Avian skin development and the evolutionary origin of feathers

The discovery of several dinosaurs with filamentous integumentary appendages of different morphologies has stimulated models for the evolutionary origin of feathers. In order to understand these models, knowledge of the development of the avian integument must be put into an evolutionary context. Thus, we present a review of avian scale and feather development, which summarizes the morphogenetic events involved, as well as the expression of the beta (beta) keratin multigene family that characterizes the epidermal appendages of reptiles and birds. First we review information on the evolution of the ectodermal epidermis and its beta (beta) keratins. Then we examine the morphogenesis of scutate scales and feathers including studies in which the extraembryonic ectoderm of the chorion is used to examine dermal induction. We also present studies on the scaleless (sc) mutant, and, because of the recent discovery of "four-winged" dinosaurs, we review earlier studies of a chicken strain, Silkie, that expresses ptilopody (pti), "feathered feet." We conclude that the ability of the ectodermal epidermis to generate discrete cell populations capable of forming functional structural elements consisting of specific members of the beta keratin multigene family was a plesiomorphic feature of the archosaurian ancestor of crocodilians and birds. Evidence suggests that the discrete epidermal lineages that make up the embryonic feather filament of extant birds are homologous with similar embryonic lineages of the developing scutate scales of birds and the scales of alligators. We believe that the early expression of conserved signaling modules in the embryonic skin of the avian ancestor led to the early morphogenesis of the embryonic feather filament, with its periderm, sheath, and barb ridge lineages forming the first protofeather. Invagination of the epidermis of the protofeather led to formation of the follicle providing for feather renewal and diversification. The observations that scale formation in birds involves an inhibition of feather formation coupled with observations on the feathered feet of the scaleless (High-line) and Silkie strains support the view that the ancestor of modern birds may have had feathered hind limbs similar to those recently discovered in nonavian dromaeosaurids. And finally, our recent observation on the bristles of the wild turkey beard raises the possibility that similar integumentary appendages may have adorned nonavian dinosaurs, and thus all filamentous integumentary appendages may not be homologous to modern feathers.     

Structure and homology of Psittacosaurus tail bristles

We examined bristle‐like appendages on the tail of the Early Cretaceous basal ceratopsian dinosaur Psittacosaurus with laser‐stimulated fluorescence imaging. Our study reveals previously unknown details of these structures and confirms their identification as integumentary appendages. For the first time, we show that most bristles appear to be arranged in bundles and that they exhibit a pulp that widens towards the bristle base. We consider it likely that the psittacosaur bristles are structurally and developmentally homologous to similar filamentous appendages of other dinosaurs, namely the basal heterodontosaurid Tianyulong and the basal therizinosauroid theropod Beipiaosaurus, and attribute the greater robustness of the bristles of Psittacosaurus to a higher degree of cornification and calcification of its integument (both skin and bristles). Although the psittacosaur bristles are probably homologous with avian feathers in their origin from discrete cell populations, it is uncertain whether they developed from a follicle, one of the developmental hallmarks of true feathers. In particular, we note a striking resemblance between the psittacosaur bristles and the cornified spine on the head of the horned screamer, Anhima cornuta, an extant anseriform bird. Similar, albeit thinner keratinous filaments of extant birds are the ‘beard’ of the turkey, Meleagris gallopavo, and the crown of the Congo peafowl, Afropavo congensis. All of these structures of extant birds are distinct from true feathers, and because at least the turkey beard does not develop from follicles, detailed future studies of their development would be invaluable towards deepening our understanding of dinosaur filamentous integumentary structures.     

Evolution of dinosaur epidermal structures

Spectacularly preserved non-avian dinosaurs with integumentary filaments/feathers have revolutionized dinosaur studies and fostered the suggestion that the dinosaur common ancestor possessed complex integumentary structures homologous to feathers. This hypothesis has major implications for interpreting dinosaur biology, but has not been tested rigorously. Using a comprehensive database of dinosaur skin traces, we apply maximum-likelihood methods to reconstruct the phylogenetic distribution of epidermal structures and interpret their evolutionary history. Most of these analyses find no compelling evidence for the appearance of protofeathers in the dinosaur common ancestor and scales are usually recovered as the plesiomorphic state, but results are sensitive to the outgroup condition in pterosaurs. Rare occurrences of ornithischian filamentous integument might represent independent acquisitions of novel epidermal structures that are not homologous with theropod feathers.     

