Genomic signatures of fine‐scale local selection in Atlantic salmon suggest involvement of sexual maturation, energy homeostasis and immune defence‐related genes

Abstract

Elucidating the genetic basis of adaptation to the local environment can improve our understanding of how the diversity of life has evolved. In this study, we used a dense SNP array to identify candidate loci potentially underlying fine-scale local adaptation within a large Atlantic salmon (Salmo salar) population. By combining outlier, gene-environment association and haplotype homozygosity analyses, we identified multiple regions of the genome with strong evidence for diversifying selection. Several of these candidate regions had previously been identified in other studies, demonstrating that the same loci could be adaptively important in Atlantic salmon at subdrainage, regional and continental scales. Notably, we identified signals consistent with local selection around genes associated with variation in sexual maturation, energy homeostasis and immune defence. These included the large-effect age-at-maturity gene vgll3, the known obesity gene mc4r, and major histocompatibility complex II. Most strikingly, we confirmed a genomic region on Ssa09 that was extremely differentiated among subpopulations and that is also a candidate for local selection over the global range of Atlantic salmon. This region colocalized with a haplotype strongly associated with spawning ecotype in sockeye salmon (Oncorhynchus nerka), with circumstantial evidence that the same gene (six6) may be the selective target in both cases. The phenotypic effect of this region in Atlantic salmon remains cryptic, although allelic variation is related to upstream catchment area and covaries with timing of the return spawning migration. Our results further inform management of Atlantic salmon and open multiple avenues for future research.

Life history genomic regions explain differences in Atlantic salmon marine diet specialization

“…In Atlantic salmon, two genomic regions on chromosomes 9 and 25 have been shown to have a disproportionate influence on life history strategy and population differentiation within and among populations (Ayllon et al 2015, Barson et al 2015, Czorlich et al 2018, Pritchard et al 2018, Aykanat et al 2019). The so-called vgll3 and six6 genomic regions are named after the most prominent genes in their respective haploblocks on chromosomes 25 and 9, respectively.…”

Chromosomal fusion and life history-associated genomic variation contribute to within-river local adaptation of Atlantic salmon

“…Most of the outliers we detected were localized to a 250 Kb region of chromosome 9 that has previously been implicated in important life history variation for this species. In European Atlantic salmon, a particular a gene in this region, six6, has been associated with age-at-maturity in Atlantic salmon in Europe (Barson et al, 2015;Johnston et al, 2014), differences in run-timing within rivers, and local adaptation between tributaries (Cauwelier et al, 2017;Pritchard et al, 2018). Our study is the first to report direct evidence of within-river variation at this locus in a North American population of Atlantic salmon.…”

“…Clearly more work is needed to link genomic variation with important phenotypic and life history variation in this system. In Europe, Pritchard et al (Pritchard et al, 2018) found an association of the six6 locus with a variable explaining "flow volume" for Atlantic salmon in the Teno/Tana River in Norway. Our results for a North American system thus suggest that stream parameters related to river size (flow volume and velocity) that differ between upper and lower reaches of large river systems may be mechanisms driving convergent local adaptations across continents and represents avenues for future study in relation to known differences in morphology and life history.…”

“…Thirteen different genes were in proximity to outlier SNPs and could represent putative targets of selection (Table 3). Of particular note, the region on chromosome 9 includes the gene six6, which has previously been linked to age-and possibly size-at-maturity in Atlantic salmon in Europe (Barson et al, 2015;Johnston et al, 2014) as well as run-timing (Cauwelier et al, 2017;Pritchard et al, 2018).…”

Genetic correlation between sea age at maturity and iteroparity in Atlantic salmon

“…Sampled fish were captured in the last four weeks of the fishing season, in August (two to four weeks after most individuals have entered the river), to minimize the number of fish from tributary and headwater populations (Erkinaro et al, 2010). Using the abovementioned dataset, Aykanat et al (2015) identified two subpopulations that have been subsequently identified to represent the Teno mainstem (Tenojoki, referred to as sub-population 1 and Inarijoki (sub-population 2) sub-populations (Pritchard et al, 2018).…”