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Transcriptional regulatory divergence underpinning species-specific learned vocalization in songbirds

Learning of most motor skills is constrained in a species-specific manner. However, the proximate mechanisms underlying species-specific learned behaviors remain poorly understood. Songbirds acquire species-specific songs through learning, which is hypothesized to depend on species-specific patterns...

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Autores principales: Wang, Hongdi, Sawai, Azusa, Toji, Noriyuki, Sugioka, Rintaro, Shibata, Yukino, Suzuki, Yuika, Ji, Yu, Hayase, Shin, Akama, Satoru, Sese, Jun, Wada, Kazuhiro
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6853299/
https://www.ncbi.nlm.nih.gov/pubmed/31721761
http://dx.doi.org/10.1371/journal.pbio.3000476
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author Wang, Hongdi
Sawai, Azusa
Toji, Noriyuki
Sugioka, Rintaro
Shibata, Yukino
Suzuki, Yuika
Ji, Yu
Hayase, Shin
Akama, Satoru
Sese, Jun
Wada, Kazuhiro
author_facet Wang, Hongdi
Sawai, Azusa
Toji, Noriyuki
Sugioka, Rintaro
Shibata, Yukino
Suzuki, Yuika
Ji, Yu
Hayase, Shin
Akama, Satoru
Sese, Jun
Wada, Kazuhiro
author_sort Wang, Hongdi
collection PubMed
description Learning of most motor skills is constrained in a species-specific manner. However, the proximate mechanisms underlying species-specific learned behaviors remain poorly understood. Songbirds acquire species-specific songs through learning, which is hypothesized to depend on species-specific patterns of gene expression in functionally specialized brain regions for vocal learning and production, called song nuclei. Here, we leveraged two closely related songbird species, zebra finch, owl finch, and their interspecific first-generation (F(1)) hybrids, to relate transcriptional regulatory divergence between species with the production of species-specific songs. We quantified genome-wide gene expression in both species and compared this with allele-specific expression in F(1) hybrids to identify genes whose expression in song nuclei is regulated by species divergence in either cis- or trans-regulation. We found that divergence in transcriptional regulation altered the expression of approximately 10% of total transcribed genes and was linked to differential gene expression between the two species. Furthermore, trans-regulatory changes were more prevalent than cis-regulatory and were associated with synaptic formation and transmission in song nucleus RA, the avian analog of the mammalian laryngeal motor cortex. We identified brain-derived neurotrophic factor (BDNF) as an upstream mediator of trans-regulated genes in RA, with a significant correlation between individual variation in BDNF expression level and species-specific song phenotypes in F(1) hybrids. This was supported by the fact that the pharmacological overactivation of BDNF receptors altered the expression of its trans-regulated genes in the RA, thus disrupting the learned song structures of adult zebra finch songs at the acoustic and sequence levels. These results demonstrate functional neurogenetic associations between divergence in region-specific transcriptional regulation and species-specific learned behaviors.
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spelling pubmed-68532992019-11-22 Transcriptional regulatory divergence underpinning species-specific learned vocalization in songbirds Wang, Hongdi Sawai, Azusa Toji, Noriyuki Sugioka, Rintaro Shibata, Yukino Suzuki, Yuika Ji, Yu Hayase, Shin Akama, Satoru Sese, Jun Wada, Kazuhiro PLoS Biol Research Article Learning of most motor skills is constrained in a species-specific manner. However, the proximate mechanisms underlying species-specific learned behaviors remain poorly understood. Songbirds acquire species-specific songs through learning, which is hypothesized to depend on species-specific patterns of gene expression in functionally specialized brain regions for vocal learning and production, called song nuclei. Here, we leveraged two closely related songbird species, zebra finch, owl finch, and their interspecific first-generation (F(1)) hybrids, to relate transcriptional regulatory divergence between species with the production of species-specific songs. We quantified genome-wide gene expression in both species and compared this with allele-specific expression in F(1) hybrids to identify genes whose expression in song nuclei is regulated by species divergence in either cis- or trans-regulation. We found that divergence in transcriptional regulation altered the expression of approximately 10% of total transcribed genes and was linked to differential gene expression between the two species. Furthermore, trans-regulatory changes were more prevalent than cis-regulatory and were associated with synaptic formation and transmission in song nucleus RA, the avian analog of the mammalian laryngeal motor cortex. We identified brain-derived neurotrophic factor (BDNF) as an upstream mediator of trans-regulated genes in RA, with a significant correlation between individual variation in BDNF expression level and species-specific song phenotypes in F(1) hybrids. This was supported by the fact that the pharmacological overactivation of BDNF receptors altered the expression of its trans-regulated genes in the RA, thus disrupting the learned song structures of adult zebra finch songs at the acoustic and sequence levels. These results demonstrate functional neurogenetic associations between divergence in region-specific transcriptional regulation and species-specific learned behaviors. Public Library of Science 2019-11-13 /pmc/articles/PMC6853299/ /pubmed/31721761 http://dx.doi.org/10.1371/journal.pbio.3000476 Text en © 2019 Wang et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Wang, Hongdi
Sawai, Azusa
Toji, Noriyuki
Sugioka, Rintaro
Shibata, Yukino
Suzuki, Yuika
Ji, Yu
Hayase, Shin
Akama, Satoru
Sese, Jun
Wada, Kazuhiro
Transcriptional regulatory divergence underpinning species-specific learned vocalization in songbirds
title Transcriptional regulatory divergence underpinning species-specific learned vocalization in songbirds
title_full Transcriptional regulatory divergence underpinning species-specific learned vocalization in songbirds
title_fullStr Transcriptional regulatory divergence underpinning species-specific learned vocalization in songbirds
title_full_unstemmed Transcriptional regulatory divergence underpinning species-specific learned vocalization in songbirds
title_short Transcriptional regulatory divergence underpinning species-specific learned vocalization in songbirds
title_sort transcriptional regulatory divergence underpinning species-specific learned vocalization in songbirds
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6853299/
https://www.ncbi.nlm.nih.gov/pubmed/31721761
http://dx.doi.org/10.1371/journal.pbio.3000476
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