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. Author summary When 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.

Parallel transcriptome evolution in stream threespine sticklebacks

“…Therefore, differences in both gene flow and divergence time may explain the difference in the DEG number between the Canadian and Japanese pairs. A further phylogenomic analysis will enable us to more precisely estimate both the time of freshwater colonization and the magnitude of gene flow between the stream and neighboring marine populations, as previously conducted in other stickleback systems (Marques, Jones, Di Palma, Kingsley, & Reimchen, ; Ravinet et al., ; Roesti, Kueng, Moser, & Berner, ). In addition, given the fact that an antiparallel DEG was equally common as a parallel DEG in a previous study (Hanson et al., ), it is necessary to investigate the transcriptome of other stickleback systems to understand the prevalence of parallel and antiparallel types of transcriptome evolution.…”

“…The Japanese crosses were made from wild‐caught fish: The Japanese marine and stream ecotypes were collected from Akkeshi (Kitano et al., ; Ravinet et al., ) and Gifu (Cassidy, Ravinet, Mori, & Kitano, ; Ravinet, Takeuchi, Kume, Mori, & Kitano, ), respectively. The Canadian pure crosses of both marine and stream ecotypes were made from laboratory colonies originated from the Little Campbell River in Canada (Hagen, ).…”

Speciation in protists: Spatial and ecological divergence processes cause rapid species diversification in a freshwater chrysophyte

“…However, species may also emerge in sympatry when gene flow is present (Richards et al, ). Interestingly, genomic studies based primarily on animal models show that high levels of genome‐wide divergence can be established along with ongoing gene flow (Martin et al, ; Ravinet et al, ). Unfortunately, no such genomic studies have been performed in protists so far, with the exception of investigations based on yeasts (Leducq et al, ).…”

Predictors of genomic differentiation within a hybrid taxon

“…Exploiting the patterns of population differentiation within hybrid species may reveal novel insights into the selective forces shaping hybrid genomes. Interestingly, patterns of species differentiation are affected by the recombination rate landscape [37,38,39]. This can result in highly correlated patterns of divergence between closely related species pairs, such as that found in flycatchers [37].…”