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

Abstract

Natural selection can maintain local adaptation despite the presence of gene flow. However, the genomic basis and environmental factors involved in adaptation at fine-spatial scales are not well understood. Here, we address these questions using Atlantic herring (Clupea harengus), an abundant, migratory, and widely distributed marine species with substantial genomic resources including a chromosome-level genome assembly and genomic data from the eastern Atlantic and Baltic populations. We analysed whole-genome sequence and oceanographic data to examine the genetic variation of 15 spawning aggregations across the northwest Atlantic Ocean ([~]1,600 km of coastline) and the association of this variation with environmental variables. We found that population structure lies in a small fraction of the genome involving adaptive genetic variants of functional importance. We discovered 10 highly differentiated genomic regions distributed across four chromosomes. Two of these loci appear to be private to the northwest, four loci share a large number of adaptive variants between northwest and northeast Atlantic, and four shared loci exhibit an outstanding diversity in haplotype composition, including a novel putative inversion on chromosome 8. Another inversion on chromosome 12 underlies a latitudinal genetic pattern discriminating populations north and south of a biogeographic transition zone on the Scotian Shelf. Our genome-environment association analysis indicates that sea water temperature during winter is the environmental factor that best correlates with the latitudinal pattern of this inversion. We conclude that the timing and geographic location of spawning and early development are under diverse selective pressures related to environmental gradients. Natural selection appears to act on early-life performance traits with differential fitness across environments. Our study highlights the role of genomic architecture, ancestral haplotypes, and selection in maintaining adaptive divergence in species with large population sizes and presumably high gene flow.