Alternative splicing and gene expression play contrasting roles in the parallel phenotypic evolution of a salmonid fish
Abstract 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 adapt...
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crwiley:10.1111/mec.15817 2024-09-15T17:52:25+00:00 Alternative splicing and gene expression play contrasting roles in the parallel phenotypic evolution of a salmonid fish Jacobs, Arne Elmer, Kathryn R. FP7 People: Marie-Curie Actions Carnegie Trust for the Universities of Scotland Wellcome Trust 2021 http://dx.doi.org/10.1111/mec.15817 https://onlinelibrary.wiley.com/doi/pdf/10.1111/mec.15817 https://onlinelibrary.wiley.com/doi/full-xml/10.1111/mec.15817 en eng Wiley http://creativecommons.org/licenses/by/4.0/ Molecular Ecology volume 30, issue 20, page 4955-4969 ISSN 0962-1083 1365-294X journal-article 2021 crwiley https://doi.org/10.1111/mec.15817 2024-09-05T05:04:13Z Abstract 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. Article in Journal/Newspaper Arctic charr Salvelinus alpinus Wiley Online Library Molecular Ecology 30 20 4955 4969 |
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Abstract 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. |
author2 |
FP7 People: Marie-Curie Actions Carnegie Trust for the Universities of Scotland Wellcome Trust |
format |
Article in Journal/Newspaper |
author |
Jacobs, Arne Elmer, Kathryn R. |
spellingShingle |
Jacobs, Arne Elmer, Kathryn R. Alternative splicing and gene expression play contrasting roles in the parallel phenotypic evolution of a salmonid fish |
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 |
Wiley |
publishDate |
2021 |
url |
http://dx.doi.org/10.1111/mec.15817 https://onlinelibrary.wiley.com/doi/pdf/10.1111/mec.15817 https://onlinelibrary.wiley.com/doi/full-xml/10.1111/mec.15817 |
genre |
Arctic charr Salvelinus alpinus |
genre_facet |
Arctic charr Salvelinus alpinus |
op_source |
Molecular Ecology volume 30, issue 20, page 4955-4969 ISSN 0962-1083 1365-294X |
op_rights |
http://creativecommons.org/licenses/by/4.0/ |
op_doi |
https://doi.org/10.1111/mec.15817 |
container_title |
Molecular Ecology |
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30 |
container_issue |
20 |
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4955 |
op_container_end_page |
4969 |
_version_ |
1810294452987625472 |