c e

p a r t i c i p a t i n g in a m i x e d cluster. At the g e n e level we m a y say that pink genes are favoured in a gene-pool dominated by pink genes, and blue genes are favoured in a gene-pool dominated by blue genes. We n o w invent a n o t h e r insect, say a caterpillar, w h i c h is large e n o u g h to m i m i c a w h o l e lupin inflorescence, instead of a single flower. E a c h segment o f t h e c a t e r p i l l a r m i m i c s a different f l o w e r o f t h e i n f l o r e s c e n c e . T h e c o l o u r o f e a c h s e g m e n t i s c o n t r o l l e d a t a different l o c u s , t h e a l t e r n a t i v e s b e i n g p i n k a n d b l u e . A c a t e r p i l l a r t h a t i s a l l b l u e o r a l l p i n k i s m o r e successful t h a n o n e that is a m i x t u r e of colours because, o n c e a g a i n , predators h a v e learned that m i x e d colour lupins do not occur. T h e r e is no theoretical reason w h y twot o n e c a t e r p i l l a r s s h o u l d n o t o c c u r , b u t s u p p o s e t h a t , a s a result o f s e l e c t i o n , they do n o t : in a n y o n e a r e a the local caterpillars are either all pink or all blue. We have 'harmonious cooperation' again. How

might

the

harmonious

cooperation

come

about?

definition,

M o d e l 1 w o u l d b e a p p l i c a b l e o n l y i f t h e g e n e s r e s p o n s i b l e for t h e c o l o r a t i o n of the different s e g m e n t s w e r e linked tightly in a supergene. M u l t i - c o l o u r e d supergenes w o u l d be p e n a l i z e d at the expense of p u r e pink and pure blue supergenes.

I n this h y p o t h e t i c a l s p e c i e s , h o w e v e r , t h e r e l e v a n t g e n e s a r e

w i d e l y spread on different c h r o m o s o m e s , and we h a v e to a p p l y M o d e l 2. In a n y g i v e n l o c a l a r e a , o n c e o n e c o l o u r starts t o p r e d o m i n a t e a t a m a j o r i t y o f loci, selection w o r k s to increase the f r e q u e n c y of that c o l o u r at all loci. In a p a r t i c u l a r area, if all the loci save one are d o m i n a t e d by pink genes, the odd l o c u s w h i c h i s d o m i n a t e d b y b l u e g e n e s w i l l s o o n b e b r o u g h t i n t o line b y selection. As in the case of the hypothetical cicadas, historical accidents in different l o c a l a r e a s a u t o m a t i c a l l y set u p s e l e c t i o n p r e s s u r e s i n f a v o u r o f o n e o r a n o t h e r o f t w o e v o l u t i o n a r i l y s t a b l e states. T h e p o i n t o f this t h o u g h t e x p e r i m e n t i s t h a t M o d e l 2 i s e q u a l l y a p p l i c a b l e both b e t w e e n a n d w i t h i n i n d i v i d u a l s . In both the caterpillar a n d the c i c a d a case,

pink genes are favoured in gene-pools already d o m i n a t e d by pink

genes, and blue genes are favoured in gene-pools already dominated by blue g e n e s . I n t h e c a t e r p i l l a r s t h e r e a s o n i s t h a t e a c h g e n e benefits i f i t shares a body w i t h o t h e r g e n e s p r o d u c i n g t h e s a m e c o l o u r a s itself. I n t h e c i c a d a s t h e r e a s o n i s t h a t e a c h g e n e b e n e f i t s i f t h e b o d y i t i s i n m e e t s another b o d y b e a r i n g a g e n e p r o d u c i n g t h e s a m e c o l o u r a s itself. I n t h e c a t e r p i l l a r e x a m p l e , t h e c o o p e r a t i n g g e n e s o c c u p y different l o c i i n t h e s a m e i n d i v i d u a l . I n t h e c i c a d a example

the

cooperating

genes

occupy

the

same

locus

different

i n d i v i d u a l s . M y p u r p o s e i s t o c l o s e t h e c o n c e p t u a l g a p b e t w e e n these t w o kinds of g e n e interaction, by s h o w i n g that genetic interaction at a distance is n o t , i n p r i n c i p l e , different f r o m g e n e t i c i n t e r a c t i o n w i t h i n o n e b o d y . T o r e s u m e m y series o f q u o t a t i o n s f r o m M a y r : T h e result of the c o a d a p t i n g selection is a h a r m o n i o u s l y integrated g e n e c o m p l e x . T h e c o a c t i o n o f the genes m a y o c c u r a t m a n y levels,

A c t i o n at a D i s t a n c e

that

of the

chromosome,

nucleus,

cell,

tissue,

organ,

and

245

whole

organism. T h e r e a d e r w i l l b y n o w h a v e n o d i f f i c u l t y i n g u e s s i n g h o w M a y r ' s list i s t o b e e x t e n d e d . C o a c t i o n a m o n g g e n e s i n different o r g a n i s m s i s n o t f u n d a m e n t a l l y different f r o m c o a c t i o n a m o n g g e n e s i n t h e s a m e o r g a n i s m . E a c h g e n e w o r k s in a world of p h e n o t y p i c consequences of other genes. S o m e of those other genes will be m e m b e r s of the same g e n o m e . O t h e r s will be m e m b e r s of the same gene-pool operating through other bodies. Y e t others m a y be m e m b e r s o f different g e n e - p o o l s , different s p e c i e s , different p h y l a . T h e n a t u r e o f the f u n c t i o n a l m e c h a n i s m s o f p h y s i o l o g i c a l i n t e r a c t i o n are

[sic]

only

of minor

interest

the

evolutionist,

whose

main

c o n c e r n is the viability of the u l t i m a t e p r o d u c t , the p h e n o t y p e . M a y r hits t h e n a i l o n t h e h e a d a g a i n , b u t his ' p h e n o t y p e ' i s n o t t h e u l t i m a t e : it can be e x t e n d e d outside the i n d i v i d u a l b o d y . Many

devices

tend

maintain

the

status

quo

gene

pools,

quantitatively and qualitatively. T h e lower limit of genetic diversity is determined

b y the frequent a d v a n t a g e o f h e t e r o z y g o s i t y . . . T h e

u p p e r limit is d e t e r m i n e d by the fact that o n l y those g e n e s c a n be incorporated that are able to ' c o a d a p t ' h a r m o n i o u s l y . No g e n e has a f i x e d selective v a l u e ; the same g e n e m a y confer h i g h f i t n e s s o n o n e genetic b a c k g r o u n d and be virtually lethal on another. Excellent, but r e m e m b e r that 'genetic b a c k g r o u n d ' c a n i n c l u d e genes in other organisms as well as genes w i t h i n the s a m e o r g a n i s m . T h e result o f t h e c l o s e i n t e r d e p e n d e n c e o f a l l g e n e s i n a g e n e p o o l i s tight cohesion. N o g e n e frequency c a n b e c h a n g e d , nor a n y g e n e b e a d d e d t o t h e g e n e p o o l , w i t h o u t a n effect o n t h e g e n o t y p e a s a w h o l e , and thus indirectly on the selective v a l u e of o t h e r genes. M a y r h i m s e l f has n o w s u b t l y shifted t o t a l k i n g a b o u t a c o a d a p t e d g e n e pool, rather than a c o a d a p t e d individual g e n o m e . T h i s is a g r e a t step in the right d i r e c t i o n , b u t w e m u s t still t a k e o n e f u r t h e r s t e p . M a y r i s h e r e t a l k i n g a b o u t interactions b e t w e e n all the genes in o n e g e n e - p o o l , regardless of the bodies they

happen

be sitting

in.

T h e doctrine

of the

extended

phenotype

ultimately requires us to a c k n o w l e d g e the same kind of interactions a m o n g g e n e s o f different g e n e - p o o l s , different p h y l a , d i f f e r e n t k i n g d o m s . Consider a g a i n the w a y s in w h i c h a pair of genes in the same gene-pool can interact, m o r e specifically the w a y s in w h i c h the f r e q u e n c y of e a c h in the

246

A c t i o n at a D i s t a n c e

g e n e - p o o l c a n affect t h e s u r v i v a l p r o s p e c t s o f t h e o t h e r . T h e first w a y , a n d t h e o n e w h i c h I s u s p e c t M a y r h a d m a i n l y i n m i n d , i s t h r o u g h s h a r i n g the s a m e b o d y . T h e s u r v i v a l prospects of g e n e A are influenced by the frequency i n t h e p o p u l a t i o n o f g e n e B , b e c a u s e B's f r e q u e n c y i n f l u e n c e s t h e p r o b a b i l i t y t h a t A w i l l find i t s e l f s h a r i n g a b o d y w i t h B . T h e i n t e r a c t i o n b e t w e e n the l o c i d e t e r m i n i n g m o t h stripe direction and sitting direction w a s an e x a m p l e of this. S o w a s t h e h y p o t h e t i c a l l u p i n - m i m i c k i n g c a t e r p i l l a r . S o i s a p a i r o f genes

c o d i n g for

enzymes

that

are

necessary

for s u c c e s s i v e

stages

p a r t i c u l a r p a t h w a y s y n t h e s i z i n g a useful s u b s t a n c e . C a l l this t y p e o f g e n e interaction 'within-body' interaction. T h e second w a y in w h i c h the frequency of a gene B in a population can affect t h e s u r v i v a l p r o s p e c t s o f a g e n e A i s ' b e t w e e n - b o d y ' i n t e r a c t i o n . T h e v i t a l i n f l u e n c e h e r e i s o n t h e p r o b a b i l i t y t h a t a n y b o d y i n w h i c h A sits w i l l m e e t a n o t h e r b o d y i n w h i c h B sits. M y h y p o t h e t i c a l c i c a d a s p r o v i d e d a n e x a m p l e of this. So does Fisher's sex ratio theory. As I h a v e e m p h a s i z e d , it h a s b e e n o n e o f m y p u r p o s e s i n this c h a p t e r t o m i n i m i z e t h e d i s t i n c t i o n b e t w e e n the t w o kinds of g e n e interaction, w i t h i n - b o d y and b e t w e e n - b o d y interaction. But

now

consider

interactions

between

genes

different

gene-pools,

d i f f e r e n t s p e c i e s . I t w i l l b e s e e n t h a t t h e r e i s r a t h e r little d i s t i n c t i o n b e t w e e n a cross-species g e n e interaction a n d a within-species b e t w e e n - i n d i v i d u a l gene interaction. In neither case do the i n t e r a c t i n g genes share a b o d y . In both c a s e s t h e s u r v i v a l p r o s p e c t s o f e a c h m a y d e p e n d o n t h e f r e q u e n c y , i n its o w n g e n e - p o o l , of the o t h e r g e n e .

L e t me illustrate the point using the lupin

t h o u g h t e x p e r i m e n t a g a i n . S u p p o s e there is a species of beetle w h i c h is p o l y m o r p h i c like the c i c a d a s . In s o m e areas it turns out that the pink morphs of b o t h species, c i c a d a s a n d beetles, p r e d o m i n a t e , w h i l e in other areas the b l u e m o r p h s o f b o t h s p e c i e s p r e d o m i n a t e . T h e t w o s p e c i e s differ i n b o d y s i z e . T h e y ' c o o p e r a t e ' in faking inflorescences, the smaller-bodied cicadas tending t o sit n e a r t h e tips o f s t e m s , w h e r e s m a l l f l o w e r s m i g h t b e e x p e c t e d , t h e l a r g e r b e e t l e s t e n d i n g t o sit n e a r e r t h e b a s e o f e a c h f a k e i n f l o r e s c e n c e . A j o i n t b e e t l e / c i c a d a ' i n f l o r e s c e n c e ' fools b i r d s m o r e e f f e c t i v e l y t h a n e i t h e r a pure beetle or a pure c i c a d a one. M o d e l 2's f r e q u e n c y - d e p e n d e n t s e l e c t i o n w i l l t e n d t o l e a d t o t h e e v o l u t i o n o f o n e o f t w o e v o l u t i o n a r i l y s t a b l e states, j u s t a s b e f o r e , e x c e p t t h a t t w o species are n o w i n v o l v e d . If historical accident leads to one local area being dominated

pink morphs

(regardless of species),

selection

species will f a v o u r pink m o r p h s o v e r b l u e ; and vice versa.

within

both

If the beetle

s p e c i e s w a s r e l a t i v e l y r e c e n t l y i n t r o d u c e d i n t o a r e a s a l r e a d y c o l o n i z e d b y the c i c a d a species, the d i r e c t i o n of selection w i t h i n the beetle species will d e p e n d o n the c o l o u r o f the l o c a l l y p r e d o m i n a n t m o r p h o f c i c a d a s . T h u s there will be frequency-dependent interaction between genes in pools,

the

gene-pools

of two

non-interbreeding

t w o different g e n e -

species.

faking

the

A c t i o n at a D i s t a n c e

247

inflorescence of a lupin, c i c a d a s m i g h t c o o p e r a t e w i t h spiders or snails just as effectively as w i t h beetles or w i t h c i c a d a s of a n o t h e r species. M o d e l 2 w o r k s across s p e c i e s a n d a c r o s s p h y l a , a s w e l l a s a c r o s s i n d i v i d u a l s a n d w i t h i n individuals. Across usitissimum)

kingdoms, and

the

too.

Consider

rust

fungus

the

interaction

Melampsora

lini,

antagonistic rather than a cooperative interaction.

between although

flax

(Linum

this

' T h e r e is e s s e n t i a l l y a

one-to-one m a t c h i n g in w h i c h a specific allele in the flax confers resistance to a specific a l l e l e i n t h e rust. T h i s " g e n e - f o r - g e n e " s y s t e m h a s s i n c e b e e n f o u n d in numerous other plant species . . . M o d e l s of gene-for-gene interactions are not formulated in

terms of e c o l o g i c a l p a r a m e t e r s b e c a u s e of the specific

n a t u r e o f the g e n e t i c s y s t e m s . I t i s o n e c a s e i n w h i c h t h e g e n e t i c i n t e r a c t i o n s b e t w e e n species c a n be understood w i t h o u t reference to the p h e n o t y p e s . A model of a gene-for-gene system w o u l d necessarily h a v e between-species frequency dependence . . . (Slatkin & M a y n a r d Smith 1979, pp. 2 5 5 - 2 5 6 ) . I n this c h a p t e r , a s i n o t h e r s , I h a v e u s e d h y p o t h e t i c a l t h o u g h t e x p e r i m e n t s to aid clear e x p l a n a t i o n . In case they are found too far-fetched, let me turn t o W i c k l e r a g a i n for a n e x a m p l e o f a r e a l c i c a d a w h i c h d o e s s o m e t h i n g a t least as f a r - f e t c h e d as a n y t h i n g I h a v e i n v e n t e d . Ityraea nigrocincta, l i k e I. gregorii,

practises c o o p e r a t i v e

m i m i c r y of lupin-like

inflorescences,

but

'possesses a f u r t h e r p e c u l i a r i t y i n t h a t b o t h s e x e s h a v e t w o m o r p h s , a g r e e n form a n d a y e l l o w f o r m . T h e s e t w o m o r p h s m a y s q u a t t o g e t h e r , a n d t h e g r e e n forms t e n d t o sit a t t h e t o p o f t h e s t e m , e s p e c i a l l y o n v e r t i c a l s t e m s , with

the

yellow

"inflorescence",

forms

below.

because

the

The

true

result

flowers

extremely

convincing

of inflorescences

often

open

p r o g r e s s i v e l y f r o m b a s e t o a p e x , s o t h a t g r e e n b u d s a r e still p r e s e n t a t t h e tip w h e n the base is c o v e r e d w i t h o p e n flowers' ( W i c k l e r 1968). T h e s e three chapters h a v e e x t e n d e d the c o n c e p t o f p h e n o t y p i c expression of genes by easy stages. We b e g a n with the recognition that e v e n within a b o d y there are m a n y degrees o f distance o f g e n e control o v e r p h e n o t y p e s . F o r a n u c l e a r g e n e t o c o n t r o l t h e s h a p e o f t h e c e l l i n w h i c h i t sits i s p r e s u m a b l y simpler than to control the shape of s o m e o t h e r cell, or of the w h o l e b o d y i n w h i c h t h e c e l l sits. Y e t w e c o n v e n t i o n a l l y l u m p t h e t h r e e t o g e t h e r a n d c a l l t h e m a l l g e n e t i c c o n t r o l o f p h e n o t y p e . M y thesis h a s b e e n t h a t the s l i g h t

further c o n c e p t u a l step outside

the

immediate

b o d y is

c o m p a r a t i v e l y m i n o r o n e . N e v e r t h e l e s s i t i s a n u n f a m i l i a r o n e , a n d I tried t o d e v e l o p the i d e a i n s t a g e s , w o r k i n g t h r o u g h i n a n i m a t e a r t e f a c t s t o i n t e r n a l parasites

controlling

their

hosts'

behaviour.

