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.

Fig. 1

The formation and regionalization of the dense dermis. (A,A′) In the chick Ottawa naked mutant (OT/OT), a dorsal view at E10 shows that most part of the skin stays glabrous (A); a transversal section at E7 shows that most parts of the mesenchyme remain loose over the neural tube (A′). Compare with the formation of feather primordia and of a dense dermis formation in a wild type embryo (WT/WT) at the same stages (B,B′). After Olivera-Martinez et al. 2004b. Reproduced with permission of Int J Dev Biol. (C) Production of an ectopic feathered skin in the chick amnion at E14, following the graft of aggregate of Shh- and Noggin-producing cells under the ectoderm at E2 in the extra-embryonic area. After Fliniaux et al. 2004a. Reproduced with permission of the Company of Biologists. (D) Production of a skin with a pluristratified epidermis and three stage 3 hair pegs by a graft under the kidney capsule of mouse amnion associated to a mixed clump of Noggin- and Shh-producing cells. After Fliniaux et al. 2004b. Reproduced with permission of Differentiation. (E–H) The chick scaleless mutant forms a skin that comprises a dense dermis and that has potential regional characteristics which can be revealed by FGF2 treatment (tmt, tarsometatarsus; mva, midventral apterium). The white arrowhead in (F) shows the FGF2 beads, and in (H) the midventral line. After Prin & Dhouailly, 2004. Reproduced with permission of Int J Dev Biol. a, apterium; dd, dense dermis; ec, ectoderm; ep, epidermis; f, feather; fpr, feather primordial; g, glabrous; h, hair bud; me, mesenchyme; r, reticula; s, scuta; u, umbilical chord. Bars: A–C: 1 mm, A′,B′: 400 µm, D: 150 µm, E–H: 200 µm.

Fig. 3

Scale-feather metaplasia. (A,B′) Chick skin morphogenesis at 18 days and Shh expression at 12 days in control (A,A′) and retinoic acid-treated (B,B′) embryos. After retinoic acid treatment, overlapping scutate scales in the control are replaced upon by feathered scuta at 10 and 11 days. The expression of Shh, which is at a low level at the distal tip of the scuta, is up-regulated in two or three spots (arrowheads) of the scuta distal tip. After Prin & Dhouailly, 2004. Reproduced with permission of Int J Dev Biol. (C,D) The over-expression of beta-catenin results not only in the formation of supernumerary small buds in the feather fields (C), but also in scale-feather metaplasia (D). (C) After Noramly et al. 1999. Reproduced with permission of the Company of Biologists. (D) After Widelitz et al. 2000. Reproduced with permission of the Company of Biologists. f, feather; s, scuta. Bars: A,B: 1mm A′,B′,D: 200 µm, C: 250 µm.

Fig. 2

Four-winged birds, today and yesterday. (A) The Peking Bantam chick epidermis expresses its feather program on the dorsal IV digit and tarsometatarsus of the foot. Téléoptile feathers, which had appeared concomitantly with the wing remiges 7 days after hatching, display at 3 weeks a remex-type and not a simple covert-type. After Prin & Dhouailly 2004. Reproduced with permission of Int J Dev Biol. (B) The well-preserved remex-type feathers at the distal hindlimb position (on tarsometatarsus) of the four-winged dinosaur Microraptor gui, the most interesting discovery among the feathered dinosaurs. After Xu et al. 2003. Reproduced with permission of the Company of Biologists. Bars: A: 5 mm, B: 5 cm.

