GAIA N'15, LlSBOAlLISBON, 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. Uchfield Street. Wolverhampton WV1 10J. UNITED KINGDOM

ABSTRACT: The significance of finding feathered theropod dinosaurs is discussed in terms _ ofthe theories of the evolution offeathers, 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 tis­ sue would have played a major role in providing insulation in endothermic ancestral thero­ pod 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 ofthe unique 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".

RESUME: La decouverte significative de dinosaures theropodes a plumes a entraine une dis­ cussion en fonction des theories sur I'evolution des plumes, des oiseaux et de I'endother­ mie. La partie proximale duveteuse de la plume isolee de I' Archaeopteryx suggere une evolution de I'endothermie dans la lignee dinosaure-oiseau a la fin du Jurassique. On pense que Ie tissu adipeux auraitjoue un role majeur en fournissant de la chaleur chez les dinosau­ res theropodes endothermes. Ainsi, les petits auraient pu en trouver un avantage supple­ mentaire. Chez les dinosaures, il y aurait d'abord pu avoir une evolution vers des "poils" plutot que des plumes ramifiees, morphologiquement tres compliquees. Etant donne que les tissus epidermaux des animaux a plumes sont composes de I'unique famille keratine <1>, iI est improbable que les plumes aient directement derive des ecailles archosauriennes, mais ont dO faire intervenir des structures intermediaires. Par consequent, les plumes auraient pu provenir des "poi Is" de dinosaures.

INTRODUCTION supporting evidence forthe hypothesis thatfeathers evolved initially for the purpose of insulation or The recent discovery of several species of display, becoming secondarily adapted for flight. In feathered theropod dinosaur from the Liaoning addition, the discovery of feathered non-avian Province of China, locality of the early birds Sinornis dinosaurs gives support to the hypothesis that birds (SERENO & RAo, 1992) and Confuciusornis (HOU et evolved from the theropods, and that dinosaurs al. 1995), has fuelled the debate regarding the origin ancestral to birds were endothermic. and initial function offeathers, and also speculation concerning the possibility that dinosaurs were THE THEROPOD ANCESTRY OF BIRDS endothermic. Sinosauropteryx prima (J I & J I, 1996), a small compsognathid dinosaur is described as It is generally accepted by most palaeontologists having epidermal appendages resembling the that birds evolved from the theropod dinosaurs plumules of modern birds (CHEN, DONG & ZHEN, (OSTROM, 1973), and cladistic analyses suggests 1998). Protoarchaeopteryx robusta (JI & JI, 1997) that among the theropod dinosaurs, the dro­ and Caudipteryx zoui (JI et al., 1998) are both maeosaurs share the most characters with the earli­ described as having pennaceous feathers attached est known bird Archaeopteryx, and also with modern to the fore limbs and tail, while Caudipteryx is birds (GAUTH IER, 1986; HOLTZ, 1994). reported as also having plumulaceous feathers The hypothesis that birds evolved from the thero­ around the body (JI et al., 1998). The discovery of pod dinosaurs has recently received further support feathered non-avian theropod dinosaurs provides