从新的古生物学及今生物学资料看羽毛的起源与早期演化(英文)

近年来关于羽毛和羽状皮肤衍生物的研究极大促进了我们对羽毛起源与早期演化的理解。结合最新的古生物学与今生物学资料,对一些保存了皮肤衍生物的非鸟恐龙标本进行观察研究,为这个重要的进化问题提供了新见解。推测羽毛的演化在鸟类起源之前就以下列顺序完成了5个主要的形态发生事件:1)丝状和管状结构的出现;2)羽囊及羽枝脊形成;3)羽轴的发生;4)羽平面的形成;5)羽状羽小支的产生。这些演化事件形成了多种曾存在于各类非鸟初龙类中的羽毛形态,但这些形态在鸟类演化过程中可能退化或丢失了;这些演化事件也产生了一些近似现代羽毛或者与现代羽毛完全相同的羽毛形态。非鸟恐龙身上的羽毛有一些现代羽毛具有的独特特征,但也有一些现生鸟羽没有的特征。尽管一些基于发育学资料建立的有关鸟类羽毛起源和早期演化的模型推测羽毛的起源是一个全新的演化事件,与爬行动物的鳞片无关,我们认为用来定义现代鸟羽的特征应该是逐步演化产生的,而不是突然出现。因此,对于羽毛演化而言,一个兼具逐步变化与完全创新的模型较为合理。从目前的证据推断,最早的羽毛既不是用来飞行也不是用来保暖,各种其他假说皆有可能,其中包括展示或者散热假说。展开整合性的研究有望为羽毛的起源问题提供更多思路。     

Hox genes as synchronized temporal regulators: implications for morphological innovation

This special issue on the development and evolution of the amniote integument begins with a discussion of the adaptations to terrestrial conditions, the acquisition of water-impermeability of the reptilian integument, and the initial formation of filamentous integumentary appendages that prepare the way towards avian flight. Recent feather fossils are reviewed, and a definition of feathers is developed. Hierarchical models are proposed for the formation of complex structures, such as feathers. Molecular signals that alter the phenotype of integumentary appendages at different levels of the hierarchy are presented. Tissue interactions and the roles of keratins in evolution are discussed and linked to their bio-mechanical properties. The role of mechanical forces on patterning is explored. Elaborate extant feather variants are introduced. The regeneration/gene mis-expression protocol for the chicken feather is established as a testable model for the study of biological structures. The adaptations of the mammalian distal limb end organs to terrestrial, arboreal and aquatic conditions are discussed. The development and cycling of hair are reviewed from a molecular perspective. These contributions reveal that the structure and function of diverse integumentary appendages are variations that are superimposed on a common theme, and that their formation is modular, hierarchical and cyclical. They further reveal that these mechanisms can be understood at the molecular level, and that an integrative and organismal approach to studying integumentary appendages is called for. We propose that future research should foster interdisciplinary approaches, pursue understanding at the cellular and molecular level, analyze interactions between the environment and genome, and recognize the contributions of variation in morphogenesis and evolution.     

When did theropods become feathered?--evidence for pre-Archaeopteryx feathery appendages

Filamentous impressions associated with locomotive theropod tracks in the Lower Jurassic Turners Falls Formation of western Massachusetts, U.S.A. represent the oldest evidence of feathered dinosaurs. Feather impressions are preserved with sitting traces which bear integumentary structures along the outlines of the pre-pubic and ischiadic impressions. Extant palaeognathous down feathers provide a valuable comparative model for these filamentous integumental structures and for similar structures described in Chinese theropods from younger deposits. The described morphologies are congruent with Stage II of Prum ('99) and support that plumulaceous morphologies evolved before the origin of the rhachis and the planar vane. Appearance of feathery appendages in theropods may be linked to evolution of higher metabolic rates, improved locomotory abilities, and/or distinct behavior(s) and visual communication. Development of feathery integument might have also played a crucial role in the competitiveness and successful radiation of maniraptoriform theropods and their actively flying descendants in the Jurassic.     

