Beyond large-effect loci: large-scale GWAS reveals a mixed large-effect and polygenic architecture for age at maturity of Atlantic salmon

Abstract

Background Understanding genetic architecture is essential for determining how traits will change in response to evolutionary processes such as selection, genetic drift and/or gene flow. In Atlantic salmon, age at maturity is an important life history trait that affects factors such as survival, reproductive success, and growth. Furthermore, age at maturity can seriously impact aquaculture production. Therefore, characterizing the genetic architecture that underlies variation in age at maturity is of key interest. Results Here, we refine our understanding of the genetic architecture for age at maturity of male Atlantic salmon using a genome-wide association study of 11,166 males from a single aquaculture strain, using imputed genotypes at 512,397 single nucleotide polymorphisms (SNPs). All individuals were genotyped with a 50K SNP array and imputed to higher density using parents genotyped with a 930K SNP array and pedigree information. We found significant association signals on 28 of 29 chromosomes (P-values: 8.7 × 10−133–9.8 × 10−8), including two very strong signals spanning the six6 and vgll3 gene regions on chromosomes 9 and 25, respectively. Furthermore, we identified 116 independent signals that tagged 120 candidate genes with varying effect sizes. Five of the candidate genes found here were previously associated with age at maturity in other vertebrates, including humans. Discussion These results reveal a mixed architecture of large-effect loci and a polygenic component that consists of multiple smaller-effect loci, suggesting a more complex genetic architecture of Atlantic salmon age at maturity than previously thought. This more complex architecture will have implications for selection on this key trait in aquaculture and for management of wild salmon populations.

Consequences of Single-Locus and Tightly Linked Genomic Architectures for Evolutionary Responses to Environmental Change

“… Sinclair-Waters et al (2020) recently characterized the mixed-effect architecture of age-at-maturity in Atlantic salmon, using an extensive genome-wide association study of 11,166 males from a single aquaculture strain, combined with high-density SNP arrays and pedigree information. Including the previously known large-effect vgll3 and six6 loci, they identified 120 genes contributing to age-at-maturity with various effect sizes.…”

“…Unfortunately, such large-scale, high-throughput approaches as used for Atlantic salmon ( Sinclair-Waters et al 2020 ) are not feasible for most non-model species, which typically lack pedigree information and sufficient sample sizes and genomic resources, especially when they are of conservation concern. When the precise architecture is unknown, the genomic background (e.g., population or ecotype) in which a large-effect variant occurs can be considered as to whether it potentially influences expression of the focal variant for the trait of interest, but only if the variant is polymorphic within different genomic backgrounds.…”

A mobile sex-determining region, male-specific haplotypes, and rearing environment influence age at maturity in Chinook salmon

“…This tradeoff might be particularly critical in semelparous species which experience a single reproductive episode before death. Age at maturity is often assumed to be influenced by many genes of small effect; however, recent studies have shown that the genomics of maturation age can be complex with mixed large-effect and polygenic architecture (Barson et al 2015, Sinclair-Waters et al 2020). While there are few cases where the genetic architecture of age at maturity is known, the genetic basis of age at maturation has important implications for how populations respond to selection (Kuparinen and Hutchings 2017) and how age diversity can be recovered if lost.…”

“…In Atlantic salmon, a single gene (VGLL3) explains 39% of the variation in age at maturity in European populations (Barson et al 2015) but does not appear to influence age at maturity in North American populations (Boulding et al 2019). In an aquacultural strain of Atlantic salmon, multiple genomic regions, including the VGLL3 gene, explained a total of 78% of the variation in age at maturity (Sinclair-Waters et al 2020). In Chinook salmon, the specific genes underlying variation in age at maturity are unknown but GWAS has identified SNPs associated with age at maturity on several autosomes (Micheletti and Narum 2018, Waters et al 2018) and male-specific sex chromosome haplotypes are associated with variation in size and age at maturity in male Chinook salmon from Alaska (McKinney et al 2019b).…”

Life history shifts in an exploited African fish following invasion by a castrating parasite

“…In this case, smaller fish are likely to have a higher probability of survival than the larger ones, and among them, those that can mature and reproduce early will be selected (Jorgensenet al , 2007;Jørgensen et al , 2009). Assuming that early maturation is heritable to some extent, this should result in life histories changing towards earlier reproduction at smaller sizes (Heathet al , 2002;Olsen et al , 2004;Ayllon et al , 2015;Sinclair-Waters et al , 2020).…”