Evolutionary origin of the feather epidermis

Abstract

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.

Topographical mapping of α- and β-keratins on developing chicken skin integuments: Functional interaction and evolutionary perspectives

“…The periderm is an embryonic epidermis layer that will be shed before hatching (1). Morphological and immunohistochemical studies showed that scale subperiderm may be homologous with feather barb and barbule cells (34)(35)(36)(37). The embryonic layers of scutate scales are shed at hatching, but their homologs may be retained in feathers (34)(35)(36), which remain to be investigated further.…”

“…Because avian scales seem to resemble reptilian scales and are also composed mainly of β-keratins, some scholars have proposed that they are homologous. Alternatively, the overlapping scales of birds have been proposed to develop later in evolution, being secondarily derived (34,35). Given the evidence of the four winged feathered dinosaurs (63), birds might have originally been entirely covered by feathers, except for the plantar surface of their feet, in which the feather formation program is blocked at its initiation step.…”

“…Given the evidence of the four winged feathered dinosaurs (63), birds might have originally been entirely covered by feathers, except for the plantar surface of their feet, in which the feather formation program is blocked at its initiation step. Studies on the avian embryonic cell lineage of feathers and scales and the reptilian lineage of scales suggest that these processes are homologous (34)(35)(36). These processes probably use conserved signaling modules in their common ancestors (34), but then modify the signaling modules to form different mature appendage phenotypes.…”

Cell interactions in barb ridges of developing chick downfeather and the origin of feather branching

“…Feathers derive from inductive mesenchymal-epidermal interactions in the embryonic skin that produce feather germs (Chuong & Widelitz 1999;Chuong et al 2003;Yu et al 2004); these elongate into feather filaments in which some cells keratinize due to accumulation of feather keratin (Matulionis 1970;Sawyer & Knapp 2003;Sawyer et al 2004). Barb ridges are formed within feather filaments and columns of cells are assembled to form barbules and barbs.…”

“…the outer periderm, inner periderm, subperiderm and basal layers, of the generalized avian epidermis (Sawyer et al 2004). The embryonic epidermis of birds and of their closest extant relatives, the crocodilians, consists of an outer periderm, an inner periderm, a subperidermal layer and a germinal layer (Sawyer et al 2000;Alibardi & Thompson 2001, 2002Sawyer & Knapp 2003).…”