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Dinosaur fossils possessing integumentary appendages of various morphologies, interpreted as feathers, have greatly enhanced our understanding of the evolutionary link between birds and dinosaurs, as well as the origins of feathers and avian flight. In extant birds, the unique expression and amino acid composition of proteins in mature feathers have been shown to determine their biomechanical properties, such as hardness, resilience, and plasticity. Here, we provide molecular and ultrastructural evidence that the pennaceous feathers of the Jurassic nonavian dinosaur Anchiornis were composed of both feather β-keratins and α-keratins. This is significant, because mature feathers in extant birds are dominated by β-keratins, particularly in the barbs and barbules forming the vane. We confirm here that feathers were modified at both molecular and morphological levels to obtain the biomechanical properties for flight during the dinosaur-bird transition, and we show that the patterns and timing of adaptive change at the molecular level can be directly addressed in exceptionally preserved fossils in deep time., Competing Interests: The authors declare no conflict of interest.

Gene co-expression network analysis has been a research method widely used in systematically exploring gene function and interaction. Using the Weighted Gene Co-expression Network Analysis (WGCNA) approach to construct a gene co-expression network using data from a customized 44K microarray transcriptome of chicken epidermal embryogenesis, we have identified two distinct modules that are highly correlated with scale or feather development traits. Signaling pathways related to feather development were enriched in the traditional KEGG pathway analysis and functional terms relating specifically to embryonic epidermal development were also enriched in the Gene Ontology analysis. Significant enrichment annotations were discovered from customized enrichment tools such as Modular Single-Set Enrichment Test (MSET) and Medical Subject Headings (MeSH). Hub genes in both trait-correlated modules showed strong specific functional enrichment toward epidermal development. Also, regulatory elements, such as transcription factors and miRNAs, were targeted in the significant enrichment result. This work highlights the advantage of this methodology for functional prediction of genes not previously associated with scale- and feather trait-related modules.

MicroRNAs (miRNAs) are small non-coding RNAs that regulate gene expression at the post-transcriptional level. Previous studies have shown that miRNA regulation contributes to a diverse set of processes including cellular differentiation and morphogenesis which leads to the creation of different cell types in multicellular organisms and is thus key to animal development. Feathers are one of the most distinctive features of extant birds and are important for multiple functions including flight, thermal regulation, and sexual selection. However, the role of miRNAs in feather development has been woefully understudied despite the identification of cell signaling pathways, cell adhesion molecules and structural genes involved in feather development. In this study, we performed a microarray experiment comparing the expression of miRNAs and mRNAs among three embryonic stages of development and two tissues (scutate scale and feather) of the chicken. We combined this expression data with miRNA target prediction tools and a curated list of feather related genes to produce a set of 19 miRNA-mRNA duplexes. These targeted mRNAs have been previously identified as important cell signaling and cell adhesion genes as well as structural genes involved in feather and scale morphogenesis. Interestingly, the miRNA target site of the cell signaling pathway gene, Aldehyde Dehydrogenase 1 Family, Member A3 (ALDH1A3), is unique to birds indicating a novel role in Aves. The identified miRNA target site of the cell adhesion gene, Tenascin C (TNC), is only found in specific chicken TNC splice variants that are differentially expressed in developing scutate scale and feather tissue indicating an important role of miRNA regulation in epidermal differentiation. Additionally, we found that β-keratins, a major structural component of avian and reptilian epidermal appendages, are targeted by multiple miRNA genes. In conclusion, our work provides quantitative expression data on miRNAs and mRNAs during feather and scale development and has produced a highly diverse, but manageable list of miRNA-mRNA duplexes for future validation experiments., (Copyright © 2016 Elsevier B.V. All rights reserved.)