The colour of fossil feathers

Feathers are complex integumentary appendages of birds and some other theropod dinosaurs. They are frequently coloured and function in camouflage and display. Previous investigations have concluded that fossil feathers are preserved as carbonized traces composed of feather-degrading bacteria. Here, an investigation of a colour-banded feather from the Lower Cretaceous Crato Formation of Brazil revealed that the dark bands are preserved as elongate, oblate carbonaceous bodies 1-2mum long, whereas the light bands retain only relief traces on the rock matrix. Energy dispersive X-ray analysis showed that the dark bands preserve a substantial amount of carbon, whereas the light bands show no carbon residue. Comparison of these oblate fossil bodies with the structure of black feathers from a living bird indicates that they are the eumelanin-containing melanosomes. We conclude that most fossil feathers are preserved as melanosomes, and that the distribution of these structures in fossil feathers can preserve the colour pattern in the original feather. The discovery of preserved melanosomes opens up the possibility of interpreting the colour of extinct birds and other dinosaurs.     

Dinosaur protofeathers: pushing back the origin of feathers into the Middle Triassic?

Reports of primordial feathers (protofeathers) in dinosaurs have received widespread interest. Recently, it was proposed that a novel protofeather in the theropod dinosaur Beipiaosaurus completes the transitional series in the evolution of the feather and provides the first evidence of filamentous feathers as display in nonavian theropods. A more far-reaching evolutionary ramification is the claim that these structures push the origin of monofilamentous integumentary structures into the Middle Triassic or earlier. I discuss problems with the analyses within the broader context of studies concerning the hypothesis of protofeathers, and show that affinity between the integumentary structures in Beipiaosaurus and feathers is improbable. The scientific methodology is questioned by its failure to make phenomena perceivable by objective means, by questionable rationalizations in critical issues, and by lack of consideration of exceptions to the postulated thesis. The notion that primordial feathers occurred in a clade more inclusive than the Coelurosauria and that it is supported by the presence of integumental structures in Psittacosaurus is analyzed and rejected.     

Integument structure in ornithischian dinosaurs (Hypsilophodontia,Ornithopoda) from the Late Jurassic of Transbaikalia

Integumentary structures of ornithischain dinosaurs of the taxon Hypsilophodontia (Ornithopoda) from the Ukureiskaya Formation (Upper Jurassic) of the Kulinda locality (Transbaikal Region, Russia) are described in detail. It is shown that members of this group had so-called bristle scales, integumentary appendages previously unknown in ornithischian dinosaurs. These are relatively small horn plates embedded in the skin, the distal margin of which has several long, flat, and probably constantly growing bristles. The monobristle variant of bristle scale is probably homologous to the protofeather of theropods; if this is the case, it is possible to reconstruct the protofeather as an elongated and constantly growing scale.     

On the purported presence of fossilized collagen fibres in an ichthyosaur and a theropod dinosaur

Since the discovery of exceptionally preserved theropod dinosaurs with soft tissues in China in the 1990s, there has been much debate about the nature of filamentous structures observed in some specimens. Sinosauropteryx was the first non‐avian theropod to be described with these structures, and remains one of the most studied examples. Despite a general consensus that the structures represent feathers or feather homologues, a few identify them as degraded collagen fibres derived from the skin. This latter view has been based on observations of low‐quality images of Sinosauropteryx, as well as the suggestion that because superficially similar structures are seen in Jurassic ichthyosaurs they cannot represent feathers. Here, we highlight issues with the evidence put forward in support of this view, showing that integumentary structures have been misinterpreted based on sedimentary features and preparation marks, and that these errors have led to incorrect conclusions being drawn about the existence of collagen in Sinosauropteryx and the ichthyosaur Stenopterygius. We find that there is no evidence to support the idea that the integumentary structures seen in the two taxa are collagen fibres, and confirm that the most parsimonious interpretation of fossilized structures that look like feather homologues in Sinosauropteryx is that they are indeed the remains of feather homologues.     

Bristles before down: A new perspective on the functional origin of feathers

Over the course of the last two decades, the understanding of the early evolution of feathers in nonavian dinosaurs has been revolutionized. It is now recognized that early feathers had a simple form comparable in general structure to the hairs of mammals. Insight into the prevalence of simple feathers throughout the dinosaur family tree has gradually arisen in tandem with the growing evidence for endothermic dinosaur metabolisms. This has led to the generally accepted opinion that the early feather coats of dinosaurs functioned as thermo insulation. However, thermo insulation is often erroneously stated to be a likely functional explanation for the origin of feathers. The problem with this explanation is that, like mammalian hair, simple feathers could serve as insulation only when present in sufficiently high concentrations. The theory therefore necessitates the origination of feathers en masse. We advocate for a novel origin theory of feathers as bristles. Bristles are facial feathers common among modern birds that function like mammalian tactile whiskers, and are frequently simple and hair‐like in form. Bristles serve their role in low concentrations, and therefore offer a feasible first stage in feather evolution.     

