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Review
. 2003 Aug 15;298(1):42-56.
doi: 10.1002/jez.b.25.

Adaptation to the sky: Defining the feather with integument fossils from mesozoic China and experimental evidence from molecular laboratories

Cheng-Ming Chuong  1 , Ping Wu, Fu-Cheng Zhang, Xing Xu, Minke Yu, Randall B Widelitz, Ting-Xin Jiang, Lianhai Hou
Affiliations
Review

Adaptation to the sky: Defining the feather with integument fossils from mesozoic China and experimental evidence from molecular laboratories

Cheng-Ming Chuong et al. J Exp Zool B Mol Dev Evol. .

Abstract

In this special issue on the Evo-Devo of amniote integuments, Alibardi has discussed the adaptation of the integument to the land. Here we will discuss the adaptation to the sky. We first review a series of fossil discoveries representing intermediate forms of feathers or feather-like appendages from dinosaurs and Mesozoic birds from the Jehol Biota of China. We then discuss the molecular and developmental biological experiments using chicken integuments as the model. Feather forms can be modulated using retrovirus mediated gene mis-expression that mimics those found in nature today and in the evolutionary past. The molecular conversions among different types of integument appendages (feather, scale, tooth) are discussed. From this evidence, we recognize that not all organisms with feathers are birds, and that not all skin appendages with hierarchical branches are feathers. We develop a set of criteria for true avian feathers: 1) possessing actively proliferating cells in the proximal follicle for proximo-distal growth mode; 2) forming hierarchical branches of rachis, barbs, and barbules, with barbs formed by differential cell death and bilaterally or radially symmetric; 3) having a follicle structure, with mesenchyme core during development; 4) when mature, consisting of epithelia without mesenchyme core and with two sides of the vane facing the previous basal and supra-basal layers, respectively; and 5) having stem cells and dermal papilla in the follicle and hence the ability to molt and regenerate. A model of feather evolution from feather bud --> barbs --> barbules --> rachis is presented, which is opposite to the old view of scale plate --> rachis --> barbs --> barbules (Regal, '75; Q Rev Biol 50:35).

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Figures

Fig. 1
Fig. 1. Representatives of feathered dinosaurs and Mesozoic birds from Jehol Biota
a. Map showing the location of the excavated site. b. Sinosauropteryx. c. Sinornithosaurus. d. Caudipteryx. e. Microraptor gui. f. Confuciusornis. g, h. Tail feathers of Protopteryx and Confuciusornis that were used to support scale feather transformation (Zhang and Zhou, 2000) as suggested by Regal, 1975 (Fig. 5A). Panel b and d are from National Geographic. Panel e is from Xu et al., 2003. Panel f is from Hou, 1997.
Fig. 2
Fig. 2. Morphology and topological organizations of feathers, scales and hairs
A, Avian foot scales and reptiles are very similar in morphology. However, their homology in evolution remains to be determined. Note the radial and bilateral symmetry of downy and flight feathers respectively. Also see Fig. 1 of Prum and Dyck in this issue for a contour feather. Panel A is modified from Lucas and Stettenheim, 1972 and Chuong et al., 2000. B, Comparison of epithelium and mesenchyme composition of feathers, scales and hairs. Mature feathers are made of supra-basal epithelia only. The two sides of feather vanes originally face the suprabasal and basal side, respectively. The mesenchyme core only exists transiently during feather morphogenesis. Mature scales still have a mesenchymal core. All the scale surfaces are covered by the suprabasal layer. The mature hairs are made of suprabasal epidermal cells. Blue, epithelium, or suprbasal epithelia; purple, basal side of the epithelium (note in mature feather, the basal layer is gone, but still shown here to illustrate the topology of feather follicles); red, mesenchyme.
Fig. 3
Fig. 3. Molecular biology technology used to mis-express genes and convert developmental pathways of skin appendages
A. RCAS retroviral vectors used to mis-express genes in chicken. B. Demonstration of mis-expressed genes (in this case alkaline phosphatase, AP) in chicken embryos (The head is toward the left and not shown). Note the patchy staining. The insert in the lower right corner shows high expression of AP genes in the elongating feather buds. C. Strategies to mis-express genes in feather follicles of hatched chickens. After feather plucking, stem cells regenerate a new feather. This is the opportunity to transduce exogenous genes to these regenerating epithelial stem cells (gray color, and panel D). E. The balance of molecular pathways is perturbed and the forms of feathers are altered. Here we show noggin, a BMP antagonist, can split the rachis into multiples and enhance barbs to branch more. In contrast, BMP2 and BMP4 can produce a giant rachis and enhance barb fusion. Therefore, noggin favors barb formation while BMP favors rachis formation. Modified from Yu et al., 2002.
Fig. 4
Fig. 4. Molecular conversion of feathers / scales and tooth / oral mucosa
A. When RCAS beta catenin was used to infect embryonic chicken hind limb, scales are converted into feathers. a. feathers growing out from scale region. b, Follicles are seen to form from part of the scutate scale surface. c, Barb ridges form in these induced feathers. The newly induced feathers do have follicular structures and form barb ridges. Note it is part of the scale surface that is converted into feathers, not the transformation of the whole scales into feathers. It appears that some appendage stem cells may have remained in scale epidermis and are activated by beta catenin to form a feather. Modified from Widelitz et al., 2000. B. Embryonic epithelia containing oral mucosa and chin epidermis were recombined with feather mesenchyma from the dorsal skin (a). The explant is put to develop in culture. Chin regions form feather buds while the oral mucosa regions form many tooth like appendages (left part of the explant, panel b), while the right part forms feather buds. Sections show follicular structures (panel c). Modified from Chen et al., 2000.
Fig. 5
Fig. 5. Models of scale / feather transformation
Panel A is from Regal, 1975 that suggested the order being the scale like planes → partial pennaceous vanes with emerging rachis → bilaterally symmetric feather → plumulaceous barbs → radially symmetric downy feathers. We propose the order in panel B, favoring the order being cylindrical feather filaments splitting to form primitive barbs without barbules → radially symmetric downy feathers with plumulaceous barbs → bilaterally symmetric plumulaceous feathers → bilaterally symmetric pennaceous vanes → bilaterally asymmetric vanes. There are likely to be some lineages not depicted here. Some lineages may have been lost through selection during Mesozoic time and become extinct while some lineages persisted and flourished till today. Some of the molecular pathways known to be involved under each new evolution process are indicated. Equipped with the new knowledge here and new technology (also see Widelitz et al., this issue), we are positioned to identify more molecular basis of evolutionary novelty using the feather Evo-Devo model.
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