The archosauria consist of two living groups, crocodilians, and birds. Here we compare the structure, expression, and phylogeny of the beta (β)-keratins in two crocodilian genomes and two avian genomes to gain a better understanding of the evolutionary origin of the feather β-keratins. Unlike squamates such as the green anole with 40 β-keratins in its genome, the chicken and zebra finch genomes have over 100 β-keratin genes in their genomes, while the American alligator has 20 β-keratin genes, and the saltwater crocodile has 21 β-keratin genes. The crocodilian β-keratins are similar to those of birds and these structural proteins have a central filament domain and N- and C-termini, which contribute to the matrix material between the twisted β-sheets, which form the 2-3 nm filament. Overall the expression of alligator β-keratin genes in the integument increases during development. Phylogenetic analysis demonstrates that a crocodilian β-keratin clade forms a monophyletic group with the avian scale and feather β-keratins, suggesting that avian scale and feather β-keratins along with a subset of crocodilian β-keratins evolved from a common ancestral gene/s. Overall, our analyses support the view that the epidermal appendages of basal archosaurs used a diverse array of β-keratins, which evolved into crocodilian and avian specific clades. In birds, the scale and feather subfamilies appear to have evolved independently in the avian lineage from a subset of archosaurian claw β-keratins. The expansion of the avian specific feather β-keratin genes accompanied the diversification of birds and the evolution of feathers., (Copyright © 2013 Wiley Periodicals, Inc.)

Feathers of today's birds are constructed of beta (β)-keratins, structural proteins of the epidermis that are found solely in reptiles and birds. Discoveries of "feathered dinosaurs" continue to stimulate interest in the evolutionary origin of feathers, but few studies have attempted to link the molecular evolution of their major structural proteins (β-keratins) to the appearance of feathers in the fossil record. Using molecular dating methods, we show that before the appearance of Anchiornis (∼155 Million years ago (Ma)) the basal β-keratins of birds began diverging from their archosaurian ancestor ∼216 Ma. However, the subfamily of feather β-keratins, as found in living birds, did not begin diverging until ∼143 Ma. Thus, the pennaceous feathers on Anchiornis, while being constructed of avian β-keratins, most likely did not contain the feather β-keratins found in the feathers of modern birds. Our results demonstrate that the evolutionary origin of feathers does not coincide with the molecular evolution of the feather β-keratins found in modern birds. More likely, during the Late Jurassic, the epidermal structures that appeared on organisms in the lineage leading to birds, including early forms of feathers, were constructed of avian β-keratins other than those found in the feathers of modern birds. Recent biophysical studies of the β-keratins in feathers support the view that the appearance of the subfamily of feather β-keratins altered the biophysical nature of the feather establishing its role in powered flight., (Copyright © 2011 Wiley Periodicals, Inc., A Wiley Company.)

Background: The epidermal appendages of reptiles and birds are constructed of beta (beta) keratins. The molecular phylogeny of these keratins is important to understanding the evolutionary origin of these appendages, especially feathers. Knowing that the crocodilian beta-keratin genes are closely related to those of birds, the published genomes of the chicken and zebra finch provide an opportunity not only to compare the genomic organization of their beta-keratins, but to study their molecular evolution in archosaurians., Results: The subfamilies (claw, feather, feather-like, and scale) of beta-keratin genes are clustered in the same 5' to 3' order on microchromosome 25 in chicken and zebra finch, although the number of claw and feather genes differs between the species. Molecular phylogenies show that the monophyletic scale genes are the basal group within birds and that the monophyletic avian claw genes form the basal group to all feather and feather-like genes. Both species have a number of feather clades on microchromosome 27 that form monophyletic groups. An additional monophyletic cluster of feather genes exist on macrochromosome 2 for each species. Expression sequence tag analysis for the chicken demonstrates that all feather beta-keratin clades are expressed., Conclusions: Similarity in the overall genomic organization of beta-keratins in Galliformes and Passeriformes suggests similar organization in all Neognathae birds, and perhaps in the ancestral lineages leading to modern birds, such as the paravian Anchiornis huxleyi. Phylogenetic analyses demonstrate that evolution of archosaurian epidermal appendages in the lineage leading to birds was accompanied by duplication and divergence of an ancestral beta-keratin gene cluster. As morphological diversification of epidermal appendages occurred and the beta-keratin multigene family expanded, novel beta-keratin genes were selected for novel functions within appendages such as feathers.

