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

Panmictic species, with their random mating and dispersal, challenge adaptation concepts. The European eel, a panmictic and threatened fish, presents various estuarine migration patterns at juvenile (glass eel) stage, ranging from sedentarization in brackish/saltwater of the estuary (Non-migrant individuals-NM) to Upstream colonization of freshwater ecosystems (Migrant individuals-M). We hypothesize that the propensity to migrate is partly genetically determined in glass eel, and employed two approaches to test our hypothesis. First, in a natural population, six pools were collected over three years at two extreme sites along a gradient from ocean to the tidal limit of the Adour River ("Ocean" vs. "Upstream"). Secondly, migrant vs. non-migrant glass eels were phenotypically sorted using an experimental device mimicking alternating tidal currents. 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 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 outlier SNPs with a significant genetic differentiation between migrant vs. non-migrant phenotypes (average FST = 0.51). These 28 outlier SNPs mapped to genes mainly involved in neuronal development, cell migration and tissue remodeling, transcriptional regulation, and metabolic or stress-related processes. Our results support that variation in eel migration propensity is partly genetically determined. Thus, 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.