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.
Highlights
The vertebrate skin carries a highly ordered arrangement of pigments and morphological structures such as hairs and feathers
In this study we explore the basis of loss of neck feathering, a feature associated with heat tolerance that has arisen independently several times during bird evolution
We find that in chickens a bare neck is caused by increased production of bone morphogenetic protein (BMP), factors previously implicated in defining the size of the gaps between neighboring feathers
Summary
The vertebrate skin carries a highly ordered arrangement of pigments and morphological structures such as hairs and feathers These patterns in the skin occur on two distinct spatial scales. On a larger anatomical scale, different parts of the body display periodic pattern variations in terms of the density and size of the repeated structures, and in regions of bare skin no periodic micropattern is present at all These regional differences in micropattern across the skin constitute the macropattern. Both levels of organization arise in the embryo, beginning with the stereotypical positioning of the 14 feather tracts In chicken this macropatterning is initiated at embryonic day 7 (E7) by dermal signals that induce stripes of cells that are competent to undergo feather development. The placodes contain tightly packed cells that undergo rapid proliferation to produce a tubular outgrowth and subsequently undergo branching and differentiation to yield a mature feather fiber [5,6,7]
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