Fig. 4

Engrailed-1 and the inhibition of cutaneous appendage morphogenesis in the chick foot. Skin differentiation at 18 days on dorsal side of the foot of a RCAS mEn-1-infected chick embryo. The overlapping scuta (compare with the control, Fig. 3A) are replaced by glabrous skin together with convoluted (arrowhead) or rounded reticula. (B,C) Heterotreated recombinants morphogenesis shows that the RCAS-En-1 infection affects only the epidermis and does not change the dorsal tarsometatarsus properties of the dermis. (D–F′) The usual expression of En-1 in the epidermis of the plantar region prevents the formation of beta-keratinized (β-ker) cutaneous appendages (D,D′), while the association of a plantar dermis with a tarsometatarsal epidermis leads to the formation of small scuta (E,E′) and that with a neutral epidermis from the midventral apterium leads to feather morphogenesis (F,F′). Note that the pattern in all cases depends on plantar dermis. After Prin & Dhouailly 2004. Reproduced with permission of Int J Dev Biol. br, barb ridges; derm, dermis; epid, epidermis; f, feather; g, glabrous; r, reticula; s, scuta. Bars: A: 400 µm, B–F′: 150 µm.

Fig. 5

Gland-hair metaplasia in mouse plantar region and supernumerary hair follicles. (A,A′) The inhibition of the BMP pathway in K14-Nogginmouse leads to the formation of hair follicles (A′) instead of sweat glands (A). After Plikus et al. 2004. Reprinted with permission from the American Society for Investigative Pathology. (B–D′) The sustained expression of beta-catenin leads not only to the formation of precocious and supplementary hair pelage (compare B and B′, C and C′), but also to the formation of hair buds on the plantar surface (compare D and D′). The arrows and arrowheads attract attention on normal and abnormal skin pattern. After Nähri et al. 2008. Reproduced with permission of the Company of Biologists. swg, sweat gland; h, hair. Bars: A,A′: 100 µm, B,B′: 2 mm, C,C′: 200 µm, D,D′: 4 mm.

Fig. 6

Corneal epithelium-hair metaplasia. (A–E) After a few days of recombination of a corneal rabbit adult corneal epithelium with a mouse embryonic dorsal dermis (A), keratin 12 (K12) expression is down-regulated in the basal layer, whereas that of beta-catenin (βcat) is up-regulated (B). After 1 week, the beta-catenin-expressing cells form hair plugs (C). The hair that differentiates, originates from the rabbit cells, as shown by the label of mouse genomic DNA (D). After 2 weeks, islands of epidermal keratin 10 (K10)-expressing cells appear at the junction of hair follicles and what remains of corneal epithelium (E). After Pearton et al. 2005. Reproduced with permission of the Company of Biologists. (F–G′) The corneal phenotype of Dkk2^−/− mutant mice is opaque. An epidermis with a few hairs has formed (G,G′) instead of the transparent cornea (F,F′). After Mukhopadhyay et al. 2006. Reproduced with permission of the Company of Biologists. bl, basal layer; dc, dermal condensation; h, hair; hp, hair peg. Bars: A–E: 100 µm, F–G: 1 mm, F′,G′: 50 µm.

Fig. 7

Evolution of amniote cutaneous appendages: a new hypothesis. (The interconnection of the chelonian branch of sauropsids being controversial, their skin evolution is not proposed here).The integument of basal amniotes may have presented both a glandular (green color) and an alpha-keratinized (black color) structure. After the synapsid/sauropsid divergence in the Pennsylvanian, a glandular integument was positively selected in synapsids, which evolved both pilosebaceous units and independent glands, whereas the sauropsids may have almost entirely lost the glandular ability. Two innovations occurred: (1) beta-keratin (red color) formation for the sauropsid branch and (2) a system involving a dermal condensation (blue color), together with an up-regulation of the epidermal beta-catenin. The latter innovation may had happened independently twice during skin evolution, in synapsids and in archosaurs. This system allowed the long outgrowth of both the hair shaft and the feather barbs. In crocodilian lineage, the dermal condensation appears after scale morphogenesis, and is diverted to osteoderm formation. The overlapping scales of the squamates, as well as the avian feather and the crocodilian scutes, may have independently evolved from a primitive granulated integument of first sauropsids. Avian scales, reticula and scuta, made respectively of alpha- and beta-keratins are secondarily derived from feathers (see arguments in text).