399 artigos/papers P. J. GRIFFITHS

with the discovery of a new species of fossil bird morphologically very similar to those of modern from the Upper Cretaceous of Madagascar, Rahona birds. ostromi (FORSTER et a/., 1998). Rahona has bony The earliest known fossil feather is that of Ar­ protrusions on the forearms which in modern birds chl;leopteryx lithographica (MEYER, 1861). A recent serve as the attachment points for flight feathers, analysis shows the feather to be morphologically suggesting not only that it was feathered but also identical to the tenth secondary flight feather of the that it was capable of flight. Most interestingly, Ra­ magpie which has a wing shape (and presumably hona has a large, retractable sickle-shaped claw on aerodynamic characteristics) similar to that of Ar­ the second toe ofthe hind foot, similar to the slashing chaeopteryx (GRIFFITHS, 1996). This is the only de­ claws of Velociraptor(OSBORN , 1924) and Deinony­ scribed individual fossil feather attnbutable to chus (OSTROM, 1969). Archaeopteryx, and so it is not known if the species It has been suggested that the second toe of possessed feathers specialised specifically for inSU­ Archaeopteryx may have been hyperextensible lation. (PAUL, 1988; SERENO, 1997). In addition, although However, an examination of the morphology of the pedal claws are considerably smaller than those the isolated Archaeopteryx feather reveals some in­ of the wing (GRIFFITHS, 1994), the claw of the teresting features. On distal portions of the feather, second toe is significantly larger than those of the individual barbs and even barbules can clearly be other toes, and has a different morphology. For observed forming the usual pennaceous structure example, in the Eichstatt specimen WELLNHOFFER which allows the barbs to zip together creating the (1974) reports that the claw of the second toe has a typical flight-feather vane capable of generating curvature with a greater angle from the vertical aerodynamic lift. In comparison, the morphology of chord across the articular facet to claw tip (160°) the feather is quite different proximally where indi­ compared to the other toes (132°_146°) , which vidual barbs cannot be distinguished. In this region, supports the suggestion that the second toe of the feather has a tufted appearance suggesting that Archaeopteryx may have been hyperextenslble. the hooklets attached to the barbules are fewer in While a slashing claw is found in Rahona , such a number or are absent, and that the barbs are much claw is not present in Iberomesornis (SANZ et a/., thinner than in the distal parts of the feather. Conse­ 1988)or Concornis(SANZ& BUSCALIONI, 1992)from quently the isolated Archaeopteryx feather appears the Lower Cretaceous of Spain, or Confuc/Usorms to have a plumulaceous region at the base which (HOU et a/., 1995) and Sinornis (SERENO & RAO, would efficiently trap air against the skin. This fea­ 1992) from China. This would suggest that the ture is identical to that found in the flight feathers of slashing claw of Rahona may be a retained modern birds which have few if any down feathers plesiomorphic character. on the wing. The plumulaceous base of the Archae­ opteryx feather indicates that it was capable of pro­ EVOLUTION OF ENDOTHERMY AND DOWN viding insulation and so supports the hypothesIs that FEATHERS Archaeopteryxwas endothermic (GRIFFITHS, 1996). The discovery of apparently flightless, feathered As the Archaeopteryx feather is already morpho­ non-avian theropod dinosaurs provides strong logically specialised and exhibits characteristics supporting evidence for the hypothesis that feathers enabling the dual functions both of flight and Insula­ evolved initially for the purpose of display or Insula­ tion, Archaeopteryx can give no indication of the ini­ tion, becoming secondarily adapted for flight during tial role of feathers, but does make clear that the subsequent evolution of birds (REGAL, 1975). An feathers capable of providing insulation as well as alternative hypothesis for the origin of feathers (FE­ flight were already present during the Late Jurassic. DUCCIA 1974) is that they evolved initially for flight, It is logical to assume that endothermy and feathers and subsequently become adapted for insulation evolved in taxa ancestral to Archaeopteryx. when the birds became endothermic, although this now seems less likely in view of the recent finds. THE ROLE OF ADIPOSE TISSUE FOR Modern birds are unquestionably endothermic INSULATION and have down feathers which are specialised for in­ In contrast to birds, mammals use two different sulation as well as flight feathers. At some point mechanisms for insulation, hair and also a layer of along the dinosaur - bird lineage, both endothermy adipose tissue under the dermis. Hair plays a similar and feathers for insulation evolved, although not role in insulation as down feathers, trapping a layer necessarily at the same time. The first discovered of air against the skin thus reducing heat loss by con­ fossil down feather has been classified as lIerdop­ vection and radiation. In adipose tissue, lipid drop­ teryx viai (LACASA, 1985) from the Lower Creta­ lets are stored in large specialised cells which are ceous of EI Montsec, Spain. This location has embedded in connective tissue, particularly in the yielded a variety of specialised feathers which are

