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THE POSTGLACIAL HISTORY OF TREES C. FERRIS For most peoplc the tcrm migration conjures up images of long distances travelled by the likes of birds in flight, zebra or wildebcest gallĂśping across plains, and locusts swarming over fields of crops. That is, animals fulfilling a basic instinct to move to pastures new for food or to secure new breeding grounds. In this context, migration is clearly a very motile process and the animal examples presented in other papers in this volume fit the bill perfectly.

But what about plants? Does a sedentary life style precludc migration in plants? The intention of this paper is to show that plants can be very successful migrants, to outline some of the differences between the processes of migration in plants and animals and to show how, ultimately, they may be dependent upon each other.

Migration may be defined as "to move from one country or locality to another", "to pass, usually periodically, from one region or climate to another for the purposes of feeding, breeding, etc." (Longman, 1984). In a general definition such as this there is no inference on time scale, return journey, age or stage of the migrant (e.g. adult or larva etc.) distance travelled, nor whether the process is active or passive. The main differences between migration in most animals versus most plants are given in Table 1. The primary differences are the time scale involved and the migratory stage, which in most animals is the adult individual whereas in most plants it is the seed.

Table 1. Comparing plant vs. animal migration Animal

Plant

Adult motile Embryo / egg sessile Gametes sessile Purpose - breeding / feeding Time scale - short/occasionally long

Adult sessile Seed motile Pollen motile Purpose - breeding Time scale - long/occasionally Short

To understand the migratory history of plants we need to go back thousands of years to the time of the last period of glaciation to see where our flora and fauna have migrated from. That is we have to identify their areas of refuge during the ice-age.

Glaciations Prior to about three million years ago the climate of the earth was fairly stable.

Cycles of warming and cooling caused by the Milankovitch cycles (Variation in earth's orbit affecting the amount of solar radiation) existed, but were not extreme. There were no major ränge expansions or contractions and thus no streng selection pressures for plants to be able to migrate quickly. Trees such as magnolias were widespread and common (Ingrouille, 1995). The movement of the continents through plate tectonics, including the rising of mountain ranges and the Tibetan plateau, in addition to the movement of Antarctica to cover the south pole, caused the warming and cooling effects of the

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Milankovitch cycles to be exaggerated enough to cause a changc from relatively stable to unstable conditions (Imbrie, 1985; Imbric & Imbric, 1979; Ruddiman & Raymo, 1988). This lead to thc occurrence of glaciations which have regularly advanced and retreated on a 100,000 year cycle sincc about 2.6 million years ago (Hays et al„ 1976). This resulted in the dccline of gencra such as Magnolia to a few subtropical arcas. The temperate areas of the globc became dominated by species which could migrate fairly rapidly Over vast distances to cope with climate change giving rise to the more 'weedy' flora of today.

Refugia Before we can trace the routes taken by plants during colonisation after the last ice-age, we need to know where they were at any given time during the last 20,000 years or so. Unfortunately this is not possible for the majority of plants.

However, the pollen of many tree genera is distinctive and there is a suitable fossil pollen record (Huntley & Birks, 1983). Lake-bed cores from all over Britain and Europe have been analysed to give fossil pollen maps for many tree genera. Radiocarbon dating helps to show when a tree first started to produce pollen in an area thus indicating time of presence. Using these data the refugia for many European tree species have been inferred (Bennett et al., 1991).

Migration rates Comparisons between lake-bed cores from different areas in Europe provides a fairly comprehensive postglacial colonisation pattem for each genus from which good estimates of postglacial migration can be made (Table 2). It can be seen that the maximum rates occurred during migration through mainland Europe but the rates began to slow down as colonisation proceeded further north and into Britain. Given that we now know the general migration rates for many species, we are most interested in the specific routes and pattern of migration taken by the different genera. For this we need a suitable marker or tagging system.

