Genomic signatures of fine-scale local selection in Atlantic salmon suggest involvement of sexual maturation, energy homeostasis and immune defence-related genes

Elucidating the genetic basis of adaptation to the local environment can improve our understanding of how the diversity of life has evolved. In this study, we used a dense SNP array to identify candidate loci potentially underlying fine-scale local adaptation within a large Atlantic salmon (Salmo sa...

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Published in:Molecular Ecology
Main Authors: Pritchard, Victoria L., Makinen, Hannu, Vähä, Juha-Pekka, Erkinaro, Jaakko, Orell, Panu, Primmer, Craig R.
Other Authors: Biosciences, Organismal and Evolutionary Biology Research Programme, Evolution, Conservation, and Genomics, Helsinki Institute of Sustainability Science (HELSUS), Doctoral Programme in Wildlife Biology
Format: Article in Journal/Newspaper
Language:English
Published: Wiley 2021
Subjects:
Online Access:http://hdl.handle.net/10138/326500
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spelling ftunivhelsihelda:oai:helda.helsinki.fi:10138/326500 2024-01-07T09:42:10+01:00 Genomic signatures of fine-scale local selection in Atlantic salmon suggest involvement of sexual maturation, energy homeostasis and immune defence-related genes Pritchard, Victoria L. Makinen, Hannu Vähä, Juha-Pekka Erkinaro, Jaakko Orell, Panu Primmer, Craig R. Biosciences Organismal and Evolutionary Biology Research Programme Evolution, Conservation, and Genomics Helsinki Institute of Sustainability Science (HELSUS) Doctoral Programme in Wildlife Biology 2021-02-16T08:53:01Z 16 application/pdf http://hdl.handle.net/10138/326500 eng eng Wiley 10.1111/mec.14705 Suomen Akatemia, Grant/Award Number: 284941, 314254; Suomen Kulttuurirahasto Pritchard , V L , Makinen , H , Vähä , J-P , Erkinaro , J , Orell , P & Primmer , C R 2018 , ' Genomic signatures of fine-scale local selection in Atlantic salmon suggest involvement of sexual maturation, energy homeostasis and immune defence-related genes ' , Molecular Ecology , vol. 27 , no. 11 , pp. 2560-2575 . https://doi.org/10.1111/mec.14705 ORCID: /0000-0002-3687-8435/work/47430067 85051777368 7388b976-8225-433b-b6f7-6fe5bfbace90 http://hdl.handle.net/10138/326500 000434152100006 openAccess info:eu-repo/semantics/openAccess Atlantic salmon ecotype local selection microgeographic adaptation sockeye salmon MAJOR HISTOCOMPATIBILITY COMPLEX HOMEODOMAIN PROTEIN SIX6 CLASS-II COMBINATIONS MHC CLASS-I SOCKEYE-SALMON ONCORHYNCHUS-TSHAWYTSCHA STRUCTURED POPULATIONS EVOLUTIONARY ECOLOGY POSITIVE SELECTION WILD POPULATIONS 1181 Ecology evolutionary biology Article acceptedVersion 2021 ftunivhelsihelda 2023-12-14T00:02:20Z Elucidating the genetic basis of adaptation to the local environment can improve our understanding of how the diversity of life has evolved. In this study, we used a dense SNP array to identify candidate loci potentially underlying fine-scale local adaptation within a large Atlantic salmon (Salmo salar) population. By combining outlier, gene-environment association and haplotype homozygosity analyses, we identified multiple regions of the genome with strong evidence for diversifying selection. Several of these candidate regions had previously been identified in other studies, demonstrating that the same loci could be adaptively important in Atlantic salmon at subdrainage, regional and continental scales. Notably, we identified signals consistent with local selection around genes associated with variation in sexual maturation, energy homeostasis and immune defence. These included the large-effect age-at-maturity gene vgll3, the known obesity gene mc4r, and major histocompatibility complex II. Most strikingly, we confirmed a genomic region on Ssa09 that was extremely differentiated among subpopulations and that is also a candidate for local selection over the global range of Atlantic salmon. This region colocalized with a haplotype strongly associated with spawning ecotype in sockeye salmon (Oncorhynchus nerka), with circumstantial evidence that the same gene (six6) may be the selective target in both cases. The phenotypic effect of this region in Atlantic salmon remains cryptic, although allelic variation is related to upstream catchment area and covaries with timing of the return spawning migration. Our results further inform management of Atlantic salmon and open multiple avenues for future research. Peer reviewed Article in Journal/Newspaper Atlantic salmon Salmo salar HELDA – University of Helsinki Open Repository Sockeye ENVELOPE(-130.143,-130.143,54.160,54.160) Molecular Ecology 27 11 2560 2575
institution Open Polar
collection HELDA – University of Helsinki Open Repository
op_collection_id ftunivhelsihelda
language English
topic Atlantic salmon
ecotype
local selection
microgeographic adaptation
sockeye salmon
MAJOR HISTOCOMPATIBILITY COMPLEX
HOMEODOMAIN PROTEIN SIX6
CLASS-II COMBINATIONS
MHC CLASS-I
SOCKEYE-SALMON
ONCORHYNCHUS-TSHAWYTSCHA
STRUCTURED POPULATIONS
EVOLUTIONARY ECOLOGY
POSITIVE SELECTION
WILD POPULATIONS
1181 Ecology
evolutionary biology
spellingShingle Atlantic salmon
ecotype
local selection
microgeographic adaptation
sockeye salmon
MAJOR HISTOCOMPATIBILITY COMPLEX
HOMEODOMAIN PROTEIN SIX6
CLASS-II COMBINATIONS
MHC CLASS-I
SOCKEYE-SALMON
ONCORHYNCHUS-TSHAWYTSCHA
STRUCTURED POPULATIONS
EVOLUTIONARY ECOLOGY
POSITIVE SELECTION
WILD POPULATIONS
1181 Ecology
evolutionary biology
Pritchard, Victoria L.