From

internal

parasites

m o v e d via c u c k o o s to action at a distance. In theory, g e n e t i c action at a distance c o u l d i n c l u d e almost all interactions b e t w e e n i n d i v i d u a l s of the s a m e o r different s p e c i e s . T h e l i v i n g w o r l d c a n b e s e e n a s a n e t w o r k o f interlocking fields of replicator power. It

hard

for

imagine

the

kind

mathematics

that

the

A c t i o n at a D i s t a n c e

248

u n d e r s t a n d i n g of the details w i l l e v e n t u a l l y d e m a n d . I h a v e a d i m vision of p h e n o t y p i c c h a r a c t e r s i n a n e v o l u t i o n a r y s p a c e b e i n g t u g g e d i n different directions by replicators u n d e r selection. It is of the essence of my a p p r o a c h that the replicators t u g g i n g on a n y given p h e n o t y p i c feature will include s o m e f r o m o u t s i d e t h e b o d y a s w e l l a s t h o s e i n s i d e it. S o m e w i l l o b v i o u s l y b e tugging

harder

than

others,

the

arrows

of force

will

have

varying

m a g n i t u d e as w e l l as d i r e c t i o n . P r e s u m a b l y the theory of arms racesâ&#x20AC;&#x201D;the r a r e - e n e m y effect, t h e l i f e / d i n n e r p r i n c i p l e , e t c . â&#x20AC;&#x201D; w i l l h a v e a p r o m i n e n t role to p l a y in the assignment of these m a g n i t u d e s . S h e e r physical p r o x i m i t y will p r o b a b l y p l a y a role: genes seem likely, other things b e i n g equal, to exert more p o w e r over n e a r b y phenotypic characters than over distant ones. As an i m p o r t a n t s p e c i a l c a s e o f this, c e l l s a r e l i k e l y t o b e q u a n t i t a t i v e l y m o r e h e a v i l y influenced by genes inside t h e m than by genes inside other cells. T h e s a m e w i l l g o for b o d i e s . B u t t h e s e w i l l b e q u a n t i t a t i v e effects, t o b e w e i g h e d in the b a l a n c e w i t h other considerations from arms r a c e theory. S o m e t i m e s , s a y b e c a u s e o f t h e r a r e - e n e m y effect, g e n e s i n o t h e r b o d i e s m a y e x e r t m o r e p o w e r t h a n t h e b o d y ' s ' o w n ' g e n e s , o v e r p a r t i c u l a r a s p e c t s o f its p h e n o t y p e . M y h u n c h i s t h a t a l m o s t a l l p h e n o t y p i c c h a r a c t e r s w i l l t u r n o u t t o b e a r the m a r k s o f c o m p r o m i s e b e t w e e n internal a n d external replicator forces. T h e i d e a o f c o n f l i c t a n d c o m p r o m i s e b e t w e e n m a n y s e l e c t i o n pressures b e a r i n g o n a g i v e n p h e n o t y p i c c h a r a c t e r is, o f c o u r s e , f a m i l i a r f r o m o r d i n a r y b i o l o g y . W e o f t e n s p e a k of, s a y , t h e s i z e o f a b i r d ' s tail a s a c o m p r o m i s e b e t w e e n the needs of a e r o d y n a m i c s a n d the needs of sexual attractiveness. I d o n o t k n o w w h a t k i n d o f m a t h e m a t i c s a r e c o n s i d e r e d s u i t a b l e for d e s c r i b i n g this k i n d o f w i t h i n - b o d y c o n f l i c t a n d c o m p r o m i s e , b u t w h a t e v e r t h e y a r e , they should be g e n e r a l i z e d to c o p e with the analogous problems of genetic action at a distance and extended phenotypes. But I h a v e not the w i n g s to fly in m a t h e m a t i c a l spaces. T h e r e must be a v e r b a l m e s s a g e for t h o s e t h a t s t u d y a n i m a l s i n t h e field. W h a t d i f f e r e n c e w i l l the

doctrine

of the

extended

phenotype

make

how we

a c t u a l l y see

a n i m a l s ? M o s t s e r i o u s field b i o l o g i s t s n o w s u b s c r i b e t o t h e t h e o r e m , l a r g e l y d u e to H a m i l t o n , that a n i m a l s are e x p e c t e d to b e h a v e as if m a x i m i z i n g the s u r v i v a l c h a n c e s o f a l l t h e g e n e s i n s i d e t h e m . I h a v e a m e n d e d this t o a n e w c e n t r a l t h e o r e m o f the e x t e n d e d p h e n o t y p e : A n a n i m a l ' s b e h a v i o u r tends t o m a x i m i z e t h e s u r v i v a l o f t h e g e n e s ' f o r ' t h a t b e h a v i o u r , w h e t h e r o r n o t those g e n e s h a p p e n t o b e i n t h e b o d y o f t h e p a r t i c u l a r a n i m a l p e r f o r m i n g the b e h a v i o u r . T h e t w o theorems w o u l d a m o u n t to the same thing if animal phenotypes

were

always

under

the

unadulterated

control

of their o w n

g e n o t y p e s , a n d u n i n f l u e n c e d b y the genes o f other organisms. I n a d v a n c e o f a

mathematical

theory

handle

the

quantitative

interactions

between

c o n f l i c t i n g p r e s s u r e s , p e r h a p s t h e s i m p l e s t q u a l i t a t i v e c o n c l u s i o n i s t h a t the b e h a v i o u r w e a r e l o o k i n g a t m a y b e , a t l e a s t p a r t l y , a n a d a p t a t i o n for the

A c t i o n at a D i s t a n c e

249

preservation of some other animal's or plant's genes. It m a y therefore be p o s i t i v e l y m a l a d a p t i v e for t h e o r g a n i s m p e r f o r m i n g t h e b e h a v i o u r . O n c e w h e n I tried to p e r s u a d e a c o l l e a g u e of thisâ&#x20AC;&#x201D;he is a s t a u n c h b e l i e v e r in the p o w e r of D a r w i n i a n selection, a n d a g o o d field i n v e s t i g a t o r of i t â&#x20AC;&#x201D; h e thought that I was m a k i n g an anti-adaptation point. He w a r n e d me that t i m e a n d a g a i n p e o p l e h a d w r i t t e n off s o m e q u i r k o f a n i m a l b e h a v i o u r o r m o r p h o l o g y as functionless or m a l a d a p t i v e , only to d i s c o v e r that they h a d n o t fully u n d e r s t o o d it. H e w a s r i g h t . B u t t h e p o i n t I a m m a k i n g i s d i f f e r e n t . W h e n I s a y h e r e t h a t a b e h a v i o u r p a t t e r n is m a l a d a p t i v e , I o n l y m e a n it is m a l a d a p t i v e for t h e individual animal p e r f o r m i n g it. I am s u g g e s t i n g t h a t t h e i n d i v i d u a l p e r f o r m i n g t h e b e h a v i o u r i s n o t t h e e n t i t y for w h o s e b e n e f i t t h e behaviour responsible

for

adaptation. them,

and

Adaptations only

benefit

incidentally

the

genetic

replicators

individual

organisms

involved. This

could

have

been

the

end

of the

book.

have

extended

the

p h e n o t y p e o u t a s far a s i t c a n g o . T h e p a s t t h r e e c h a p t e r s b u i l d t o a c l i m a x o f a sort, a n d w e m i g h t h a v e b e e n c o n t e n t w i t h this a s c o n s u m m a t i o n . B u t I prefer

to end

upbeat,

to begin

the arousing of a

tentative

new

c u r i o s i t y . I c o n f e s s e d a t t h e o u t s e t t o b e i n g a n a d v o c a t e , a n d a n e a s y w a y for a n y a d v o c a t e t o p r e p a r e t h e g r o u n d for his c a s e i s t o a t t a c k t h e a l t e r n a t i v e . Before a d v o c a t i n g the d o c t r i n e o f the e x t e n d e d p h e n o t y p e o f a n a c t i v e g e r m line r e p l i c a t o r , t h e r e f o r e , I t r i e d t o u n d e r m i n e t h e r e a d e r ' s c o n f i d e n c e i n t h e individual o r g a n i s m as the unit of a d a p t i v e benefit. B u t , n o w that we h a v e discussed the e x t e n d e d p h e n o t y p e itself, i t i s t i m e t o r e o p e n t h e q u e s t i o n o f t h e o r g a n i s m ' s e x i s t e n c e a n d o b v i o u s i m p o r t a n c e i n t h e h i e r a r c h y o f life, a n d see w h e t h e r w e see i t a n y c l e a r e r i n t h e l i g h t o f t h e e x t e n d e d p h e n o t y p e . G i v e n t h a t life d i d n o t have t o b e p a c k a g e d i n t o d i s c r e t e o r g a n i s m s , a n d a l l o w i n g that organisms are not a l w a y s totally discrete, w h y , nevertheless, d i d a c t i v e g e r m - l i n e r e p l i c a t o r s s o c o n s p i c u o u s l y o p t for t h e o r g a n i s m a l w a y of doing things?

14 Rediscovering the O r g a n i s m

H a v i n g d e v o t e d m o s t o f this b o o k t o p l a y i n g d o w n t h e i m p o r t a n c e o f the

individual

organism,

and

building up an

alternative image of a

t u r m o i l o f selfish r e p l i c a t o r s , b a t t l i n g for t h e i r o w n s u r v i v a l a t t h e e x p e n s e o f their alleles, r e a c h i n g u n i m p e d e d through individual b o d y walls as though those walls w e r e transparent, interacting w i t h the w o r l d a n d w i t h e a c h other w i t h o u t regard to organismal boundaries, we n o w hesitate. T h e r e really is something pretty impressive about individual organisms. If we actually could w e a r s p e c t a c l e s t h a t m a d e b o d i e s t r a n s p a r e n t a n d d i s p l a y e d o n l y D N A , the d i s t r i b u t i o n o f D N A t h a t w e w o u l d see i n t h e w o r l d w o u l d b e o v e r w h e l m i n g l y n o n - r a n d o m . I f c e l l n u c l e i g l o w e d l i k e stars a n d a l l else w a s i n v i s i b l e , multicellular bodies would show up as close-packed galaxies with cavernous space b e t w e e n them. A million billion g l o w i n g pinpricks m o v e in unison with e a c h o t h e r a n d o u t o f step w i t h all the m e m b e r s o f other such g a l a x i e s . T h e o r g a n i s m i s a p h y s i c a l l y d i s c r e t e m a c h i n e , u s u a l l y w a l l e d off from other such machines.

It has an internal organization,

often o f s t a g g e r i n g

c o m p l e x i t y , a n d it displays to a h i g h d e g r e e the q u a l i t y that J u l i a n H u x l e y (1912) labelled 'individuality'—literally indivisibility—the quality of being sufficiently h e t e r o g e n e o u s in form to be rendered non-functional if cut in half. G e n e t i c a l l y s p e a k i n g , t o o , t h e i n d i v i d u a l o r g a n i s m i s u s u a l l y a c l e a r l y d e f i n a b l e u n i t , w h o s e c e l l s h a v e t h e s a m e g e n e s a s e a c h o t h e r b u t different genes from the cells o f o t h e r organisms. T o a n i m m u n o l o g i s t the i n d i v i d u a l o r g a n i s m has a special kind of 'uniqueness' ( M e d a w a r 1 9 5 7 ) , in that it will r e a d i l y a c c e p t g r a f t s f r o m o t h e r p a r t s o f its o w n b o d y , b u t n o t f r o m o t h e r bodies.

the

ethologist—and

indivisibility—the

organism

s t r o n g e r sense t h a n , s a y ,

this

really

aspect

unit of b e h a v i o u r a l

action

of in

Huxley's a

much

two organisms, or a limb of an organism. T h e

organism has one coordinated central nervous system.

It takes 'decisions'

( D a w k i n s & D a w k i n s 1 9 7 3 ) a s a u n i t . A l l its l i m b s c o n s p i r e h a r m o n i o u s l y t o g e t h e r to a c h i e v e o n e end at a time. On those occasions w h e n t w o or more organisms

try

coordinate

their

efforts, 250

say

when

pride

o f lions

R e d i s c o v e r i n g the O r g a n i s m

251

c o o p e r a t i v e l y s t a l k s p r e y , t h e feats o f c o o r d i n a t i o n a m o n g i n d i v i d u a l s a r e feeble

compared

with

the

intricate orchestration,

with

high

spatial

and

temporal precision, of the hundreds of muscles within e a c h i n d i v i d u a l . E v e n a starfish, w h o s e t u b e - f e e t e n j o y a m e a s u r e o f a u t o n o m y a n d m a y t e a r t h e a n i m a l in t w o if the c i r c u m - o r a l nerve ring has b e e n s u r g i c a l l y cut, looks like a single entity, a n d in n a t u r e b e h a v e s as if it h a d a single p u r p o s e . I

am grateful

to Dr J.

H a i l m a n for n o t w i t h h o l d i n g f r o m m e t h e

s a r c a s t i c r e a c t i o n o f a c o l l e a g u e t o t h e p a p e r t h a t w a s a b r i e f t r i a l - r u n for this book ( D a w k i n s 1 9 7 8 a ) : ' R i c h a r d D a w k i n s has rediscovered the o r g a n i s m . ' T h e i r o n y w a s n o t lost o n m e , b u t t h e r e a r e w h e e l s w i t h i n w h e e l s . W e a g r e e that there is s o m e t h i n g special a b o u t the i n d i v i d u a l o r g a n i s m as a l e v e l in the h i e r a r c h y o f life, b u t i t i s n o t s o m e t h i n g o b v i o u s , t o b e a c c e p t e d w i t h o u t q u e s t i o n . M y h o p e i s t h a t this b o o k h a s r e v e a l e d t h a t t h e r e i s a s e c o n d side t o the N e c k e r C u b e . B u t N e c k e r C u b e s h a v e a h a b i t o f f l i p p i n g b a c k a g a i n t o their original orientation, a n d then c o n t i n u i n g to a l t e r n a t e . W h a t e v e r it is t h a t i s s p e c i a l a b o u t t h e i n d i v i d u a l o r g a n i s m a s a u n i t o f life, w e s h o u l d a t least see i t m o r e c l e a r l y for h a v i n g v i e w e d t h e o t h e r s i d e o f t h e N e c k e r C u b e , for h a v i n g t r a i n e d o u r e y e s t o see t h r o u g h b o d y w a l l s i n t o t h e w o r l d o f replicators, and out and b e y o n d to their e x t e n d e d p h e n o t y p e s . S o , w h a t i s i t t h a t i s s p e c i a l a b o u t t h e i n d i v i d u a l o r g a n i s m ? G i v e n t h a t life can be v i e w e d as consisting of replicators w i t h their e x t e n d e d p h e n o t y p i c tools o f s u r v i v a l , w h y i n p r a c t i c e h a v e r e p l i c a t o r s c h o s e n t o g r o u p t h e m s e l v e s together b y the h u n d r e d s o f thousands i n cells, a n d w h y h a v e they influenced those cells t o c l o n e t h e m s e l v e s b y t h e m i l l i o n s o f b i l l i o n s i n o r g a n i s m s ? O n e kind o f a n s w e r i s suggested b y the logic o f c o m p l e x systems. S i m o n (1962) has written a s t i m u l a t i n g essay on ' T h e a r c h i t e c t u r e of c o m p l e x i t y ' , w h i c h suggests

