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Noncoding regions underpin avian bill shape diversification at macroevolutionary scales

Recent progress has been made in identifying genomic regions implicated in trait evolution on a microevolutionary scale in many species, but whether these are relevant over macroevolutionary time remains unclear. Here, we directly address this fundamental question using bird beak shape, a key evolut...

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Autores principales: Yusuf, Leeban, Heatley, Matthew C., Palmer, Joseph P.G., Barton, Henry J., Cooney, Christopher R., Gossmann, Toni I.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cold Spring Harbor Laboratory Press 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7197477/
https://www.ncbi.nlm.nih.gov/pubmed/32269134
http://dx.doi.org/10.1101/gr.255752.119
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author Yusuf, Leeban
Heatley, Matthew C.
Palmer, Joseph P.G.
Barton, Henry J.
Cooney, Christopher R.
Gossmann, Toni I.
author_facet Yusuf, Leeban
Heatley, Matthew C.
Palmer, Joseph P.G.
Barton, Henry J.
Cooney, Christopher R.
Gossmann, Toni I.
author_sort Yusuf, Leeban
collection PubMed
description Recent progress has been made in identifying genomic regions implicated in trait evolution on a microevolutionary scale in many species, but whether these are relevant over macroevolutionary time remains unclear. Here, we directly address this fundamental question using bird beak shape, a key evolutionary innovation linked to patterns of resource use, divergence, and speciation, as a model trait. We integrate class-wide geometric-morphometric analyses with evolutionary sequence analyses of 10,322 protein-coding genes as well as 229,001 genomic regions spanning 72 species. We identify 1434 protein-coding genes and 39,806 noncoding regions for which molecular rates were significantly related to rates of bill shape evolution. We show that homologs of the identified protein-coding genes as well as genes in close proximity to the identified noncoding regions are involved in craniofacial embryo development in mammals. They are associated with embryonic stem cell pathways, including BMP and Wnt signaling, both of which have repeatedly been implicated in the morphological development of avian beaks. This suggests that identifying genotype-phenotype association on a genome-wide scale over macroevolutionary time is feasible. Although the coding and noncoding gene sets are associated with similar pathways, the actual genes are highly distinct, with significantly reduced overlap between them and bill-related phenotype associations specific to noncoding loci. Evidence for signatures of recent diversifying selection on our identified noncoding loci in Darwin finch populations further suggests that regulatory rather than coding changes are major drivers of morphological diversification over macroevolutionary times.
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spelling pubmed-71974772020-10-01 Noncoding regions underpin avian bill shape diversification at macroevolutionary scales Yusuf, Leeban Heatley, Matthew C. Palmer, Joseph P.G. Barton, Henry J. Cooney, Christopher R. Gossmann, Toni I. Genome Res Research Recent progress has been made in identifying genomic regions implicated in trait evolution on a microevolutionary scale in many species, but whether these are relevant over macroevolutionary time remains unclear. Here, we directly address this fundamental question using bird beak shape, a key evolutionary innovation linked to patterns of resource use, divergence, and speciation, as a model trait. We integrate class-wide geometric-morphometric analyses with evolutionary sequence analyses of 10,322 protein-coding genes as well as 229,001 genomic regions spanning 72 species. We identify 1434 protein-coding genes and 39,806 noncoding regions for which molecular rates were significantly related to rates of bill shape evolution. We show that homologs of the identified protein-coding genes as well as genes in close proximity to the identified noncoding regions are involved in craniofacial embryo development in mammals. They are associated with embryonic stem cell pathways, including BMP and Wnt signaling, both of which have repeatedly been implicated in the morphological development of avian beaks. This suggests that identifying genotype-phenotype association on a genome-wide scale over macroevolutionary time is feasible. Although the coding and noncoding gene sets are associated with similar pathways, the actual genes are highly distinct, with significantly reduced overlap between them and bill-related phenotype associations specific to noncoding loci. Evidence for signatures of recent diversifying selection on our identified noncoding loci in Darwin finch populations further suggests that regulatory rather than coding changes are major drivers of morphological diversification over macroevolutionary times. Cold Spring Harbor Laboratory Press 2020-04 /pmc/articles/PMC7197477/ /pubmed/32269134 http://dx.doi.org/10.1101/gr.255752.119 Text en © 2020 Yusuf et al.; Published by Cold Spring Harbor Laboratory Press http://creativecommons.org/licenses/by-nc/4.0/ This article is distributed exclusively by Cold Spring Harbor Laboratory Press for the first six months after the full-issue publication date (see http://genome.cshlp.org/site/misc/terms.xhtml). After six months, it is available under a Creative Commons License (Attribution-NonCommercial 4.0 International), as described at http://creativecommons.org/licenses/by-nc/4.0/.
spellingShingle Research
Yusuf, Leeban
Heatley, Matthew C.
Palmer, Joseph P.G.
Barton, Henry J.
Cooney, Christopher R.
Gossmann, Toni I.
Noncoding regions underpin avian bill shape diversification at macroevolutionary scales
title Noncoding regions underpin avian bill shape diversification at macroevolutionary scales
title_full Noncoding regions underpin avian bill shape diversification at macroevolutionary scales
title_fullStr Noncoding regions underpin avian bill shape diversification at macroevolutionary scales
title_full_unstemmed Noncoding regions underpin avian bill shape diversification at macroevolutionary scales
title_short Noncoding regions underpin avian bill shape diversification at macroevolutionary scales
title_sort noncoding regions underpin avian bill shape diversification at macroevolutionary scales
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7197477/
https://www.ncbi.nlm.nih.gov/pubmed/32269134
http://dx.doi.org/10.1101/gr.255752.119
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