The genomic landscape at a late stage of stickleback speciation: high genomic divergence interspersed by small localized regions of introgression

Abstract

Speciation is a continuous process and analysis of species pairs at different stages of divergence provides insight into how it unfolds. Genomic studies on young species pairs have often revealed peaks of divergence and heterogeneous genomic differentiation. Yet it remains unclear how localised peaks of differentiation progress to genome-wide divergence during the later stages of speciation with gene flow. Spanning the speciation continuum, stickleback species pairs are ideal for investigating how genomic divergence builds up during speciation. However, attention has largely focused on young postglacial species pairs, with little known of the genomic signatures of divergence and introgression in older systems. The Japanese stickleback species pair, composed of the Pacific Ocean three-spined stickleback (Gasterosteus aculeatus) and the Japan Sea stickleback (G. nipponicus), which co-occur in the Japanese islands, is at a late stage of speciation. Divergence likely started well before the end of the last glacial period and crosses between Japan Sea females and Pacific Ocean males result in hybrid male sterility. Here we use coalescent analyses and Approximate Bayesian computation to show that the two species split approximately 0.68-1 million years ago but that they have continued to hybridise at a low rate throughout divergence. Population genomic data revealed that high levels of genomic differentiation are maintained across the majority of the genome when gene flow occurs. However despite this, we identified multiple, small regions of introgression, strongly correlated with recombination rate. Our results demonstrate that a high level of genome-wide divergence can establish in the face of persistent introgression and that gene flow can be localized to small genomic regions at the later stages of speciation with gene flow.\n\nAuthor summaryWhen species evolve, reproductive isolation leads to a build-up of differentiation in the genome where genes involved in the process occur. Much of our understanding of this comes from early stage speciation, with relatively few examples from more divergent species pairs that still exchange genes. To address this, we focused on Pacific Ocean and Japan Sea sticklebacks, which co-occur in the Japanese islands. We established that they are the oldest and most divergent known stickleback species pair, that they evolved in the face of gene flow and that this gene flow is still on going. We found introgression is confined to small, localised genomic regions where recombination rate is high. Our results show high divergence can be maintained between species, despite extensive gene flow.