400 THE EVOLUTION OF FEATHERS FROM DINOSAUR HAIR

dermis. The dermal layer of adipose tissue prevents Cretaceous birds Iberomesomis, Concornis and the loss of heat from deep within the body, helping to also Sinornis were much smaller than Archaeop­ maintain core temperature. teryx. Bird evolution therefore appears to have in­ volved an initial reduction in size, probably because The potential role of adipose tissue for insulation it is easier for small birds to generate aerodynamic must be taken into account when considering the lift (SANZ & BONAPARTE , 1992), although Confuciu­ evolution of endothermy in birds, particularly with re­ somis appears to be an exception as they were of a gard to the ancestral dinosaurs and the debate as to similar size to Archaeopteryx. whether they were endothermic. Once there is a ne­ cessity for regulation of the internal temperature to THE EVOLUTION OF FEATHERS within small tolerances, then insulation becomes an immediate advantage due to the high energetic ex­ MADERSON (1972) has suggested that proto­ pense of the metabolic generation of heat. This feathers may have evolved from the tips of archo­ wou ld be particularly important for smaller species saurian scales with the scale eventually regress,i ng with a high surface area to volume ratio where heat to leave the feather, on the basis that both fe athers loss would be more sign ificant. There wou ld there­ and the epidermis of scales in birds were thought to fore be a very high selection pressure, particularly contain f3 keratin, while the interfollicular skin adja­ for small species of dinosaur living in a colder cli­ cent to feathers and the inner surface of scales con­ mate, to evolve some form of insulation. This could tained a keratin. This hypothesis received support most simply be achieved with a layer of adipose tis­ from the work of DHOUAILLY, HARDY & SEN GEL sue under the skin. Adipose tissue is widely distrib­ (1980), who showed that it was possible to convert uted among modern sauropsids, and in modern the prospective scales on the feet of ch ick embryos birds is used not only for energy storage but also in­ to feathers with the use of Retinioc Acid, known to sulation, particularly in species which come into fre­ play an important role in positional signalling and quent contact with water. pattern formation during cell differentiation in devel­ A thick layer of adipose tissue, wh ile it may pro­ oping embryos. vide excellent insulation, is however relatively However, BRUSH (1993) has shown that the heavy. In terms of insulation efficiency to weight, the avian keratins in feathers, down, scutes and beaks ratio is low (GRIFFITHS, 1996). This is not normally a are quite different from the keratin of reptiles, and is problem, but becomes a serious disadvantage composed of a family of keratins. These are more where weight is of consideration such as when at­ closely related to a keratins than f3 keratins. There is tempting to fly. little evidence that keratin and a keratin diverged Conversely, down feathers and hair have a high from a common ancestral gene, or that keratin was insulation efficiency to weight ratio and therefore derived from existing a keratin genes, although have the advantage over adipose tissue where keratin cou ld perhaps be derived from a cytokeratin weight is of consideration. The early mammals are protein. keratin forms f3-pleated sheets which thought to have been small shrew-like creatures spontaneously assemble into filaments by self asso­ with a large surface area to volume ratio, thus heat ciation, rather than the a helixes which a keratin can loss from the surface would have been a major prob­ form. The keratins exist as two main groups: a lem. Hair would have been a big advantage in pro­ larger molecule of 13,500 Da found in scales, claws viding extra insulation and reducing heat loss, and beaks, and a smaller molecule of 10,500 Da particularly if the early mammals were mainly noc­ found in feathers and down. The amino acid se­ turnal and active when ambient temperatures were quences of the keratin of feathers and down is lower. Mammals seem to have increased in size more similar to the sequence of amino acids in later in their evolutionary history, and large mam­ scutes than in reticulate scales, and closer still to mals frequently have reduced hair cover, particu­ beak and then claw keratins (BRUSH, 1980). larly those living in warmer climates, as seen in modern elephants, although large mammals such As Archaeopteryx has feathers which are essen­ as mammoths retained a thick hair covering when tially modern in structure, it could be assumed that faced with adverse climatic conditions. they were also composed of keratin. In addition to The situation appears to be the reverse for birds feathers, the keratin sheaths of the claws have been which probably originated from larger theropod an­ preserved in Archaeopteryx. There is no sign of a cestors and initially became progressively smaller beak in any of the specimens although it is unlikely as flight evolved. Archaeopteryx is smaller than that Archaeopteryx possessed a beak as teeth were most known theropods, with the exception of Comp­ still present. Also, there are no indications of scutes sognathus (WAGNER, 1861) wh ich was an unusually or reticulate scales in any of the specimens. small theropod. Similarly, the thrush sized Lower

