Alternative splicing and gene expression play contrasting roles in the parallel phenotypic evolution of a salmonid fish

Jacobs, A. and Elmer, K. R. (2021) Alternative splicing and gene expression play contrasting roles in the parallel phenotypic evolution of a salmonid fish. Molecular Ecology, 30(20), pp. 4955-4969. (doi: 10.1111/mec.15817) (PMID:33502030) (PMCID:PMC8653899)

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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‐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.

Item Type:Articles
Additional Information:This work was supported by Wellcome Trust ISSF (097821/Z/11/Z and 204820/Z/16/Z to KRE), EU FP7 Marie Curie Career Integration Grant (321999 “GEN ECOL ADAPT” to KRE), and Carnegie Trust for the Universities of Scotland Research Incentive Grant (70287).
Status:Published
Refereed:Yes
Glasgow Author(s) Enlighten ID:Jacobs, Mr Arne and Elmer, Professor Kathryn
Authors: Jacobs, A., and Elmer, K. R.
College/School:College of Medical Veterinary and Life Sciences > Institute of Biodiversity Animal Health and Comparative Medicine
Journal Name:Molecular Ecology
Publisher:Wiley
ISSN:0962-1083
ISSN (Online):1365-294X
Published Online:27 January 2021
Copyright Holders:Copyright © 2021 The Authors
First Published:First published in Molecular Biology 30(20): 4955-4969
Publisher Policy:Reproduced under a Creative Commons License

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Project CodeAward NoProject NamePrincipal InvestigatorFunder's NameFunder RefLead Dept
190536Integrated Health - Polyomics and Systems Biomedicine (ISSF Bid)Anna DominiczakWellcome Trust (WELLCOTR)097821/Z/11/ZInstitute of Cardiovascular & Medical Sciences
173707Institutional Strategic Support Fund (2016)Anna DominiczakWellcome Trust (WELLCOTR)204820/Z/16/ZInstitute of Cardiovascular & Medical Sciences
171939Environmental and genomic drivers of diversity in Scottish fishes of high natural heritage valueKathryn ElmerThe Carnegie Trust for the Universities of Scotland (CARNEGTR)70287Institute of Biodiversity, Animal Health and Comparative Medicine