A new scenario for the evolutionary origin of hair, feather, and avian scales

Abstract

In zoology it is well known that birds are characterized by the presence of feathers, and mammals by hairs. Another common point of view is that avian scales are directly related to reptilian scales. As a skin embryologist, I have been fascinated by the problem of regionalization of skin appendages in amniotes throughout my scientific life. Here I have collected the arguments that result from classical experimental embryology, from the modern molecular biology era, and from the recent discovery of new fossils. These arguments shape my view that avian ectoderm is primarily programmed toward forming feathers, and mammalian ectoderm toward forming hairs. The other ectoderm derivatives -scales in birds, glands in mammals, or cornea in both classes -can become feathers or hairs through metaplastic process, and appear to have a negative regulatory mechanism over this basic program. How this program is altered remains, in most part, to be determined. However, it is clear that the regulation of the Wnt/ beta-catenin pathway is a critical hub. The level of beta-catenin is crucial for feather and hair formation, as its down-regulation appears to be linked with the formation of avian scales in chick, and cutaneous glands in mice. Furthermore, its inhibition leads to the formation of nude skin and is required for that of corneal epithelium. Here I propose a new theory, to be further considered and tested when we have new information from genomic studies. With this theory, I suggest that the alpha-keratinized hairs from living synapsids may have evolved from the hypothetical glandular integument of the first amniotes, which may have presented similarities with common day terrestrial amphibians. Concerning feathers, they may have evolved independently of squamate scales, each originating from the hypothetical roughened beta-keratinized integument of the first sauropsids. The avian overlapping scales, which cover the feet in some bird species, may have developed later in evolution, being secondarily derived from feathers.

Experimental relationships between levels of corticosterone in plasma and feathers in a free-living bird

“…Similarly, skin secretions or external deposits on feathers cannot account for our results. Birds did not evolve a glandular skin as in mammals (Dhouailly, 2009), but it is possible that hormone manipulation in our experiment could have resulted in increased CORT in preen oil (waxes), which then would have been deposited on feathers and elevated CORT f . However, previous experimental work has ruled out external deposits as the source of CORT in feathers [see appendixS1 in Bortolotti et al (Bortolotti et al, 2008)], and preen oil from starlings did not contain detectable levels of CORT (Lattin et al, 2011).…”

“…Slominski, 2005;Slominski et al, 2007), to our knowledge no studies have provided evidence of local production of glucocorticoids in bird skin (Taves et al, 2011). Without such evidence, the extrapolation of findings in mammals to the situation in birds may not be warranted because hair and feathers evolved independently in lineages separated by over 300million years of evolution (Dhouailly, 2009). All birds in our study were handled similarly, with the exception of treatments, and all treatments were applied within each nest box.…”

Control of Hoxd gene transcription in the mammary bud by hijacking a preexisting regulatory landscape

“…7A). Hairs and feathers are other skinderived appendages whose early development shares similarities with MP induction and invagination (58)(59)(60)(61). Of note, they also express different Hox gene combinations (32)(33)(34)62).…”

p53/p63/p73 in the Epidermis in Health and Disease

“…The function of other isoforms of p53 and p73 in epidermal morphogenesis has not been as well studied, but they may also play different roles or form heterotetramers with the isoforms of p63, leading to various types of tetramers with varying transactivation ability that induce a certain complement of target genes depending on spatial and temporal cues. The process of skin development results in the formation of a stratified epidermis with selfrenewing ability and a number of skin appendages (hair follicles, nails, glands) (Blanpain and Fuchs 2009;Chuong and Richardson 2009;Dhouailly 2009). The p63 transcription factor serves as a master regulator of epidermal development and differentiation ( Fig.…”