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 conflict 1,2 . Under such sexual antagonism, theory predicts the evolution of genetic architectures that resolve this sexual conflict 2-6 . 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 evolution 4,7,8 and the maintenance of genetic diversity 8,9 . 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 females 10 , 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 selection 11-13 . 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.

Consequences of genetic linkage for the maintenance of sexually antagonistic polymorphism in hermaphrodites

“…SA alleles have been shown to play an important role in the maintenance of genetic variation in fitness, the evolution of reproductive and life‐history traits, and genome evolution in a variety of theoretical and empirical contexts (Rice ; Prout ; Rice and Chippindale ; Bonduriansky and Chenoweth ; Cox and Calsbeek ; Fry ; Connallon and Clark ; Barson et al. ).…”

Association mapping reveals candidate loci for resistance and anaemic response to an emerging temperature‐driven parasitic disease in a wild salmonid fish

“…However, for the robust detection of a genotype–phenotype link, a much larger number of SNPs should preferably be used. For example, earlier attempts to identify genes that control the time of maturity in Atlantic salmon based on a 5.5‐K SNP chip did not detect a particular region in chromosome 25 (Johnston et al., ); the region was later discovered using a 220‐K SNP chip (Barson et al., ). Thus, it is possible that our study identified only a subset of genes that associate with variability in T. bryosalmonae infection resistance and severity of PKD in brown trout.…”

Single nucleotide polymorphisms to discriminate different classes of hybrid between wild Atlantic salmon and aquaculture escapees

“…New Teno Mainstem and Tornio fish were individually genotyped on the 220K array as part of the Barson et al. () study. New Teno Mainstem individuals were also combined into four separate pools and allelotyped.…”

“…To ensure correct identification of genotype clusters, we applied the Affymetrix Best Practices Protocol for SNP calling simultaneously to a large data set that included the Old Teno Mainstem and Teno Escapee samples and all individuals genotyped for Barson et al. (). For allelotyping, pooled samples were subjected to the standard genotyping methodology, but normalized and summarized Allele A and Allele B probe intensities were returned instead of genotype calls.…”

“…Individuals from Teno headwater and tributaries, and Finnmark Escapees, were pooled by population for allelotyping, which is a cost-effective approach for estimation of samplewide allele frequencies using SNP chips (Johnston et al, 2013;Sham, Bader, Craig, O'Donovan, & Owen, 2002). New Teno Mainstem and Tornio fish were individually genotyped on the 220K array as part of the Barson et al (2015) study. New Teno Mainstem individuals were also combined into four separate pools and allelotyped.…”