GAIA Nº 15, LISBOA/LISBON, DEZEMBRO/DECEMBER 1998, pp. 399-403 (ISSN: 0871-5424)
THE EVOLUTION OF FEATHERS FROM DINOSAUR HAIR Peter J. GRIFFITHS University of Wolverhampton, School of Health Sciences. Lichfield Street, Wolverhampton WV1 1DJ. UNITED KINGDOM
ABSTRACT: The significance of finding feathered theropod dinosaurs is discussed in terms of the theories of the evolution of feathers, birds and endothermy. The plumulous proximal portion of the isolated Archaeopteryx feather suggests that endothermy had already evolved in the dinosaur - bird lineage by the Late Jurassic. It is suggested that adipose tissue would have played a major role in providing insulation in endothermic ancestral theropod dinosaurs. Small endothermic dinosaurs may have found an additional form of insulation an advantage. This may initially have evolved as"hair" in the dinosaurs, rather than the more morphologically complex branched feather. As avian epidermal appendages are composed of the unique f keratin family, it is unlikely that feathers were derived directly from archosaurian scales, but must have involved intermediate structures. It is suggested that feathers could consequently have been derived from dinosaur "hair". RÉSUMÉ: La découverte significative de dinosaures théropodes à plumes a entraîné une discussion en fonction des théories sur l'évolution des plumes, des oiseaux et de l'endothermie. La partie proximale duveteuse de la plume isolée de l' Archaeopteryx suggère une évolution de l'endothermie dans la lignée dinosaure-oiseau à la fin du Jurassique. On pense que le tissu adipeux aurait joué un rôle majeur en fournissant de la chaleur chez les dinosaures théropodes endothermes. Ainsi, les petits auraient pu en trouver un avantage supplémentaire. Chez les dinosaures, il y aurait d'abord pu avoir une évolution vers des "poils" plutôt que des plumes ramifiées, morphologiquement très compliquées. Etant donné que les tissus épidermaux des animaux à plumes sont composés de l'unique famille kératine f, il est improbable que les plumes aient directement dérivé des écailles archosauriennes, mais ont dû faire intervenir des structures intermédiaires. Par conséquent, les plumes auraient pu provenir des "poils" de dinosaures. INTRODUCTION The recent discovery of several species of feathered theropod dinosaur from the Liaoning Province of China, locality of the early birds Sinornis (SERENO & RAO, 1992) and Confuciusornis (HOU et al. 1995), has fuelled the debate regarding the origin and initial function of feathers, and also speculation concerning the possibility that dinosaurs were endothermic. Sinosauropteryx prima (JI & JI, 1996), a small compsognathid dinosaur is described as having epidermal appendages resembling the plumules of modern birds (CHEN, DONG & ZHEN, 1998). Protoarchaeopteryx robusta (JI & JI, 1997) and Caudipteryx zoui (JI et al., 1998) are both described as having pennaceous feathers attached to the fore limbs and tail, while Caudipteryx is reported as also having plumulaceous feathers around the body (JI et al., 1998). The discovery of feathered non-avian theropod dinosaurs provides
supporting evidence for the hypothesis that feathers evolved initially for the purpose of insulation or display, becoming secondarily adapted for flight. In addition, the discovery of feathered non-avian dinosaurs gives support to the hypothesis that birds evolved from the theropods, and that dinosaurs ancestral to birds were endothermic. THE THEROPOD ANCESTRY OF BIRDS It is generally accepted by most palaeontologists that birds evolved from the theropod dinosaurs (OSTROM, 1973), and cladistic analyses suggests that among the theropod dinosaurs, the dromaeosaurs share the most characters with the earliest known bird Archaeopteryx, and also with modern birds (GAUTHIER, 1986; HOLTZ, 1994). The hypothesis that birds evolved from the theropod dinosaurs has recently received further support
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with the discovery of a new species of fossil bird from the Upper Cretaceous of Madagascar, Rahona ostromi (FORSTER et al., 1998). Rahona has bony protrusions on the forearms which in modern birds serve as the attachment points for flight feathers, suggesting not only that it was feathered but also that it was capable of flight. Most interestingly, Rahona has a large, retractable sickle-shaped claw on the second toe of the hind foot, similar to the slashing claws of Velociraptor (OSBORN, 1924) and Deinonychus (OSTROM, 1969). It has been suggested that the second toe of Archaeopteryx may have been hyperextensible (PAUL, 1988; SERENO, 1997). In addition, although the pedal claws are considerably smaller than those of the wing (G RIFFITHS , 1994), the claw of the second toe is significantly larger than those of the other toes, and has a different morphology. For example, in the Eichst채tt specimen