Modular chromosome rearrangements reveal parallel and nonparallel adaptation in a marine fish

Abstract Genomic architecture and standing variation can play a key role in ecological adaptation and contribute to the predictability of evolution. In Atlantic cod (Gadus morhua), four large chromosomal rearrangements have been associated with ecological gradients and migratory behavior in regional...

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Published in:Ecology and Evolution
Main Authors: Tony Kess, Paul Bentzen, Sarah J. Lehnert, Emma V. A. Sylvester, Sigbjørn Lien, Matthew P. Kent, Marion Sinclair‐Waters, Corey Morris, Brendan Wringe, Robert Fairweather, Ian R. Bradbury
Format: Article in Journal/Newspaper
Language:English
Published: Wiley 2020
Subjects:
Online Access:https://doi.org/10.1002/ece3.5828
https://doaj.org/article/f67f5318c44c42a3b89760e39e6eac06
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spelling ftdoajarticles:oai:doaj.org/article:f67f5318c44c42a3b89760e39e6eac06 2023-05-15T15:26:55+02:00 Modular chromosome rearrangements reveal parallel and nonparallel adaptation in a marine fish Tony Kess Paul Bentzen Sarah J. Lehnert Emma V. A. Sylvester Sigbjørn Lien Matthew P. Kent Marion Sinclair‐Waters Corey Morris Brendan Wringe Robert Fairweather Ian R. Bradbury 2020-01-01T00:00:00Z https://doi.org/10.1002/ece3.5828 https://doaj.org/article/f67f5318c44c42a3b89760e39e6eac06 EN eng Wiley https://doi.org/10.1002/ece3.5828 https://doaj.org/toc/2045-7758 2045-7758 doi:10.1002/ece3.5828 https://doaj.org/article/f67f5318c44c42a3b89760e39e6eac06 Ecology and Evolution, Vol 10, Iss 2, Pp 638-653 (2020) Atlantic cod environmental association genomic architecture marine migration parallel evolution Ecology QH540-549.5 article 2020 ftdoajarticles https://doi.org/10.1002/ece3.5828 2022-12-31T11:23:50Z Abstract Genomic architecture and standing variation can play a key role in ecological adaptation and contribute to the predictability of evolution. In Atlantic cod (Gadus morhua), four large chromosomal rearrangements have been associated with ecological gradients and migratory behavior in regional analyses. However, the degree of parallelism, the extent of independent inheritance, and functional distinctiveness of these rearrangements remain poorly understood. Here, we use a 12K single nucleotide polymorphism (SNP) array to demonstrate extensive individual variation in rearrangement genotype within populations across the species range, suggesting that local adaptation to fine‐scale ecological variation is enabled by rearrangements with independent inheritance. Our results demonstrate significant association of rearrangements with migration phenotype and environmental gradients across the species range. Individual rearrangements exhibit functional modularity, but also contain loci showing multiple environmental associations. Clustering in genetic distance trees and reduced differentiation within rearrangements across the species range are consistent with shared variation as a source of contemporary adaptive diversity in Atlantic cod. Conversely, we also find that haplotypes in the LG12 and LG1 rearranged region have diverged across the Atlantic, despite consistent environmental associations. Exchange of these structurally variable genomic regions, as well as local selective pressures, has likely facilitated individual diversity within Atlantic cod stocks. Our results highlight the importance of genomic architecture and standing variation in enabling fine‐scale adaptation in marine species. Article in Journal/Newspaper atlantic cod Gadus morhua Directory of Open Access Journals: DOAJ Articles Ecology and Evolution 10 2 638 653
institution Open Polar
collection Directory of Open Access Journals: DOAJ Articles
op_collection_id ftdoajarticles
language English
topic Atlantic cod
environmental association
genomic architecture
marine
migration
parallel evolution
Ecology
QH540-549.5