Table 2. Postglacial migration rates for European tree species. The relative rates between colonisation of Britain and mainland Europe are shown. (After Birks, 1989) Dispersal Migration rate m/yr km/generation Europe Britain Tree Birch Hazel Elm Oak Pine Alder Lime Ash Beech

250 500 550 350-500 100-700 500-600 450-500 50-200 100-200

>2000 1500 500-1000 150-500 1500 500-2000 300-500 200-500 200-300

2.5 7.5

8 7-10 1-7 5-6 10 1-3 4-8

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Markers Tracking an animal's present migration routcs today is fairly simple by using thc appropriate tagging or tracking system devices. Clearly this is not possible for tracking postglacial migration as the migration has already taken place.

However, we can use the latest m e t h o d s in D N A technology to look for differences between populations of a species and thus produce D N A marker profiles. These are analogous to using barcodes to ring birds. Although we cannot tag a tree and follow its migration, w e can use the D N A marker profiles as rcady made internal tags in the D N A of the plant. We can then look for patterns of Variation in the D N A profiles across Europe and relate the patterns found to the recolonisation of Europe from the glacial refugia of the species.

Thc markers used are o f t e n f r o m the chloroplast D N A in plants and from the mitochondrial D N A in animals because these g e n o m e s are easy to work with experimentally.

Materials For the molecular analyses we require the extraction of D N A f r o m fresh, dried, or frozen leaves. In order to prevent the results being confounded from non-native planted sources the trees f r o m which the samples are taken must wherever possible c o m e f r o m k n o w n native sources. To this end trees f r o m ancient wildwood are favoured as are ancient pollarded trees; e.g. for oaks, the B o w t h o r p e Oak in Lincolnshire (the largest girthed c o m m o n oak in Britain) and the Q u e e n ' s Oak (see Plate 12) in Suffolk (estimated to b e over 1000 years old) . Aiternatively, trees with a k n o w n history can be used e.g. Kett's Oak in Norfolk. Problems with native versus planted source of material are much less serious in species such as alder where planting has not been so prevalent. Once the samples have been chosen and analysed for the D N A markers, it is then possible to identify the putative migration routes taken following the retreat of the last ice-age.

Tree examples from Europe Oak Perhaps the best studied plant example of postglacial migration to date is of the genus Quercus, which is well represented in the fossil record and for which detailed fossil pollen m a p s for E u r o p e are readily available (Huntley & Birks, 1983). From these m a p s it is clear that populations of oaks survived the glaciation in refugia in southern Iberia, Italy and the Balkans (Bennett et al., 1991; Huntley & Birks, 1983). A s Europe began to warm up after the end of the last ice-age, some 10,000 years ago, migration of oaks northward into mainland Europe was remarkably fast with m a x i m u m speeds of up to 500 m/yr, (Table 2). Long distance dispersal events must have been c o m m o n during these early stages of colonisation with an inevitable thinning of genetic diversity.

Chloroplast D N A ( c p D N A ) does indeed indicate that the diversity in the north is merely a subset of that in the south (Dumolin-Lapegue et al., 1997).

P o p u l a t i o n genetic studies have revealed striking patterns of genetic subdivision within Europe for the north European deciduous oaks, Q. robur and Q. petraea (Dumolin-Lapegue et al., 1997; Ferris et al., 1993; 1995; 1998; Petit et al., 1993). T h e natural patterns of c p D N A Variation indicate a

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subdivision of Europc into three main regions; western, central, and castcm (Fig. 1), with each region being founded from its own respective refugium (Ferris et al., 1998). The cpDNA markers dcfine the extent to which each migration proceeded and indicate zones of contact between them. The clear boundary between the central and eastern cytotypes in southem Finland shows that there is litile opportunity for gene flow via seed between the populations upon contact (Ferris et al., 1998). The average sequence divergence between the eastern and the western and central cytotypes is 0.3%, and when compared with an average divergence rate of 0.1 % per million years for chloroplast DNA (Zurawski et al. 1984; Wolfe et al., 1987) this represents about 3 million years of isolation between the refugial areas. Clearly the refugial areas for oak were isolated for many glaciations if not for the whole of the Pleistocene (Ferris et al., 1999).

Figure 1. European distribution pattem of chloroplast DNA Variation in the common oak, (After Ferris et al., 1998).

