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‐seq data to test the importance of alternative splicing and differential gene expression in a case of parallel adaptive evolution, t...
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ftuglasgow:oai:eprints.gla.ac.uk:227770 2023-05-15T14:30:12+02:00 Alternative splicing and gene expression play contrasting roles in the parallel phenotypic evolution of a salmonid fish Jacobs, Arne Elmer, Kathryn R. 2021-10 text https://eprints.gla.ac.uk/227770/ https://eprints.gla.ac.uk/227770/1/227770.pdf en eng Wiley https://eprints.gla.ac.uk/227770/1/227770.pdf Jacobs, A. <http://eprints.gla.ac.uk/view/author/47202.html> and Elmer, K. R. <http://eprints.gla.ac.uk/view/author/29070.html> (2021) Alternative splicing and gene expression play contrasting roles in the parallel phenotypic evolution of a salmonid fish. Molecular Ecology <https://eprints.gla.ac.uk/view/journal_volume/Molecular_Ecology.html>, 30(20), pp. 4955-4969. (doi:10.1111/mec.15817 <https://doi.org/10.1111/mec.15817>) (PMID:33502030) (PMCID:PMC8653899) cc_by_4 CC-BY Articles PeerReviewed 2021 ftuglasgow https://doi.org/10.1111/mec.15817 2022-09-22T22:16:14Z Understanding the contribution of different molecular processes to evolution and development is crucial for identifying the mechanisms of adaptation. Here, we used RNA‐seq 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 non‐differentially 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 Arctic Salvelinus alpinus University of Glasgow: Enlighten - Publications Arctic Molecular Ecology |
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Open Polar |
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University of Glasgow: Enlighten - Publications |
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ftuglasgow |
language |
English |
description |
Understanding the contribution of different molecular processes to evolution and development is crucial for identifying the mechanisms of adaptation. Here, we used RNA‐seq 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 non‐differentially 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 |
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 |
https://eprints.gla.ac.uk/227770/ https://eprints.gla.ac.uk/227770/1/227770.pdf |
geographic |
Arctic |
geographic_facet |
Arctic |
genre |
Arctic charr Arctic Salvelinus alpinus |
genre_facet |
Arctic charr Arctic Salvelinus alpinus |
op_relation |
https://eprints.gla.ac.uk/227770/1/227770.pdf Jacobs, A. <http://eprints.gla.ac.uk/view/author/47202.html> and Elmer, K. R. <http://eprints.gla.ac.uk/view/author/29070.html> (2021) Alternative splicing and gene expression play contrasting roles in the parallel phenotypic evolution of a salmonid fish. Molecular Ecology <https://eprints.gla.ac.uk/view/journal_volume/Molecular_Ecology.html>, 30(20), pp. 4955-4969. (doi:10.1111/mec.15817 <https://doi.org/10.1111/mec.15817>) (PMID:33502030) (PMCID:PMC8653899) |
op_rights |
cc_by_4 |
op_rightsnorm |
CC-BY |
op_doi |
https://doi.org/10.1111/mec.15817 |
container_title |
Molecular Ecology |
_version_ |
1766304087566974976 |