(using a p a r a b l e of t w o w a t c h m a k e r s called T e m p u s a n d

H o r a , w h i c h has b e c o m e well k n o w n ) , a g e n e r a l functional reason w h y complex

organization

of any

kind,

biological

artificial,

tends

o r g a n i z e d i n t o n e s t e d h i e r a r c h i e s o f r e p e a t e d s u b u n i t s . I h a v e d e v e l o p e d his argument

the

ethological

context,

concluding

that

the

evolution

statistically ' i m p r o b a b l e assemblies p r o c e e d s m o r e r a p i d l y if there is a succession o f i n t e r m e d i a t e s t a b l e s u b - a s s e m b l i e s . S i n c e t h e a r g u m e n t c a n b e applied to e a c h sub-assembly, it follows that h i g h l y c o m p l e x systems w h i c h exist i n t h e w o r l d a r e l i k e l y t o h a v e a h i e r a r c h i c a l a r c h i t e c t u r e ' ( D a w k i n s 1976b).

the

present

context

the

hierarchy

consists

of genes

within

cells a n d cells w i t h i n o r g a n i s m s . M a r g u l i s ( 1 9 8 1 ) m a k e s a p e r s u a s i v e a n d f a s c i n a t i n g c a s e for a n o l d i d e a t h a t the h i e r a r c h y c o n t a i n s y e t a n o t h e r intermediate level:

eukaryotic

'cells'

are themselves,

in a sense,

multi-

cellular clusters, s y m b i o t i c unions of entities such as m i t o c h o n d r i a , plastids and cilia, w h i c h are h o m o l o g o u s to, a n d d e s c e n d e d from, p r o k a r y o t i c cells. I will not pursue the m a t t e r further here. S i m o n ' s point is a v e r y g e n e r a l one, a n d we need a m o r e specific a n s w e r to the question of w h y replicators

252

R e d i s c o v e r i n g the O r g a n i s m

chose to o r g a n i z e their p h e n o t y p e s into functional units, especially at the t w o levels of the cell a n d the m u l t i c e l l u l a r o r g a n i s m . I n o r d e r t o a s k q u e s t i o n s a b o u t w h y t h e w o r l d i s t h e w a y i t is, w e h a v e t o i m a g i n e h o w i t m i g h t h a v e b e e n . W e i n v e n t p o s s i b l e w o r l d s i n w h i c h life m i g h t h a v e b e e n o r g a n i z e d d i f f e r e n t l y , a n d ask w h a t w o u l d h a v e h a p p e n e d i f i t h a d b e e n . W h a t i n s t r u c t i v e a l t e r n a t i v e s t o t h e w a y life is, t h e n , c a n w e i m a g i n e ? F i r s t , i n o r d e r t o see w h y r e p l i c a t i n g m o l e c u l e s g a n g e d u p i n cells, w e i m a g i n e a w o r l d i n w h i c h t h e r e a r e r e p l i c a t i n g m o l e c u l e s f l o a t i n g freely in the sea. T h e r e are different varieties of replicator, and they are c o m p e t i n g w i t h e a c h o t h e r for s p a c e a n d for t h e c h e m i c a l r e s o u r c e s n e e d e d t o b u i l d copies of themselves, b u t they are not g r o u p e d together in chromosomes of nuclei. E a c h solitary replicator exerts p h e n o t y p i c p o w e r to m a k e copies of itself, a n d s e l e c t i o n f a v o u r s t h o s e w i t h t h e m o s t e f f e c t i v e p h e n o t y p i c p o w e r . I t i s e a s y t o b e l i e v e t h a t this f o r m o f life w o u l d n o t b e e v o l u t i o n a r i l y s t a b l e . I t w o u l d be i n v a d e d by m u t a n t replicators that ' g a n g up'. C e r t a i n replicators w o u l d h a v e c h e m i c a l effects t h a t c o m p l e m e n t t h o s e o f o t h e r r e p l i c a t o r s , c o m p l e m e n t t h e m i n t h e s e n s e t h a t w h e n t h e t w o c h e m i c a l effects a r e p u t together replication of b o t h is facilitated ( M o d e l 2 in the previous c h a p t e r ) . I h a v e a l r e a d y u s e d t h e e x a m p l e o f g e n e s c o d i n g for e n z y m e s t h a t c a t a l y s e successive stages of a b i o c h e m i c a l chain reaction. T h e same principle m a y be applied to larger groups of mutually complementary replicating molecules I n d e e d , e a r t h l y b i o c h e m i s t r y suggests that the m i n i m a l unit of replication, e x c e p t p o s s i b l y i n t h e f o o d - r i c h e n v i r o n m e n t o f a t o t a l p a r a s i t e , i s a b o u t fifty cistrons ( M a r g u l i s 1 9 8 1 ) . It m a k e s no difference to the a r g u m e n t w h e t h e r n e w g e n e s arise by d u p l i c a t i o n of old ones and r e m a i n close together, or w h e t h e r p r e v i o u s l y i n d e p e n d e n t g e n e s p o s i t i v e l y c o m e t o g e t h e r . W e c a n still discuss the e v o l u t i o n a r y stability of the state of b e i n g ' g a n g e d u p ' . G a n g i n g up of genes together into cells, then, is easily understood, but w h y d i d c e l l s g a n g t o g e t h e r i n t o m u l t i c e l l u l a r c l o n e s ? I n this c a s e i t m i g h t b e thought

that

not

have

invent

thought

experiments,

because

unicellular, or acellular, organisms abound on our world. These, however, a r e a l l s m a l l , a n d i t m a y b e useful t o i m a g i n e a p o s s i b l e w o r l d i n w h i c h t h e r e exist l a r g e a n d c o m p l e x u n i c e l l u l a r o r m o n o n u c l e a t e organisms. C o u l d there b e a f o r m o f life i n w h i c h o n e s i n g l e set o f g e n e s , e n t h r o n e d i n a s i n g l e c e n t r a l nucleus, directed the biochemistry of a macroscopic b o d y with c o m p l e x o r g a n s , either a single g i g a n t i c ' c e l l ' , or a m u l t i c e l l u l a r b o d y in w h i c h all but o n e of the cells l a c k e d their o w n p r i v a t e copies of the g e n o m e ? I think such a f o r m o f life c o u l d o n l y e x i s t i f its e m b r y o l o g y f o l l o w e d

principles very

different from those w i t h w h i c h we are familiar. In the e m b r y o l o g i e s that we know,

only

minority

of genes

are

'turned

on'

any

one

type

d i f f e r e n t i a t i n g tissue a t a n y o n e t i m e ( G u r d o n 1 9 7 4 ) . I t i s a d m i t t e d l y a w e a k a r g u m e n t a t this s t a g e , b u t i f t h e r e w e r e o n l y o n e set o f g e n e s i n t h e e n t i r e b o d y , i t i s n o t e a s y t o see h o w the a p p r o p r i a t e g e n e p r o d u c t s c o u l d b e

R e d i s c o v e r i n g the O r g a n i s m

conveyed

the v a r i o u s parts of the differentiating

body

the

253

appro-

priate times. B u t w h y d o e s t h e r e h a v e t o b e a complete set o f g e n e s i n e v e r y c e l l o f a d e v e l o p i n g b o d y ? I t i s s u r e l y e a s y t o i m a g i n e a f o r m o f life i n w h i c h p a r t s o f t h e g e n o m e a r e h i v e d off d u r i n g d i f f e r e n t i a t i o n , s o t h a t a g i v e n t y p e o f tissue, l i v e r tissue o r k i d n e y tissue s a y , h a s o n l y t h e g e n e s t h a t i t n e e d s . O n l y t h e germ-line cells, it w o u l d seem, really need to preserve the entire g e n o m e . It m a y be that the reason is simply that there is no easy w a y , p h y s i c a l l y , to h i v e off p a r t s o f t h e g e n o m e . I t i s n o t , after a l l , a s t h o u g h t h e g e n e s n e e d e d i n any particular differentiated region of the d e v e l o p i n g b o d y are all segregated o n o n e c h r o m o s o m e . W e c o u l d , I s u p p o s e , n o w a s k o u r s e l v e s w h y this h a d t o b e the c a s e . G i v e n t h a t i t i s t h e c a s e , full d i v i s i o n o f t h e e n t i r e g e n o m e a t e v e r y c e l l d i v i s i o n m a y s i m p l y b e t h e easiest a n d m o s t e c o n o m i c a l w a y o f doing things. H o w e v e r , in the light of my p a r a b l e ( C h a p t e r 9) of the rosys p e c t a c l e d M a r t i a n a n d t h e n e e d for c y n i c i s m , t h e r e a d e r m a y b e t e m p t e d t o s p e c u l a t e further. C o u l d i t b e t h a t t h e t o t a l , r a t h e r t h a n p a r t i a l , d u p l i c a t i o n of the g e n o m e in mitosis is an a d a p t a t i o n by s o m e genes to k e e p t h e m s e l v e s in

position

oversee

and

thwart

would-be

outlaws

among

their

c o l l e a g u e s ? P e r s o n a l l y I d o u b t it, n o t b e c a u s e t h e i d e a i s i n h e r e n t l y farf e t c h e d b u t b e c a u s e i t i s h a r d t o see h o w a g e n e i n t h e l i v e r , s a y , c o u l d s t a n d to gain from b e i n g an o u t l a w a n d m a n i p u l a t i n g the liver in a w a y that w o u l d be to the d e t r i m e n t of genes in the k i d n e y or the spleen. F o l l o w i n g the logic o f t h e c h a p t e r o n p a r a s i t e s , t h e interests o f ' l i v e r g e n e s ' a n d ' k i d n e y g e n e s ' w o u l d overlap because they share the same germ-line a n d the same g a m e t i c route out of the present b o d y . I h a v e n o t p r o v i d e d a r i g o r o u s d e f i n i t i o n o f t h e o r g a n i s m . I t is, i n d e e d , a r g u a b l e that the o r g a n i s m is a c o n c e p t of d u b i o u s utility, precisely b e c a u s e i t i s s o difficult t o d e f i n e s a t i s f a c t o r i l y . F r o m t h e i m m u n o l o g i c a l o r g e n e t i c points of v i e w , a pair of m o n o z y g o t i c twins w o u l d h a v e to c o u n t as a single organism, yet clearly they w o u l d not so qualify from the point of v i e w of the physiologist, the ethologist, or H u x l e y ' s indivisibility criterion. W h a t is 'the individual' in a colonial siphonophore or b r y o z o a n ? Botanists h a v e good r e a s o n t o b e less f o n d o f t h e p h r a s e ' i n d i v i d u a l o r g a n i s m ' t h a n z o o l o g i s t s a r e : ' T h e i n d i v i d u a l fruit f l y , f l o u r b e e t l e , r a b b i t ,

flatworm

or e l e p h a n t is a

population at the cellular but not at a n y h i g h e r level. S t a r v a t i o n does not c h a n g e the n u m b e r o f l e g s , h e a r t s o r l i v e r s o f a n a n i m a l b u t t h e effect o f stress on a plant is to alter both the rate of formation of n e w leaves a n d the rate of d e a t h o f o l d o n e s : a p l a n t m a y r e a c t t o stress b y v a r y i n g t h e n u m b e r o f its parts' (Harper 1 9 7 7 , p p . 2 0 - 2 1 ) . To H a r p e r , as a plant p o p u l a t i o n biologist, the l e a f m a y b e a m o r e s a l i e n t ' i n d i v i d u a l ' t h a n ' t h e p l a n t ' , s i n c e t h e p l a n t i s a s t r a g g l i n g , v a g u e e n t i t y for w h o m r e p r o d u c t i o n m a y b e h a r d t o d i s t i n g u i s h from w h a t a z o o l o g i s t w o u l d h a p p i l y c a l l ' g r o w t h ' . H a r p e r feels o b l i g e d t o coin

two

new

t e r m s for different

kinds of 'individual'

botany.

'The

254

R e d i s c o v e r i n g the O r g a n i s m

" r a m e t " i s t h e u n i t o f c l o n a l g r o w t h , t h e m o d u l e t h a t m a y often f o l l o w a n i n d e p e n d e n t e x i s t e n c e i f s e v e r e d f r o m the p a r e n t p l a n t . ' S o m e t i m e s , a s i n strawberries, the r a m e t is the unit that we ordinarily call a 'plant'. In other c a s e s s u c h a s w h i t e c l o v e r t h e r a m e t m a y b e t h e s i n g l e leaf. T h e ' g e n e t ' , o n t h e o t h e r h a n d , i s t h e u n i t w h i c h s p r i n g s f r o m o n e s i n g l e - c e l l e d z y g o t e , the ' i n d i v i d u a l ' in the sense of a zoologist w h o s e a n i m a l s r e p r o d u c e sexually. J a n z e n ( 1 9 7 7 ) faces up to the s a m e difficulty, suggesting that a clone of dandelions should be regarded as one 'evolutionary individual'

(Harper's

g e n e t ) , e q u i v a l e n t t o a s i n g l e tree a l t h o u g h s p r e a d o u t a l o n g t h e g r o u n d rather than raised up in the air on a trunk, and a l t h o u g h d i v i d e d up into s e p a r a t e p h y s i c a l ' p l a n t s ' ( H a r p e r ' s r a m e t s ) . A c c o r d i n g t o this v i e w , t h e r e m a y b e a s f e w a s f o u r i n d i v i d u a l d a n d e l i o n s c o m p e t i n g w i t h e a c h o t h e r for t h e t e r r i t o r y o f t h e w h o l e o f N o r t h A m e r i c a . J a n z e n sees a c l o n e o f a p h i d s i n the s a m e w a y . H i s p a p e r has no literature citations at all, but the v i e w is not a n e w o n e . I t g o e s b a c k a t least a s far a s 1 8 5 4 , w h e n T . H . H u x l e y ' t r e a t e d e a c h life c y c l e a s a n i n d i v i d u a l , w i t h a l l t h e p r o d u c t s f r o m s e x u a l e v e n t t o sexual event b e i n g a single unit. He even treated an asexual lineage of aphids a s a n i n d i v i d u a l ' ( G h i s e l i n i n p r e s s ) . T h e r e i s m e r i t i n this w a y o f t h i n k i n g , but I shall show that it leaves out something important. O n e w a y to re-express the H u x l e y / J a n z e n a r g u m e n t is as follows. T h e g e r m - l i n e of a t y p i c a l o r g a n i s m , say a h u m a n , goes t h r o u g h a sequence of perhaps a few d o z e n mitotic divisions b e t w e e n each meiosis. E m p l o y i n g C h a p t e r 5's ' b a c k w a r d s ' w a y o f l o o k i n g a t t h e ' p a s t e x p e r i e n c e o f a g e n e ' , a n y g i v e n g e n e in a living h u m a n has a history of cell divisions as follows: meiosis

mitosis

mitosis . . . mitosis

meiosis.

every

successive

body,

parallel w i t h the mitotic division of the g e r m - l i n e , other mitotic divisions h a v e furnished the g e r m - l i n e with a large clone of 'helper' cells, grouped together into a b o d y in w h i c h the germ-line is housed. In every generation the g e r m - l i n e is funnelled d o w n into a one-celled ' b o t t l e n e c k '

(a g a m e t e

f o l l o w e d b y a z y g o t e ) , t h e n i t fans o u t i n t o a m a n y - c e l l e d b o d y , t h e n i t i s funnelled d o w n into a n e w bottleneck, etc. (Bonner 1 9 7 4 ) . T h e m a n y - c e l l e d b o d y i s a m a c h i n e for t h e p r o d u c t i o n o f s i n g l e - c e l l e d p r o p a g u l e s . L a r g e b o d i e s , l i k e e l e p h a n t s , a r e best s e e n a s h e a v y p l a n t a n d m a c h i n e r y , a t e m p o r a r y resource drain, invested in so as to i m p r o v e later propagule production (Southwood

1 9 7 6 ) . I n a sense t h e g e r m - l i n e w o u l d

'like' to r e d u c e c a p i t a l i n v e s t m e n t in h e a v y m a c h i n e r y , r e d u c e the n u m b e r of cell divisions in the g r o w t h part of the c y c l e , so as to r e d u c e the interval b e t w e e n r e c u r r e n c e o f t h e r e p r o d u c t i o n p a r t o f t h e c y c l e . B u t this r e c u r r e n c e i n t e r v a l h a s a n o p t i m a l l e n g t h w h i c h i s d i f f e r e n t for d i f f e r e n t w a y s o f life. G e n e s that caused elephants to reproduce w h e n too y o u n g and small w o u l d propagate

themselves

less

efficiently than alleles

tending to produce an

o p t i m a l r e c u r r e n c e i n t e r v a l . T h e o p t i m a l r e c u r r e n c e i n t e r v a l for g e n e s t h a t h a p p e n t o f i n d t h e m s e l v e s i n e l e p h a n t g e n e - p o o l s i s m u c h l o n g e r t h a n the