The formation of scales and feathers in reptiles and birds has fascinated biologists for decades. How might the developmental processes involved in the evolution of the amniote ectoderm be interpreted to shed light on the evolution of integumental appendages? An Evo-Devo approach to this question is proving essential to understand the observation that there is homology between the transient embryonic layers covering the scale epidermis of alligators and birds and the epidermal cell populations of embryonic feather filaments. Whereas the embryonic layers of scutate scales are sloughed off at hatching, that their homologues persist in feathers demonstrates that the predecessors of birds took advantage of the ability of their ectoderm to generate embryonic layers by recruiting them to make the epidermis of the embryonic feather filament. Furthermore, observations on mutant chickens with altered scale and feather development (Abbott and Asmundson [1957] J. Hered. 18:63-70; Abbott [1965] Poult. Sci. 44:1347; Abbott [1967] Methods in developmental biology. New York: Thomas Y. Crowell) suggest that the ectodermal placodes of feathers, which direct the formation of unique dermal condensations and subsequently appendage outgrowth, provided the mechanism by which the developmental processes generating the embryonic layers diverged during evolution to support the morphogenesis of the epidermis of the primitive feather filament with its barb ridges., (Copyright 2004 Wiley-Liss, Inc.)

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., (Copyright 2003 Wiley-Liss, Inc.)

The feathers of birds develop from embryonic epidermal lineages that differentiate during outgrowth of the feather germ. Independent cell populations also form an embryonic epidermis on scutate scales, which consists of peridermal layers, a subperiderm, and an alpha stratum. Using an antiserum (anti-FbetaK) developed to react specifically with the beta (beta) keratins of feathers, we find that the feather-type beta keratins are expressed in the subperiderm cells of embryonic scutate scales, as well as the barb ridge lineages of the feather. However, unlike the subperiderm of scales, which is lost at hatching, the cells of barb ridges, in conjunction with adjacent cell populations, give rise to the structural elements of the feather. The observation that an embryonic epidermis, consisting of peridermal and subperidermal layers, also characterizes alligator scales (Thompson, 2001. J Anat 198:265-282) suggests that the epidermal populations of the scales and feathers of avian embryos are homologous with those forming the embryonic epidermis of alligators. While the embryonic epidermal populations of archosaurian scales are discarded at hatching, those of the feather germ differentiate into the periderm, sheath, barb ridges, axial plates, barbules, and marginal plates of the embryonic feather filament. We propose that the development of the embryonic feather filament provides a model for the evolution of the first protofeather. Furthermore, we hypothesize that invagination of the epidermal lineages of the feather filament, namely the barb ridges, initiated the formation of the follicle, which then allowed continuous renewal of the feather epidermal lineages, and the evolution of diverse feather forms.

The evolution of a mechanically resilient epidermis was a key adaptation in the transition of amniotes to a fully terrestrial lifestyle. Skin appendages usually form via a specialized type of programmed cell death known as cornification which is characterized by the formation of an insoluble cornified envelope (CE). Many of the substrates of cornification are encoded by linked genes located at a conserved genetic locus known as the epidermal differentiation complex (EDC). Loricrin is the main protein component of the mammalian CE and is encoded for by a gene located within the EDC. Recently, genes resembling mammalian loricrin, along with several other proteins most likely involved in CE formation, have been identified within the EDC of birds and several reptiles. To better understand the evolution and function of loricrin in birds, we screened the genomes of 50 avian species and 3 crocodilians to characterize their EDC regions. We found that loricrin is present within the EDC of all species investigated, and that three loricrin genes were present in birds. Phylogenetic and molecular evolution analyses found evidence that gene deletions and duplications as well as concerted evolution has shaped the evolution of avian loricrins. Our results suggest a complex evolutionary history of avian loricrins which has accompanied the evolution of bird species with diverse morphologies and lifestyles. [ABSTRACT FROM AUTHOR]

Dinosaur fossils possessing integumentary appendages of various morphologies, interpreted as feathers, have greatly enhanced our understanding of the evolutionary link between birds and dinosaurs, as well as the origins of feathers and avian flight. In extant birds, the unique expression and amino acid composition of proteins in mature feathers have been shown to determine their biomechanical properties, such as hardness, resilience, and plasticity. Here, we provide molecular and ultrastructural evidence that the pennaceous feathers of the Jurassic nonavian dinosaur Anchiornis were composed of both feather β-keratins and α-keratins. This is significant, because mature feathers in extant birds are dominated by β-keratins, particularly in the barbs and barbules forming the vane. We confirm here that feathers were modified at both molecular and morphological levels to obtain the biomechanical properties for flight during the dinosaur-bird transition, and we show that the patterns and timing of adaptive change at the molecular level can be directly addressed in exceptionally preserved fossils in deep time. [ABSTRACT FROM AUTHOR]