The origin and evolution of avian feathers

True powered flight has arisen three independent times in vertebrate evolutionary history encompassing changes in the morphology and function of forelimb structures in the pterosaur, bird, and bat lineages. In all three cases, the leading edge of the wing is stabilized by the forelimb skeletal elements. But, in contrast to the pterosaurs and bats, which use a membranous lifting surface, the majority of the flight surface in birds consists of feathers. Feather-like structures have been found on fossils of several nonavian dinosaurs, suggesting that early feathers may have been used for camouflage, thermoregulation, or color display purposes. The subsequent co-option of feathers for flight involved changes in the shape and structure of feathers as well as numerous other changes in the anatomy and physiology of birds.

Like hair, nails, and scales, feathers are integumentary or epithelial appendages that arise from controlled proliferation of the epidermis. All epithelial appendages originate as epithelial placodes, or small regions of thickened epidermal cells, that will eventually give rise to individual outgrowths (Fig. 6.1a). The diversity of epithelial appendage morphologies belies the extensive similarities in their initial developmental stages. The spatial distribution of epithelial primordia in ordered arrays is established by a series of signals, involving the Shh, Wnt, FGF, Notch, and BMP (Bone Morphogenetic Proteins, members of the TGF-P super-family) signaling pathways, between the mesenchymal (dermal) and epithelial (epidermal) tissue layers. The identity of epithelial appendages is determined by the underlying mesen-chyme and affected by the timing and level of expression of these signaling molecules. Birds have both feathers and scales (on their feet) and feathers develop in response to high levels of Wnt and Notch signaling and low levels of BMP signaling, whereas scales develop in regions with inverse levels of these signals (Fig. 6.1b). Thus modulations in the strength or duration of these early signaling events appears to establish the identities of scales versus feathers.

Further development of the feather is regulated, in part, by Shh and Bmps . These two signaling pathways appear to be integrated in order to maintain a balance between proliferation (Shh) and differentiation (BMP) that is crucial to proper feather formation. Shortly after formation of the feather primordia in chicks and ducks, expression of Bmp2 and Shh becomes polarized with Bmp2 expression in the anterior and Shh expression in the posterior of each primordium. This same pattern of gene expression can be found in the developing scutate scales on the feet of chick and ducks and also in alligator scales (Fig. 6.1c) These data suggest that early Shh and Bmp2 expression was regulated in a similar manner in epithelial appendages of birds and crocodilians and was co-opted for further use in feather development.

After hatching, the feather primordia differentiate into the feather proper. A typical feather is a branched structure comprising a central rachis, a series of barbs attached to the rachis, numerous barbules connected to the barbs, and cilia or hooklets attached to the barbules. The Shh-BMP circuit is reused repeatedly during these later stages of feather development. The

Feather Evolution From Scale

Figure 6.1

Epithelial appendage development

(a) The early stages of epithelial appendage development (scales, feathers, and hair) begin with the formation of an epidermal placode. Signaling between the mesenchyme (dermis) and epithelium (epidermis) establishes the ordered array of placodes on the skin. Outgrowth of the placode is followed by the formation of a follicle, which supports growth and differentiation of feather and hair development. (b) The difference between the identities of avian scales and feathers reflects the timing and level of early signaling events. (c) Sequential redeployment of Shh-Bmp2 module during the development and evolution of a feather. Congruence between patterns of expression of the Shh-Bmp2 module in feathers and archosaurian scales (top), and the developmental theory of the origin and early evolution of feathers (bottom). The Stages I-IIIa of the developmental theory of feather evolution are proposed to have evolved by novel regulation of Shh-Bmp2 module expression. Stage I—the first, elongate tubular feather evolved from a primitive archosaurian scale by the derived distal Shh-Bmp2 co-expression (Event 1). Stage II—the first, branched plumulaceous feather evolved by the origin of derived longitudinal Shh-Bmp2 expression domains (Event 2) that created differentiated filaments from the tubular epithelium of the feather germ. The central-peripheral ((c)-(ph)) polarity of Shh-Bmp2 expression in the marginal plate epithelium between the barb ridges is shown in the inset. Stage IIIa evolved by the controlled dorsal (d) cessation and ventral (v) division of the longitudinal Shh-Bmp2 expression domains (Event 3) producing helical growth of barb ridges, indeterminate barb number, a rachis, serial fusion of barbs to the rachis, and a planar vane.

Source: Part c from Harris MP, Fallon JF, et al. J Exp Zool2002; 294: 160-176. Copyright © 2002. Reprinted by permission of Wiley-Liss, Inc., a subsidiary of John Wiley & Sons, Inc.

balance between the antagonistic activities of Shh and BMPs sets the number and spacing of the primary branches. Variations in the patterns of Shh and Bmp expression correlate with the changes in the organization of these branching structures in different types of feathers, suggesting that the co-option of these two signaling pathways has played a fundamental role in the origin and elaboration of feathers. The co-option of single genes, regulatory circuits, or entire regulatory hierarchies is a common theme in the development of evolutionary novelties.

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