Genomics of Rapid Incipient Speciation in Sympatric Threespine Stickleback

Abstract

Ecological speciation is the process by which reproductively isolated populations emerge as a consequence of divergent natural or ecologically-mediated sexual selection. Most genomic studies of ecological speciation have investigated allopatric populations, making it difficult to infer reproductive isolation. The few studies on sympatric ecotypes have focused on advanced stages of the speciation process after thousands of generations of divergence. As a consequence, we still do not know what genomic signatures of the early onset of ecological speciation look like. Here, we examined genomic differentiation among migratory lake and resident stream ecotypes of threespine stickleback reproducing in sympatry in one stream, and in parapatry in another stream. Importantly, these ecotypes started diverging less than 150 years ago. We obtained 34,756 SNPs with restriction-site associated DNA sequencing and identified genomic islands of differentiation using a Hidden Markov Model approach. Consistent with incipient ecological speciation, we found significant genomic differentiation between ecotypes both in sympatry and parapatry. Of 19 islands of differentiation resisting gene flow in sympatry, all were also differentiated in parapatry and were thus likely driven by divergent selection among habitats. These islands clustered in quantitative trait loci controlling divergent traits among the ecotypes, many of them concentrated in one region with low to intermediate recombination. Our findings suggest that adaptive genomic differentiation at many genetic loci can arise and persist in sympatry at the very early stage of ecotype divergence, and that the genomic architecture of adaptation may facilitate this.

Author Summary

Ecological speciation can be defined as the evolution of new, reproductively isolated, species driven by natural selection and ecologically-mediated sexual selection. Its genomic signature has mainly been studied in ecotypes and emerging species that started diverging hundreds to thousands of generations ago, while little is known about the very early stages of species divergence. To fill this knowledge gap, we studied whether and how threespine stickleback, which have adapted either to lake or to stream environments in less than 150 years, differ across their genomes. We found several segments of the genome to be clearly divergent between lake and stream ecotypes, even when both forms breed side by side in the same area. Strikingly, this genomic differentiation was mainly concentrated in one region with low to intermediate recombination rates and clustered around genes controlling ecotype-specific phenotypic traits. Our findings suggest that genomic differentiation can arise despite gene flow already very early at the onset of speciation, and that its occurrence may be facilitated by the genomic organization of genes that control traits involved in adaptation and reproductive isolation.