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.

A genome scan for selection signatures comparing farmed Atlantic salmon with two wild populations: Testing colocalization among outlier markers, candidate genes, and quantitative trait loci for production traits

“…(2015); Ssa 25: 28.64 to 28.78 Mb for males and females in Barson et al. (2015)). The gene “ccdc138” containing these three SNPs was near the “sea age” at maturity region only 0.0386 Mb downstream from the associated locus “chmp2b” and only 0.116474 Mb downstream from the candidate gene “vgll3”.…”

“…In addition, our hierarchical Arlequin analysis of TOB_WILD versus AQUA identified an outlier locus in a similar position (ESTNV_34703_1491 on Ssa 09: 27.5 Mb and 52.7 cM female map) to one previously associated with sea age in wild Atlantic salmon populations (Johnston et al., 2014) that was not significant in a second GWAS after accounting for population structure (Barson et al., 2015). It also identified a consistent outlier GCR_cBin15233_Ctg1_136_V2 on Ssa 15 near the TSHR (the thyrotropin receptor) (Table 4).…”

Understanding and monitoring the consequences of human impacts on intraspecific variation

“…For instance, by combining genotypic and phenotypic data of Atlantic salmon ( Salmo salar ), Barson et al. (2015) found a sex‐dependent dominance of the gene affecting age maturity; a heterozygote induces late maturity in females and early maturity in males. This finding in the genetic mechanism controlling the key traits may have significant impact on the population managements where the harvesting consequentially selected for early maturation (e.g., Olsen et al., 2005).…”

Characterization of natural variation in North American Atlantic Salmon populations (Salmonidae: Salmo salar) at a locus with a major effect on sea age

“…A combined approach of a SNP‐based genomewide association study on 1,404 individuals from 57 populations and whole‐genome resequencing of 32 individuals revealed that vgll3 explained 39% of the variation in sea age (Barson et al., 2015). Moreover, an independently conducted study on both domesticated and wild Atlantic Salmon from Western Norway narrowed down the candidate region to a 2.4‐kb stretch within the vgll3 gene (Ayllon et al., 2015).…”

“…The two alleles at the vgll3 locus are associated either with early (E) maturation and thus low sea age, or with late (L) maturation and higher sea age (Ayllon et al., 2015; Barson et al., 2015). Moreover, sex‐dependent dominance of E and L alleles was documented (Barson et al., 2015).…”