Mammary glands and feathers: comparing two skin appendages which help define novel classes during vertebrate evolution

Abstract

It may appear counter-intuitive to compare feathers and mammary glands. However, through this Evo-Devo analysis, we appreciate how species interact with the environment, requiring different ectodermal organs. Novel ectodermal organs help define evolutionary directions, leading to new organism classes as exemplified by feathers for Aves and mammary glands for Mammals. Here, we review their structure, function, morphogenesis and regenerative cycling. Interestingly, both organs undergo extensive branching for different reasons; feather branching is driven by mechanical advantage while mammary glands nourish young. Besides natural selection, both are regulated by sex hormones and acquired a secondary function for attracting mates, contributing to sexual selection.

Fig. 1

Evo-Devo of ectodermal organs with emphasis on feathers and mammary glands. (A) Evolutionarily novel developmental mechanisms (x axis) result in new phenotypes (y axis) upon which natural selection acts. The arrows are in broken lines since they are hypothetical. (B) When a male peacock reaches sexual maturity, tail coverts are replaced by the colorful giant feathers. Also note the different feather types on different body regions. (C) Venus by Botticelli shows the standard of female beauty today with hairs and breasts. This is in contrast to the Venus of Willendorf (D) which probably shows the standard of beauty for the ancient humans who lived 24,000 years ago with enlarged breasts, probably due to the needs at that time. Panel B, C are photos by Chuong. Panel D is from (www.northernsun.com).

Fig. 2

Formation of appendages. (A) Embryonic feather morphogenesis. Molecules which 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 right most feather shows the height from which the adjacent cross section was taken to show barb ridge (red arrow) and rachis (red arrowhead) formation. AP-axis: anterior–posterior axis; P-D axis: proximal-distal axis. (B) Embryonic mammary gland morphogenesis. Key stages in mammary gland development are shown. Known molecules which regulate each morphogenetic step are presented. The legend identifies the tissues shown in the schematic. Modified from [32].

Fig. 3

Adult feather follicle cycling. (A) Representative feather forms. (B) Components of feather follicle (left). Barb ridge morphogenesis. cl, collar; dp, dermal papilla; pp, pulp. (C) Barb ridge orientation in an open follicle preparation. Barb ridges are oriented parallel to the feather follicle in radially symmetric feathers (left). In bilaterally symmetric feathers (right) the barb ridges form an angle, α, with the rachis. The barbs slant (A–D) because they are made from a horizontal component (A–C) and a vertical component (A–B) due to feather growth. Asymmetric feathers form in response to a Wnt3a gradient, forming an angled stem cell ring (yellow line). Cells at the anterior end (rachis) have to move further than cells at the posterior end (compare m₁ and m₂) to be at the same height. Light blue; rachis, dark blue; ant, anterior, post; posterior. (D) Regenerative feather cycle. The initiation, growth and resting phases are depicted. Red, dermal papilla at the base and dermal sheath rising along the side; light blue, collar epithelia; dark blue, feather sheath; pink, collar mesenchyme; orange, stem cells; speckled brown, pulp. (E) Spatial distribution of apoptotic cells (purple) during successive stages of feather branching morphogenesis. Cross sections at different levels from proximal to distal are depicted.

Fig. 4

Adult mammary gland cycling. Glands are shown in a ventral (left) to dorsal (right) orientation. (−) indicates the molecules are inhibitory to this step in morphogenetic progression. Lists of molecules are not all-inclusive. The legend identifies the tissues shown–in the schematic.