R e d i s c o v e r i n g the O r g a n i s m

255

o p t i m a l r e c u r r e n c e i n t e r v a l for g e n e s i n m o u s e g e n e - p o o l s . I n t h e e l e p h a n t case, m o r e c a p i t a l i n v e s t m e n t is required to be laid d o w n before returns on investment are sought. A p r o t o z o a n largely dispenses w i t h the g r o w t h phase o f t h e c y c l e a l t o g e t h e r , a n d its c e l l d i v i s i o n s a r e a l l ' r e p r o d u c t i v e ' c e l l divisions. I t f o l l o w s f r o m this w a y o f l o o k i n g a t o r g a n i s m s t h a t t h e e n d p r o d u c t , t h e ' g o a l ' o f the g r o w t h phase o f the c y c l e , i s r e p r o d u c t i o n . T h e m i t o t i c cell divisions w h i c h p u t together an e l e p h a n t are all d i r e c t e d to the end of finally propagating viable gametes w h i c h succeed in p e r p e t u a t i n g the germ-line. N o w , h o l d i n g this i n m i n d , l o o k a t a p h i d s . D u r i n g t h e s u m m e r , a s e x u a l females g o t h r o u g h r e p e a t e d g e n e r a t i o n s o f a s e x u a l r e p r o d u c t i o n c u l m i n a t i n g i n a s i n g l e s e x u a l g e n e r a t i o n w h i c h restarts t h e c y c l e . C l e a r l y , b y a n a l o g y with the e l e p h a n t , it is easy to follow J a n z e n in seeing the s u m m e r a s e x u a l g e n e r a t i o n s a s a l l d i r e c t e d t o w a r d s t h e final e n d o f s e x u a l r e p r o d u c t i o n i n a u t u m n . A s e x u a l r e p r o d u c t i o n , a c c o r d i n g t o this v i e w , i s n o t r e a l l y r e p r o duction at all. It is g r o w t h , just like the g r o w t h of a single e l e p h a n t ' s b o d y . For J a n z e n the w h o l e clone of female a p h i d s is a single e v o l u t i o n a r y indiv i d u a l because it is the p r o d u c t of a single sexual fusion. It is an u n u s u a l individual in that it h a p p e n s to be split up into a n u m b e r of p h y s i c a l l y s e p a r a t e u n i t s , b u t s o w h a t ? E a c h o f t h o s e p h y s i c a l u n i t s c o n t a i n s its o w n f r a g m e n t o f g e r m - l i n e , b u t t h e n s o d o e s t h e left o v a r y a n d t h e r i g h t o v a r y o f a female elephant. T h e fragments of g e r m - l i n e in the a p h i d case are s e p a r a t e d b y thin air, w h i l e t h e t w o o v a r i e s o f a n e l e p h a n t a r e s e p a r a t e d b y g u t s b u t , again, so w h a t ? P e r s u a s i v e a s this l i n e o f a r g u m e n t is, I h a v e a l r e a d y m e n t i o n e d t h a t I t h i n k i t misses a n i m p o r t a n t p o i n t . I t i s r i g h t t o r e g a r d m o s t m i t o t i c c e l l divisions as ' g r o w t h ' , ' a i m e d ' at the final g o a l of r e p r o d u c t i o n , a n d it is right t o r e g a r d the i n d i v i d u a l o r g a n i s m a s t h e p r o d u c t o f o n e r e p r o d u c t i v e e v e n t , but J a n z e n is w r o n g to e q u a t e the r e p r o d u c t i o n / g r o w t h distinction w i t h the s e x u a l / a s e x u a l d i s t i n c t i o n . T h e r e is, t o b e s u r e , a n i m p o r t a n t d i s t i n c t i o n lurking here, but it is not the distinction b e t w e e n sex a n d non-sex, nor is it the distinction b e t w e e n meiosis a n d mitosis. T h e distinction that I wish to emphasize is that b e t w e e n germ-line cell division (reproduction), and somatic or ' d e a d - e n d ' cell division ( g r o w t h ) . A germ-line cell division is one w h e r e the genes b e i n g d u p l i c a t e d h a v e a c h a n c e o f b e i n g the a n c e s t o r s o f a n i n d e f i n i t e l y l o n g l i n e o f d e s c e n d a n t s , w h e r e t h e genes are, in fact, true g e r m - l i n e replicators in the sense of C h a p t e r 5. A germ-line cell division m a y be a mitosis or a meiosis. If we s i m p l y look at a cell division u n d e r a m i c r o s c o p e , there m a y be no w a y of telling w h e t h e r it is a germ-line division or not. Both germ-line and somatic cell divisions m a y be mitoses o f i d e n t i c a l a p p e a r a n c e . I f w e l o o k a t a g e n e i n a n y c e l l i n a l i v i n g o r g a n i s m a n d t r a c e its h i s t o r y b a c k w a r d s i n e v o l u t i o n a r y t i m e , t h e m o s t r e c e n t f e w c e l l d i v i s i o n s o f its

256

R e d i s c o v e r i n g the O r g a n i s m

' e x p e r i e n c e ' m a y be somatic, but once we reach a g e r m - l i n e cell division in o u r b a c k w a r d s m a r c h , a l l p r e v i o u s o n e s i n the g e n e ' s h i s t o r y m u s t b e g e r m line divisions. G e r m - l i n e cell divisions m a y be thought of as proceeding forwards in evolutionary time, while somatic cell divisions are proceeding s i d e w a y s . S o m a t i c c e l l d i v i s i o n s a r e u s e d t o m a k e m o r t a l tissues, o r g a n s a n d instruments w h o s e ' p u r p o s e ' is the p r o m o t i n g of g e r m - l i n e cell divisions. T h e world

populated

genes

which

have survived

germ-lines

c o n s e q u e n c e of aid that they r e c e i v e d from their e x a c t d u p l i c a t e s in somatic cells. G r o w t h c o m e s a b o u t t h r o u g h the p r o p a g a t i o n o f d e a d - e n d somatic cells, w h i l e r e p r o d u c t i o n is the m e a n s of the p r o p a g a t i o n of g e r m - l i n e cells. H a r p e r (1977) makes a distinction between reproduction and growth in plants, w h i c h w i l l n o r m a l l y a m o u n t to the s a m e as my distinction b e t w e e n germ-line and somatic cell division:

' T h e distinction m a d e here between

" r e p r o d u c t i o n " a n d " g r o w t h " is that r e p r o d u c t i o n involves the formation of a n e w i n d i v i d u a l f r o m a s i n g l e c e l l : this i s u s u a l l y ( t h o u g h n o t a l w a y s e . g . a p o m i c t s ) a z y g o t e . I n this p r o c e s s a n e w i n d i v i d u a l i s " r e p r o d u c e d " b y the i n f o r m a t i o n t h a t i s c o d e d i n t h e c e l l . G r o w t h , i n c o n t r a s t , results from the development

of organized

meristems'

(Harper

1977,

fn.).

What

matters here is w h e t h e r there really is an important biological distinction b e t w e e n g r o w t h a n d r e p r o d u c t i o n w h i c h is not the same as the distinction between

mitosis

and

meiosis + sex.

there

really

crucial

difference

b e t w e e n ' r e p r o d u c i n g ' t o m a k e t w o aphids o n the o n e h a n d , and ' g r o w i n g ' t o m a k e o n e a p h i d t w i c e a s l a r g e o n t h e o t h e r ? J a n z e n w o u l d p r e s u m a b l y say no. H a r p e r w o u l d p r e s u m a b l y say yes. I a g r e e w i t h H a r p e r , but I w o u l d not h a v e b e e n a b l e to justify my position until I had read J. T. Bonner's (1974) i n s p i r i n g b o o k O n Development. T h e j u s t i f i c a t i o n i s best m a d e w i t h t h e aid o f thought experiments. I m a g i n e a p r i m i t i v e p l a n t c o n s i s t i n g o f a flat, p a d - l i k e t h a l l u s , f l o a t i n g o n t h e s u r f a c e o f t h e s e a , a b s o r b i n g n u t r i e n t s t h r o u g h its l o w e r s u r f a c e a n d s u n l i g h t t h r o u g h its u p p e r s u r f a c e . I n s t e a d o f ' r e p r o d u c i n g ' (i.e. s e n d i n g off s i n g l e - c e l l e d p r o p a g u l e s t o g r o w e l s e w h e r e ) , i t s i m p l y g r o w s a t its m a r g i n s , s p r e a d i n g i n t o a n e v e r l a r g e r c i r c u l a r g r e e n c a r p e t , l i k e a m o n s t r o u s lily p a d s e v e r a l m i l e s a c r o s s a n d still g r o w i n g .

M a y b e older parts of the thallus

e v e n t u a l l y die, so that it consists of an e x p a n d i n g r i n g rather than a filled c i r c l e l i k e a t r u e l i l y p a d . P e r h a p s a l s o , f r o m t i m e t o t i m e , c h u n k s o f the t h a l l u s s p l i t off, l i k e i c e f l o e s s h e a r i n g a w a y f r o m t h e p a c k i c e , a n d s e p a r a t e c h u n k s drift t o d i f f e r e n t p a r t s o f t h e o c e a n . E v e n i f w e a s s u m e this k i n d o f fission, I s h a l l s h o w t h a t it is n o t r e p r o d u c t i o n in an i n t e r e s t i n g sense. N o w c o n s i d e r a s i m i l a r k i n d o f p l a n t w h i c h differs i n o n e c r u c i a l r e s p e c t . I t s t o p s g r o w i n g w h e n i t a t t a i n s a d i a m e t e r o f 1 foot, a n d r e p r o d u c e s i n s t e a d . It manufactures single-celled propagules, either sexually or asexually, and sheds t h e m into the air w h e r e they m a y be carried a l o n g w a y on the w i n d . W h e n o n e o f t h e s e p r o p a g u l e s l a n d s o n the w a t e r s u r f a c e i t b e c o m e s a n e w

R e d i s c o v e r i n g the O r g a n i s m

257

t h a l l u s , w h i c h g r o w s u n t i l i t i s 1 foot w i d e , t h e n r e p r o d u c e s a g a i n . I s h a l l c a l l the t w o s p e c i e s G (for g r o w t h ) a n d R (for r e p r o d u c t i o n ) r e s p e c t i v e l y . F o l l o w i n g t h e l o g i c o f J a n z e n ' s p a p e r , w e s h o u l d see a c r u c i a l d i f f e r e n c e b e t w e e n the t w o s p e c i e s o n l y i f t h e ' r e p r o d u c t i o n ' o f t h e s e c o n d s p e c i e s , R , i s sexual.

If it is asexual,

the propagules shed into the air b e i n g mitotic

p r o d u c t s g e n e t i c a l l y i d e n t i c a l t o t h e c e l l s o f t h e p a r e n t t h a l l u s , t h e r e is, for Janzen,

no i m p o r t a n t difference

between

the

two

species.

The

separate

'individuals' in R are no m o r e g e n e t i c a l l y distinct than different regions of the t h a l l u s i n G m i g h t b e . I n e i t h e r s p e c i e s , m u t a t i o n c a n i n i t i a t e n e w c l o n e s of cells. T h e r e is no p a r t i c u l a r reason w h y , in R, m u t a t i o n s s h o u l d o c c u r during propagule formation any more than during thallus g r o w t h .

R is

simply a m o r e fragmented version of G, just as a c l o n e of d a n d e l i o n s is like a fragmented tree. M y purpose i n m a k i n g the t h o u g h t e x p e r i m e n t , h o w e v e r , was to disclose an i m p o r t a n t difference b e t w e e n the t w o h y p o t h e t i c a l species, representing the difference b e t w e e n g r o w t h a n d r e p r o d u c t i o n , e v e n w h e n r e p r o d u c t i o n is a s e x u a l . G just grows, while R g r o w s and reproduces in alternation. W h y is the distinction i m p o r t a n t ? T h e answer cannot be a genetic one in a n y simple sense b e c a u s e , a s w e h a v e s e e n , m u t a t i o n s a r e j u s t a s l i k e l y t o i n i t i a t e g e n e t i c change during growth-mitosis as d u r i n g reproduction-mitosis. I suggest that the i m p o r t a n t d i s t i n c t i o n b e t w e e n t h e t w o s p e c i e s i s t h a t a l i n e a g e o f R i s capable of evolving c o m p l e x adaptations in a w a y

that G is not. T h e

reasoning goes as follows. C o n s i d e r a g a i n t h e p a s t h i s t o r y of a g e n e , in this c a s e a g e n e s i t t i n g in a cell o f R . I t h a s h a d a h i s t o r y o f p a s s i n g r e p e a t e d l y f r o m o n e ' v e h i c l e ' t o a n o t h e r s i m i l a r v e h i c l e . E a c h o f its s u c c e s s i v e b o d i e s b e g a n a s a s i n g l e - c e l l e d propagule, then g r e w through a fixed c y c l e , then passed the g e n e on into a n e w s i n g l e - c e l l e d p r o p a g u l e a n d h e n c e a n e w m u l t i c e l l u l a r b o d y . Its h i s t o r y h a s b e e n a c y c l i c a l o n e , a n d n o w h e r e i s t h e p o i n t . S i n c e e a c h o f this l o n g series o f s u c c e s s i v e b o d i e s d e v e l o p e d a n e w f r o m s i n g l e - c e l l e d b e g i n n i n g s , i t i s possible

for

predecessors.

successive Evolution

bodies

develop

of complex

body

slightly structure

differently with

from

organs,

their say

c o m p l e x a p p a r a t u s for c a t c h i n g i n s e c t s like a V e n u s fly t r a p , i s o n l y p o s s i b l e if t h e r e is a c y c l i c a l l y r e p e a t i n g d e v e l o p m e n t a l p r o c e s s to e v o l v e . I s h a l l r e t u r n to this p o i n t in a m o m e n t . M e a n w h i l e , c o m p a r e G. A g e n e sitting in a y o u n g cell at the g r o w i n g m a r g i n of the h u g e thallus has a history w h i c h is not c y c l i c a l , or is c y c l i c a l only at the cellular level. T h e ancestor of the present cell w a s a n o t h e r cell, a n d the c a r e e r o f t h e t w o c e l l s w a s v e r y s i m i l a r . E a c h c e l l o f a n R p l a n t , b y contrast, has a definite place in the g r o w t h sequence. It is either n e a r the c e n t r e o f t h e 1-foot t h a l l u s , o r n e a r t h e r i m , o r a t s o m e p a r t i c u l a r p l a c e i n b e t w e e n . I t c a n t h e r e f o r e d i f f e r e n t i a t e t o f i l l its s p e c i a l r o l e i n its a p p o i n t e d p l a c e i n a n o r g a n o f the p l a n t . A c e l l o f G h a s n o s u c h s p e c i f i c d e v e l o p m e n t a l

258

R e d i s c o v e r i n g the O r g a n i s m

identity.

