Data from: Sex-dependent dominance at a single locus maintains variation in age at maturity in salmon

Males and females share many traits that have a common genetic basis; however, selection on these traits often differs between the sexes, leading to sexual conflict. Under such sexual antagonism, theory predicts the evolution of genetic architectures that resolve this sexual conflict. Yet, despite i...

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Main Authors: Barson, Nicola J., Aykanat, Tuku, Hindar, Kjetil, Baranski, Matthew, Bolstad, Geir H., Fiske, Peder, Jacq, Céleste, Jensen, Arne J., Johnston, Susan E., Karlsson, Sten, Kent, Matthew, Moen, Thomas, Niemelä, Eero, Nome, Torfinn, Næsje, Tor F., Orell, Panu, Romakkaniemi, Atso, Sægrov, Harald, Urdal, Kurt, Erkinaro, Jaakko, Lien, Sigbjørn, Primmer, Craig R.
Format: Article in Journal/Newspaper
Language:unknown
Published: 2015
Subjects:
Online Access:http://hdl.handle.net/10255/dryad.99100
https://doi.org/10.5061/dryad.23h4q
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spelling ftdryad:oai:v1.datadryad.org:10255/dryad.99100 2023-05-15T15:32:58+02:00 Data from: Sex-dependent dominance at a single locus maintains variation in age at maturity in salmon Barson, Nicola J. Aykanat, Tuku Hindar, Kjetil Baranski, Matthew Bolstad, Geir H. Fiske, Peder Jacq, Céleste Jensen, Arne J. Johnston, Susan E. Karlsson, Sten Kent, Matthew Moen, Thomas Niemelä, Eero Nome, Torfinn Næsje, Tor F. Orell, Panu Romakkaniemi, Atso Sægrov, Harald Urdal, Kurt Erkinaro, Jaakko Lien, Sigbjørn Primmer, Craig R. Norway Finland 2015-11-05T18:58:52Z http://hdl.handle.net/10255/dryad.99100 https://doi.org/10.5061/dryad.23h4q unknown doi:10.5061/dryad.23h4q/1 doi:10.5061/dryad.23h4q/2 doi:10.1038/nature16062 PMID:26536110 doi:10.5061/dryad.23h4q Barson NJ, Aykanat T, Hindar K, Baranski M, Bolstad GH, Fiske P, Jacq C, Jensen AJ, Johnston SE, Karlsson S, Kent M, Moen T, Niemelä E, Nome T, Næsje TF, Orell P, Romakkaniemi A, Sægrov H, Urdal K, Erkinaro J, Lien S, Primmer CR (2015) Sex-dependent dominance at a single locus maintains variation in age at maturity in salmon. Nature 528(7582): 405-408. http://hdl.handle.net/10255/dryad.99100 age at maturity sexual conflict local adaptation evolutionary genetics population genetics fisheries GWAS Article 2015 ftdryad https://doi.org/10.5061/dryad.23h4q https://doi.org/10.5061/dryad.23h4q/1 https://doi.org/10.5061/dryad.23h4q/2 https://doi.org/10.1038/nature16062 2020-01-01T15:25:30Z Males and females share many traits that have a common genetic basis; however, selection on these traits often differs between the sexes, leading to sexual conflict. Under such sexual antagonism, theory predicts the evolution of genetic architectures that resolve this sexual conflict. Yet, despite intense theoretical and empirical interest, the specific loci underlying sexually antagonistic phenotypes have rarely been identified, limiting our understanding of how sexual conflict impacts genome evolution and the maintenance of genetic diversity. Here we identify a large effect locus controlling age at maturity in Atlantic salmon (Salmo salar), an important fitness trait in which selection favours earlier maturation in males than females and show it is a clear example of sex-dependent dominance that reduces intralocus sexual conflict and maintains adaptive variation in wild populations. Using high-density single nucleotide polymorphism data across 57 wild populations and whole genome re-sequencing, we find that the vestigial-like family member 3 gene (VGLL3) exhibits sex-dependent dominance in salmon, promoting earlier and later maturation in males and females, respectively. VGLL3, an adiposity regulator associated with size and age at maturity in humans, explained 39% of phenotypic variation, an unexpectedly large proportion for what is usually considered a highly polygenic trait. Such large effects are predicted under balancing selection from either sexually antagonistic or spatially varying selection. Our results provide the first empirical example of dominance reversal allowing greater optimization of phenotypes within each sex, contributing to the resolution of sexual conflict in a major and widespread evolutionary trade-off between age and size at maturity. They also provide key empirical evidence for how variation in reproductive strategies can be maintained over large geographical scales. We anticipate these findings will have a substantial impact on population management in a range of harvested species where trends towards earlier maturation have been observed. Article in Journal/Newspaper Atlantic salmon Salmo salar Dryad Digital Repository (Duke University) Norway
institution Open Polar
collection Dryad Digital Repository (Duke University)
op_collection_id ftdryad
language unknown
topic age at maturity
sexual conflict
local adaptation
evolutionary genetics
population genetics
fisheries
GWAS
spellingShingle age at maturity
sexual conflict
local adaptation
evolutionary genetics
population genetics
fisheries
GWAS
Barson, Nicola J.
Aykanat, Tuku
Hindar, Kjetil
Baranski, Matthew
Bolstad, Geir H.
