Cargando…
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...
Autores principales: | , , , , , |
---|---|
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 |
_version_ | 1783528859446018048 |
---|---|
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. |
format | Online Article Text |
id | pubmed-7197477 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2020 |
publisher | Cold Spring Harbor Laboratory Press |
record_format | MEDLINE/PubMed |
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 |
work_keys_str_mv | AT yusufleeban noncodingregionsunderpinavianbillshapediversificationatmacroevolutionaryscales AT heatleymatthewc noncodingregionsunderpinavianbillshapediversificationatmacroevolutionaryscales AT palmerjosephpg noncodingregionsunderpinavianbillshapediversificationatmacroevolutionaryscales AT bartonhenryj noncodingregionsunderpinavianbillshapediversificationatmacroevolutionaryscales AT cooneychristopherr noncodingregionsunderpinavianbillshapediversificationatmacroevolutionaryscales AT gossmanntonii noncodingregionsunderpinavianbillshapediversificationatmacroevolutionaryscales |