All

cells

first

appear

the

growing

margin,

and

later find

t h e m s e l v e s e n c l o s e d b y o t h e r , y o u n g e r c e l l s . T h e r e i s c y c l i c i t y o n l y a t the cellular level, w h i c h m e a n s that in G evolutionary c h a n g e can take place o n l y a t t h e c e l l u l a r l e v e l . C e l l s m i g h t i m p r o v e o n t h e i r p r e d e c e s s o r s i n the cell lineage, d e v e l o p i n g more c o m p l e x internal organelle structure, say. But t h e e v o l u t i o n o f o r g a n s a n d a d a p t a t i o n s a t t h e m u l t i c e l l u l a r l e v e l c o u l d not t a k e p l a c e , b e c a u s e r e c u r r e n t , c y c l i c a l d e v e l o p m e n t o f w h o l e g r o u p s o f cells d o e s n o t o c c u r . I t is, o f c o u r s e , t r u e t h a t i n G t h e c e l l s a n d t h e i r a n c e s t o r s a r e i n p h y s i c a l c o n t a c t w i t h o t h e r c e l l s , a n d i n this sense f o r m a m u l t i c e l l u l a r ' s t r u c t u r e ' . B u t a s far a s p u t t i n g t o g e t h e r c o m p l e x m u l t i c e l l u l a r o r g a n s i s concerned, they might just as well have been free-swimming protozoa. In order

put

together

complex

multicellular organ

you

need

c o m p l e x d e v e l o p m e n t a l s e q u e n c e . A c o m p l e x d e v e l o p m e n t a l s e q u e n c e has t o h a v e e v o l v e d f r o m a n e a r l i e r d e v e l o p m e n t a l s e q u e n c e w h i c h w a s s l i g h t l y less c o m p l e x . T h e r e has to be an evolutionary progression of developmental sequences,

each

one

the

series

being

slight

improvement

its

predecessor. G does not h a v e a recurring d e v e l o p m e n t a l sequence other than t h e h i g h - f r e q u e n c y c y c l e o f d e v e l o p m e n t a t the s i n g l e - c e l l l e v e l . T h e r e f o r e i t c a n n o t e v o l v e multicellular differentiation and organ-level complexity. T o t h e e x t e n t t h a t i t c a n b e s a i d t o h a v e a m u l t i c e l l u l a r d e v e l o p m e n t a l process at all, that d e v e l o p m e n t continues non-cyclically through geological time: the species m a k e s no s e p a r a t i o n b e t w e e n would-be cycle

evolution

available

time-scale. it

the

The

cell

only

cycle.

the g r o w t h

time-scale and

high-frequency R,

the

developmental

other

hand,

has

m u l t i c e l l u l a r d e v e l o p m e n t a l c y c l e w h i c h i s fast c o m p a r e d w i t h e v o l u t i o n a r y time. T h e r e f o r e , as the ages succeed, later d e v e l o p m e n t a l cycles can be different from earlier d e v e l o p m e n t a l cycles, a n d m u l t i c e l l u l a r c o m p l e x i t y c a n e v o l v e . W e a r e m o v i n g t o w a r d s a d e f i n i t i o n o f t h e o r g a n i s m a s the u n i t which

initiated

developmental

new

act

reproduction

via

single-celled

'bottleneck'.

T h e i m p o r t a n c e of the difference b e t w e e n g r o w t h and reproduction is that each act of reproduction involves a new developmental cycle. G r o w t h simply i n v o l v e s s w e l l i n g o f t h e e x i s t i n g b o d y . W h e n a n a p h i d g i v e s rise t o a n e w aphid by parthenogenetic reproduction the n e w aphid, if it is a mutant, m a y b e r a d i c a l l y d i f f e r e n t f r o m its p r e d e c e s s o r . W h e n a n a p h i d g r o w s t o t w i c e its o r i g i n a l s i z e , o n t h e o t h e r h a n d , a l l its o r g a n s a n d c o m p l e x s t r u c t u r e s s i m p l y swell.

It might

be said

that somatic mutations could

o c c u r within cell

lineages of the g r o w i n g giant aphid. T r u e , but a mutation within a somatic c e l l l i n e i n a h e a r t , s a y , c a n n o t r a d i c a l l y r e - o r g a n i z e t h e s t r u c t u r e o f the h e a r t . T o s w i t c h t h e e x a m p l e t o v e r t e b r a t e s , i f the p r e s e n t h e a r t i s t w o c h a m b e r e d , w i t h o n e a u r i c l e f e e d i n g o n e v e n t r i c l e , n e w m u t a t i o n s i n the m i t o t i c cells at the g r o w i n g m a r g i n of the heart are v e r y unlikely to a c h i e v e r a d i c a l r e s t r u c t u r i n g o f t h e h e a r t s o t h a t i t c o m e s t o h a v e four c h a m b e r s w i t h

R e d i s c o v e r i n g the O r g a n i s m

259

a p u l m o n a r y c i r c u l a t i o n k e p t s e p a r a t e f r o m t h e rest. I n o r d e r t o p u t t o g e t h e r new complexity, n e w d e v e l o p m e n t a l beginnings are required. A n e w e m b r y o m u s t start f r o m s c r a t c h , w i t h o u t a n y h e a r t a t a l l . T h e n a m u t a t i o n c a n a c t o n sensitive key points in e a r l y d e v e l o p m e n t to b r i n g a b o u t a n e w f u n d a m e n t a l architecture of the heart. D e v e l o p m e n t a l r e c y c l i n g a l l o w s a return ' b a c k to t h e d r a w i n g b o a r d ' (see b e l o w ) i n e v e r y g e n e r a t i o n . W e b e g a n this c h a p t e r b y w o n d e r i n g w h y r e p l i c a t o r s h a v e g a n g e d u p i n t o large, multicellular clones called organisms, and we initially g a v e a rather unsatisfactory answer. A m o r e satisfying a n s w e r is n o w starting to e m e r g e . A n o r g a n i s m i s t h e p h y s i c a l u n i t a s s o c i a t e d w i t h o n e s i n g l e life c y c l e . Replicators that g a n g up in multicellular organisms a c h i e v e a regularly r e c y c l i n g life h i s t o r y , a n d c o m p l e x a d a p t a t i o n s t o a i d t h e i r p r e s e r v a t i o n , a s they progress through e v o l u t i o n a r y time. S o m e a n i m a l s h a v e a life c y c l e i n v o l v i n g m o r e t h a n o n e d i s t i n c t b o d y . A b u t t e r f l y i s u t t e r l y d i f f e r e n t f r o m t h e c a t e r p i l l a r w h i c h p r e c e d e d it. I t i s h a r d to i m a g i n e a butterfly g r o w i n g from a caterpillar by slow, w i t h i n - o r g a n change:

caterpillar

organ

growing

into

corresponding

butterfly

organ.

Instead, w h a t h a p p e n s is that the c o m p l e x o r g a n structure of the c a t e r p i l l a r i s l a r g e l y b r o k e n d o w n a n d t h e tissues o f t h e c a t e r p i l l a r a r e u s e d a s fuel for the d e v e l o p m e n t o f a w h o l e n e w b o d y . T h e n e w b u t t e r f l y b o d y d o e s n o t q u i t e restart f r o m a s i n g l e c e l l , b u t t h e p r i n c i p l e i s t h e s a m e . I t d e v e l o p s a radically

new

bodily

structure

from

simple,

relatively

undifferentiated

i m a g i n a l discs. T h e r e is a partial return to the d r a w i n g b o a r d . R e t u r n i n g t o t h e g r o w t h / r e p r o d u c t i o n d i s t i n c t i o n itself, J a n z e n w a s n o t a c t u a l l y w r o n g . D i s t i n c t i o n s c a n b e u n i m p o r t a n t for s o m e p u r p o s e s , w h i l e t h e y r e m a i n i m p o r t a n t for o t h e r p u r p o s e s . F o r d i s c u s s i n g c e r t a i n k i n d s o f ecological or economic questions, there m a y be no i m p o r t a n t distinction between

growth

and

asexual

reproduction.

sisterhood

of aphids

may

i n d e e d b e a n a l o g o u s t o a s i n g l e b e a r . B u t for o t h e r p u r p o s e s , for d i s c u s s i n g the e v o l u t i o n a r y p u t t i n g t o g e t h e r o f c o m p l e x o r g a n i z a t i o n , t h e d i s t i n c t i o n i s crucial. A certain type of ecologist m a y gain illumination from c o m p a r i n g a field full o f d a n d e l i o n s w i t h a s i n g l e t r e e . important to u n d e r s t a n d the differences,

B u t for o t h e r p u r p o s e s i t i s

a n d t o see t h e s i n g l e d a n d e l i o n

r a m e t as a n a l o g o u s to the tree. B u t J a n z e n ' s p o s i t i o n is, i n a n y c a s e , a m i n o r i t y o n e . A m o r e t y p i c a l biologist m i g h t think it perverse of J a n z e n to r e g a r d a s e x u a l r e p r o d u c t i o n in aphids

vegetative

growth,

and

propagation

equally by

perverse

multicellular

of Harper runners,

and as

growth

regard

and

not

reproduction. O u r decision is based on the assumption that the r u n n e r is a multicellular meristem rather than a single-celled propagule, but w h y should w e r e g a r d this a s a n i m p o r t a n t p o i n t ? A g a i n , t h e a n s w e r m a y b e s e e n i n a t h o u g h t e x p e r i m e n t i n v o l v i n g t w o h y p o t h e t i c a l s p e c i e s o f p l a n t s , i n this c a s e s t r a w b e r r y - l i k e p l a n t s c a l l e d M a n d S ( D a w k i n s in p r e s s ) .

260

R e d i s c o v e r i n g the O r g a n i s m

B o t h the h y p o t h e t i c a l s t r a w b e r r y - l i k e species p r o p a g a t e v e g e t a t i v e l y , by runner.

In both

there is a p o p u l a t i o n of w h a t a p p e a r to be distinct and

r e c o g n i z a b l e ' p l a n t s ' c o n n e c t e d by a n e t w o r k of runners. In both species, e a c h ' p l a n t ' ( i . e . r a m e t ) c a n g i v e rise t o m o r e t h a n o n e d a u g h t e r p l a n t , s o that w e h a v e the possibility o f e x p o n e n t i a l g r o w t h o f the ' p o p u l a t i o n '

(or

g r o w t h o f the ' b o d y ' d e p e n d i n g o n y o u r point o f v i e w ) . E v e n t h o u g h there i s n o s e x , t h e r e c a n b e e v o l u t i o n s i n c e m u t a t i o n s w i l l s o m e t i m e s o c c u r i n the m i t o t i c c e l l d i v i s i o n s ( W h i t h a m & S l o b o d c h i k o f f i n p r e s s ) . N o w c o m e s the crucial difference b e t w e e n the t w o species. multicellular,

meristem),

the

runner

In species M a

(for m a n y , o r

broad-fronted

multicellular

m e r i s t e m . T h i s m e a n s t h a t t w o c e l l s i n a n y o n e ' p l a n t ' m a y b e the m i t o t i c descendants of t w o different cells in the p a r e n t plant.

In terms of mitotic

descent, a cell m a y therefore be a closer cousin of a cell in a n o t h e r 'plant' t h a n i t i s o f a n o t h e r c e l l i n its o w n p l a n t . I f m u t a t i o n h a s i n t r o d u c e d g e n e t i c h e t e r o g e n e i t y i n t o t h e c e l l p o p u l a t i o n , this m e a n s t h a t i n d i v i d u a l p l a n t s m a y be g e n e t i c m o s a i c s , w i t h s o m e cells h a v i n g closer genetic relatives in other p l a n t s t h a n i n t h e i r o w n . W e w i l l see t h e c o n s e q u e n c e s o f this for e v o l u t i o n i n a m o m e n t . M e a n w h i l e we turn to the other h y p o t h e t i c a l species. S p e c i e s S (for s i n g l e ) i s e x a c t l y l i k e M , e x c e p t t h a t e a c h r u n n e r c u l m i n a t e s i n a s i n g l e a p i c a l c e l l . T h i s c e l l a c t s a s t h e b a s a l m i t o t i c a n c e s t o r o f a l l the c e l l s o f t h e n e w d a u g h t e r p l a n t . T h i s m e a n s t h a t a l l cells i n a g i v e n p l a n t a r e closer cousins to e a c h other t h a n t h e y are to a n y cells in other plants. If m u t a t i o n i n t r o d u c e s g e n e t i c h e t e r o g e n e i t y into the p o p u l a t i o n of cells, there will be relatively few mosaic plants. R a t h e r , each plant will tend to be a g e n e t i c a l l y u n i f o r m c l o n e , b u t i t m a y differ g e n e t i c a l l y f r o m s o m e o t h e r plants, w h i l e b e i n g genetically identical to yet other plants. T h e r e will be a t r u e p o p u l a t i o n o f plants, e a c h o n e o f w h i c h has a g e n o t y p e c h a r a c t e r i s t i c o f a l l its c e l l s . I t i s t h e r e f o r e p o s s i b l e t o c o n c e i v e o f s e l e c t i o n , i n t h e sense w h i c h I h a v e c a l l e d ' v e h i c l e selection', a c t i n g at the level of the w h o l e plant. S o m e w h o l e plants m a y be better than others, because of their superior genotypes. In species M, especially if the runners are very broad-fronted meristems, a geneticist will not discern a p o p u l a t i o n of plants at all.

H e w i l l see a

p o p u l a t i o n o f c e l l s , e a c h w i t h its o w n g e n o t y p e . S o m e c e l l s w i l l b e g e n e t i c a l l y i d e n t i c a l , o t h e r s w i l l h a v e different g e n o t y p e s . A f o r m o f n a t u r a l s e l e c t i o n m i g h t go on a m o n g cells, but it is hard to i m a g i n e selection a m o n g 'plants', b e c a u s e ' t h e p l a n t ' i s n o t a u n i t t h a t c a n b e i d e n t i f i e d a s h a v i n g its o w n characteristic g e n o t y p e . R a t h e r , the w h o l e mass o f s t r a g g l i n g v e g e t a t i o n will h a v e to be r e g a r d e d as a p o p u l a t i o n of cells, w i t h cells of a n y one g e n o t y p e b e i n g u n t i d i l y p e p p e r e d a c r o s s t h e different ' p l a n t s ' . T h e u n i t w h i c h I h a v e called the ' g e n e v e h i c l e ' , a n d w h i c h J a n z e n has called the ' e v o l u t i o n a r y i n d i v i d u a l ' , w i l l , i n s u c h a c a s e , b e n o l a r g e r t h a n t h e c e l l . I t i s cells t h a t w i l l be the g e n e t i c c o m p e t i t o r s . E v o l u t i o n m a y take the form of i m p r o v e m e n t s in c e l l s t r u c t u r e a n d p h y s i o l o g y , b u t i t i s h a r d t o see h o w i t c o u l d t a k e t h e form of i m p r o v e m e n t s in i n d i v i d u a l plants or their organs.

R e d i s c o v e r i n g the O r g a n i s m

261

It might be thought that i m p r o v e m e n t s in o r g a n structure c o u l d e v o l v e , if it regularly happened

that particular subpopulations of cells,

in discrete

a r e a s o f the p l a n t , w e r e a c l o n e , d e s c e n d e d f r o m a s i n g l e m i t o t i c a n c e s t o r . F o r i n s t a n c e , t h e r u n n e r g i v i n g rise t o a n e w ' p l a n t ' m i g h t b e a b r o a d - f r o n t e d m e r i s t e m , b u t i t m i g h t still b e t h e c a s e t h a t e a c h l e a f s p r a n g f r o m a s i n g l e c e l l a t its o w n b a s e . A l e a f c o u l d t h e r e f o r e b e a c l o n e o f c e l l s m o r e c l o s e l y r e l a t e d t o e a c h o t h e r t h a n t o c e l l s a n y w h e r e else i n t h e p l a n t . G i v e n t h e c o m m o n n e s s of somatic mutation in plants ( W h i t h a m & S l o b o d c h i k o f f in press), m i g h t one not therefore i m a g i n e the e v o l u t i o n of i m p r o v e d c o m p l e x a d a p t a t i o n at the l e v e l o f t h e leaf, i f n o t a t t h e l e v e l o f t h e w h o l e p l a n t ? A g e n e t i c i s t c o u l d now discern a genetically heterogeneous p o p u l a t i o n of leaves, e a c h one m a d e up of genetically h o m o g e n o u s cells, so m i g h t not natural selection go on b e t w e e n successful l e a v e s a n d u n s u c c e s s f u l l e a v e s ? I t w o u l d b e t i d y i f t h e a n s w e r t o this q u e s t i o n c o u l d b e y e s ; t h a t is, i f w e c o u l d assert t h a t v e h i c l e selection will go on at a n y level in the h i e r a r c h y of m u l t i c e l l u l a r units, provided

that

compared

the

with

cells

within

other

unit

units

tend

the

same

genetically level.

uniform

Unfortunately,

h o w e v e r , s o m e t h i n g h a s b e e n left o u t o f t h e r e a s o n i n g . It

will

replicators

remembered

and

dead-end

that

classified

replicators.

Natural

replicators

into

selection

results

germ-line in

some

replicators b e c o m i n g m o r e n u m e r o u s at the e x p e n s e of rival replicators, b u t this l e a d s t o e v o l u t i o n a r y c h a n g e o n l y i f t h e r e p l i c a t o r s a r e i n g e r m - l i n e s . A m u l t i c e l l u l a r u n i t q u a l i f i e s a s a v e h i c l e , i n a n e v o l u t i o n a r i l y i n t e r e s t i n g sense, only

if at

normally

least do

replicators.

some

o f its

qualify,

not

L e a f cells

cells for

synthesize

contain their

germ-line nuclei

chemical

replicators.

contain

substances

only

which

Leaves

dead-end ultimately

benefit o t h e r c e l l s t h a t d o c o n t a i n g e r m - l i n e c o p i e s o f t h e l e a f g e n e s , t h e genes w h i c h g a v e the leaves their characteristically leafy p h e n o t y p e s . B u t we cannot

the

conclusion of the

paragraph,

that

inter-leaf

vehicle selection, a n d inter-organ selection g e n e r a l l y , c o u l d go on if o n l y the cells w i t h i n a n o r g a n w e r e c l o s e r m i t o t i c c o u s i n s t h a n c e l l s i n d i f f e r e n t organs.

