Ontogenetic variation in the marine foraging of Atlantic salmon functionally links genomic diversity with a major life history polymorphism

The ecological role of heritable phenotypic variation in free-living populations remains largely unknown. Knowledge of the genetic basis of functional ecological processes can link genomic and phenotypic diversity, providing insight into polymorphism evolution and how populations respond to environmental change. By quantifying the marine diet, of sub-adult Atlantic salmon, we assessed how foraging behavior changes along the ontogeny, and in relation to genetic variation in two loci with major effect on age-at-maturity (six6 and vgll3). We used a two-component, zero-inflated negative binomial model to simultaneously quantify foraging frequency (zero-inflation components) and foraging outcome (count component), separately for fish and crustaceans in the diet. We found that older salmon forage for both prey types more actively (as evidenced by increased foraging frequency), but with a decreased efficiency (as evidenced by fewer prey items in the diet), suggesting an age-dependent shift in foraging dynamics. The vgll3 locus was linked to age-dependent changes in foraging behavior: younger salmon with vgll3^LL (the genotype associated with late maturation) tend to forage crustaceans more often than those with vgll3^EE (the genotype associated with early maturation), while the pattern was reversed in older salmon. Vgll3 ^LL genotype was also linked to marginal increase in fish acquisition especially in younger salmon, while six6 was not a factor explaining the diet variation. Our results suggest a functional role for variation in marine feeding behavior linking genomic diversity at vgll3 with age-at-maturity among salmon, with potential age-dependent trade-offs maintaining the genetic variation. A shared genetic basis between dietary ecology and age-at-maturity likely subjects Atlantic salmon populations to evolution induced by bottom-up changes in marine productivity.