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

Age at maturity in Atlantic salmon (Salmo salar) is governed to a substantial extent by a locus showing dominance reversal, providing a resolution for sexual conflict in this trait, for which selection favours different ages in the two sexes. Craig Primmer and colleagues use genome-wide association studies for age at maturity in Atlantic salmon to show that a single gene, VGLL3, strongly influences the variation in age at maturity, and therefore body size—a key trait in an important fished species. They find that the VGLL3 locus is an example of sex-dependent dominance, promoting earlier and later maturation in males and females, respectively. This mechanism provides a resolution for sexual conflict in this trait, for which selection favours different reproductive ages in the two sexes. Females benefit from being large (5–15 kg), and stay longer at sea feeding by maturing later, while males can have high fitness maturing at smaller sizes (1–3 kg). This discovery will have a substantial impact on population management of Atlantic salmon, where a decrease in the frequency of late maturation has been observed in many populations. 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.