Inter-leaf selection could h a v e evolutionary consequences only if

leaves directly s p a w n e d d a u g h t e r leaves. L e a v e s are organs, not organisms. For inter-organ selection to occur, it is necessary that the organs c o n c e r n e d s h o u l d h a v e t h e i r o w n g e r m l i n e s a n d d o t h e i r o w n r e p r o d u c i n g , a n d this they normally do not. O r g a n s are parts of organisms, and r e p r o d u c t i o n is the prerogative of organisms. For clarity

have

been

a bit

extreme.

There

could

a r a n g e of

intermediates between my two strawberry-like plants. Species M ' s runner w a s said to be a broad-fronted m e r i s t e m , w h i l e species S's r u n n e r n a r r o w e d d o w n to a one-celled bottleneck at the base of e a c h n e w plant. B u t w h a t if there w a s an i n t e r m e d i a t e species w i t h a t w o - c e l l e d b o t t l e n e c k at the base of e a c h n e w p l a n t ? T h e r e are t w o m a i n possibilities here.

If the pattern of

d e v e l o p m e n t is such that it is u n p r e d i c t a b l e w h i c h cells in the d a u g h t e r p l a n t

262

R e d i s c o v e r i n g the O r g a n i s m

will be d e s c e n d e d from w h i c h of the t w o stem cells, the point I h a v e m a d e about developmental bottlenecks will simply be weakened quantitatively: g e n e t i c m o s a i c s m a y o c c u r i n t h e p o p u l a t i o n o f p l a n t s , b u t t h e r e w i l l still b e a s t a t i s t i c a l t e n d e n c y for c e l l s t o b e g e n e t i c a l l y c l o s e r t o f e l l o w m e m b e r s o f t h e s a m e p l a n t t h a n t o c e l l s i n o t h e r p l a n t s . T h e r e f o r e w e m a y still t a l k meaningfully plants,

but

about vehicle selection the

inter-plant selection

between

plants in

pressure m a y

have

a population of to

be strong

o u t w e i g h s e l e c t i o n a m o n g c e l l s w i t h i n p l a n t s . T h i s is, i n c i d e n t a l l y , a n a l o g o u s t o o n e o f t h e c o n d i t i o n s for ' k i n - g r o u p s e l e c t i o n ' ( H a m i l t o n 1 9 7 5 a ) t o w o r k . T o m a k e t h e a n a l o g y , w e h a v e o n l y t o see t h e p l a n t a s a ' g r o u p ' o f c e l l s . The

second

possibility arising out

of the

assumption

of a

two-celled

b o t t l e n e c k a t t h e b a s e o f e a c h p l a n t i s t h a t t h e p a t t e r n o f d e v e l o p m e n t o f the species m i g h t be such that certain organs of the plant are a l w a y s the mitotic d e s c e n d a n t s o f a d e s i g n a t e d o n e o f t h e t w o c e l l s . F o r i n s t a n c e , c e l l s o f the root system m i g h t d e v e l o p from a cell in the l o w e r part of the runner, w h i l e t h e rest o f t h e p l a n t d e v e l o p e d f r o m t h e o t h e r c e l l , i n t h e u p p e r p a r t o f the r u n n e r . If, f u r t h e r , t h e l o w e r c e l l i s a l w a y s d e s c e n d e d f r o m a r o o t c e l l i n the p a r e n t plant, w h i l e the u p p e r cell is recruited from an a b o v e - g r o u n d cell in the p a r e n t p l a n t , w e w o u l d h a v e a n interesting situation. R o o t cells w o u l d b e closer cousins of o t h e r root cells in the p o p u l a t i o n at large than they w o u l d b e o f s t a l k a n d l e a f c e l l s i n t h e i r ' o w n ' p l a n t . M u t a t i o n w o u l d o p e n u p the possibility of e v o l u t i o n a r y c h a n g e , but it w o u l d be split-level evolution. G e n o t y p e s b e l o w g r o u n d c o u l d e v o l v e a w a y from g e n o t y p e s a b o v e g r o u n d , irrespective of a p p a r e n t joint m e m b e r s h i p in discrete 'plants'. Theoretically we could even have a kind of within-organism 'speciation'. To recapitulate, reproduction

the significance o f the difference b e t w e e n g r o w t h and that

reproduction

permits

new

beginning,

new

developmental cycle and a new organism which m a y be an improvement, in terms

of the

fundamental

organization

of complex

structure,

over

its

p r e d e c e s s o r . O f c o u r s e i t m a y not b e a n i m p r o v e m e n t , i n w h i c h c a s e its g e n e t i c basis w i l l b e e l i m i n a t e d b y n a t u r a l selection. B u t g r o w t h w i t h o u t r e p r o d u c t i o n d o e s n o t e v e n a l l o w the possibility o f r a d i c a l c h a n g e a t t h e o r g a n level, either in the direction of i m p r o v e m e n t or the reverse. It allows only s u p e r f i c i a l t i n k e r i n g . Y o u m a y d i v e r t a d e v e l o p i n g B e n t l e y i n t o a fully g r o w n R o l l s R o y c e , s i m p l y b y t i n k e r i n g w i t h t h e a s s e m b l y p r o c e s s a t the l a t e p o i n t w h e r e the r a d i a t o r is a d d e d . B u t if y o u w a n t to c h a n g e a F o r d into a R o l l s R o y c e y o u m u s t s t a r t a t t h e d r a w i n g b o a r d , b e f o r e t h e c a r starts ' g r o w i n g ' o n t h e a s s e m b l y l i n e a t a l l . T h e p o i n t a b o u t r e c u r r e n t r e p r o d u c t i o n life c y c l e s , a n d h e n c e , by i m p l i c a t i o n , the point a b o u t organisms, is that they a l l o w repeated returns to the d r a w i n g board during evolutionary time. W e must b e w a r e here o f the heresy o f 'biotic' a d a p t a t i o n i s m

(Williams

1 9 6 6 ) . W e h a v e s e e n t h a t r e c u r r e n t r e p r o d u c t i o n life c y c l e s , i.e. ' o r g a n i s m s ' , m a k e t h e e v o l u t i o n o f c o m p l e x o r g a n s p o s s i b l e . I t i s a l l t o o e a s y t o t r e a t this

R e d i s c o v e r i n g the O r g a n i s m

263

as a sufficient a d a p t i v e e x p l a n a t i o n for t h e existence of o r g a n i s m a l life c y c l e s , o n the g r o u n d s t h a t c o m p l e x o r g a n s a r e , i n s o m e v a g u e s e n s e , a g o o d i d e a . A related point is that repeated r e p r o d u c t i o n is possible o n l y if i n d i v i d u a l s die (Maynard

Smith

1969),

but we should

not

therefore wish

to say that

individuals die as an adaptation to keep evolution g o i n g ! T h e same could be said of m u t a t i o n : its e x i s t e n c e is a n e c e s s a r y p r e c o n d i t i o n for e v o l u t i o n to occur, but it is nevertheless quite likely that natural selection has favoured evolution

attained

the

direction

(Williams

1966).

of a The

zero

mutation

rateâ&#x20AC;&#x201D;fortunately

growth/reproduction/death

type

never o f life

c y c l e â&#x20AC;&#x201D; t h e m u l t i c e l l u l a r c l o n a l ' o r g a n i s m ' t y p e o f life c y c l e â&#x20AC;&#x201D; h a s h a d farreaching consequences

and

was probably

essential

for

the

evolution

a d a p t i v e c o m p l e x i t y , b u t this i s n o t t a n t a m o u n t t o a n a d a p t i v e e x p l a n a t i o n for the e x i s t e n c e o f this t y p e o f life c y c l e . T h e D a r w i n i a n m u s t b e g i n b y s e e k i n g i m m e d i a t e b e n e f i t s t o g e n e s p r o m o t i n g this k i n d o f life c y c l e , a t t h e expense o f their alleles. H e m a y g o o n t o a c k n o w l e d g e the possibility o f other levels of selection, differential l i n e a g e e x t i n c t i o n , say. B u t he m u s t s h o w the s a m e c i r c u m s p e c t i o n i n this difficult t h e o r e t i c a l f i e l d a s F i s h e r Williams (1975)

and M a y n a r d Smith (1978a)

suggestions a b o u t sexual

reproduction

(1930a),

b r o u g h t to the a n a l o g o u s

being there

because it speeds up

evolution. T h e organism has the f o l l o w i n g attributes. It is either a single cell, or if it is multicellular

its c e l l s a r e c l o s e g e n e t i c

kin

of e a c h other:

they are

descended from a single stem cell, w h i c h m e a n s that they h a v e a m o r e recent c o m m o n ancestor w i t h e a c h other than w i t h the cells o f a n y o t h e r o r g a n i s m . T h e o r g a n i s m i s a u n i t w i t h a life c y c l e w h i c h , h o w e v e r c o m p l i c a t e d i t m a y b e , r e p e a t s t h e e s s e n t i a l c h a r a c t e r i s t i c s o f p r e v i o u s life c y c l e s , a n d m a y b e a n i m p r o v e m e n t o n p r e v i o u s life c y c l e s . T h e o r g a n i s m e i t h e r c o n s i s t s o f g e r m line c e l l s , o r i t c o n t a i n s g e r m - l i n e c e l l s a s a s u b s e t o f its o w n c e l l s , o r , a s i n t h e c a s e of a sterile s o c i a l i n s e c t w o r k e r , it is in a p o s i t i o n to w o r k for t h e w e l f a r e o f g e r m - l i n e cells i n c l o s e l y r e l a t e d o r g a n i s m s . I h a v e n o t a s p i r e d in this final c h a p t e r to g i v e a c o m p l e t e l y s a t i s f y i n g a n s w e r t o the q u e s t i o n o f w h y t h e r e a r e l a r g e m u l t i c e l l u l a r o r g a n i s m s . I w i l l be content if I accepting

that

c a n arouse n e w curiosity a b o u t the question. organisms

exist

and

asking

how

adaptations

Instead of benefit

the

o r g a n i s m s d i s p l a y i n g t h e m , I h a v e tried t o s h o w t h a t t h e v e r y e x i s t e n c e o f o r g a n i s m s s h o u l d b e t r e a t e d a s a p h e n o m e n o n d e s e r v i n g o f e x p l a n a t i o n i n its o w n right. R e p l i c a t o r s exist. T h a t is f u n d a m e n t a l . P h e n o t y p i c manifestations of them, including extended phenotypic manifestations, m a y be expected to function complex

a s tools

to keep replicators existing.

assemblages

of such

tools,

Organisms are

assemblages

shared

huge and gangs

replicators w h o in principle need not h a v e g o n e a r o u n d t o g e t h e r but in fact do go a r o u n d together a n d share a c o m m o n interest in the survival a n d reproduction

the

organism.

well

drawing

attention

the

264

R e d i s c o v e r i n g the O r g a n i s m

p h e n o m e n o n o f t h e o r g a n i s m a s o n e t h a t n e e d s e x p l a n a t i o n , I h a v e tried i n this last c h a p t e r t o s k e t c h t h e g e n e r a l d i r e c t i o n i n w h i c h w e m i g h t p r o c e e d i n s e e k i n g a n e x p l a n a t i o n . I t i s o n l y a p r e l i m i n a r y s k e t c h , b u t , for w h a t i t i s w o r t h , I s u m m a r i z e it here. The

replicators

that

exist

tend

the

ones

that

are

good

m a n i p u l a t i n g t h e w o r l d t o t h e i r o w n a d v a n t a g e . I n d o i n g this t h e y e x p l o i t t h e o p p o r t u n i t i e s offered b y t h e i r e n v i r o n m e n t s , a n d a n i m p o r t a n t a s p e c t o f the e n v i r o n m e n t of a replicator is other replicators a n d their p h e n o t y p i c manifestations. T h o s e r e p l i c a t o r s are successful w h o s e beneficial p h e n o t y p i c effects a r e c o n d i t i o n a l u p o n t h e p r e s e n c e o f o t h e r r e p l i c a t o r s w h i c h h a p p e n t o b e c o m m o n . T h e s e o t h e r replicators are also successful, o t h e r w i s e they w o u l d not b e c o m m o n . T h e w o r l d therefore tends t o b e c o m e populated b y m u t u a l l y c o m p a t i b l e sets o f s u c c e s s f u l r e p l i c a t o r s , r e p l i c a t o r s t h a t g e t o n w e l l together.

I n p r i n c i p l e this a p p l i e s t o r e p l i c a t o r s i n different g e n e p o o l s ,

different species, classes, p h y l a a n d k i n g d o m s . B u t a relationship of specially i n t i m a t e m u t u a l c o m p a t i b i l i t y has g r o w n u p b e t w e e n subsets o f replicators that share cell nuclei a n d , w h e r e the existence of s e x u a l r e p r o d u c t i o n makes the expression m e a n i n g f u l , share gene-pools. T h e cell n u c l e u s as a p o p u l a t i o n of uneasily c o h a b i t i n g replicators is a r e m a r k a b l e p h e n o m e n o n i n itself. J u s t a s r e m a r k a b l e , a n d q u i t e d i s t i n c t , i s the p h e n o m e n o n o f m u l t i c e l l u l a r c l o n i n g , the p h e n o m e n o n o f the multicellular

organism.

replicators

Replicators produce

whose

effects

multicellular

interact

organisms

with

achieve

those for

of other

themselves

vehicles w i t h c o m p l e x organs and behaviour patterns. C o m p l e x organs and b e h a v i o u r patterns are favoured in arms races. T h e evolution of complex organs a n d b e h a v i o u r patterns is possible b e c a u s e the o r g a n i s m is an entity w i t h a r e c u r r e n t life c y c l e , e a c h c y c l e b e g i n n i n g w i t h a s i n g l e c e l l . T h e f a c t that each cycle

restarts

every generation

from a single cell permits

m u t a t i o n s to a c h i e v e r a d i c a l e v o l u t i o n a r y c h a n g e s by g o i n g ' b a c k to the d r a w i n g b o a r d ' o f e m b r y o l o g i c a l e n g i n e e r i n g . I t a l s o , b y c o n c e n t r a t i n g the efforts o f a l l c e l l s i n t h e o r g a n i s m o n t h e w e l f a r e o f a n a r r o w , s h a r e d g e r m l i n e , p a r t l y r e m o v e s t h e ' t e m p t a t i o n ' for o u t l a w s t o w o r k for t h e i r o w n p r i v a t e g o o d at the e x p e n s e of the other replicators w i t h a stake in the same germ-line. T h e integrated multicellular organism is a phenomenon which has e m e r g e d as a result of n a t u r a l selection on primitively i n d e p e n d e n t selfish

replicators.

phenotypic

power

It has by

paid

which

replicators

they

ensure

behave gregariously.

their survival is in

The

principle

e x t e n d e d a n d u n b o u n d e d . In p r a c t i c e the o r g a n i s m has arisen as a partially bounded local concentration, a shared knot of replicator power.

