Weak but consistent genomic signals of intragenerational selection during estuarine migration in the European eel ( Anguilla anguilla )

A bstract Migration events can act as strong selective filters by spatially sorting individuals according to their migration ability, behaviour, and associated functional traits. The European eel, a panmictic and threatened fish, presents various estuarine migration patterns at juvenile stage (glass eel), ranging from sedentarization in brackish/saltwater of the estuary (non-migrant phenotype) to upstream colonisation of freshwater ecosystems (migrant phenotype). We hypothesize that migration propensity is partly genetically determined in glass eel, and that migration-related genotypes are spatially sorted during estuarine migration. To test these hypotheses, we first collected six pools of individuals over three years at two extreme sites along a gradient from ocean to Adour River tidal limit (Ocean vs. Upstream). Secondly, we collected additional glass eels and phenotypically sorted migrant vs. non-migrant individuals using an experimental device mimicking alternating tidal currents, producing two other pools. Whole genome pool sequencing and analysis of these eight pools generated 18.99 10 6 SNP variants. Controlling for linked selection through a local score approach, we found five best outlier SNPs with a significant genetic differentiation between Ocean vs. Upstream sites (average F ST = 0.21) compared to the pangenomic estimate ( F ST = 0.0086). These five SNPs were all found in the same gene (gpb2), involved in interferon-mediated antiviral immune responses. We also found 28 best outlier SNPs with a significant genetic differentiation between migrant vs. non-migrant phenotypes (average F ST = 0.51). They were located in genes mainly involved in neuronal development, cell migration and tissue remodelling, transcriptional regulation, and metabolic or stress-related processes. Our results support that variation in eel migration propensity is partly genetically determined and that, while panmixia maintains high level of genetic diversity, spatial sorting could promote intra-generational genetic divergence between habitats of European eels. However, the absence of shared genes among the best outliers between in-situ and experimental contrasts suggests a complex and context-dependent genetic control of migration.