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

Mark Ravinet,Atsushi Toyoda,Shuji Shigenobu,Kohta Yoshida,Asao Fujiyama,Jun Kitano,Bret A Payseur

doi:10.1371/journal.pgen.1007358

Abstract

Speciation is a continuous process and analysis of species pairs at different stages of divergence provides insight into how it unfolds. Previous genomic studies on young species pairs have revealed peaks of divergence and heterogeneous genomic differentiation. Yet less known is how localised peaks of differentiation progress to genome-wide divergence during the later stages of speciation in the presence of persistent 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 knowledge of the genomic signatures of divergence and introgression in older stickleback 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 exchange genes at a low rate throughout divergence. Population genomic data revealed that, despite gene flow, a high level of genomic differentiation is maintained across the majority of the genome. However, we identified multiple, small regions of introgression, occurring mainly in areas of low 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.

Highlights

Speciation is a continuous process through which reproductive isolation is established [1,2,3]
98.8% support the split between species, while only 0.51% indicate clustering of fish occurring in Japan
Since the consensus autosomal phylogeny suggests a more recent split between the Japanese Pacific and Atlantic G. aculeatus lineages than the split in the mitochondrial phylogeny, the two mitogenome clades may represent the split between G. aculeatus and G. nipponicus lineages with mitochondrial introgression likely having occurred from the Japan Sea G. nipponicus into the Pacific Ocean G. aculeatus in sympatry

Summary

Introduction

Speciation is a continuous process through which reproductive isolation is established [1,2,3]. According to the genic view of speciation [4], when populations are in contact, gene flow is initially restricted at barrier loci (i.e. loci underlying reproductive isolation), leading to the emergence of peaks of genetic differentiation surrounding such barriers; i.e. heterogeneous genomic differentiation [5,6]. As speciation progresses, this localised build-up of reproductive isolation spreads to nearby regions due to linkage disequilibrium [4,5,7]. Several thorough genomic studies on old sympatric species pairs exist, including European rabbits [13], Drosophila species [14], sunflowers [15], whitefishes [16], flycatchers [17,18], wild mice [19], Mimulus [20] and stick insects [9]; except in a few cases, such as with Heliconius [21,22], divergence is thought to have occurred during periods of geographical isolation

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