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Positive selection in noncoding genomic regions of vocal learning birds is associated with genes implicated in vocal learning and speech functions in humans

Vocal learning, the ability to imitate sounds from conspecifics and the environment, is a key component of human spoken language and learned song in three independently evolved avian groups—oscine songbirds, parrots, and hummingbirds. Humans and each of these three bird clades exhibit specialized be...

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Autores principales: Cahill, James A., Armstrong, Joel, Deran, Alden, Khoury, Carolyn J., Paten, Benedict, Haussler, David, Jarvis, Erich D.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cold Spring Harbor Laboratory Press 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8559704/
https://www.ncbi.nlm.nih.gov/pubmed/34667117
http://dx.doi.org/10.1101/gr.275989.121
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author Cahill, James A.
Armstrong, Joel
Deran, Alden
Khoury, Carolyn J.
Paten, Benedict
Haussler, David
Jarvis, Erich D.
author_facet Cahill, James A.
Armstrong, Joel
Deran, Alden
Khoury, Carolyn J.
Paten, Benedict
Haussler, David
Jarvis, Erich D.
author_sort Cahill, James A.
collection PubMed
description Vocal learning, the ability to imitate sounds from conspecifics and the environment, is a key component of human spoken language and learned song in three independently evolved avian groups—oscine songbirds, parrots, and hummingbirds. Humans and each of these three bird clades exhibit specialized behavioral, neuroanatomical, and brain gene expression convergence related to vocal learning, speech, and song. To understand the evolutionary basis of vocal learning gene specializations and convergence, we searched for and identified accelerated genomic regions (ARs), a marker of positive selection, specific to vocal learning birds. We found avian vocal learner-specific ARs, and they were enriched in noncoding regions near genes with known speech functions or brain gene expression specializations in humans and vocal learning birds, including FOXP2, NEUROD6, ZEB2, and MEF2C, and near genes with major neurodevelopmental functions, including NR2F1, NRP2, and BCL11B. We also found enrichment near the SFARI class S genes associated with syndromic vocal communication forms of autism spectrum disorders. These findings reveal strong candidate noncoding regions near genes for the evolutionary adaptations that distinguish vocal learning species from their close vocal nonlearning relatives and provide further evidence of molecular convergence between birdsong and human spoken language.
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spelling pubmed-85597042021-11-10 Positive selection in noncoding genomic regions of vocal learning birds is associated with genes implicated in vocal learning and speech functions in humans Cahill, James A. Armstrong, Joel Deran, Alden Khoury, Carolyn J. Paten, Benedict Haussler, David Jarvis, Erich D. Genome Res Research Vocal learning, the ability to imitate sounds from conspecifics and the environment, is a key component of human spoken language and learned song in three independently evolved avian groups—oscine songbirds, parrots, and hummingbirds. Humans and each of these three bird clades exhibit specialized behavioral, neuroanatomical, and brain gene expression convergence related to vocal learning, speech, and song. To understand the evolutionary basis of vocal learning gene specializations and convergence, we searched for and identified accelerated genomic regions (ARs), a marker of positive selection, specific to vocal learning birds. We found avian vocal learner-specific ARs, and they were enriched in noncoding regions near genes with known speech functions or brain gene expression specializations in humans and vocal learning birds, including FOXP2, NEUROD6, ZEB2, and MEF2C, and near genes with major neurodevelopmental functions, including NR2F1, NRP2, and BCL11B. We also found enrichment near the SFARI class S genes associated with syndromic vocal communication forms of autism spectrum disorders. These findings reveal strong candidate noncoding regions near genes for the evolutionary adaptations that distinguish vocal learning species from their close vocal nonlearning relatives and provide further evidence of molecular convergence between birdsong and human spoken language. Cold Spring Harbor Laboratory Press 2021-11 /pmc/articles/PMC8559704/ /pubmed/34667117 http://dx.doi.org/10.1101/gr.275989.121 Text en © 2021 Cahill et al.; Published by Cold Spring Harbor Laboratory Press https://creativecommons.org/licenses/by-nc/4.0/This article, published in Genome Research, is available under a Creative Commons License (Attribution-NonCommercial 4.0 International), as described at http://creativecommons.org/licenses/by-nc/4.0/ (https://creativecommons.org/licenses/by-nc/4.0/) .
spellingShingle Research
Cahill, James A.
Armstrong, Joel
Deran, Alden
Khoury, Carolyn J.
Paten, Benedict
Haussler, David
Jarvis, Erich D.
Positive selection in noncoding genomic regions of vocal learning birds is associated with genes implicated in vocal learning and speech functions in humans
title Positive selection in noncoding genomic regions of vocal learning birds is associated with genes implicated in vocal learning and speech functions in humans
title_full Positive selection in noncoding genomic regions of vocal learning birds is associated with genes implicated in vocal learning and speech functions in humans
title_fullStr Positive selection in noncoding genomic regions of vocal learning birds is associated with genes implicated in vocal learning and speech functions in humans
title_full_unstemmed Positive selection in noncoding genomic regions of vocal learning birds is associated with genes implicated in vocal learning and speech functions in humans
title_short Positive selection in noncoding genomic regions of vocal learning birds is associated with genes implicated in vocal learning and speech functions in humans
title_sort positive selection in noncoding genomic regions of vocal learning birds is associated with genes implicated in vocal learning and speech functions in humans
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8559704/
https://www.ncbi.nlm.nih.gov/pubmed/34667117
http://dx.doi.org/10.1101/gr.275989.121
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