WELLNHOFFER (1974) reports that the claw of the second toe has a curvature with a greater angle from the vertical chord across the articular facet to claw tip (160o) compared to the other toes (132 o -146 o ), which supports the suggestion that the second toe of Archaeopteryx may have been hyperextensible. While a slashing claw is found in Rahona, such a claw is not present in Iberomesornis (SANZ et al., 1988) or Concornis (SANZ & BUSCALIONI, 1992) from the Lower Cretaceous of Spain, or Confuciusornis (HOU et al., 1995) and Sinornis (SERENO & RAO, 1992) from China. This would suggest that the slashing claw of Rahona may be a retained plesiomorphic character. EVOLUTION OF ENDOTHERMY AND DOWN FEATHERS The discovery of apparently flightless, feathered non-avian theropod dinosaurs provides strong supporting evidence for the hypothesis that feathers evolved initially for the purpose of display or insulation, becoming secondarily adapted for flight during the subsequent evolution of birds (REGAL, 1975). An alternative hypothesis for the origin of feathers (FEDUCCIA, 1974) is that they evolved initially for flight, and subsequently become adapted for insulation when the birds became endothermic, although this now seems less likely in view of the recent finds. Modern birds are unquestionably endothermic and have down feathers which are specialised for insulation as well as flight feathers. At some point along the dinosaur - bird lineage, both endothermy and feathers for insulation evolved, although not necessarily at the same time. The first discovered fossil down feather has been classified as Ilerdopteryx viai (LACASA, 1985) from the Lower Cretaceous of El Montsec, Spain. This location has yielded a variety of specialised feathers which are
morphologically very similar to those of modern birds. The earliest known fossil feather is that of Archaeopteryx lithographica (MEYER, 1861). A recent analysis shows the feather to be morphologically identical to the tenth secondary flight feather of the magpie which has a wing shape (and presumably aerodynamic characteristics) similar to that of Archaeopteryx (GRIFFITHS, 1996). This is the only described individual fossil feather attributable to Archaeopteryx, and so it is not known if the species possessed feathers specialised specifically for insulation. However, an examination of the morphology of the isolated Archaeopteryx feather reveals some interesting features. On distal portions of the feather, individual barbs and even barbules can clearly be observed forming the usual pennaceous structure which allows the barbs to zip together creating the typical flight-feather vane capable of generating aerodynamic lift. In comparison, the morphology of the feather is quite different proximally where individual barbs cannot be distinguished. In this region, the feather has a tufted appearance suggesting that the hooklets attached to the barbules are fewer in number or are absent, and that the barbs are much thinner than in the distal parts of the feather. Consequently the isolated Archaeopteryx feather appears to have a plumulaceous region at the base which would efficiently trap air against the skin. This feature is identical to that found in the flight feathers of modern birds which have few if any down feathers on the wing. The plumulaceous base of the Archaeopteryx feather indicates that it was capable of providing insulation and so supports the hypothesis that Archaeopteryx was endothermic (GRIFFITHS, 1996). As the Archaeopteryx feather is already morphologically specialised and exhibits characteristics enabling the dual functions both of flight and insulation, Archaeopteryx can give no indication of the initial role of feathers, but does make clear that feathers capable of providing insulation as well as flight were already present during the Late Jurassic. It is logical to assume that endothermy and feathers evolved in taxa ancestral to Archaeopteryx. THE ROLE OF ADIPOSE TISSUE FOR INSULATION In contrast to birds, mammals use two different mechanisms for insulation, hair and also a layer of adipose tissue under the dermis. Hair plays a similar role in insulation as down feathers, trapping a layer of air against the skin thus reducing heat loss by convection and radiation. In adipose tissue, lipid droplets are stored in large specialised cells which are embedded in connective tissue, particularly in the