Makinen, Hannu
Vähä, Juha-Pekka
Erkinaro, Jaakko
Orell, Panu
Primmer, Craig R.
Genomic signatures of fine-scale local selection in Atlantic salmon suggest involvement of sexual maturation, energy homeostasis and immune defence-related genes
topic_facet Atlantic salmon
ecotype
local selection
microgeographic adaptation
sockeye salmon
MAJOR HISTOCOMPATIBILITY COMPLEX
HOMEODOMAIN PROTEIN SIX6
CLASS-II COMBINATIONS
MHC CLASS-I
SOCKEYE-SALMON
ONCORHYNCHUS-TSHAWYTSCHA
STRUCTURED POPULATIONS
EVOLUTIONARY ECOLOGY
POSITIVE SELECTION
WILD POPULATIONS
1181 Ecology
evolutionary biology
description Elucidating the genetic basis of adaptation to the local environment can improve our understanding of how the diversity of life has evolved. In this study, we used a dense SNP array to identify candidate loci potentially underlying fine-scale local adaptation within a large Atlantic salmon (Salmo salar) population. By combining outlier, gene-environment association and haplotype homozygosity analyses, we identified multiple regions of the genome with strong evidence for diversifying selection. Several of these candidate regions had previously been identified in other studies, demonstrating that the same loci could be adaptively important in Atlantic salmon at subdrainage, regional and continental scales. Notably, we identified signals consistent with local selection around genes associated with variation in sexual maturation, energy homeostasis and immune defence. These included the large-effect age-at-maturity gene vgll3, the known obesity gene mc4r, and major histocompatibility complex II. Most strikingly, we confirmed a genomic region on Ssa09 that was extremely differentiated among subpopulations and that is also a candidate for local selection over the global range of Atlantic salmon. This region colocalized with a haplotype strongly associated with spawning ecotype in sockeye salmon (Oncorhynchus nerka), with circumstantial evidence that the same gene (six6) may be the selective target in both cases. The phenotypic effect of this region in Atlantic salmon remains cryptic, although allelic variation is related to upstream catchment area and covaries with timing of the return spawning migration. Our results further inform management of Atlantic salmon and open multiple avenues for future research. Peer reviewed
author2 Biosciences
Organismal and Evolutionary Biology Research Programme
Evolution, Conservation, and Genomics
Helsinki Institute of Sustainability Science (HELSUS)
Doctoral Programme in Wildlife Biology
format Article in Journal/Newspaper
author Pritchard, Victoria L.
Makinen, Hannu
Vähä, Juha-Pekka
Erkinaro, Jaakko
Orell, Panu
Primmer, Craig R.
author_facet Pritchard, Victoria L.
Makinen, Hannu
Vähä, Juha-Pekka
Erkinaro, Jaakko
Orell, Panu
Primmer, Craig R.
author_sort Pritchard, Victoria L.
title Genomic signatures of fine-scale local selection in Atlantic salmon suggest involvement of sexual maturation, energy homeostasis and immune defence-related genes
title_short Genomic signatures of fine-scale local selection in Atlantic salmon suggest involvement of sexual maturation, energy homeostasis and immune defence-related genes
title_full Genomic signatures of fine-scale local selection in Atlantic salmon suggest involvement of sexual maturation, energy homeostasis and immune defence-related genes
title_fullStr Genomic signatures of fine-scale local selection in Atlantic salmon suggest involvement of sexual maturation, energy homeostasis and immune defence-related genes
title_full_unstemmed Genomic signatures of fine-scale local selection in Atlantic salmon suggest involvement of sexual maturation, energy homeostasis and immune defence-related genes
title_sort genomic signatures of fine-scale local selection in atlantic salmon suggest involvement of sexual maturation, energy homeostasis and immune defence-related genes
publisher Wiley
publishDate 2021
url http://hdl.handle.net/10138/326500
long_lat ENVELOPE(-130.143,-130.143,54.160,54.160)
geographic Sockeye
geographic_facet Sockeye
genre Atlantic salmon
Salmo salar
genre_facet Atlantic salmon
Salmo salar
op_relation 10.1111/mec.14705
Suomen Akatemia, Grant/Award Number: 284941, 314254; Suomen Kulttuurirahasto
Pritchard , V L , Makinen , H , Vähä , J-P , Erkinaro , J , Orell , P & Primmer , C R 2018 , ' Genomic signatures of fine-scale local selection in Atlantic salmon suggest involvement of sexual maturation, energy homeostasis and immune defence-related genes ' , Molecular Ecology , vol. 27 , no. 11 , pp. 2560-2575 . https://doi.org/10.1111/mec.14705
ORCID: /0000-0002-3687-8435/work/47430067
85051777368
7388b976-8225-433b-b6f7-6fe5bfbace90
http://hdl.handle.net/10138/326500
000434152100006
op_rights openAccess
info:eu-repo/semantics/openAccess
container_title Molecular Ecology
container_volume 27
container_issue 11
container_start_page 2560
op_container_end_page 2575
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