Fiske, Peder
Jacq, Céleste
Jensen, Arne J.
Johnston, Susan E.
Karlsson, Sten
Kent, Matthew
Moen, Thomas
Niemelä, Eero
Nome, Torfinn
Næsje, Tor F.
Orell, Panu
Romakkaniemi, Atso
Sægrov, Harald
Urdal, Kurt
Erkinaro, Jaakko
Lien, Sigbjørn
Primmer, Craig R.
Data from: Sex-dependent dominance at a single locus maintains variation in age at maturity in salmon
topic_facet age at maturity
sexual conflict
local adaptation
evolutionary genetics
population genetics
fisheries
GWAS
description Males and females share many traits that have a common genetic basis; however, selection on these traits often differs between the sexes, leading to sexual conflict. Under such sexual antagonism, theory predicts the evolution of genetic architectures that resolve this sexual conflict. Yet, despite intense theoretical and empirical interest, the specific loci underlying sexually antagonistic phenotypes have rarely been identified, limiting our understanding of how sexual conflict impacts genome evolution and the maintenance of genetic diversity. Here we identify a large effect locus controlling age at maturity in Atlantic salmon (Salmo salar), an important fitness trait in which selection favours earlier maturation in males than females and show it is a clear example of sex-dependent dominance that reduces intralocus sexual conflict and maintains adaptive variation in wild populations. Using high-density single nucleotide polymorphism data across 57 wild populations and whole genome re-sequencing, we find that the vestigial-like family member 3 gene (VGLL3) exhibits sex-dependent dominance in salmon, promoting earlier and later maturation in males and females, respectively. VGLL3, an adiposity regulator associated with size and age at maturity in humans, explained 39% of phenotypic variation, an unexpectedly large proportion for what is usually considered a highly polygenic trait. Such large effects are predicted under balancing selection from either sexually antagonistic or spatially varying selection. Our results provide the first empirical example of dominance reversal allowing greater optimization of phenotypes within each sex, contributing to the resolution of sexual conflict in a major and widespread evolutionary trade-off between age and size at maturity. They also provide key empirical evidence for how variation in reproductive strategies can be maintained over large geographical scales. We anticipate these findings will have a substantial impact on population management in a range of harvested species where trends towards earlier maturation have been observed.
format Article in Journal/Newspaper
author Barson, Nicola J.
Aykanat, Tuku
Hindar, Kjetil
Baranski, Matthew
Bolstad, Geir H.
Fiske, Peder
Jacq, Céleste
Jensen, Arne J.
Johnston, Susan E.
Karlsson, Sten
Kent, Matthew
Moen, Thomas
Niemelä, Eero
Nome, Torfinn
Næsje, Tor F.
Orell, Panu
Romakkaniemi, Atso
Sægrov, Harald
Urdal, Kurt
Erkinaro, Jaakko
Lien, Sigbjørn
Primmer, Craig R.
author_facet Barson, Nicola J.
Aykanat, Tuku
Hindar, Kjetil
Baranski, Matthew
Bolstad, Geir H.
Fiske, Peder
Jacq, Céleste
Jensen, Arne J.
Johnston, Susan E.
Karlsson, Sten
Kent, Matthew
Moen, Thomas
Niemelä, Eero
Nome, Torfinn
Næsje, Tor F.
Orell, Panu
Romakkaniemi, Atso
Sægrov, Harald
Urdal, Kurt
Erkinaro, Jaakko
Lien, Sigbjørn
Primmer, Craig R.
author_sort Barson, Nicola J.
title Data from: Sex-dependent dominance at a single locus maintains variation in age at maturity in salmon
title_short Data from: Sex-dependent dominance at a single locus maintains variation in age at maturity in salmon
title_full Data from: Sex-dependent dominance at a single locus maintains variation in age at maturity in salmon
title_fullStr Data from: Sex-dependent dominance at a single locus maintains variation in age at maturity in salmon
title_full_unstemmed Data from: Sex-dependent dominance at a single locus maintains variation in age at maturity in salmon
title_sort data from: sex-dependent dominance at a single locus maintains variation in age at maturity in salmon
publishDate 2015
url http://hdl.handle.net/10255/dryad.99100
https://doi.org/10.5061/dryad.23h4q
op_coverage Norway
Finland
geographic Norway
geographic_facet Norway
genre Atlantic salmon
Salmo salar
genre_facet Atlantic salmon
Salmo salar
op_relation doi:10.5061/dryad.23h4q/1
doi:10.5061/dryad.23h4q/2
doi:10.1038/nature16062
PMID:26536110
doi:10.5061/dryad.23h4q
Barson NJ, Aykanat T, Hindar K, Baranski M, Bolstad GH, Fiske P, Jacq C, Jensen AJ, Johnston SE, Karlsson S, Kent M, Moen T, Niemelä E, Nome T, Næsje TF, Orell P, Romakkaniemi A, Sægrov H, Urdal K, Erkinaro J, Lien S, Primmer CR (2015) Sex-dependent dominance at a single locus maintains variation in age at maturity in salmon. Nature 528(7582): 405-408.
http://hdl.handle.net/10255/dryad.99100
op_doi https://doi.org/10.5061/dryad.23h4q
https://doi.org/10.5061/dryad.23h4q/1
https://doi.org/10.5061/dryad.23h4q/2
https://doi.org/10.1038/nature16062
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