Cryptic Patterning of Avian Skin Confers a Developmental Facility for Loss of Neck Feathering

Abstract

Vertebrate skin is characterized by its patterned array of appendages, whether feathers, hairs, or scales. In avian skin the distribution of feathers occurs on two distinct spatial levels. Grouping of feathers within discrete tracts, with bare skin lying between the tracts, is termed the macropattern, while the smaller scale periodic spacing between individual feathers is referred to as the micropattern. The degree of integration between the patterning mechanisms that operate on these two scales during development and the mechanisms underlying the remarkable evolvability of skin macropatterns are unknown. A striking example of macropattern variation is the convergent loss of neck feathering in multiple species, a trait associated with heat tolerance in both wild and domestic birds. In chicken, a mutation called Naked neck is characterized by a reduction of body feathering and completely bare neck. Here we perform genetic fine mapping of the causative region and identify a large insertion associated with the Naked neck trait. A strong candidate gene in the critical interval, BMP12/GDF7, displays markedly elevated expression in Naked neck embryonic skin due to a cis-regulatory effect of the causative mutation. BMP family members inhibit embryonic feather formation by acting in a reaction-diffusion mechanism, and we find that selective production of retinoic acid by neck skin potentiates BMP signaling, making neck skin more sensitive than body skin to suppression of feather development. This selective production of retinoic acid by neck skin constitutes a cryptic pattern as its effects on feathering are not revealed until gross BMP levels are altered. This developmental modularity of neck and body skin allows simple quantitative changes in BMP levels to produce a sparsely feathered or bare neck while maintaining robust feather patterning on the body.

Evolved tooth gain in sticklebacks is associated with acis-regulatory allele ofBmp6

“…BMP family members have been implicated in several vertebrate evolved traits: size and shape of the beak in Darwin's finches, size and shape of the jaw in cichlids, jaw and skull variation in brachycephalic dogs, and avian feather patterning (47)(48)(49)(50). Although based on a limited number of reported cases and possibly affected by ascertainment biases, this apparent reuse of the same signaling pathway across taxa may reflect a predisposition for Bmp genes to be used during morphological evolution, perhaps due to having complex, modular cis-regulatory architecture to generate evolutionary variation (51,52).…”

Using wavelength and slope to infer the historical origin of semiarid vegetation bands

“…There a stability change might result from a particular gene being expressed during development (e.g., ref. 33), which would correspond to an abrupt change in the parameter values in a mathematical model. Alternatively a uniform state might be stable in an embryo that is too small to permit the destabilizing frequencies, but becomes unstable as the embryo grows (e.g., ref.…”

Coevolutionary patterning of teeth and taste buds

“…Hair, feathers, glands, teeth, taste buds, and intestinal crypt villi are similarly induced under the direction of epithelial and mesenchymal interactions. Similar reaction-diffusion models have been proposed to control the size and spacing of manifold placode-derived organs (3), such as hair (4), feathers (5), and teeth (6). Activators and inhibitors in the bone morphogenetic protein (BMP), fibroblast growth factor (FGF), Hedgehog (Hh), and Wingless (Wnt) pathways execute the pattern.…”