Cryptic patterning of avian skin confers a developmental facility for loss of neck feathering.

TitleCryptic patterning of avian skin confers a developmental facility for loss of neck feathering.
Publication TypeJournal Article
Year of Publication2011
AuthorsMou, C, Pitel, F, Gourichon, D, Plisson-Petit, F, Tzika, A, Tato, P, Yu, L, Burt, DW, Bed'hom, B, Tixier-Boichard, M, Painter, KJ, Headon, DJ
JournalPLoS Biol
Volume9
Issue3
Paginatione1001028
Date Published2011 Mar
ISSN1545-7885
KeywordsAnimals, Base Sequence, Body Patterning, Bone Morphogenetic Proteins, Chick Embryo, Chickens, DNA Mutational Analysis, Feathers, Gene Expression Profiling, Gene Expression Regulation, Developmental, Microarray Analysis, Molecular Sequence Data, Phenotype, Signal Transduction, Skin, Tretinoin
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.

DOI10.1371/journal.pbio.1001028
Alternate JournalPLoS Biol.
PubMed ID21423653
PubMed Central IDPMC3057954
Grant ListBB/D523578/2 / / Biotechnology and Biological Sciences Research Council / United Kingdom
/ / Biotechnology and Biological Sciences Research Council / United Kingdom