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Fossil pollcn data for thc common becch (Fagus sylvatica L.) indicate two main refugia in the south of Europe; thc Carpathian mountains and Italy (Dcmesure et al„ 1996). These refugia are supported by the patterns of cpDNA types throughout Europe. The phylogeographic strueture indicates the Carpathian mountains to have been the main refugium from which the north and west were colonised. The Italian refuge gave rise to a migration which only proeeeded as far as northern Italy, just south of thc Alps. The pollen data suggest maximum rates of migration of 300 m/yr representing up to 8 km per generation (Table 2). Again long distance dispersal is evident and diversity will be lost during the colonisation process. Patterns of cpDNA Variation support this with most of the cpDNA diversity in Italy and the Crimea as compared to the north and west (Dcmesure et al., 1996). Indeed, most of northern Europe is represented by a Single type.

Alder Refugia for common alder (Alnus glutinosa (L.) Gaertn.) have been proposed in the Carpathian mountains and south-west Russia, the Bay of Biscay,

Figure 2 Thc geographical distribution pattern of chloroplast Variation in the common alder, Alnus glutinosa, throughout Europe (After King & Ferns, 1998)

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southern Italy, Greece (Bennett et al., 1991; Huntley & Birks, 1983) and possibly Turkey (Van Zeist et al., 1975). Clearly with so many rcfugia during ihe last glaciation there is the potential for high levels of diversity in the south of Europe. This has been confirmed by cpDNA studies which reveal hotspots of diversity in south-eastem Europe and Turkey (Fig. 2) (King & Ferris, 1998).

Populations north of 45°N are comprised of one of two common types. One type primarily filled Britain and northern Europe, whilst the second is common in central regions. Of the 12 types found, 9 occur only in southern Europe, mostly in the south-east. The decrease in cpDNA diversity from south to north can be attributed to the rapid migration at the end of the ice age with speeds of up to 2000 m/yr (Table 2). The pattems of migration in alder are similar to those of beech with two common chloroplast types migrating north and west from south-eastern refugia (King & Ferris, 1998).

Migration Patterns The pattern of migration for oak is clearly very different to that for beech and alder. Few examples are available for animals or plants that indicate the postglacial migration pattems taken. Table 3 gives a summary of twelve clear examples that have been published. These represent four major patterns of migration following the last ice-age which are outlined in Fig. 3. Failure to migrate north out of a particular refugial area may be the result of one or more factors. Of great importance is the ability to overcome barriers such as Table 3. Phylogeography studies from the literature indicating a comparison of postglacial migration routes taken by different animals and plants as shown in Figure 3.

Species

Routes

Reference

D

King & Ferris, (1998)

A

Santucci et al., (1998)

D

Demesure et al., (1996)

Silver fir, Abies alba

C

Parducci et al., (1996)

Brown bear, Ursus

Alder, Alnus

glutinosa

Hedgehog, Erinaceus Beech, Fagus

europaeus

sylvatica

B

Taberlet & Bouvet, (1994)

Lesser white-toothed shrew, Crocidura suaveolens

B

Cosson et al., (In prep)

Crested newt, Triturus

D

Wallis & Arntzen, (1989)

A

Dumolin-Lapegue et al., (1997)

Oak, Quercus

aretos

cristatus

robur

Norway Spruce, Picea

abies

C

Konnert & Bergmann, (1995)

Meadow grasshopper, parallelus

Chorthippus

D

Cooper et al., (1995)

araneus

B

Taberlet et al., (1994)

B

Jaarola & Tegelstrom, (1995)

Common shrew, Sorex Field vole, Microtus

agrestis

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Figure 3. The four general patterns of migration taken by plants and animals after the last ice age. mountain ranges. For those species taking pattern A there are cleariy n o Problems crossing the Pyrenees or the Alps, or moving around the Carpathian mountains. Pattern B involves the ability to take the eastern and we lern routes but the inability to cross the Alps. Pattern C indicates the inability to cross the Pyrenees whilst being able to take both the central and western routes^Finally pattern D indicates the inability to cross either the Pyrenees or the Alps and thus the whole of n o r t h e m Europe is colonised f r o m the eastern refuge.

