Comparison of anadromous and landlocked Atlantic salmon genomes reveals signatures of parallel and relaxed selection across the Northern Hemisphere

Abstract Most Atlantic salmon (Salmo salar L.) populations follow an anadromous life cycle, spending early life in freshwater, migrating to the sea for feeding, and returning to rivers to spawn. At the end of the last ice age ~10,000 years ago, several populations of Atlantic salmon became landlocke...

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Main Authors: Erik Kjærner‐Semb, Rolf B. Edvardsen, Fernando Ayllon, Petra Vogelsang, Tomasz Furmanek, Carl Johan Rubin, Alexey E. Veselov, Tom Ole Nilsen, Stephen D. McCormick, Craig R. Primmer, Anna Wargelius
Format: Article
Language:English
Published: Wiley 2021-02-01
Series:Evolutionary Applications
Subjects:
Online Access:https://doi.org/10.1111/eva.13129
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spelling doaj-89857d12ce504f158aee83a97d68ea502021-02-20T16:47:35ZengWileyEvolutionary Applications1752-45712021-02-0114244646110.1111/eva.13129Comparison of anadromous and landlocked Atlantic salmon genomes reveals signatures of parallel and relaxed selection across the Northern HemisphereErik Kjærner‐Semb0Rolf B. Edvardsen1Fernando Ayllon2Petra Vogelsang3Tomasz Furmanek4Carl Johan Rubin5Alexey E. Veselov6Tom Ole Nilsen7Stephen D. McCormick8Craig R. Primmer9Anna Wargelius10Institute of Marine Research Bergen NorwayInstitute of Marine Research Bergen NorwayInstitute of Marine Research Bergen NorwayInstitute of Marine Research Bergen NorwayInstitute of Marine Research Bergen NorwayUppsala University Uppsala SwedenInstitute of Biology of the Karelian Research Centre Petrozavodsk RussiaDepartment of Biological Sciences University of Bergen Bergen NorwayConte Anadromous Fish Research Laboratory U.S. Geological Survey, Leetown Science Center Turners Falls MA USAOrganismal and Evolutionary Biology Research Program Faculty of Biological and Environmental Sciences University of Helsinki Helsinki FinlandInstitute of Marine Research Bergen NorwayAbstract Most Atlantic salmon (Salmo salar L.) populations follow an anadromous life cycle, spending early life in freshwater, migrating to the sea for feeding, and returning to rivers to spawn. At the end of the last ice age ~10,000 years ago, several populations of Atlantic salmon became landlocked. Comparing their genomes to their anadromous counterparts can help identify genetic variation related to either freshwater residency or anadromy. The objective of this study was to identify consistently divergent loci between anadromous and landlocked Atlantic salmon strains throughout their geographical distribution, with the long‐term aim of identifying traits relevant for salmon aquaculture, including fresh and seawater growth, omega‐3 metabolism, smoltification, and disease resistance. We used a Pool‐seq approach (n = 10–40 individuals per population) to sequence the genomes of twelve anadromous and six landlocked Atlantic salmon populations covering a large part of the Northern Hemisphere and conducted a genomewide association study to identify genomic regions having been under different selection pressure in landlocked and anadromous strains. A total of 28 genomic regions were identified and included cadm1 on Chr 13 and ppargc1a on Chr 18. Seven of the regions additionally displayed consistently reduced heterozygosity in fish obtained from landlocked populations, including the genes gpr132, cdca4, and sertad2 on Chr 15. We also found 16 regions, including igf1 on Chr 17, which consistently display reduced heterozygosity in the anadromous populations compared to the freshwater populations, indicating relaxed selection on traits associated with anadromy in landlocked salmon. In conclusion, we have identified 37 regions which may harbor genetic variation relevant for improving fish welfare and quality in the salmon farming industry and for understanding life‐history traits in fish.https://doi.org/10.1111/eva.13129disease resistancefreshwater residentGWASpool sequencingSalmo salarseawater adaptation
