Polygenic Adaptation to Variable Costal Environments in the Gilthead Sea Bream (Sparus aurata), Linking Selected Variants with Adaptive Phenotypes and Fitness

Understanding the genetic underpinnings of adaptation to ecologically contrasted habitats remains a major challenge in evolutionary biology. In the Mediterranean gilthead sea bream (Sparus aurata), juveniles use various marine and lagoonal nursery habitats characterized by a trade-off between food availability and stress linked to environmental instability. Phenotypic differences between habitats are observed at the end of the first year, but the extent to which differential survival among genotypes shape these phenotypic differences remains unclear. We screened genetic polymorphism genome-wide using RAD-sequencing in three samples from the same cohort, consisting of pre-settlement larvae and young juveniles that lived in two different habitats. Population genomic analyses provided evidence for divergent selection operating at multiple loci that have antagonistic additive effects on two fitness-related traits (growth and condition factor) across environments. We measured the adaptive landscape in each environment using pre-selection and post-selection samples, and found evidence for genotype-by-environment interaction for fitness, and a positive relationship between individual growth and fitness. Altogether, these results close the genotype-phenotype-fitness loop in a natural panmictic population, and provide an empirical estimate of the genetic load due to the segregation of locally adaptive polymorphisms underlying complex traits.