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

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...

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Published in:Ecology and Evolution
Main Authors: Kess, Tony, Bentzen, Paul, Lehnert, Sarah, Sylvester, Emma V. A., Lien, Sigbjørn, Kent, Matthew Peter, Sinclair-Waters, Marion, Morris, Corey, Wringe, Brendan, Fairweather, Robert, Bradbury, Ian R.
Format: Article in Journal/Newspaper
Language:English
Published: John Wiley & Sons 2019
Subjects:
Online Access:http://hdl.handle.net/11250/2638598
https://doi.org/10.1002/ece3.5828
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spelling ftntnutrondheimi:oai:ntnuopen.ntnu.no:11250/2638598 2023-05-15T15:27:04+02:00 Modular chromosome rearrangements reveal parallel and nonparallel adaptation in a marine fish Kess, Tony Bentzen, Paul Lehnert, Sarah Sylvester, Emma V. A. Lien, Sigbjørn Kent, Matthew Peter Sinclair-Waters, Marion Morris, Corey Wringe, Brendan Fairweather, Robert Bradbury, Ian R. 2019 http://hdl.handle.net/11250/2638598 https://doi.org/10.1002/ece3.5828 eng eng John Wiley & Sons Ecology and Evolution. 2020 urn:issn:2045-7758 http://hdl.handle.net/11250/2638598 https://doi.org/10.1002/ece3.5828 cristin:1781074 Navngivelse 4.0 Internasjonal http://creativecommons.org/licenses/by/4.0/deed.no CC-BY Ecology and Evolution Journal article Peer reviewed 2019 ftntnutrondheimi https://doi.org/10.1002/ece3.5828 2020-02-05T23:32:30Z 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. publishedVersion © 2019 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. Article in Journal/Newspaper atlantic cod Gadus morhua NTNU Open Archive (Norwegian University of Science and Technology) Ecology and Evolution 10 2 638 653
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collection NTNU Open Archive (Norwegian University of Science and Technology)
op_collection_id ftntnutrondheimi
language English
description 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. publishedVersion © 2019 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
format Article in Journal/Newspaper
author Kess, Tony
Bentzen, Paul
Lehnert, Sarah
Sylvester, Emma V. A.
Lien, Sigbjørn
Kent, Matthew Peter
Sinclair-Waters, Marion
Morris, Corey
Wringe, Brendan
Fairweather, Robert
Bradbury, Ian R.
spellingShingle Kess, Tony
Bentzen, Paul
Lehnert, Sarah
Sylvester, Emma V. A.
Lien, Sigbjørn
Kent, Matthew Peter
Sinclair-Waters, Marion
Morris, Corey
Wringe, Brendan
Fairweather, Robert
Bradbury, Ian R.
Modular chromosome rearrangements reveal parallel and nonparallel adaptation in a marine fish
author_facet Kess, Tony
Bentzen, Paul
Lehnert, Sarah
Sylvester, Emma V. A.
Lien, Sigbjørn
Kent, Matthew Peter
Sinclair-Waters, Marion
Morris, Corey
Wringe, Brendan
Fairweather, Robert
Bradbury, Ian R.
author_sort Kess, Tony
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 John Wiley & Sons
publishDate 2019
url http://hdl.handle.net/11250/2638598
https://doi.org/10.1002/ece3.5828
genre atlantic cod
Gadus morhua
genre_facet atlantic cod
Gadus morhua
op_source Ecology and Evolution
op_relation Ecology and Evolution. 2020
urn:issn:2045-7758
http://hdl.handle.net/11250/2638598
https://doi.org/10.1002/ece3.5828
cristin:1781074
op_rights Navngivelse 4.0 Internasjonal
http://creativecommons.org/licenses/by/4.0/deed.no
op_rightsnorm CC-BY
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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