Glossary

T h i s b o o k i s p r i m a r i l y i n t e n d e d for b i o l o g i s t s w h o w i l l h a v e n o n e e d of a glossary,

but it has been suggested

to me that it w o u l d

be w o r t h

e x p l a i n i n g a few t e c h n i c a l terms to m a k e the b o o k m o r e w i d e l y accessible. M a n y of the terms are w e l l defined in other places

(e.g. W i l s o n

1975;

B o d m e r & C a v a l l i - S f o r z a 1976). My definitions are certainly no i m p r o v e ment on

those

already

available,

but

have

added

personal

asides on

c o n t r o v e r s i a l w o r d s , o r o n m a t t e r s o f p a r t i c u l a r r e l e v a n c e t o t h e t h e s i s o f this b o o k . I h a v e tried t o a v o i d c l u t t e r i n g u p t h e g l o s s a r y w i t h e x c e s s i v e n u m b e r s of explicit cross-references, but m a n y of the w o r d s used in the definitions w i l l be found to h a v e their o w n definitions elsewhere in the glossary.

adaptation A technical term which has evolved somewhat a w a y from its c o m m o n usage as a near synonym of 'modification'. From sentences like 'cricket wings are adapted (modified from their primary function of flying) for singing' (and by implication are well designed for singing), 'an adaptation' has c o m e to m e a n approximately an attribute of an organism that is ' g o o d ' for something. G o o d in what sense?, and good for what or for w h o m ? , are difficult questions w h i c h are discussed at length in this book. alleles (short for allelomorphs) E a c h gene is able to o c c u p y only a particular region of chromosome, its locus. At any given locus there m a y exist, in the population, alternative forms of the gene. T h e s e alternatives are called alleles of one another. T h i s book emphasizes that there is a sense in w h i c h alleles are competitors of each other, because over evolutionary time successful alleles achieve numerical superiority over others at the same locus, in all the chromosomes of the population. allometry A disproportionate relationship between size of a body part and size of the whole body, the comparisons being made either across individuals or across different life stages in the same individual. For e x a m p l e , large ants (but small humans) tend to have relatively very large heads; the head grows at a different rate from the body as a whole. M a t h e m a t i c a l l y , the size of the part is usually taken as being related to the size of the whole raised to a power, w h i c h m a y be fractional. 283

284

Glossary

allopatric theory of speciation T h e widely supported view that the evolutionary divergence of populations into separate species (which no longer interbreed) takes place in g e o g r a p h i c a l l y separate places. T h e alternative, sympatric theory gives rise to difficulties in understanding how the incipient species can separate if they are continuously in a position to interbreed with each other, and therefore to mix their gene-pools (q.v.). altruism Biologists use the word in a restricted (some would say misleadingly so) sense, only superficially related to c o m m o n usage. An entity, such as a baboon or a gene, is said to be altruistic if it has the effect (not purpose) of promoting the welfare of another entity, at the expense of its o w n welfare. V a r i o u s shades of m e a n i n g of 'altruism' result from various interpretations of 'welfare' (see page 57). Selfish is used in exactly the opposite sense. anaphase T h a t phase of the cycle of cell division during w h i c h the paired chromosomes m o v e apart. In meiosis (q.v.) there are two successive divisions and correspondingly t w o anaphases. anisogamy A sexual system in w h i c h fusion takes place at fertilization between a large (female) and a small (male) gamete. Contrast with isogamy in which there is sexual fusion but no male/female separation: all gametes are of roughly the same size. antibodies Protein molecules, produced in the i m m u n e response of animals, which neutralize i n v a d i n g foreign bodies (antigens). antigens Foreign bodies, usually protein molecules, which provoke the formation of antibodies. aposematism T h e p h e n o m e n o n w h e r e b y distasteful or dangerous organisms like wasps ' w a r n ' enemies by bright colours or equivalent strong stimuli. These are presumed to work by m a k i n g it easy for the enemies to learn to avoid them, but there are (not insuperable) theoretical difficulties over how the phenomenon might evolve in the first place. assortative m a t i n g T h e tendency of individuals to choose mates that resemble (positive assortative m a t i n g or h o m o g a m y ) or specifically do not resemble (negative assortative mating) themselves. S o m e people use the word only in the positive sense. autosome

A chromosome that is not one of the sex chromosomes.

Baldwin/Waddington Effect First proposed by S p a l d i n g in 1873. A largely hypothetical evolutionary process (also called genetic assimilation) whereby natural selection c a n create an illusion of the inheritance of acquired characteristics. Selection in favour of a genetic tendency to acquire a characteristic in response to environmental stimuli leads to the evolution of increased sensitivity to the same environmental stimuli, and eventual emancipation from the need for them. On page 44 I suggest that we might breed a race of spontaneously milk-producing male m a m m a l s by treating successive generations of males with female hormones and selecting for increased sensitivity to female hormones. T h e role of the hormones, or other environmental treatment, is to bring out into the open genetic variation w h i c h w o u l d otherwise lie dormant.

Glossary

285

central d o g m a In molecular biology the d o g m a that nucleic acids act as templates for the synthesis of proteins, but never the reverse. M o r e generally, the d o g m a that genes exert an influence over the form of a body, but the form of a b o d y is never translated back into genetic c o d e : acquired characteristics are not inherited. chromosome O n e of the chains of genes found in cells. In addition to D N A itself, there is usually a complicated supporting structure of protein. Chromosomes become visible under the light microscope only at certain times in the cell c y c l e , but their number and linearity m a y be inferred by statistical reasoning from the facts of inheritance alone (see linkage). T h e chromosomes are usually present in all cells in the body, even though only a minority of them will be active in any one cell. T h e r e are usually two sex chromosomes in every diploid cell as well as a number of autosomes (44 in humans). cistron O n e w a y of defining a gene. In molecular genetics the cistron has a precise definition in terms of a specific experimental test. M o r e loosely it is used to refer to a length of chromosome responsible for the encoding of one chain of a m i n o acids in a protein. codon A triplet of units (nucleotides) in the genetic code, specifying the synthesis of a single unit (amino acid) in a protein chain. clone In cell biology, a set of genetically identical cells, all derived from the same ancestral cell. A h u m a n body is a gigantic clone of some 10 cells. T h e w o r d is also used of a set of organisms all of whose cells are members of the same clone. T h u s a pair of identical twins may be said to be members of the same clone. 15

Cope's Rule An empirical generalization that evolutionary trends towards larger body size are c o m m o n . crossing-over A complicated process w h e r e b y chromosomes, while engaged in meiosis, e x c h a n g e portions of genetic material. T h e result is the permutation of an almost infinite variety of gametes. D ' A r c y Thompson's transformations A g r a p h i c a l technique demonstrating that an animal shape can be transformed into the shape of a related animal by a mathematically specifiable distortion. D ' A r c y T h o m p s o n w o u l d d r a w one of the two shapes on ordinary graph paper, then show that it was transformed approximately into the other shape if the coordinate system were distorted in some particular w a y . diploid A cell is said to be diploid if it has chromosomes in pairs, in sexual cases one from each parent. An organism is said to be diploid if its body cells are diploid. Most sexually reproducing organisms are diploid. dominance A gene is said to be dominant to one of its alleles if it suppresses the phenotypic effect of that (recessive) allele when the two are together. For example, if brown eyes are dominant to blue, only individuals with two blue-eyed genes (homozygous recessive) would actually have blue eyes; those with one blue and one brown gene (heterozygotes) would be indistinguishable from those with two brown genes (homozygous dominant). D o m i n a n c e may be incomplete, in w h i c h case heterozygotes have an intermediate phenotype. T h e opposite of dominant is recessive. Dominance/recessiveness is a property of a phenotypic effect, not of a

286

Glossary

gene as s u c h : thus a gene m a y be dominant in one of its phenotypic effects and recessive in another (see pleiotropy). epigenesis A w o r d with a long history of controversy in embryology. As opposed to preformationism (q.v.) it is the doctrine that bodily complexity emerges by a developmental process of gene/environment interaction from a relatively simple zygote, rather than being totally mapped out in the egg. In this book it is used for the idea, w h i c h I favour, that the genetic code is more like a recipe than a blueprint. It is sometimes said that the epigenesis/preformationism distinction has been m a d e irrelevant by modern molecular biology. I disagree, and have made m u c h of the distinction in C h a p t e r 9, where I claim that epigenesis, but not preformationism, implies that embryonic development is fundamentally, and in principle, irreversible (see central d o g m a ) . epistasis A class of interactions between pairs of genes in their phenotypic effects. T e c h n i c a l l y the interactions are non-additive w h i c h means, roughly, that the combined effect of the two genes is not the same as the sum of their separate effects. For instance, one gene might mask the effects of the other. T h e word is mostly used of genes at different loci, but some authors use it to include interactions between genes at the same locus, in which case dominance/recessiveness is a special case. See also d o m i n a n c e . eukaryotes O n e of the two major groups of organisms on Earth, including all animals, plants, protozoa and fungi. C h a r a c t e r i z e d by the possession of a cell nucleus, and other m e m b r a n e - b o u n d e d cell organelles (analogue of 'organ' within the cell) such as mitochondria. Contrast with prokaryotes (q.v.). T h e prokaryote/eukaryote distinction is m u c h more fundamental than the animal/plant distinction (not to mention the relatively negligible h u m a n / ' a n i m a l ' distinction!). eusociality T h e most a d v a n c e d of the grades of sociality recognized by entomologists. C h a r a c t e r i z e d by a complex of features, the most important of w h i c h is the presence of a caste of sterile 'workers' w h o assist the reproduction of their long-lived mother, the queen. It is usually considered to be confined to wasps, bees, ants and termites, but various other kind of animals approach eusociality in interesting w a y s . evolutionarily stable strategy (ESS) [Note 'evolutionarily' not 'evolutionary'. T h e latter is a c o m m o n g r a m m a t i c a l error in this context.] A strategy that does well in a population dominated by the same strategy. T h i s definition captures the intuitive essence of the idea (see C h a p t e r 7), but is somewhat imprecise; for a m a t h e m a t i c a l definition, see M a y n a r d Smith, 1974. extended phenotype A l l effects of a gene upon the world. As always, 'effect' of a gene is understood as m e a n i n g in comparison with its alleles. T h e conventional phenotype is the special case in w h i c h the effects are regarded as being confined to the individual b o d y in which the gene sits. In practice it is convenient to limit 'extended p h e n o t y p e ' to cases where the effects influence the survival chances of the gene, positively or negatively. fitness A technical term with so m a n y confusing meanings that I have devoted a whole chapter to discussing them (Chapter 10).

Glossary

game theory A mathematical theory originally developed for generalized to human economics and military strategy, and theory of evolutionarily stable strategy (q.v.). G a m e theory wherever the optimum policy is not fixed, but depends upon statistically most likely to be adopted by opponents.

287

h u m a n games, and to evolution in the comes into its o w n the policy w h i c h is

gamete O n e of the sex cells w h i c h fuse in sexual reproduction. Sperms and eggs are both gametes. gemmule A discredited concept espoused by D a r w i n in his 'pangenesis' theory of the inheritance of acquired characteristicsâ&#x20AC;&#x201D;probably the only serious scientific error he ever made, and an example of the 'pluralism' for w h i c h he has recently been praised. G e m m u l e s were supposed to be small hereditary particles w h i c h carried information from all parts of the body into the germ cells. gene A unit of heredity. M a y be defined in different w a y s for different purposes (see page 85). M o l e c u l a r biologists usually employ it in the sense of cistron (q.v.). Population biologists sometimes use it in a more abstract sense. F o l l o w i n g W i l l i a m s (1966, p. 24), I sometimes use the term gene to m e a n 'that w h i c h segregates and recombines with appreciable frequency', and (p. 25) as 'any hereditary information for which there is a favorable or unfavorable selection bias equal to several or many times its rate of endogenous c h a n g e ' . gene-pool T h e whole set of genes in which the term is based is a h a p p y undeniable fact that genes actually go idea of genes flowing about the world

a breeding population. T h e metaphor on one for this book, for it de-emphasizes the about in discrete bodies, and emphasizes the like a liquid.

genetic drift C h a n g e s in gene frequencies over generations, resulting from c h a n c e rather than selection. genome

T h e entire collection of genes possessed by one organism.

genotype T h e genetic constitution of an organism at a particular locus or set of loci. Sometimes used more loosely as the whole genetic counterpart to phenotype (q.v.). gens (pl. gentes) ' R a c e ' of female cuckoos all parasitizing one host species. T h e r e must be genetic differences between gentes, and these are presumed to be on the Y chromosome. M a l e s have no Y chromosomes, and do not belong to gentes. T h e word is poorly chosen, since in the Latin it refers to a clan tracing descent through the male line. germ-line T h a t part of bodies w h i c h is potentially immortal in the form of reproductive copies: the genetic contents of gametes and of cells that give rise to gametes. Contrast with soma, the parts w h i c h are mortal and w h i c h work for the preservation of genes in the germ-line. gradualism T h e doctrine that evolutionary change is g r a d u a l and does not go in jumps. In modern palaeontology it is the subject of an interesting controversy over whether the gaps in the fossil record are artefactual or real (see C h a p t e r 6). Journalists have blown this up into a pseudo-controversy over the validity of Darwinism, w h i c h they say is a gradualist theory. It is true that all sane Darwinians are gradualists in the extreme sense that they do not believe in the de

288

Glossary

novo creation of very complex and therefore statistically improbable new adaptations like eyes. T h i s is surely what D a r w i n understood by the aphorism ' N a t u r e does not make leaps'. But within the spectrum of gradualism in this sense, there is room for disagreement about whether evolutionary change occurs smoothly or in small jerks punctuating long periods of stasis. It is this that is the subject of the modern controversy, and it does not remotely bear, one w a y or the other, on the validity of D a r w i n i s m . group selection A hypothetical process of natural selection a m o n g groups of organisms. Often invoked to explain the evolution of altruism (q.v.). Sometimes confused with kin selection (q.v.). In C h a p t e r 6 I use the replicator/vehicle distinction to distinguish g r o u p selection of altruistic traits from species selection (q.v.) resulting in macroevolutionary trends. haplodiploid A genetic system in which males grow from unfertilized eggs and are haploid, while females grow from fertilized eggs and are diploid. Therefore males have no father and no sons. M a l e s pass all their genes on to their daughters, while females receive only half their genes from their fathers. Haplodiploidy occurs in nearly all social and non-social H y m e n o p t e r a (ants, bees, wasps, etc.), and also a few bugs, beetles, mites, ticks and rotifers. T h e complications which haplodiploidy introduces into closeness of genetic kinship have been ingeniously invoked in theories of the evolution of eusociality (q.v.) in H y m e n o p t e r a . haploid A cell is said to be haploid if it has a single set of chromosomes. Gametes are haploid, and w h e n they fuse in fertilization a diploid cell (q.v.) is produced. S o m e organisms (e.g. fungi and male bees) are haploid in all their cells, and are referred to as haploid organisms. heterozygous T h e condition of h a v i n g nonidentical alleles at a chromosomal locus. Is usually applied to an individual organism, in which case it refers to two alleles at a given locus. M o r e loosely it may refer to the overall statistical withinlocus heterogeneity of alleles averaged over all loci in an individual or in a population. homeotic mutation A mutation causing one part of a body to develop in a manner appropriate to another part. For example, the homeotic mutation 'antennopedia' in Drosophila causes a leg to grow where an antenna normally does. T h i s is interesting, as it shows the power of a single mutation to have elaborate and c o m p l e x effects, but only w h e n there is elaborate complexity already there to be altered. homozygous T h e condition of h a v i n g identical alleles at a chromosomal locus. Is usually applied to an individual organism, in which case it indicates that the individual has two identical alleles at the locus. M o r e loosely it may refer to the overall statistical within-locus homogeneity of alleles averaged over all loci in an individual or in a population. K-selection Selection for the qualities needed to succeed in stable, predictable environments where there is likely to be heavy competition for limited resources between individuals well-equipped to compete, at population sizes close to the