spellingShingle Atlantic cod
environmental association
genomic architecture
marine
migration
parallel evolution
Ecology
QH540-549.5
Tony Kess
Paul Bentzen
Sarah J. Lehnert
Emma V. A. Sylvester
Sigbjørn Lien
Matthew P. Kent
Marion Sinclair‐Waters
Corey Morris
Brendan Wringe
Robert Fairweather
Ian R. Bradbury
Modular chromosome rearrangements reveal parallel and nonparallel adaptation in a marine fish
topic_facet Atlantic cod
environmental association
genomic architecture
marine
migration
parallel evolution
Ecology
QH540-549.5
description Abstract Genomic architecture and standing variation can play a key role in ecological adaptation and contribute to the predictability of evolution. In Atlantic cod (Gadus morhua), four large chromosomal rearrangements have been associated with ecological gradients and migratory behavior in regional analyses. However, the degree of parallelism, the extent of independent inheritance, and functional distinctiveness of these rearrangements remain poorly understood. Here, we use a 12K single nucleotide polymorphism (SNP) array to demonstrate extensive individual variation in rearrangement genotype within populations across the species range, suggesting that local adaptation to fine‐scale ecological variation is enabled by rearrangements with independent inheritance. Our results demonstrate significant association of rearrangements with migration phenotype and environmental gradients across the species range. Individual rearrangements exhibit functional modularity, but also contain loci showing multiple environmental associations. Clustering in genetic distance trees and reduced differentiation within rearrangements across the species range are consistent with shared variation as a source of contemporary adaptive diversity in Atlantic cod. Conversely, we also find that haplotypes in the LG12 and LG1 rearranged region have diverged across the Atlantic, despite consistent environmental associations. Exchange of these structurally variable genomic regions, as well as local selective pressures, has likely facilitated individual diversity within Atlantic cod stocks. Our results highlight the importance of genomic architecture and standing variation in enabling fine‐scale adaptation in marine species.
format Article in Journal/Newspaper
author Tony Kess
Paul Bentzen
Sarah J. Lehnert
Emma V. A. Sylvester
Sigbjørn Lien
Matthew P. Kent
Marion Sinclair‐Waters
Corey Morris
Brendan Wringe
Robert Fairweather
Ian R. Bradbury
author_facet Tony Kess
Paul Bentzen
Sarah J. Lehnert
Emma V. A. Sylvester
Sigbjørn Lien
Matthew P. Kent
Marion Sinclair‐Waters
Corey Morris
Brendan Wringe
Robert Fairweather
Ian R. Bradbury
author_sort Tony Kess
title Modular chromosome rearrangements reveal parallel and nonparallel adaptation in a marine fish
title_short Modular chromosome rearrangements reveal parallel and nonparallel adaptation in a marine fish
title_full Modular chromosome rearrangements reveal parallel and nonparallel adaptation in a marine fish
title_fullStr Modular chromosome rearrangements reveal parallel and nonparallel adaptation in a marine fish
title_full_unstemmed Modular chromosome rearrangements reveal parallel and nonparallel adaptation in a marine fish
title_sort modular chromosome rearrangements reveal parallel and nonparallel adaptation in a marine fish
publisher Wiley
publishDate 2020
url https://doi.org/10.1002/ece3.5828
https://doaj.org/article/f67f5318c44c42a3b89760e39e6eac06
genre atlantic cod
Gadus morhua
genre_facet atlantic cod
Gadus morhua
op_source Ecology and Evolution, Vol 10, Iss 2, Pp 638-653 (2020)
op_relation https://doi.org/10.1002/ece3.5828
https://doaj.org/toc/2045-7758
2045-7758
doi:10.1002/ece3.5828
https://doaj.org/article/f67f5318c44c42a3b89760e39e6eac06
op_doi https://doi.org/10.1002/ece3.5828
container_title Ecology and Evolution
container_volume 10
container_issue 2
container_start_page 638
op_container_end_page 653
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