collection DOAJ
language English
format Article
sources DOAJ
author Erik Kjærner‐Semb
Rolf B. Edvardsen
Fernando Ayllon
Petra Vogelsang
Tomasz Furmanek
Carl Johan Rubin
Alexey E. Veselov
Tom Ole Nilsen
Stephen D. McCormick
Craig R. Primmer
Anna Wargelius
spellingShingle Erik Kjærner‐Semb
Rolf B. Edvardsen
Fernando Ayllon
Petra Vogelsang
Tomasz Furmanek
Carl Johan Rubin
Alexey E. Veselov
Tom Ole Nilsen
Stephen D. McCormick
Craig R. Primmer
Anna Wargelius
Comparison of anadromous and landlocked Atlantic salmon genomes reveals signatures of parallel and relaxed selection across the Northern Hemisphere
Evolutionary Applications
disease resistance
freshwater resident
GWAS
pool sequencing
Salmo salar
seawater adaptation
author_facet Erik Kjærner‐Semb
Rolf B. Edvardsen
Fernando Ayllon
Petra Vogelsang
Tomasz Furmanek
Carl Johan Rubin
Alexey E. Veselov
Tom Ole Nilsen
Stephen D. McCormick
Craig R. Primmer
Anna Wargelius
author_sort Erik Kjærner‐Semb
title Comparison of anadromous and landlocked Atlantic salmon genomes reveals signatures of parallel and relaxed selection across the Northern Hemisphere
title_short Comparison of anadromous and landlocked Atlantic salmon genomes reveals signatures of parallel and relaxed selection across the Northern Hemisphere
title_full Comparison of anadromous and landlocked Atlantic salmon genomes reveals signatures of parallel and relaxed selection across the Northern Hemisphere
title_fullStr Comparison of anadromous and landlocked Atlantic salmon genomes reveals signatures of parallel and relaxed selection across the Northern Hemisphere
title_full_unstemmed Comparison of anadromous and landlocked Atlantic salmon genomes reveals signatures of parallel and relaxed selection across the Northern Hemisphere
title_sort comparison of anadromous and landlocked atlantic salmon genomes reveals signatures of parallel and relaxed selection across the northern hemisphere
publisher Wiley
series Evolutionary Applications
issn 1752-4571
publishDate 2021-02-01
description Abstract Most Atlantic salmon (Salmo salar L.) populations follow an anadromous life cycle, spending early life in freshwater, migrating to the sea for feeding, and returning to rivers to spawn. At the end of the last ice age ~10,000 years ago, several populations of Atlantic salmon became landlocked. Comparing their genomes to their anadromous counterparts can help identify genetic variation related to either freshwater residency or anadromy. The objective of this study was to identify consistently divergent loci between anadromous and landlocked Atlantic salmon strains throughout their geographical distribution, with the long‐term aim of identifying traits relevant for salmon aquaculture, including fresh and seawater growth, omega‐3 metabolism, smoltification, and disease resistance. We used a Pool‐seq approach (n = 10–40 individuals per population) to sequence the genomes of twelve anadromous and six landlocked Atlantic salmon populations covering a large part of the Northern Hemisphere and conducted a genomewide association study to identify genomic regions having been under different selection pressure in landlocked and anadromous strains. A total of 28 genomic regions were identified and included cadm1 on Chr 13 and ppargc1a on Chr 18. Seven of the regions additionally displayed consistently reduced heterozygosity in fish obtained from landlocked populations, including the genes gpr132, cdca4, and sertad2 on Chr 15. We also found 16 regions, including igf1 on Chr 17, which consistently display reduced heterozygosity in the anadromous populations compared to the freshwater populations, indicating relaxed selection on traits associated with anadromy in landlocked salmon. In conclusion, we have identified 37 regions which may harbor genetic variation relevant for improving fish welfare and quality in the salmon farming industry and for understanding life‐history traits in fish.
topic disease resistance
freshwater resident
GWAS
pool sequencing
Salmo salar
seawater adaptation
url https://doi.org/10.1111/eva.13129
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