Sex-dependent dominance at a single locus maintains variation in age at maturity in Atlantic 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 conflict1,2. Under such sexual antagonism, theory predicts the evolution of genetic architectures that resolve this sexual conflict2-6. Yet, despite intense theoretical and empirical interest, the specific genetic loci behind sexually antagonistic phenotypes have rarely been identified, limiting our understanding of how sexual conflict impacts genome evolution4,7,8 and the maintenance of genetic diversity8,9. Here, we identify a large effect locus controlling age at maturity in 57 salmon populations, an important fitness trait in which selection favours earlier maturation in males than females10, and show it is a clear example of sex dependent dominance reducing intralocus sexual conflict and maintaining adaptive variation in wild populations. Using high density SNP data and whole genome re-sequencing, we found that vestigial-like family member 3 (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 39.4% of phenotypic variation, an unexpectedly high effect size for what is usually considered a highly polygenic trait. Such large effects are predicted under balancing selection from either sexually antagonistic or spatially varying selection11-13. Our results provide the first empirical example of dominance reversal permitting greater optimisation 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 further 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.