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

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 macropatter...

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Autores principales: Chunyan Mou, Frederique Pitel, David Gourichon, Florence Vignoles, Athanasia Tzika, Patricia Tato, Le Yu, Dave W Burt, Bertrand Bed'hom, Michele Tixier-Boichard, Kevin J Painter, Denis J Headon
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Publicado: Public Library of Science (PLoS) 2011
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Acceso en línea:https://doaj.org/article/bb1a0b453c83491b99b3b3bab1cf5274
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spelling oai:doaj.org-article:bb1a0b453c83491b99b3b3bab1cf52742021-11-18T05:36:17ZCryptic patterning of avian skin confers a developmental facility for loss of neck feathering.1544-91731545-788510.1371/journal.pbio.1001028https://doaj.org/article/bb1a0b453c83491b99b3b3bab1cf52742011-03-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/21423653/?tool=EBIhttps://doaj.org/toc/1544-9173https://doaj.org/toc/1545-7885Vertebrate 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.Chunyan MouFrederique PitelDavid GourichonFlorence VignolesAthanasia TzikaPatricia TatoLe YuDave W BurtBertrand Bed'homMichele Tixier-BoichardKevin J PainterDenis J HeadonPublic Library of Science (PLoS)articleBiology (General)QH301-705.5ENPLoS Biology, Vol 9, Iss 3, p e1001028 (2011)
institution DOAJ
collection DOAJ
language EN
topic Biology (General)
QH301-705.5
spellingShingle Biology (General)
QH301-705.5
Chunyan Mou
Frederique Pitel
David Gourichon
Florence Vignoles
Athanasia Tzika
Patricia Tato
Le Yu
Dave W Burt
Bertrand Bed'hom
Michele Tixier-Boichard
Kevin J Painter
Denis J Headon
Cryptic patterning of avian skin confers a developmental facility for loss of neck feathering.
description 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.
format article
author Chunyan Mou
Frederique Pitel
David Gourichon
Florence Vignoles
Athanasia Tzika
Patricia Tato
Le Yu
Dave W Burt
Bertrand Bed'hom
Michele Tixier-Boichard
Kevin J Painter
Denis J Headon
author_facet Chunyan Mou
Frederique Pitel
David Gourichon
Florence Vignoles
Athanasia Tzika
Patricia Tato
Le Yu
Dave W Burt
Bertrand Bed'hom
Michele Tixier-Boichard
Kevin J Painter
Denis J Headon
author_sort Chunyan Mou
title Cryptic patterning of avian skin confers a developmental facility for loss of neck feathering.
title_short Cryptic patterning of avian skin confers a developmental facility for loss of neck feathering.
title_full Cryptic patterning of avian skin confers a developmental facility for loss of neck feathering.
title_fullStr Cryptic patterning of avian skin confers a developmental facility for loss of neck feathering.
title_full_unstemmed Cryptic patterning of avian skin confers a developmental facility for loss of neck feathering.
title_sort cryptic patterning of avian skin confers a developmental facility for loss of neck feathering.
publisher Public Library of Science (PLoS)
publishDate 2011
url https://doaj.org/article/bb1a0b453c83491b99b3b3bab1cf5274
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