Research

Remarkable fossils of theropod dinosaurs displaying a wide range of epidermal structures (Fucheng et al., 2006; Ortega et al., 2010) have been discovered in the past two decades. The "four-winged" theropod, Anchiornis huxleyi (dated ~155 Million years ago [Ma]) shows that extensive feathering including pennaceous wing and leg feathers was present by the early Late Jurassic (Hu et al., 2009), implying that the evolutionary origin of feathers occurred before this time.

The epidermal appendages of extant reptiles and birds, such as scales, claws and feathers, are constructed of beta (β) keratin, a unique fibrous protein, in which a filament-matrix structure is formed by each single β-keratin molecule, unlike the situation in mammalian epidermal appendages where alpha (α) keratin molecules interact with distinct matrix molecules to form cornified appendages, such as hair (see Fraser and Parry, 2008, 2010). The amino acid sequence (31-32 residues) of the central filament region of β-keratins is highly conserved throughout all reptiles and birds suggesting that this domain has changed little in ~285 Ma of evolution (Fraser and Parry, 2010).

In birds, the β-keratin multigene family has diverged into four major subfamilies, scale, claw, feather-like, and feather (Presland et al., '89 a, b). As the genomes of birds become available (i.e., chicken, turkey, and zebra finch), comparative studies of the genomic organization of the β keratin subfamilies provide information on how the genotype influences phenotype (Greenwold and Sawyer, 2010).

Furthermore, phylogenetic analyses of the avian β-keratin genes from the chicken and zebra finch genomes have shown that the avian scale β-keratin subfamily is closely related to the β-keratins of crocodilians and basal to the claw β-keratin subfamily, which is basal to the feather-like and feather β-keratin subfamilies (Greenwold and Sawyer, 2010).

Presently we are using molecular dating approaches, such as BEAST, to gain a better understanding of the how the molecular evolution of the avian β-keratins relates to the evolutionary origin of feathers. Our approach is to combine molecular dating techniques with knowledge of the sauropsid fossil record, feather development, molecular evolution of the avian β-keratins, and the biophysical properties of feathers to gain a better understanding of feather evolution.

Greenwold and Sawyer (2011) demonstrate that the basal β-keratins of birds began diverging from their archosaurian ancestor ~216 million years ago, while the subfamily of feather β-keratins, as found in living birds, began diverging ~143 million years ago. Thus the evolutionary origin of feathers does not coincide with the molecular evolution of feather β-keratins found in modern birds. Recent biophysical studies of the β-keratins in today's 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.

Publications

Bao, W., Greenwald, M. J., Sawyer, R. H., 2016. Expressed miRNAs target feather related mRNAs involved in cell signaling, cell adhesion and structure during chicken epidermal development. Gene 591: 393-402

Zhang, G., et al., 2014. Comparative genomics reveals insights into avian genome evolution and adaptation. Science 346:1311

Greenwold, M.J., Bao, W., Jarvis, E., Hu, H., Gilbert, M.T.P., Zhang, G. and Sawyer, R.H. 2014. Dynamic evolution of the alpha and beta keratins has accompanied integument diversification and the adaptation of birds into novel lifestyles. BMC Evolutionary Biology 14:249 (selected as Editor's Choice)

Greenwold MJ, Sawyer RH. 2013. Molecular evolution and expression of
archosaurian b‐keratins: Diversification and expansion of archosaurian β‐keratins and the origin of feather β‐keratins. J. Exp. Zool. (Mol. Dev. Evol.) 320B:393–405.

John A. St. John et al. 2012. Sequencing three crocodilian genomes to illuminate the evolution of archosaurs and amniotes.

Matthew J. Greenwold and Roger H. Sawyer. 2011. Linking the molecular evolution of avian beta keratins to the evolution of feathers. J. Exp. Zool (Mol. Dev. Evol.) 316B: 609-616. [Link]

Matthew J. Greenwold and Roger H. Sawyer. 2010. Genomic organization and molecular phylogenies of the beta keratin multigene family in the chicken (Gallus gallus) and zebra finch (Taeniopygia guttata): implications for feather evolution. BMC Evolutionary Biology. 10:148. BMC Evolutionary Biology 2010, 10:148

Glenn,T.C.,French,J.O.,Heincelman,T.J.,Jones,K.L.,Sawyer,R.H. 2008. Evolutionary relationships among copies of feather beta (β) keratin genes from several avian orders: Integrative and Comparative Biology, 48(4):463-475. [Link]

Alibardi, L. and R.H. Sawyer. 2006. Cell structure of developing down feathers in the zebra finch with emphasis on barb ridge morphogenesis: J. Anat., 208, 621-642. [Link]

Alibardi, L., LW. Knapp, R.H. Sawyer. 2006. Beta-keratin localization in developing alligator scales and feathers in relation to the development and evolution of feathers. J. Submicrosc. Cytol. Pathol., 38 (2-3), 175-192. [Link]

Sawyer, R.H., T.C. Glenn, J.O. French and L.W. Knapp. 2005. Developing Antibodies to Synthetic Peptides Based on Comparative DNA sequencing of Multigene Families, in Methods in Enzymology, Molecular Evolution: Producing the Biochemical Data, Part B, Vol. 395. E.A. Zimmer and E.H. Roalson (eds.), Academic Press, San Diego. pp. 636-652. [Link]

Sawyer, R.H., L. Rogers, L. Washington, T.C. Glenn and L.W. Knapp. 2005. The Evolutionary Origin of the Feather Epidermis. Developmental Dynamics. 232:256-267. [Link]

Sawyer, R.H. and L.W. Knapp. 2003. Avian Skin Development and the Evolutionary origin of feathers.  J. Exp. Zool. (Mol. Dev. Evol.) 298B:57-72. [Link]