What causes the inability to cross a mountain ränge is unknown, bu possible causes includc: the t.ming of colonisation (e.g. whether there are still ice-caps on the mountains); the soil and Vegetation types already present the stagc of succession); availability of moisture; the presence of specific factors such as mycorrhizae; and the dispersal abilities of the species. Many of these factors may be combined or interdependent.

B S Ă„ S 3 some patterns are already evident. Four of the s p c i e s 8 2 plant and 2 an,mal, took only the eastern route. These s p e c e s c l e a r l y do not cross the mountain barriers of the Alps or the Pyrenees For alder and the meadow grasshopper this may be due to the.r early time of migration^ For cxamplc grasshoppers may have been prevented from colon.smg high into the mounta ns due to the continued presence of ice-caps. Howcver, the castcrn K w o u l d have skirted around the Carpathians to the east and started to fill

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northern Europe whilst thc central and western typcs wcrc hcld back by mountains. As time passcd and temperatures rose so thc grasshoppcrs migratcd higher up either side of the mountain chains until they mct at thc highest points whcre they now form hybrid zones (Hewitt, 1993; 1996). By contrast, bccch is a late successional spccies which bcgan migrating much latcr than most othcr trcc species. It does not cope well with cold conditions and could not cross thc Pyrcnees or Alps, evcn today. Thus it could only migratc via the eastern route.

Patterns B and C each represent a two route pattern of migration with thc third route blockcd by a mountain chain. Of the four animal species which took a two route pattern, cach show pattern B, that is they all found the Alps to be a barrier. However, the two plant species that took a two route migration, each show pattern C and thus found the Pyrenees to be a barrier. Why there should bc such a difference bctween animals and plants is unclear.

Two species took all three routes, these being the common oak and the European hedgehog. Their migration patterns are strikingly similar (Fig. 4).

Figure 4. Postglacial migration routes for the common oak (after DumolinLapegue et al„ 1997) and the European hedgehog (after Santucci et al„ 1998).

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This may indicate a dcpendencc of the hedgehog on the previous colonisation of oak. Hedgehogs depend upon mixed deciduous woodland for their habitat and prcsumably, thcrefore, closely followed the colonisation of oak through Europc. They probably also occupied similar refugia during the period of glaciation.

As more species are studied for their glacial history so we will get a clearer picture of the processes involved in the postglacial migration of species. It is clear from the oak and hedgehog that animals may be dependent upon the colonisation of plants and thus show similar patterns of migration. It must also bc remembered that plants themselves may be dependent upon animals for their dispersal and their patterns of migration may be related to that of their dispcrsal agents. For example, in the common oak it is known that dispersal occurred via birds such as the passenger pigeon and the jay (Bossema, 1979).

The north-south migrations of birds may have forged the migration patterns we see in oak and ultimately, the pattem we see in the hedgehog.

References Bennett, K. D„ Tzedakis, P. C. & Willis, K. J. (1991). Quaternary refugia of north European trees. Journal of biogeography 18: 103-115.

Birks, H. J. B. (1989). Holocene isochrone maps and pattems of tree.-spreading in the British Isles. Journal of biogeography 16: 503-540.

Bossema, I. (1979). Jays and oaks: an eco-ethological study of a symbiosis.

Behaviour, 70: 1-117.

Cooper, S. J., Ibrahim, K. M. & Hewitt, G. M. (1995). Postglacial expansion and genome subdivision in the European grasshopper Chorthippus parallelus. Molecular ecology, 4: 49-60.

Cosson, J. F., Taberlet, P., Fumagalli, L. et al. Phylogeography of the lesser white-toothed shrew Crocidura suaveolens (Mammalia, Insectivora) in Europe inferred from mitochondrial DNA Variation. (In Prep.).

Demesure, B„ Comps, B. & Petit, R. J. (1996). Chloroplast DNA phylogeography of the Common Beech (Fagus sylvatica L.) in Europe.

Evolution 50: 2515-2520.

Dumolin-Lapegue, S„ Demesure, B., Fineschi, S., Le Corre, V. & Petit, R. J. (1997). Phylogeographic strueture of white oaks throughout the European continent. Genetics 146: 1475-1487.

