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

Abstract

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 changes. By quantifying the marine diet of Atlantic salmon, we assessed how foraging behavior changes along the ontogeny, and in relation to genetic variation in two loci with major effects on age at maturity (six6 and vgll3). We used a two-component, zero-inflated negative binomial model to simultaneously quantify foraging frequency and foraging outcome, separately for fish and crustaceans diets. 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 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 vgll3LL (the genotype associated with late maturation) tended to forage crustaceans more often than those with vgll3EE (the genotype associated with early maturation), whereas the pattern was reversed in older salmon. Vgll3 LL genotype was also linked to a 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 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.