Glossary

289

m a x i m u m that the habitat can bear. A variety of qualities are thought to be favoured by K-selection, including large size, long life, and small numbers of intensively cared-for offspring. Contrast with r-selection ( q . v . ) . T h e 'K' and V are symbols in the conventional algebra of population biologists. kin selection Selection of genes causing individuals to favour close kin, o w i n g to the high probability that kin share those genes. Strictly speaking 'kin' includes immediate offspring, but it is unfortunately undeniable that m a n y biologists use the phrase 'kin selection' specifically when talking about kin other than offspring. K i n selection is also sometimes confused with g r o u p selection (q.v.), from w h i c h it is logically distinct, although where species happen to go around in discrete kin groups the two may incidentally amount to the same thingâ&#x20AC;&#x201D;'kin g r o u p selection'. Lamarckism Regardless of what L a m a r c k actually said, L a m a r c k i s m is n o w a d a y s the name given to the theory of evolution that relies on the assumption that acquired characteristics can be inherited. F r o m the point of view of this book, the significant feature of the L a m a r c k i a n theory is the idea that new genetic variation tends to be adaptively directed, rather than ' r a n d o m ' (i.e. non-directed) as in the Darwinian theory. T h e orthodox view today is that the L a m a r c k i a n theory is completely wrong. linkage T h e presence on the same chromosome of a pair (or a set) of loci. L i n k a g e is normally recognized by the statistical tendency for alleles at linked loci to be inherited together. For example, if hair colour and eye colour are linked, a child that inherits your eye colour is likely to inherit your hair colour too, while a child that fails to inherit your eye colour is also likely to fail to inherit your hair colour. Children are relatively unlikely to inherit one but not the other, though this can come about due to crossing-over (q.v.), the probability being related to the distance apart of the loci on the chromosome. T h i s is the basis for the technique of chromosome m a p p i n g . linkage disequilibrium T h e statistical tendency for alleles to occur together, in the bodies or gametes of a population, with particular alleles at other loci. For example, if we observed a tendency for fair-haired individuals to be blue-eyed, this might indicate linkage disequilibrium. R e c o g n i z e d as any tendency for the frequency of combinations of alleles at different loci to depart from the frequencies that would be expected from the overall frequencies of the alleles themselves in the population. locus T h e position on a chromosome occupied by a gene (or a set of alternative alleles). For instance, there might be an eye-colour locus, at w h i c h the alternative alleles code for green, b r o w n and red. Usually applied at the level of the cistron (q.v.), the concept of the locus can be generalized to smaller or larger lengths of chromosome. macroevolution T h e study of evolutionary changes that take place over a very large time-scale. Contrast with microevolution, the study of evolutionary changes within populations. Microevolutionary change is c h a n g e in gene frequencies in populations. M a c r o e v o l u t i o n a r y change is usually recognized as c h a n g e in gross morphology in a series of fossils. T h e r e is some controversy over whether

290

Glossary

macroevolutionary change is fundamentally just cumulated microevolutionary c h a n g e , or whether the two are 'decoupled' and driven by fundamentally different kinds of process. T h e name macroevolutionist is sometimes misleadingly restricted to partisans on one side of this controversy. It should be a neutral label for anybody studying evolution on the grand time-scale. meiosis T h e kind of cell division in which a cell (usually diploid) gives rise to daughter cells (usually haploid) with half as m a n y chromosomes. Meiosis is an essential part of normal sexual reproduction. It gives rise to the gametes which subsequently fuse to restore the original chromosome number. meiotic drive T h e p h e n o m e n o n whereby alleles affect meiosis so that they secure for themselves a greater than 50 per cent chance of finding themselves in a successful g a m e t e . S u c h genes are said to be 'driving' because they tend to spread through the population in spite of any deleterious effects they may have on organisms. See also segregation distorter. meme A unit of cultural inheritance, hypothesized as analogous to the particulate gene, and as naturally selected by virtue of its 'phenotypic' consequences on its o w n survival and replication in the cultural environment. Mendelian inheritance N o n - b l e n d i n g inheritance by means of pairs of discrete hereditary factors (now identified with genes), one member of each pair coming from each parent. T h e main theoretical alternative is 'blending inheritance'. In M e n d e l i a n inheritance genes m a y blend in their effects on a body, but they themselves do not blend, and they are passed on intact to future generations. microevolution

See m a c r o e v o l u t i o n .

mitochondria S m a l l c o m p l e x organelles within eukaryotic cells, made of membranes, the site of most of the energy-releasing biochemistry of the cells. M i t o c h o n d r i a h a v e their o w n D N A and reproduce autonomously within cells, and, a c c o r d i n g to one theory, they originated in evolution as symbiotic prokaryotes (q.v.). mitosis T h e kind of cell division in which a cell gives rise to daughter cells having a complete set of all its chromosomes. Mitosis is the ordinary cell division of bodily g r o w t h . Contrast with meiosis. modifier gene A gene whose phenotypic effect is to modify the effect of another gene. Geneticists no longer m a k e a distinction between two types of genes, 'major genes' and 'modifiers', but recognize that many (and perhaps most) genes modify the effects of m a n y (and perhaps most) other genes. monophyletic A g r o u p of organisms is said to be monophyletic if all are descended from a c o m m o n ancestor w h i c h w o u l d also have been classified as a member of the group. For instance, the birds are probably a monophyletic group since the most recent c o m m o n ancestor of all birds would probably have been classified as a bird. T h e reptiles, h o w e v e r , are probably polypkyletic, in that the most recent common ancestor of all reptiles w o u l d probably not have been classified as a reptile. Some would argue that polyphyletic groups do not deserve names, and that the Class Reptilia should not be a c k n o w l e d g e d . mutation

An inherited c h a n g e in the genetic material.

In D a r w i n i a n theory

mutations are said to be r a n d o m . T h i s does not mean that they are not lawfully

Glossary

291

caused, but only that there is no specific tendency for them to be directed towards improved adaptation. Improved adaptation comes about only through selection, but it needs mutation as the ultimate source of the variants a m o n g w h i c h it selects. muton T h e m i n i m u m unit of mutational c h a n g e . definitions of gene (with cistron and recon).

O n e of several

alternative

neo-Darwinism A term coined (actually re-coined, for the w o r d was used in the 1880s for a very different g r o u p of evolutionists) in the middle part of this century. Its purpose was to emphasize (and in my opinion exaggerate) the distinctness of the modern synthesis of Darwinism and M e n d e l i a n genetics, a c h i e v e d in the 1920s and 1930s, from D a r w i n ' s o w n view of evolution. I think the need for the ' n e o ' is fading, and D a r w i n ' s o w n a p p r o a c h to 'the e c o n o m y of nature' now looks very modern. neoteny An evolutionary slowing d o w n of bodily d e v e l o p m e n t relative to the development of sexual maturity, with the result that reproduction comes to be practised by organisms w h i c h resemble the j u v e n i l e stages of ancestral forms. It is hypothesized that some major steps in evolution, for e x a m p l e the origin of the vertebrates, c a m e about through neoteny. neutral mutation A mutation that has no selective a d v a n t a g e or d i s a d v a n t a g e in comparison with its allele. T h e o r e t i c a l l y , a neutral mutation m a y b e c o m e 'fixed' (i.e. numerically predominant in the population at its locus) after a n u m b e r of generations, and this would be a form of evolutionary c h a n g e . T h e r e is legitimate controversy over the importance of such random fixations in evolution, but there should be no controversy over their importance in the direct production of adaptation: it is zero. nucleotide A kind of biochemical molecule, notable as the basic building block of D N A and R N A . D N A and R N A are polynucleotides, consisting o f long chains o f nucleotides. T h e nucleotides are 'read' in triplets, each triplet being k n o w n as a codon. ontogeny T h e process of individual development. In practice d e v e l o p m e n t is often taken to culminate in the production of the adult, but strictly it includes later stages such as senescence. T h e doctrine of the extended p h e n o t y p e w o u l d lead us to generalize 'ontogeny' to include the ' d e v e l o p m e n t ' of extracorporeal adaptations, for example artefacts like beaver dams. optimon T h e unit of natural selection, in the sense of the unit for whose benefit adaptations m a y be said to exist. T h e thesis of this book is that the optimon is neither the individual nor the group of individuals but the g e n e or genetic replicator. But the dispute is in part a semantic one, whose resolution occupies portions of Chapters 5 and 6. orthoselection Sustained selection on the members of a lineage over a long period, causing continued evolution in a given direction. C a n create an a p p e a r a n c e of ' m o m e n t u m ' or 'inertia' in evolutionary trends. outlaw gene A gene w h i c h is favoured by selection at its o w n locus, in spite of its deleterious effects on the other genes in the organisms in w h i c h it finds itself. Meiotic drive (q.v.) provides a good e x a m p l e .

292

Glossary

Paley's watch A reference to the best known of William Paley's (1743-1805) arguments for the existence of G o d . A watch is too complicated, and too functional, to have c o m e about by accident: it carries its own evidence of having been purposefully designed. T h e argument seems to apply a fortiori to a living body, w h i c h is even more complicated than a watch. D a r w i n , as a y o u n g man, was deeply impressed by this. A l t h o u g h he later destroyed the G o d part of the argument, by showing that natural selection can play the role of watchmaker to living bodies, he did not destroy the fundamental point â&#x20AC;&#x201D; still under-appreciatedâ&#x20AC;&#x201D; that complicated design demands a very special kind of explanation. G o d apart, the natural selection of small inherited variations is probably the only agency c a p a b l e of doing the j o b . phenotype T h e manifested attributes of an organism, the joint product of its genes and their environment during ontogeny. A gene m a y be said to have phenotypic expression in, say, eye colour. In this book the concept of phenotype is extended to include functionally important consequences of gene differences, outside the bodies in w h i c h the genes sit. pheromone A chemical substance secreted by an individual, and adapted to influence the nervous systems of other individuals. Pheromones are often thought of as chemical 'signals' or 'messages', and as the inter-body analogue of hormones. In this book they are more often treated as analogous to manipulative drugs. phylogeny

Ancestral history on the evolutionary time-scale.

plasmid O n e of a set of more or less synonymous words used for small, selfreplicating fragments of genetic material, found in cells but outside chromosomes. pleiotropy T h e phenomenon whereby a change at one genetic locus can bring about a variety of apparently unconnected phenotypic changes. For instance a particular mutation might at one and the same time affect eye colour, toe length, and milk yield. Pleiotropy is probably the rule rather than the exception, and is entirely to be expected from all that we understand about the complex way in which development happens. pluralism In modern D a r w i n i a n j a r g o n , the belief that evolution is driven by m a n y agencies, not just natural selection. Enthusiasts sometimes overlook the distinction between evolution (any kind of change in gene frequencies, which may well be pluralistically caused) and adaptation (which only natural selection, as far as we know, c a n bring a b o u t ) . polygene O n e of a set of genes each exerting a small, cumulative effect on a quantitative trait. polymorphism T h e occurrence together in the same locality of two or more discontinuous forms of a species in such proportions that the rarest of them cannot be maintained merely by recurrent mutation. Polymorphism necessarily occurs during the transient course of an evolutionary change. Polymorphisms may also be maintained in stable balance by various special kinds of natural selection. polyphyletic

See monophyletic.

preformationism As opposed to epigenesis (q.v.) it is the doctrine that the form of the adult body is in some sense mapped in the zygote. O n e early partisan thought

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293

he could discern, with his microscope, a little man curled up in the head of a sperm. In C h a p t e r 9 it is used for the idea that the genetic code is more like a blueprint than a recipe, implying that the processes of embryonic d e v e l o p m e n t are in principle reversible, in the same sense as, say, you m a y reconstruct its blueprint from a house. prokaryotes O n e of the two major groups of organisms on Earth (contrast eukaryotes) including bacteria and blue-green a l g a e . They have no nucleus and no membrane-bounded organelles such as m i t o c h o n d r i a : indeed one theory has it that mitochondria and other such organelles in eukaryotic cells are, in origin, symbiotic prokaryotic cells. propagule A n y kind of reproductive particle. T h e w o r d is used specifically when we wish not to commit ourselves over whether we are speaking about sexual or asexual reproduction, about gametes or spores, etc.

r-selection Selection for the qualities needed to succeed in unstable, unpredictable environments, where ability to reproduce rapidly and opportunistically is at a premium, and where there is little value in adaptations to succeed in competition. A variety of qualities are thought to be favoured by r-selection, including high fecundity, small size, and adaptations for long-distance dispersal. W e e d s , and their animal equivalents, are examples. Contrast with K-selection ( q . v . ) . It is customary to emphasize that r-selection and K-selection are the extremes of a continuum, most real cases lying somewhere between. Ecologists enjoy a curious love/hate relationship with the r/K concept, often pretending to disapprove of it while finding it indispensable. recessiveness

Opposite of dominance (q.v.).

recon T h e minimum unit of recombination. O n e of several different definitions of gene, but, like muton, it has not yet received sufficient currency to be usable without simultaneous definition. replicator A n y entity in the universe of which copies are m a d e . C h a p t e r 5 contains an extended discussion of replicators, and a classification of active/passive, and germ-line/dead-end replicators. reproductive value A d e m o g r a p h i c technical term, a measure of an individual's expected number of future (female) children. segregation distorter A gene whose phenotypic effect is to influence meiosis so that the gene has a greater than 50 per cent chance of ending up in a successful gamete. See also meiotic drive. selfish

See altruism.

sex chromosome A special chromosome concerned with the determination of sex. In mammals there are two sex chromosomes called X and Y. M a l e s have the genotype X Y , females X X . A l l eggs therefore bear one X chromosome, but sperms may bear either one X (in which case the sperm will give rise to a daughter) or one Y (in which case the sperm will give rise to a son). T h e male sex is therefore referred to as heterogametic, the female as homogametic. Birds have a very similar

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Glossary

system, except that males are homogametic (the equivalent of X X ) and females heterogametic (the equivalent of X Y ) . Genes carried on sex chromosomes are called 'sex-linked'. T h i s is sometimes confused (e.g. page 10) with 'sex-limited', w h i c h means h a v i n g expression in one sex or the other (not necessarily carried on sex chromosomes). somatic Literally pertaining to the body. In biology it is used for the mortal part of the body, as opposed to the germ-line. speciation T h e process of evolutionary produced from one ancestral species.

divergence

whereby

two

species

are

species selection T h e theory that some evolutionary change takes place by a form of natural selection at the level of species or lineages. If species with certain qualities are more likely to go extinct than species with other qualities, large-scale evolutionary trends in the direction of the favoured qualities may result. These favoured qualities at the species level m a y in theory have nothing to do with the qualities that are favoured by selection within species. C h a p t e r 6 argues that although species selection m a y account for some simple major trends, it cannot account for the evolution of complex adaptation (see Paley's w a t c h , and m a c r o e v o l u t i o n ) . T h e theory of species selection in this sense comes from a different historical tradition from the theory of group selection (q.v.) of altruistic traits, and the two are distinguished in C h a p t e r 6. stasis In evolutionary theory, a period during w h i c h no evolutionary change takes place. See also gradualism. strategy L i k e 'altruism', used by ethologists in a special sense, almost misleadingly distantly related to its c o m m o n usage. It was imported from g a m e theory into biology in the theory of evolutionarily stable strategies (q.v.), where it is essentially synonymous with ' p r o g r a m ' in the computer sense, and means a preprogrammed rule that an animal obeys. T h i s meaning is precise, but unfortunately strategy has become a m u c h abused b u z z - w o r d , and is now bandied about as a trendy synonym for ' b e h a v i o u r pattern'. A l l individuals of a population might follow the strategy ' I f small flee, if large a t t a c k ' ; an observer would then observe two behaviour patterns, fleeing and attacking, but he would be w r o n g to call them two strategies: both behaviour patterns are manifestations of the same conditional strategy. survival value selection.

T h e quality for which a characteristic was favoured by natural

symbiosis T h e intimate living together (with mutual dependence) of members of different species. S o m e modern textbooks omit the mutual dependence proviso, and understand symbiosis to include parasitism (in parasitism, only one side, the parasite, is dependent on the other, the host, w h i c h would be better off alone). Such textbooks use mutualism in place of symbiosis as defined above. symphylic substance C h e m i c a l substance used by social insect colony parasites (e.g. beetles) to influence the behaviour of their hosts.

teleonomy T h e science of adaptation. In effect, teleonomy is teleology made respectable by D a r w i n , but generations of biologists have been schooled to avoid

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'teleology' as though it were an incorrect construction in L a t i n g r a m m a r , and many feel more comfortable with a euphemism. Not m u c h thought has been given to what the science of teleonomy will consist of, but some of its major preoccupations will presumably be the questions of units of selection, and of costs and other constraints on perfection. T h i s book is an essay in teleonomy. tetraploid H a v i n g four of each chromosome type rather than the more usual two (diploid) or one (haploid). N e w species of plants are sometimes formed by a doubling of chromosomes to tetraploidy, but subsequently the species behaves like an ordinary diploid w h i c h happens to have twice as m a n y chromosomes as a closely related species, and it is convenient to consider it diploid for most purposes. Chapter 11 suggests that although individual termites are diploid, the whole termite nest may be regarded as the extended phenotypic product of a tetraploid genotype. vehicle Used in this book for any relatively discrete entity, such as an individual organism, which houses replicators (q.v.), and w h i c h can be regarded as a machine programmed to preserve and propagate the replicators that ride inside it. Weismannism T h e doctrine of a rigid separation between an immortal germ-line and the succession of mortal bodies w h i c h house it. In particular the doctrine that the germ-line m a y influence the form of the body, but not the other w a y around. See also central d o g m a . zygote T h e cell that is the immediate product of sexual fusion between t w o gametes.