Genome annotation of Apeltes quadracus

Chromosomal fusions have been hypothesized to facilitate adaptation to divergent environments, both by bringing together previously unlinked adaptive alleles and by creating regions of low recombination that facilitate the linkage of adaptive alleles. But, there is little empirical evidence to support this hypothesis. Here, we address this knowledge gap by studying threespine stickleback (Gasterosteus aculeatus), in which ancestral marine fish have repeatedly adapted to freshwater across the northern hemisphere. By comparing the threespine stickleback genome to a de novo assembly of the fourspine stickleback (Apeltes quadracus) and an outgroup species, we find two chromosomal fusion events have occurred in the threespine stickleback lineage. On these fused chromosomes, we find an enrichment of quantitative trait loci (QTL) underlying traits that contribute to marine versus freshwater adaptation. By comparing whole genome sequences of freshwater and marine threespine stickleback populations, we also find an enrichment of regions under divergent selection on these two fused chromosomes. Surprisingly, we find elevated genetic diversity within regions under selection in the freshwater population. However, these results are consistent with a recent simulation study showing that gene flow can increase diversity in genomic regions associated with local adaptation. Our demographic models provide evidence for gene flow between the marine and freshwater populations. By combining our results with those of previous studies, we propose that these fusions created regions of low recombination that enabled the formation of adaptative clusters, thereby facilitating freshwater adaptation in the face of recurrent gene flow between marine and freshwater threespine sticklebacks.