被视为恐龙的鸟

尽管于 2 0世纪 2 0年代在亚洲地表层首次发现长有羽毛的恐龙和著名的“龙骨突位点” ,关于鸟类起源的争论仍没有休止。来自化石的证据表明 ,鸟类在进化分支上应归于兽脚类的特殊分支。本文主要阐明完好无损的化石揭示的鸟和非鸟类恐龙的亲密关系和鸟类羽毛及鸟类出现以前的羽毛的起源证据 ,分析体型缩小对飞行进化的重要意义及从新的角度论述鸟类如何飞上了天     

The early evolution of feathers: fossil evidence from Cretaceous amber of France

The developmental stages of feathers are of major importance in the evolution of body covering and the origin of avian flight. Until now, there were significant gaps in knowledge of early morphologies in theoretical stages of feathers as well as in palaeontological material. Here we report fossil evidence of an intermediate and critical stage in the incremental evolution of feathers which has been predicted by developmental theories but hitherto undocumented by evidence from both the recent and the fossil records. Seven feathers have been found in an Early Cretaceous (Late Albian, ca 100 Myr) amber of western France, which display a flattened shaft composed by the still distinct and incompletely fused bases of the barbs forming two irregular vanes. Considering their remarkably primitive features, and since recent discoveries have yielded feathers of modern type in some derived theropod dinosaurs, the Albian feathers from France might have been derived either from an early bird or from a non-avian dinosaur.     

Avian-like breathing mechanics in maniraptoran dinosaurs

In 1868 Thomas Huxley first proposed that dinosaurs were the direct ancestors of birds and subsequent analyses have identified a suite of 'avian' characteristics in theropod dinosaurs. Ossified uncinate processes are found in most species of extant birds and also occur in extinct non-avian maniraptoran dinosaurs. Their presence in these dinosaurs represents another morphological character linking them to Aves, and further supports the presence of an avian-like air-sac respiratory system in theropod dinosaurs, prior to the evolution of flight. Here we report a phylogenetic analysis of the presence of uncinate processes in Aves and non-avian maniraptoran dinosaurs indicating that these were homologous structures. Furthermore, recent work on Canada geese has demonstrated that uncinate processes are integral to the mechanics of avian ventilation, facilitating both inspiration and expiration. In extant birds, uncinate processes function to increase the mechanical advantage for movements of the ribs and sternum during respiration. Our study presents a mechanism whereby uncinate processes, in conjunction with lateral and ventral movements of the sternum and gastral basket, affected avian-like breathing mechanics in extinct non-avian maniraptoran dinosaurs.     

The evolutionary origin and diversification of feathers

Progress on the evolutionary origin and diversification of feathers has been hampered by conceptual problems and by the lack of plesiomorphic feather fossils. Recently, both of these limitations have been overcome by the proposal of the developmental theory of the origin of feathers, and the discovery of primitive feather fossils on nonavian theropod dinosaurs. The conceptual problems of previous theories of the origin of feathers are reviewed, and the alternative developmental theory is presented and discussed. The developmental theory proposes that feathers evolved through a series of evolutionary novelties in developmental mechanisms of the follicle and feather germ. The discovery of primitive and derived fossil feathers on a diversity of coelurosaurian theropod dinosaurs documents that feathers evolved and diversified in nonavian theropods before the origin of birds and before the origin of flight. The morphologies of these primitive feathers are congruent with the predictions of the developmental theory. Alternatives to the theropod origin of feathers are critique and rejected. Hypotheses for the initial function of feathers are reviewed. The aerodynamic theory of feather origins is falsified, but many other functions remain developmentally and phylogenetically plausible. Whatever their function, feathers evolved by selection for a follicle that would grow an emergent tubular appendage. Feathers are inherently tubular structures. The homology of feathers and scales is weakly supported. Feathers are composed of a suite of evolutionary novelties that evolved by the duplication, hierarchical organization, interaction, dissociation, and differentiation of morphological modules. The unique capacity for modular subdivision of the tubular feather follicle and germ has fostered the evolution of numerous innovations that characterize feathers. The evolution of feather keratin and the molecular basis of feather development are also discussed.     

