Genetic differentiation between two locations along an ocean/river gradient captures the signature of intragenerational selection in the European eel (Anguilla anguilla)

Abstract

AO_SCPLOWBSTRACTC_SCPLOWMigration 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 18.99 106 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 FST = 0.21) compared to the pangenomic estimate (FST = 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 FST = 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.