401 P. J. GRIFFITHS

This introduces additional complexity into any structures are described as consisting of a primary hypothesis concerning the origin of feathers as it is system of subparallel fibres arranged perpendicular necessary to postulate the evolution of a new family to the bone surface, with a less conspicuous secon­ of genes coding for these new proteins, which must dary system orientated in parallel. Again, it is not have been present in epidermal appendages priorto clear if these are branched structures rather than the evolution of feathers. The molecular structure of single filaments. the keratins would suggest that it is unlikely that Branching filamentous structures which can only feathers evolved directly from archosaurian scales. be described as symmetrical feathers have been As feather keratins are closer to beak and claw found associated with the two new species from the keratins than scute or scale keratins, it again sug­ Liaoning province of China, Protoarchaeopteryx gests that a number of intermediate stages were in­ and Caudipteryx (JI et al., 1998). While the volved in feather evolution (BRUSH, 1996). phylogenetic analysis places Caudipteryx as a sistergrouptothe Avialae, the systematic position of DINOSAUR HAIR Protoarchaeopteryx is less clear and appears to be Avian feathers can be morphologically unresolved from the Velociraptorinae (GAUTHIER, distinguished from mammalian hairon the basis that 1986; HOLTZ, 1994) root, and may also be a sister they have a complex branching structure, while group to the Avialae (JI et al., 1998). Although mammalian hair consists of single filaments. From a Protoarchaeopteryx has relatively long arms developmental perspective, hair is more simple to compared to non-avian coelurosaurs they are form than the structurally complex branching shorter than Archaeopteryx. The arms of feather, and consequently mammalian hair follicles Caudipteryx are shorter than non-avian are morphologically simpler than avian feather coelurosaurs. In either species it appears to be follicles. If the evolution of epidermal appendages unlikely that they were able to fly. However, there is a were driven by the necessity of providing insulation distinct possibility that they were the flightless rather than providing an aerodynamically functional descendants of birds, and inherited feathers from vane, it is parsimonious to consider the initial flying ancestors. This hypothesis is supported by the evolution of an unbranched structure to be more observation that the some of the feathers of probable than a complex branching one. Protoarchaeopteryx and perhaps Caudipteryx were Unbranched single filaments (hair) are therefore pennaceous. PAUL (1988) has even suggested that more likely than branched feathers to have initially all the dromaeosaurs are descended from flying evolved as a structure required for the purposes of protobirds. This is not impossible as they appear to insulation. have evolved after Archaeopteryx, and even Protoarchaeopteryx, Caudipteryx and If the dinosaurs were to be considered endother­ Sinosauropteryx are found in deposits that probably mic, hairwould have the advantage of conferring ad­ date from the early Cretaceous (SMITH, EVENSEN & ditional insulation to that provided by a layer of YORK, 1996). adipose tissue. This may have been important to smaller species of dinosaur with a high surface area FEATHERS FROM DINOSAUR HAIR to volume ratio which were challenged with the prob­ lem of heat loss that larger dinosaur species wou ld Feathers could conceivably have evolved from not experience. dinosaur"hair", perhaps similar in morphologytothe structures reported associated with Pelicanimimus. An analysis of the epidermal appendages of Si­ Such appendages may wel l have been composed of nosauropteryx (CHEN, DONG & ZHEN , 1998), de­ filaments of keratin, rather than IX keratin as in scribes the structures as being possibly hollow, mammalian hair. Subsequently, the epidermal ap­ rather course structures that may resemble the plu­ pendages became split to form the branching struc­ mules of modern birds, with short quills and long fila­ ture of barbs. Such a branching structure could mentous barbs, but with no signs of barbules or possibly be represented by the appendages re­ hooklets. However, as it has not yet been possible to ported associated with Sinosauropteryx, with short isolate a single structure for analysis, it is not clear if quills and long filamentous barbs. The branching these structures really are branched rather than be­ then become more complex to form barbules. Hooks ing composed of single filaments, or if they even subsequently evolved allowing the barbules to zip have any real relationship with modern feathers. together to form the pennaceous structure of mod­ Preserved impressions of possible integumen­ ern feathers, as exhibited by Archaeopteryx and tary structures have also been described associated modern birds. This hypothesis therefore proposes a with the non-avian theropod Pelecanimimus polyo­ series of progressively more complex structures, den (PEREZ-MORENO et al., 1994) from the Lower each of which is functionally advantageous in terms Cretaceous location of Las Hoyas, Spain. These of initially providing insulation, and then finally lead-

402 THE EVOLUTION OF FEA THERS FROM DINOSAUR HAIR

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