title: Sex-dependent dominance at a single locus maintains variation in age at maturity in salmon.
abstract: 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.
authors.affiliation: Centre for Integrative Genetics (CIGENE), Department of Animal and Aquacultural Sciences, Norwegian University of Life Sciences, NO-1432 Ås, Norway.
authors.forename: Nicola J
authors.initials: NJ
authors.lastname: Barson
authors.affiliation: Department of Biology, University of Turku, FI-20014, Finland.
authors.forename: Tutku
authors.initials: T
authors.lastname: Aykanat
authors.affiliation: Norwegian Institute for Nature Research (NINA), NO-7485 Trondheim, Norway.
authors.forename: Kjetil
authors.initials: K
authors.lastname: Hindar
authors.affiliation: Nofima - Norwegian Institute of Food, Fisheries and Aquaculture Research, NO-1431 Ås, Norway.
authors.forename: Matthew
authors.initials: M
authors.lastname: Baranski
authors.affiliation: Norwegian Institute for Nature Research (NINA), NO-7485 Trondheim, Norway.
authors.forename: Geir H
authors.initials: GH
authors.lastname: Bolstad
authors.affiliation: Norwegian Institute for Nature Research (NINA), NO-7485 Trondheim, Norway.
authors.forename: Peder
authors.initials: P
authors.lastname: Fiske
authors.affiliation: Nofima - Norwegian Institute of Food, Fisheries and Aquaculture Research, NO-1431 Ås, Norway.
authors.forename: Céleste
authors.initials: C
authors.lastname: Jacq
authors.affiliation: Norwegian Institute for Nature Research (NINA), NO-7485 Trondheim, Norway.
authors.forename: Arne J
authors.initials: AJ
authors.lastname: Jensen
authors.affiliation: Institute of Evolutionary Biology, University of Edinburgh, Edinburgh EH9 3FL, UK.
authors.forename: Susan E
authors.initials: SE
authors.lastname: Johnston
authors.affiliation: Norwegian Institute for Nature Research (NINA), NO-7485 Trondheim, Norway.
authors.forename: Sten
authors.initials: S
authors.lastname: Karlsson
authors.affiliation: Centre for Integrative Genetics (CIGENE), Department of Animal and Aquacultural Sciences, Norwegian University of Life Sciences, NO-1432 Ås, Norway.
authors.forename: Matthew
authors.initials: M
authors.lastname: Kent
authors.affiliation: AquaGen, NO-7462 Trondheim, Norway.
authors.forename: Thomas
authors.initials: T
authors.lastname: Moen
authors.affiliation: Natural Resources Institute Finland, Oulu, FI-90014, Finland.
authors.forename: Eero
authors.initials: E
authors.lastname: Niemelä
authors.affiliation: Centre for Integrative Genetics (CIGENE), Department of Animal and Aquacultural Sciences, Norwegian University of Life Sciences, NO-1432 Ås, Norway.
authors.forename: Torfinn
authors.initials: T
authors.lastname: Nome
authors.affiliation: Norwegian Institute for Nature Research (NINA), NO-7485 Trondheim, Norway.
authors.forename: Tor F
authors.initials: TF
authors.lastname: Næsje
authors.affiliation: Natural Resources Institute Finland, Oulu, FI-90014, Finland.
authors.forename: Panu
authors.initials: P
authors.lastname: Orell
authors.affiliation: Natural Resources Institute Finland, Oulu, FI-90014, Finland.
authors.forename: Atso
authors.initials: A
authors.lastname: Romakkaniemi
authors.affiliation: Radgivende Biologer, NO-5003 Bergen, Norway.
authors.forename: Harald
authors.initials: H
authors.lastname: Sægrov
authors.affiliation: Radgivende Biologer, NO-5003 Bergen, Norway.
authors.forename: Kurt
authors.initials: K
authors.lastname: Urdal
authors.affiliation: Natural Resources Institute Finland, Oulu, FI-90014, Finland.
authors.forename: Jaakko
authors.initials: J
authors.lastname: Erkinaro
authors.affiliation: Centre for Integrative Genetics (CIGENE), Department of Animal and Aquacultural Sciences, Norwegian University of Life Sciences, NO-1432 Ås, Norway.
authors.forename: Sigbjørn
authors.initials: S
authors.lastname: Lien
authors.affiliation: Department of Biology, University of Turku, FI-20014, Finland.
authors.forename: Craig R
authors.initials: CR
authors.lastname: Primmer
mesh_terms: D000375:Aging / Q000235:genetics*; D000818:Animals; D005075:Biological Evolution; D049628:Body Size / Q000235:genetics*; D005260:Female; D029941:Fish Proteins / Q000235:genetics* / Q000378:metabolism; D014644:Genetic Variation / Q000235:genetics*; D055106:Genome-Wide Association Study; D006128:Growth / Q000235:genetics*; D006801:Humans; D008297:Male; D008954:Models, Biological; D010641:Phenotype; D012098:Reproduction / Q000235:genetics / Q000502:physiology; D020317:Salmo salar / Q000235:genetics*; D012727:Sex Characteristics; D014157:Transcription Factors / Q000235:genetics / Q000378:metabolism
chemical_list: D029941:Fish Proteins; D014157:Transcription Factors