Alternative splicing and gene expression play contrasting roles in the parallel phenotypic evolution of a salmonid fish
Understanding the contribution of different molecular processes to evolution and development is crucial for identifying the mechanisms of adaptation. Here, we used RNA‐sequencing data to test the importance of alternative splicing and differential gene expression in a case of parallel adaptive evolu...
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ftpubmed:oai:pubmedcentral.nih.gov:8653899 2023-05-15T14:30:11+02:00 Alternative splicing and gene expression play contrasting roles in the parallel phenotypic evolution of a salmonid fish Jacobs, Arne Elmer, Kathryn R. 2021-02-18 http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8653899/ http://www.ncbi.nlm.nih.gov/pubmed/33502030 https://doi.org/10.1111/mec.15817 en eng John Wiley and Sons Inc. http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8653899/ http://www.ncbi.nlm.nih.gov/pubmed/33502030 http://dx.doi.org/10.1111/mec.15817 © 2021 The Authors. Molecular Ecology published by John Wiley & Sons Ltd. https://creativecommons.org/licenses/by/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. CC-BY Mol Ecol From the Cover Text 2021 ftpubmed https://doi.org/10.1111/mec.15817 2021-12-26T01:27:22Z Understanding the contribution of different molecular processes to evolution and development is crucial for identifying the mechanisms of adaptation. Here, we used RNA‐sequencing data to test the importance of alternative splicing and differential gene expression in a case of parallel adaptive evolution, the replicated postglacial divergence of the salmonid fish Arctic charr (Salvelinus alpinus) into sympatric benthic and pelagic ecotypes across multiple independent lakes. We found that genes differentially spliced between ecotypes were mostly not differentially expressed (<6% overlap) and were involved in different biological processes. Differentially spliced genes were primarily enriched for muscle development and functioning, while differentially expressed genes were involved in metabolism, immunity and growth. Furthermore, alternative splicing and gene expression were mostly controlled by independent cis‐regulatory quantitative trait loci (<3.4% overlap). Cis‐regulatory regions were associated with the parallel divergence in splicing (16.5% of intron clusters) and expression (6.7%–10.1% of differentially expressed genes), indicating shared regulatory variation across ecotype pairs. Contrary to theoretical expectation, we found that differentially spliced genes tended to be highly central in regulatory networks (“hub genes”) and were annotated to significantly more gene ontology terms compared to nondifferentially spliced genes, consistent with a higher level of pleiotropy. Together, our results suggest that the concerted regulation of alternative splicing and differential gene expression through different regulatory regions leads to the divergence of complementary processes important for local adaptation. This provides novel insights into the importance of contrasting but putatively complementary molecular processes in rapid parallel adaptive evolution. Text Arctic charr Arctic Salvelinus alpinus PubMed Central (PMC) Arctic Molecular Ecology 30 20 4955 4969 |
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English |
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From the Cover |
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From the Cover Jacobs, Arne Elmer, Kathryn R. Alternative splicing and gene expression play contrasting roles in the parallel phenotypic evolution of a salmonid fish |
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From the Cover |
description |
Understanding the contribution of different molecular processes to evolution and development is crucial for identifying the mechanisms of adaptation. Here, we used RNA‐sequencing data to test the importance of alternative splicing and differential gene expression in a case of parallel adaptive evolution, the replicated postglacial divergence of the salmonid fish Arctic charr (Salvelinus alpinus) into sympatric benthic and pelagic ecotypes across multiple independent lakes. We found that genes differentially spliced between ecotypes were mostly not differentially expressed (<6% overlap) and were involved in different biological processes. Differentially spliced genes were primarily enriched for muscle development and functioning, while differentially expressed genes were involved in metabolism, immunity and growth. Furthermore, alternative splicing and gene expression were mostly controlled by independent cis‐regulatory quantitative trait loci (<3.4% overlap). Cis‐regulatory regions were associated with the parallel divergence in splicing (16.5% of intron clusters) and expression (6.7%–10.1% of differentially expressed genes), indicating shared regulatory variation across ecotype pairs. Contrary to theoretical expectation, we found that differentially spliced genes tended to be highly central in regulatory networks (“hub genes”) and were annotated to significantly more gene ontology terms compared to nondifferentially spliced genes, consistent with a higher level of pleiotropy. Together, our results suggest that the concerted regulation of alternative splicing and differential gene expression through different regulatory regions leads to the divergence of complementary processes important for local adaptation. This provides novel insights into the importance of contrasting but putatively complementary molecular processes in rapid parallel adaptive evolution. |
format |
Text |
author |
Jacobs, Arne Elmer, Kathryn R. |
author_facet |
Jacobs, Arne Elmer, Kathryn R. |
author_sort |
Jacobs, Arne |
title |
Alternative splicing and gene expression play contrasting roles in the parallel phenotypic evolution of a salmonid fish |
title_short |
Alternative splicing and gene expression play contrasting roles in the parallel phenotypic evolution of a salmonid fish |
title_full |
Alternative splicing and gene expression play contrasting roles in the parallel phenotypic evolution of a salmonid fish |
title_fullStr |
Alternative splicing and gene expression play contrasting roles in the parallel phenotypic evolution of a salmonid fish |
title_full_unstemmed |
Alternative splicing and gene expression play contrasting roles in the parallel phenotypic evolution of a salmonid fish |
title_sort |
alternative splicing and gene expression play contrasting roles in the parallel phenotypic evolution of a salmonid fish |
publisher |
John Wiley and Sons Inc. |
publishDate |
2021 |
url |
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8653899/ http://www.ncbi.nlm.nih.gov/pubmed/33502030 https://doi.org/10.1111/mec.15817 |
geographic |
Arctic |
geographic_facet |
Arctic |
genre |
Arctic charr Arctic Salvelinus alpinus |
genre_facet |
Arctic charr Arctic Salvelinus alpinus |
op_source |
Mol Ecol |
op_relation |
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8653899/ http://www.ncbi.nlm.nih.gov/pubmed/33502030 http://dx.doi.org/10.1111/mec.15817 |
op_rights |
© 2021 The Authors. Molecular Ecology published by John Wiley & Sons Ltd. https://creativecommons.org/licenses/by/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. |
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CC-BY |
op_doi |
https://doi.org/10.1111/mec.15817 |
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Molecular Ecology |
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30 |
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20 |
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4955 |
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4969 |
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1766304085224456192 |