Sauropod dinosaurs evolved moderately sized genomes unrelated to body size

Sauropodomorph dinosaurs include the largest land animals to have ever lived, some reaching up to 10 times the mass of an African elephant. Despite their status defining the upper range for body size in land animals, it remains unknown whether sauropodomorphs evolved larger-sized genomes than non-avian theropods, their sister taxon, or whether a relationship exists between genome size and body size in dinosaurs, two questions critical for understanding broad patterns of genome evolution in dinosaurs. Here we report inferences of genome size for 10 sauropodomorph taxa. The estimates are derived from a Bayesian phylogenetic generalized least squares approach that generates posterior distributions of regression models relating genome size to osteocyte lacunae volume in extant tetrapods. We estimate that the average genome size of sauropodomorphs was 2.02 pg (range of species means: 1.77–2.21 pg), a value in the upper range of extant birds (mean = 1.42 pg, range: 0.97–2.16 pg) and near the average for extant non-avian reptiles (mean = 2.24 pg, range: 1.05–5.44 pg). The results suggest that the variation in size and architecture of genomes in extinct dinosaurs was lower than the variation found in mammals. A substantial difference in genome size separates the two major clades within dinosaurs, Ornithischia (large genomes) and Saurischia (moderate to small genomes). We find no relationship between body size and estimated genome size in extinct dinosaurs, which suggests that neutral forces did not dominate the evolution of genome size in this group.     

Growth patterns in brooding dinosaurs reveals the timing of sexual maturity in non-avian dinosaurs and genesis of the avian condition

The timing of sexual maturation in non-avian dinosaurs is not known. In extant squamates and crocodilians it occurs in conjunction with the initial slowing of growth rates as adult size is approached. In birds (living dinosaurs) on the other hand, reproductive activity begins well after somatic maturity. Here we used growth line counts and spacing in all of the known brooding non-avian dinosaurs to determine the stages of development when they perished. It was revealed that sexual maturation occurred well before full adult size was reached-the primitive reptilian condition. In this sense, the life history and physiology of non-avian dinosaurs was not like that of modern birds. Palaeobiological ramifications of these findings include the potential to deduce reproductive lifespan, fecundity and reproductive population sizes in non-avian dinosaurs, as well as aid in the identification of secondary sexual characteristics.     

Recent advances in amniote palaeocolour reconstruction and a framework for future research

Preserved melanin pigments have been discovered in fossilised integumentary appendages of several amniote lineages (fishes, frogs, snakes, marine reptiles, non‐avialan dinosaurs, birds, and mammals) excavated from lagerstätten across the globe. Melanisation is a leading factor in organic integument preservation in these fossils. Melanin in extant vertebrates is typically stored in rod‐ to sphere‐shaped, lysosome‐derived, membrane‐bound vesicles called melanosomes. Black, dark brown, and grey colours are produced by eumelanin, and reddish‐brown colours are produced by phaeomelanin. Specific morphotypes and nanostructural arrangements of melanosomes and their relation to the keratin matrix in integumentary appendages create the so‐called 'structural colours'. Reconstruction of colour patterns in ancient animals has opened an exciting new avenue for studying their life, behaviour and ecology. Modern relationships between the shape, arrangement, and size of avian melanosomes, melanin chemistry, and feather colour have been applied to reconstruct the hues and colour patterns of isolated feathers and plumages of the dinosaurs Anchiornis, Sinosauropteryx, and Microraptor in seminal papers that initiated the field of palaeocolour reconstruction. Since then, further research has identified countershading camouflage patterns, and informed subsequent predictions on the ecology and behaviour of these extinct animals. However, palaeocolour reconstruction remains a nascent field, and current approaches have considerable potential for further refinement, standardisation, and expansion. This includes detailed study of non‐melanic pigments that might be preserved in fossilised integuments. A common issue among existing palaeocolour studies is the lack of contextualisation of different lines of evidence and the wide variety of techniques currently employed. To that end, this review focused on fossil amniotes: (i) produces an overarching framework that appropriately reconstructs palaeocolour by accounting for the chemical signatures of various pigments, morphology and local arrangement of pigment‐bearing vesicles, pigment concentration, macroscopic colour patterns, and taphonomy; (ii) provides background context for the evolution of colour‐producing mechanisms; and (iii) encourages future efforts in palaeocolour reconstructions particularly of less‐studied groups such as non‐dinosaur archosaurs and non‐archosaur amniotes.