The vgll3 Locus Controls Age at Maturity in Wild and Domesticated Atlantic Salmon(Salmo salar L.) Males

Abstract

Wild and domesticated Atlantic salmon males display large variation for sea age at sexual maturation, which varies between 1–5 years. Previous studies have uncovered a genetic predisposition for variation of age at maturity with moderate heritability, thus suggesting a polygenic or complex nature of this trait. The aim of this study was to identify associated genetic loci, genes and ultimately specific sequence variants conferring sea age at maturity in salmon. We performed a genome wide association study (GWAS) using a pool sequencing approach (20 individuals per river and phenotype) of male salmon returning to rivers as sexually mature either after one sea winter (2009) or three sea winters (2011) in six rivers in Norway. The study revealed one major selective sweep, which covered 76 significant SNPs in which 74 were found in a 370 kb region of chromosome 25. Genotyping other smolt year classes of wild and domesticated salmon confirmed this finding. Genotyping domesticated fish narrowed the haplotype region to four SNPs covering 2386 bp, containing the vgll3 gene, including two missense mutations explaining 33–36% phenotypic variation. A single locus was found to have a highly significant role in governing sea age at maturation in this species. The SNPs identified may be both used as markers to guide breeding for late maturity in salmon aquaculture and in monitoring programs of wild salmon. Interestingly, a SNP in proximity of the VGLL3 gene in humans (Homo sapiens), has previously been linked to age at puberty suggesting a conserved mechanism for timing of puberty in vertebrates. Author Summary. For most species the factors that contribute to the genetic predisposition for age at maturity are currently unknown. In salmon aquaculture early maturation is negative for the growth, disease resistance and flesh quality. In addition, using populations of salmon selected to mature late may limit the genetic impact of aquaculture escapees, as these late maturing fish are more likely to die before they reach maturity. The aim of this study was to elucidate the genetic predisposition for salmon maturation. We determined the sequences of genomes from Atlantic salmon maturing early and late in six Norwegian rivers. This methodology enabled us to identify a short genomic region involved in determining the age at maturity in male Atlantic salmon. This region has also previously been linked to time of puberty in humans–supporting a general mechanism behind age at maturity in vertebrates. The results of this study may be used to breed salmon that are genetically predisposed to mature late which will improve welfare and production in aquaculture industry and aid in the management of escaped farmed salmon.