Adaptation to seasonal reproduction and thermal minima-related factors drives fine-scale divergence despite gene flow in Atlantic herring populations

Abstract

High connectivity and low potential for local adaptation have been common assumptions for most marine species, given their usual high fecundity and dispersal capabilities. Recent genomic studies however, have disclosed unprecedented levels of population subdivision in what were previously presumed to be panmictic or nearly panmictic species. Here we analyzed neutral and adaptive genetic variation at the whole-genome level in Atlantic herring ( Clupea harengus L.) spawning aggregations distributed across the reproductive range of the species in North America. We uncovered fine-scale population structure at putatively adaptive loci, despite low genetic differentiation at neutral loci. Our results revealed an intricate pattern of population subdivision involving two overlapping axes of divergence: a temporal axis determined by seasonal reproduction, and a spatial axis defined by a latitudinal cline establishing a steep north-south genetic break. Genetic-environment association analyses indicated that winter sea-surface temperature is the best predictor of the spatial structure observed. Thousands of outlier SNPs distributed along specific parts of the genome spanning numerous candidate genes underlined each pattern of differentiation, forming so-called “genomic regions or islands of divergence”. Our results indicate that timing of reproduction and latitudinal spawning location are features under disruptive selection leading to local adaptation in the herring. Our study highlights the importance of preserving functional and neutral intraspecific diversity, and the utility of an integrative seascape genomics approach for disentangling intricate patterns of intraspecific diversity in highly dispersive and abundant marine species.