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dermis. The dermal layer of adipose tissue prevents the loss of heat from deep within the body, helping to maintain core temperature. The potential role of adipose tissue for insulation must be taken into account when considering the evolution of endothermy in birds, particularly with regard to the ancestral dinosaurs and the debate as to whether they were endothermic. Once there is a necessity for regulation of the internal temperature to within small tolerances, then insulation becomes an immediate advantage due to the high energetic expense of the metabolic generation of heat. This would be particularly important for smaller species with a high surface area to volume ratio where heat loss would be more significant. There would therefore be a very high selection pressure, particularly for small species of dinosaur living in a colder climate, to evolve some form of insulation. This could most simply be achieved with a layer of adipose tissue under the skin. Adipose tissue is widely distributed among modern sauropsids, and in modern birds is used not only for energy storage but also insulation, particularly in species which come into frequent contact with water. A thick layer of adipose tissue, while it may provide excellent insulation, is however relatively heavy. In terms of insulation efficiency to weight, the ratio is low (GRIFFITHS, 1996). This is not normally a problem, but becomes a serious disadvantage where weight is of consideration such as when attempting to fly. Conversely, down feathers and hair have a high insulation efficiency to weight ratio and therefore have the advantage over adipose tissue where weight is of consideration. The early mammals are thought to have been small shrew-like creatures with a large surface area to volume ratio, thus heat loss from the surface would have been a major problem. Hair would have been a big advantage in providing extra insulation and reducing heat loss, particularly if the early mammals were mainly nocturnal and active when ambient temperatures were lower. Mammals seem to have increased in size later in their evolutionary history, and large mammals frequently have reduced hair cover, particularly those living in warmer climates, as seen in modern elephants, although large mammals such as mammoths retained a thick hair covering when faced with adverse climatic conditions. The situation appears to be the reverse for birds which probably originated from larger theropod ancestors and initially became progressively smaller as flight evolved. Archaeopteryx is smaller than most known theropods, with the exception of Compsognathus (WAGNER,1861) which was an unusually small theropod. Similarly, the thrush sized Lower
Cretaceous birds Iberomesornis, Concornis and also Sinornis were much smaller than Archaeopteryx. Bird evolution therefore appears to have involved an initial reduction in size, probably because it is easier for small birds to generate aerodynamic lift (SANZ & BONAPARTE, 1992), although Confuciusornis appears to be an exception as they were of a similar size to Archaeopteryx. THE EVOLUTION OF FEATHERS MADERSON (1972) has suggested that protofeathers may have evolved from the tips of archosaurian scales with the scale eventually regressing to leave the feather, on the basis that both feathers and the epidermis of scales in birds were thought to contain b keratin, while the interfollicular skin adjacent to feathers and the inner surface of scales contained a keratin. This hypothesis received support from the work of DHOUAILLY , HARDY & SENGEL (1980), who showed that it was possible to convert the prospective scales on the feet of chick embryos to feathers with the use of Retinioc Acid, known to play an important role in positional signalling and pattern formation during cell differentiation in developing embryos. However, BRUSH (1993) has shown that the avian keratins in feathers, down, scutes and beaks are quite different from the keratin of reptiles, and is composed of a family of f keratins. These are more closely related to a keratins than b keratins. There is little evidence that f keratin and a keratin diverged from a common ancestral gene, or that f keratin was derived from existing a keratin genes, although f keratin could perhaps be derived from a cytokeratin protein. f keratin forms b -pleated sheets which spontaneously assemble into filaments by self association, rather than the a helixes which a keratin can form. The f keratins exist as two main groups: a larger molecule of 13,500 Da found in scales, claws and beaks, and a smaller molecule of 10,500 Da found in feathers and down. The amino acid sequences of the f keratin of feathers and down is more similar to the sequence of amino acids in scutes than in reticulate scales, and closer still to beak and then claw keratins (BRUSH, 1980). As Archaeopteryx has feathers which are essentially modern in structure, it could be assumed that they were also composed of f keratin. In addition to feathers, the keratin sheaths of the claws have been preserved in Archaeopteryx. There is no sign of a beak in any of the specimens although it is unlikely that Archaeopteryx possessed a beak as teeth were still present. Also, there are no indications of scutes or reticulate scales in any of the specimens.
