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Review
. 2015:3:169-95.
doi: 10.1146/annurev-animal-022513-114127. Epub 2014 Nov 3.

Development, regeneration, and evolution of feathers

Chih-Feng Chen  1 , John Foley, Pin-Chi Tang, Ang Li, Ting Xin Jiang, Ping Wu, Randall B Widelitz, Cheng Ming Chuong
Affiliations
Review

Development, regeneration, and evolution of feathers

Chih-Feng Chen et al. Annu Rev Anim Biosci. 2015.

Abstract

The feather is a complex ectodermal organ with hierarchical branching patterns. It provides functions in endothermy, communication, and flight. Studies of feather growth, cycling, and health are of fundamental importance to avian biology and poultry science. In addition, feathers are an excellent model for morphogenesis studies because of their accessibility, and their distinct patterns can be used to assay the roles of specific molecular pathways. Here we review the progress in aspects of development, regeneration, and evolution during the past three decades. We cover the development of feather buds in chicken embryos, regenerative cycling of feather follicle stem cells, formation of barb branching patterns, emergence of intrafeather pigmentation patterns, interplay of hormones and feather growth, and the genetic identification of several feather variants. The discovery of feathered dinosaurs redefines the relationship between feathers and birds. Inspiration from biomaterials and flight research further fuels biomimetic potential of feathers as a multidisciplinary research focal point.

Keywords: Aves; bird; dinosaurs; endocrinology; poultry science; stem cells.

