Patterns of genomic divergence and introgression between Japanese stickleback species with overlapping breeding habitats

With only a few absolute geographic barriers in marine environments, the factors maintaining reproductive isolation among marine organisms remain elusive. However, spatial structuring in breeding habitat can contribute to reproductive isolation. This is particularly important for marine organisms that migrate to use fresh- or brackish water environments to breed. The Japanese Gasterosteus stickleback species, the Pacific Ocean three-spined stickleback (G. aculeatus) and the Japan Sea stickleback (G. nipponicus) overwinter in the sea, but migrate to rivers for spawning. Although they co-occur at several locations across the Japanese islands, they are reproductively isolated. Our previous studies in Bekanbeushi River showed that the Japan Sea stickleback spawns in the estuary, while the Pacific Ocean stickleback mainly spawns further upstream in freshwater. Overall genomic divergence was very high with many interspersed regions of introgression. Here, we investigated genomic divergence and introgression between the sympatric species in the much shorter Tokotan River, where they share spawning sites. The levels of genome-wide divergence were reduced and introgression was increased, suggesting that habitat isolation substantially contributes to a reduction in gene flow. We also found that genomic regions of introgression were largely shared between the two systems. Furthermore, some regions of introgression were located near loci with a heterozygote advantage for juvenile survival. Taken together, introgression may be partially driven by adaptation in this system. Although, the two species remain clearly genetically differentiated. Regions with low recombination rates showed especially low introgression. Speciation reversal is therefore likely prevented by barriers other than habitat isolation.

Automated summary

Maintaining reproductive isolation factors in marine environments remain elusive due to few absolute geographic barriers. Spatial structuring in breeding habitat can contribute to reproductive isolation, especially for marine organisms migrating to fresh- or brackish water environments. Geological barrier differences between Japanese Gasterosteus species contribute to high genomic divergence and varying levels of introgression, particularly in rivers where spawning sites are shared. Habitat isolation is found to significantly reduce gene flow, while certain genomic regions of introgression indicate potential adaptation driving introgression. Despite genetic differentiation, low introgression occurs in regions with low recombination rates, suggesting other barriers may prevent speciation reversal.