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This introduces additional complexity into any hypothesis concerning the origin of feathers as it is necessary to postulate the evolution of a new family of genes coding for these new proteins, which must have been present in epidermal appendages prior to the evolution of feathers. The molecular structure of the f keratins would suggest that it is unlikely that feathers evolved directly from archosaurian scales. As feather keratins are closer to beak and claw keratins than scute or scale keratins, it again suggests that a number of intermediate stages were involved in feather evolution (BRUSH, 1996). DINOSAUR HAIR Av i a n f e a t h e r s c a n b e m o r p h o l o g i c a l l y distinguished from mammalian hair on the basis that they have a complex branching structure, while mammalian hair consists of single filaments. From a developmental perspective, hair is more simple to form than the structurally complex branching feather, and consequently mammalian hair follicles are morphologically simpler than avian feather follicles. If the evolution of epidermal appendages were driven by the necessity of providing insulation rather than providing an aerodynamically functional vane, it is parsimonious to consider the initial evolution of an unbranched structure to be more probable than a complex branching one. Unbranched single filaments (hair) are therefore more likely than branched feathers to have initially evolved as a structure required for the purposes of insulation. If the dinosaurs were to be considered endothermic, hair would have the advantage of conferring additional insulation to that provided by a layer of adipose tissue. This may have been important to smaller species of dinosaur with a high surface area to volume ratio which were challenged with the problem of heat loss that larger dinosaur species would not experience. An analysis of the epidermal appendages of Sinosauropteryx (CHEN, DONG & ZHEN, 1998), describes the structures as being possibly hollow, rather course structures that may resemble the plumules of modern birds, with short quills and long filamentous barbs, but with no signs of barbules or hooklets. However, as it has not yet been possible to isolate a single structure for analysis, it is not clear if these structures really are branched rather than being composed of single filaments, or if they even have any real relationship with modern feathers. Preserved impressions of possible integumentary structures have also been described associated with the non-avian theropod Pelecanimimus polyoden (PÉREZ-MORENO et al., 1994) from the Lower Cretaceous location of Las Hoyas, Spain. These
structures are described as consisting of a primary system of subparallel fibres arranged perpendicular to the bone surface, with a less conspicuous secondary system orientated in parallel. Again, it is not clear if these are branched structures rather than single filaments. Branching filamentous structures which can only be described as symmetrical feathers have been found associated with the two new species from the Liaoning province of China, Protoarchaeopteryx and Caudipteryx (J I et al., 1998). While the phylogenetic analysis places Caudipteryx as a sister group to the Avialae, the systematic position of Protoarchaeopteryx is less clear and appears to be unresolved from the Velociraptorinae (GAUTHIER, 1986; HOLTZ, 1994) root, and may also be a sister group to the Avialae (JI et al., 1998). Although Protoarchaeopteryx has relatively long arms compared to non-avian coelurosaurs they are shorter than Archaeopteryx. The arms of Caudipteryx are shorter than non-avian coelurosaurs. In either species it appears to be unlikely that they were able to fly. However, there is a distinct possibility that they were the flightless descendants of birds, and inherited feathers from flying ancestors. This hypothesis is supported by the observation that the some of the feathers of Protoarchaeopteryx and perhaps Caudipteryx were pennaceous. PAUL (1988) has even suggested that all the dromaeosaurs are descended from flying protobirds. This is not impossible as they appear to have evolved after Archaeopteryx, and even Protoarchaeopteryx, Caudipteryx and Sinosauropteryx are found in deposits that probably date from the early Cretaceous (SMITH, EVENSEN & YORK, 1996). FEATHERS FROM DINOSAUR HAIR Feathers could conceivably have evolved from dinosaur "hair", perhaps similar in morphology to the structures reported associated with Pelicanimimus. Such appendages may well have been composed of filaments of f keratin, rather than a keratin as in mammalian hair. Subsequently, the epidermal appendages became split to form the branching structure of barbs. Such a branching structure could possibly be represented by the appendages reported associated with Sinosauropteryx, with short quills and long filamentous barbs. The branching then become more complex to form barbules. Hooks subsequently evolved allowing the barbules to zip together to form the pennaceous structure of modern feathers, as exhibited by Archaeopteryx and modern birds. This hypothesis therefore proposes a series of progressively more complex structures, each of which is functionally advantageous in terms of initially providing insulation, and then finally lead-
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