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.

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

“…Our hierarchical Arlequin analysis of STW_WILD versus AQUA identified three outlier SNPs within ContigGCR_hBin7522_Ctg1 ( Ssa 25: 28.53 Mb) downstream from a genomic region associated with sea age in wild salmon populations ( Ssa 25: 28.58 to 28.75 for males in Ayllon et al. (2015); Ssa 25: 28.64 to 28.78 Mb for males and females in Barson et al. (2015)).…”

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

“…Recently, variation in sea age in Atlantic Salmon has been attributed to a major selective sweep containing the candidate locus ( vgll3 , vestigial‐like family member 3, a 4‐kb gene located on chromosome 25 consisting of 4 exons of 460, 440, 570, and 600 bp and no splicing variants) in European populations (Ayllon et al., 2015; Barson et al., 2015). 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).…”

“…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). However, the causative SNPs or other possible causal variants still remain to be elucidated.…”

“…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).…”

“…1SW males predominantly exhibited methionine and asparagine at amino acid positions #54 and #323 in the vgll3 protein, respectively, whereas 3SW males more likely exhibited threonine and lysine at those positions and Met54Thr vgll3 and Asn323Lys vgll3 explained 33% and 36% of sea age (Ayllon et al., 2015). Besides vgll3 , two additional, but less supported candidate genes for sea age were identified: akap11 ( a‐kinase anchor protein 11 ) (Ayllon et al., 2015; Barson et al., 2015) and six6 (Barson et al., 2015).…”