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 conflict1,2. Under such sexual antagonism, theory predicts the evolution of genetic architectures that resolve this sexual conflict2,3,4,5. 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 evolution3,6 and the maintenance of genetic diversity6,7. 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 females8, 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 selection9,10. 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.

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Primary accessions

European Nucleotide Archive

Data deposits

Details of the SNPs used in the study have been deposited in dbSNP (http://www.ncbi.nlm.nih.gov/SNP/) under accession numbers ss1867919552–ss1868858426, and re-sequencing data have been deposited in EMBL Nucleotide Sequence Database (European Nucleotide Archive) under accession number PRJEB10744. SNP genotype and phenotype data and detailed DNA sequence information of the main candidate gene regions are available in Dryad (http://dx.doi.org/10.5061/dryad. 23h4q).


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We thank L. Andersson, T. F. Hansen and H. Granroth-Wilding for commenting on earlier drafts of the manuscript. We also acknowledge the numerous fishers who contributed scales and phenotypic information. We thank J. Haantie, J. G. Jensås, J. Kuusela, I. Torvi and G. Østborg for scale measurements, T. Andersstuen, T. Balstad, L. Birkeland Eriksen, S. Karoliussen, J. Kuismin, M. Lindqvist, T. Pajula, K. Salminen, K. Sõstar, M. Spets and K. Vagonyte-Hallan for laboratory assistance, M. Ellmen, O. Guttorm, T. Kanniainen, A. Koskinen, T. Pöyhönen and S. Uusi-Heikkilä for sampling assistance, and T. Mulugeta for informatics support. Bioinformatic analyses used resources at the Finnish Centre for Scientific Computing, the Abel Cluster, owned by the University of Oslo and the Norwegian Metacenter for High Performance Computing, and operated by the Department for Research Computing at the University of Oslo IT Department and the Orion Computing Cluster at CIGENE. This study was funded by the Finnish Academy (grants 137710, 141231, 272836, 284941), the Research Council of Norway (QuantEscape, grant 216105 and RCN-project 221734/O30) and by AquaGen (SNP array development).

Author information

Author notes

    • Nicola J. Barson
    •  & Tutku Aykanat

    These authors contributed equally to this work.


  1. Centre for Integrative Genetics (CIGENE), Department of Animal and Aquacultural Sciences, Norwegian University of Life Sciences, NO-1432 Ås, Norway

    • Nicola J. Barson
    • , Matthew Kent
    • , Torfinn Nome
    •  & Sigbjørn Lien
  2. Department of Biology, University of Turku, FI-20014, Finland

    • Tutku Aykanat
    •  & Craig R. Primmer
  3. Norwegian Institute for Nature Research (NINA), NO-7485 Trondheim, Norway

    • Kjetil Hindar
    • , Geir H. Bolstad
    • , Peder Fiske
    • , Arne J. Jensen
    • , Sten Karlsson
    •  & Tor F. Næsje
  4. Nofima - Norwegian Institute of Food, Fisheries and Aquaculture Research, NO-1431 Ås, Norway

    • Matthew Baranski
    •  & Céleste Jacq
  5. Institute of Evolutionary Biology, University of Edinburgh, Edinburgh EH9 3FL, UK

    • Susan E. Johnston
  6. AquaGen, NO-7462 Trondheim, Norway

    • Thomas Moen
  7. Natural Resources Institute Finland, Oulu, FI-90014, Finland

    • Eero Niemelä
    • , Panu Orell
    • , Atso Romakkaniemi
    •  & Jaakko Erkinaro
  8. Radgivende Biologer, NO-5003 Bergen, Norway

    • Harald Sægrov
    •  & Kurt Urdal


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C.R.P., S.L., N.J.B., T.A. and K.H. conceived the study. C.R.P., S.L., N.J.B., T.A., K.H., C.J., S.K. and S.E.J. designed the experiments. T.M. led the development of the 220K SNP array, and M.K. and T.N. generated and conducted bioinformatics on the molecular data. K.H., P.F., A.J.J., T.F.N., H.S., K.U., J.E., P.O., A.R. and E.N. coordinated the collection of phenotypic data. T.A., N.J.B., M.B., G.H.B., S.K. and C.J. analysed the data. N.J.B., T.A. and C.R.P. wrote the manuscript. All authors read and commented on the manuscript. C.R.P. and S.L. contributed equally as senior authors.

Corresponding authors

Correspondence to Sigbjørn Lien or Craig R. Primmer.

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