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Figures

Figure 1
Figure 1
Feather diversity: regional specificity and temporal difference. (a) Different types of feathers from different body regions of a finch. Different body regions produce feathers with specific characteristics. In distinct tracts, feathers have unique, region-specific shapes. There also can be size and pigmentation gradients. (b) A bird exhibits different plumage at various ages for different physiological needs. Chicks have downy feathers. At puberty they produce juvenal feathers, and during the reproductive stage they form sexually dimorphic feather types. These different feathers are produced from the same follicle, using similar feather stem cells, in response to different follicle microenvironments. Photo credit: female Silver Laced Wyandotte by Doug and Pete Akers; male Silver Spangled Hamburg by Jim Legendre. (c) An example of Microraptor specimen with bilateral asymmetric remiges attached to both fore and hind limbs (black arrowheads) [from Li et al. (125)].
Figure 2
Figure 2
Feather development: formation of buds and follicles. (a) Examples of restrictive (β-catenin, left panel) and de novo (Shh, right panel) expression patterns. (b) Embryonic feather morphogenesis. Molecules that affect major events along the progression to successive stages of feather development are shown. Proliferative cells are indicated in blue, with darker shades indicating areas of higher proliferation. Proliferation starts at the feather tip but recedes down toward the feather base as morphogenesis proceeds. The plane on the rightmost feather shows the height from which the adjacent cross section was taken to show barb ridge (red arrow) and rachis (red arrowhead) formation. (c) Schematic diagram of follicle invagination. (c′) Depiction of three-dimensional structure of a growing feather follicle. (d) Successive stages of feather branching morphogenesis. Cross sections at different levels from proximal to distal are depicted (corresponding levels i–iv in panel c). (d′) Schematic of barb ridge formation. (e) Schematic of adult feather follicle cycling through initiation, growth, rest, and regeneration. Filament epithelia (grey), stem cells (pink), and mesenchymal pulp (tan) are shown. Abbreviations: ap; axial plate; A-P, anterior-posterior; bb, barbules; BGZ, barb generative zone; bp, barb plate; br, barb ridge; GZ, growth zone; mp; marginal plate; P-D, proximal-distal; pe, papillar ectoderm; rm, ramogenic zone. Adapted from Reference .
Figure 3
Figure 3
Feather follicles: regeneration and branching morphogenesis. (a) Feather branching morphogenesis produces different types of chicken feathers. Adapted from Lucas & Stettenheim (1). (b) Splitting and merging the rachis in response to BMPs and their inhibitor, Noggin. Arrowheads indicate rachides. (b′) Effects of Noggin on barb ridge formation. (b, b′) Adapted from Yu et al. (48). (c) Perturbation of the Wnt-3a gradient produces different feather forms. Adapted from Yue et al. (53). (c′) Model for the stem cell niche topology in radially symmetric feathers (left) and bilaterally symmetric feathers. A ring of stem cells lies parallel to the surface of the skin in radially symmetric feathers but is canted at an angle in bilaterally symmetric feathers. Adapted from Yue et al. (52). (d) Time dimension and proximal-distal feather axis during regeneration. Proximal feather is younger than distal region. Gradients of signaling molecules regulate the shape and size of structures that form. Adapted from Lin et al. (5). Abbreviations: Ant, anterior; ap, axial plate; bp, barb plate; gz, growth zone; LRC, label retaining cells; mp, marginal plate; Post, posterior; TA, transient amplifying.
Figure 4
Figure 4
Feather variations: pigment patterns and texture. (a) Possible steps involved in modulating the homeostasis of melanocyte stem cells, which then affect pigment pattern formation. Modulation can be based on auto-feedback or cross-talk with environmental factors (peripheral pulp, body hormone status). (b) Multidimensional regulation of simple melanocyte behavior allows more temporospatial regulatory freedom. ❶ Pigmentation patterns along the proximal-distal feather axis represent a history of chronological events (60). ❷ The follicle’s cylindrical configuration (62) produces a new medial-lateral plane after the feather vane is opened by apoptosis, which increases patterning diversity. ❸ Signaling factors lying within the peripheral pulp further expand possibilities for pigmentation complexity. ❹ Systemic factors originating from outside of the feather follicle, such as hormones, day length, and temperature variation, contribute to increased diversity (132). The combination of variation from each of these four dimensions enhances the potential to form diverse patterns. (c) One-month-old frizzle chicken. The feathers curl away from rather than toward the body. (c′) Comparison of the wild-type and homozygous frizzle feathers. The wild-type feather image is overlaid with a computer-generated arrow indicating the angle of its rachis. (d) Function θ(s) describes rachis bending, plotted on the length-normalized coordinate. The functions are shifted by arbitrary offsets for clarity. (e) Double immunostaining for K75 (green) and feather keratin (red) in the rachis of normal and frizzle feathers. The yellow dotted line outlines the rachis, and the white dotted line indicates the medulla. (f) Diagram of chicken KRT75 and the cryptic splice site activated by the deletion mutation that covers positions −24 of exon 5 to +59 of intron 5. Boxes represent exon sequences; intron 5 is designated by a line. Carets designating use of the cryptic site (position −69; shown below the pre-RNA diagram) and use of the authentic site (shown above the pre-RNA diagram). (a–c) Adapted from Lin et al. (60), (d–f) adapted from Ng et al. (69). Abbreviations: A, anterior; D, dorsal; ASIP, agouti signaling protein; Dist, distal; LB, lower bulge; LRC, label retaining cell; MB, middle bulge; P, posterior; PE, papillar ectoderm; Prox, proximal; RGZ, ramogenic zone; s, distance from the proximal end of the feather used to determine the rachis angle (θ) at any point; TA, transient amplifying; UB, upper bulge; V, ventral.
Figure 5
Figure 5
Feather evolution: intermediate protofeathers in feathered dinosaurs and basal avialan (153). Schematic drawings of protofeathers, feather-like appendages or intermediate stages of feathers, in feathered dinosaurs and mesozoic birds. The novel developmental processes that allow the major transition of feather forms during evolution include (a) from a cylindrical filament to radially symmetric branched feathers (e.g., downy feathers); (b) from radially symmetric to bilaterally symmetric feathers (e.g., contour feathers); (c) the number, size, and arrangement of rachis and barbs; and (d) the difference of morphology along the proximal-distal axis of the rachis. Besides these macroscale morphological changes, there are also microscale structural modifications taking place, such as the branching of barbs into barbules and rami, specialization of barbule pennulum and base, and the differential morphogenesis of proximal and distal barbules. Adapted from Wu et al. (154).
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