Origin of archosaurian integumentary appendages: The bristles of the wild turkey beard express feather‐type β keratins

Sawyer, Roger H.; Washington, Lynette D.; Salvatore, Brian A.; Glenn, Travis C.; Knapp, Loren W.

doi:10.1002/jez.b.17

Cited by 31 publications

(26 citation statements)

References 68 publications

(55 reference statements)

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“…Observations on the scaleless (High-Line) (Abbott,'67;Brotman,'76;'77a,b) and ptilopody (Sawyer,'70) mutants and the proposal that scutate scale formation in birds involves feather inhibition (Tanaka et al,'87), support the view that the ancestor of modern birds had feathered hind limbs (Xu et al, 2003). Finally, our recent observations on the bristles of the wild turkey beard (Sawyer et al, 2003b) caution us not to assume that all the ''filamentous integumentary appendages'' associated with dinosaurs are homologues of modern feathers.…”

Section: Introductionmentioning

confidence: 56%

Avian skin development and the evolutionary origin of feathers

2003

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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.

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Section: Introductionmentioning

confidence: 56%

Avian skin development and the evolutionary origin of feathers

2003

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“…Is it a feather? This filamentous integument appendage may be considered to be one of the protofeathers (Sawyer et al, 2003b, also see Section 3 for the definition of true feathers).…”

Section: Turkey Beardmentioning

confidence: 99%

Evo-Devo of amniote integuments and appendages.

Wu¹,

Hou²,

Plikus³

et al. 2004

Int. J. Dev. Biol.

190

186

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Integuments form the boundary between an organism and the environment. The evolution of novel developmental mechanisms in integuments and appendages allows animals to live in diverse ecological environments. Here we focus on amniotes. The major achievement for reptile skin is an adaptation to the land with the formation of a successful barrier. The stratum corneum enables this barrier to prevent water loss from the skin and allowed amphibian / reptile ancestors to go onto the land. Overlapping scales and production of β-keratins provide strong protection. Epidermal invagination led to the formation of avian feather and mammalian hair follicles in the dermis. Both adopted a proximal -distal growth mode which maintains endothermy. Feathers form hierarchical branches which produce the vane that makes flight possible. Recent discoveries of feathered dinosaurs in China inspire new thinking on the origin of feathers. In the laboratory, epithelial -mesenchymal recombinations and molecular mis-expressions were carried out to test the plasticity of epithelial organ formation. We review the work on the transformation of scales into feathers, conversion between barbs and rachis and the production of "chicken teeth". In mammals, tilting the balance of the BMP pathway in K14 noggin transgenic mice alters the number, size and phenotypes of different ectodermal organs, making investigators rethink the distinction between morpho-regulation and pathological changes. Models on the evolution of feathers and hairs from reptile integuments are discussed. A hypothetical Evo-Devo space where diverse integument appendages can be placed according to complex phenotypes and novel developmental mechanisms is presented.

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“…These bristle-liked structures are much longer and thicker than the proto-feathers in Sinosauropteryx and Sinornithosaurus, and were interpreted as cylindrical and possibly tubular epidermal structures. As it is cylindrical, a character considered very important in the first step of feather evolution (Prum and Brush, 2002), should we consider it as an early proto-feather, or as a modified feather like bristle on modern birds, or similar to the bristle of the beard in wild turkeys (Sawyer et al, 2003b)? On the other hand, they may not be homologous to those integument appendages on the theropods.…”

Section: Feathered Dinosaurs?mentioning

confidence: 99%

“…Turkey beard bristles are distinct structures from feathers, although they express feather type beta keratin and show simple branching patterns (Sawyer et al, 2003b). These appendages are hollow at the distal end, and the branching may be due to partial separation (Lucas and Stettenheim, 1972).…”

Section: Feathered Dinosaurs?mentioning

confidence: 99%

“…We can also evaluate unusual integument appendages today with these criteria. For example, turkey beard bristles grow continuously from finger-like outgrowths but do not assume the localized growth mode from the proximal to the distal end seen in feathers even though they show simple branching and express feather-type beta keratins (Sawyer et al, 2003b). Using the criteria in Table 1, turkey beard bristles would not be classified as feathers.…”

Section: Developmental Biology Of the Feathermentioning

confidence: 99%

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Adaptation to the sky: Defining the feather with integument fossils from mesozoic China and experimental evidence from molecular laboratories

Chuong

Zhang

et al. 2003

J Exp Zool Pt B

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In this special issue of Evo-Devo of the amniote integument, Alibardi has discussed the adaptation of the integument to the land. Here we will discuss the adaptation to the sky. We first review a series of fossil discoveries representing intermediate forms of feathers or feather-like appendages from dinosaurs and Mesozoic birds from the Jehol Biota of China. We then discuss results from the molecular and developmental biological experiments using chicken integument as the model. Feather forms can be modulated using retrovirus mediated gene mis-expression that mimics those found in nature today and in the evolutionary past. The molecular conversions among different types of integument appendages (feather, scale, tooth) are discussed. From these evidences, we recognize that not all organisms with feathers are birds, and that not all skin appendages with hierarchical branches are feathers. We develop a set of criteria for true avian feathers: 1) possessing actively proliferating cells in the proximal follicle for a proximo -distal growth mode; 2) forming hierarchical branches of rachis, barbs and barbules, with barbs shaped by differential cell death into either bilaterally or radially symmetric structures; 3) having a follicle structure, with a mesenchyme core during development; 4) maturing into a structure consisting of epithelia without a mesenchyme core with two sides of the vane facing the previous basal and supra-basal layer, respectively; and 5) having stem cells and dermal papilla in the follicle and hence the ability to molt and regenerate. A model of feather evolution from feather bud → barbs → barbules → rachis is presented, which is opposite to the old view of scale plate → rachis → barbs → barbules.

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Origin of archosaurian integumentary appendages: The bristles of the wild turkey beard express feather‐type β keratins

Cited by 31 publications

References 68 publications

Avian skin development and the evolutionary origin of feathers

Avian skin development and the evolutionary origin of feathers

Evo-Devo of amniote integuments and appendages.

Adaptation to the sky: Defining the feather with integument fossils from mesozoic China and experimental evidence from molecular laboratories

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