Ferris, C., King, R. A„ Väinölä, R. & Hewitt, G. M. (1998). Chloroplast DNA recognises three refugial sources of European oaks and shows independent eastern and westem immigrations to Finland. Heredity 80: 584-593.

Ferris, C„ Oliver, R. P„ Davy, A. J. & Hewitt, G. M. (1993). Native oak chloroplasts reveal an ancient divide across Europe. Molecular ecology 2: 337-344.

Ferris, C„ Oliver, R. P„ Davy, A. J. & Hewitt, G. M. (1995). Using chloroplast DNA to trace postglacial migration routes of oaks into Britain. Molecular ecology 4: 731-738.

Ferris, C., King, R. A. & Hewitt, G. M. (1999). Isolation within species and the history of glacial refugia. In Molecular systematics and plant evolution. (ed. P. M. Hollingsworth, R. Bateman, & R. J. Gomall): Taylor & Francis.

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Hays, J. D„ Imbrie, J. & Shackleton, N. H. (1976). Variations in ihe earth's orbit: pacemaker of the ice ages. Science 194: 1121-1132.

Hewitt, G. M. (1993). Postglacial distribution and species substructurc: lessons from pollen, insects and hybrid zones. Biological journal of the Linnean Society 14: 98-119.

Hewitt, G. M. (1996). Some genetic consequences of icc ages, and their role in divergence and speciation. Biological journal of the Linnean Society 58: 247-276.

Huntley. B. & Birks, H. J. B. (1983). An atlas of past and present pollen maps for Europe: 0-13,000 years ago. Cambridge: Cambridge University Press.

Imbrie, J. (1985). A theoretical framework for the Pleistocene ice ages. Journal of the Geological Society of London 142: 417-432.

Imbrie, J. & Imbrie, K. P. (1979). Ice ages: solving the mystery. London: Macmillan.

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London: Chapman & Hall.

Jaarola, M. & Tegelstrom, H. (1995). Colonisation history of the north European field voles ( Microtus agrestis) revealed by mitochondrial DNA. Molecular ecology, 4: 299-310.

King, R. A„ & Ferris, C. (1998). Chloroplast DNA phylogeography of Alnus glutinosa (L.) Gaertn. Molecular ecology 7: 1151-1162.

Konnert, M. & Bergmann, F. (1995). The geographical distribution of genetic Variation of the silver fir (Abies alba, Pinaceae) in relation to its migration history. Plant systematics and evolution 196: 19-30.

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Parducci, L„ Szmidt, A. E., Villani, F., et al. (1996). Genetic Variation of Abies alba in Italy. Hereditas 125: 11-17.

Petit, R. J„ Kremer, A. & Wagner, D. B. (1993). Geographical structure of chloroplast DNA polymorphisms in European oaks. Theoretical and applied genetics 87: 122-128.

Ruddiman, W. F. & Raymo, M. E. (1988). Northern hemisphere climate regimes during the past 3Ma: possible tectonic connections. Philosophical transactions of the Royal Society of London 318B: 411^130.

Santucci, F., Emerson, B. C. & Hewitt, G. M. (1998). Mitochondrial DNA phylogeography of European hedgehogs. Molecular ecology 7: 11631172.

Taberlet, P., Bouvet, J. (1994). Mitochondrial DNA polymorphism, phylogeography and conservation genetics of the brown bear (Ursus arctos) in Europe. Proceedings of the Royal Society of London Series B 252: 195-200.

Taberlet, P., Fumagalli, L., Hausser, J. (1994). Chromosomal versus mitochondrial DNA evolution: tracking the evolutionary history of the south-western European populations of the Sorex araneus group (Mammalia, Insectivora). Evolution 48: 623-636.

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Wallis, G. P. & Arntzxn, J.W. (1989). Mitochondrial-DNA Variation in thc crested ncwl supcrspccies: limited cytoplasmic genc flow a m o n g species.

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Colin Fcrris Department of Biology University of Leicester University Road Leicester, LEI 7RH E-mail: cfl2@leicester.ac.uk

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Plate 12: The Queen's Oak at Huntingfield, May 1996. This tree is reputed to be over 1000 years old (p. 16).