Genomics of Rapid Incipient Speciation in Sympatric Threespine Stickleback

David A Marques,Catherine E Wagner,Kay Lucek,Salome Mwaiko,Laurent Excoffier,Joana I Meier,Ole Seehausen,Graham Coop

doi:10.1371/journal.pgen.1005887

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.

Highlights

The question of how and why populations split and diverge into new species is foundational to the field of evolutionary biology
Ecological speciation can be defined as the evolution of new, reproductively isolated, species driven by natural selection and ecologically-mediated sexual selection
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. This genomic differentiation was mainly concentrated in one region with low to intermediate recombination rates and clustered around genes controlling ecotype-specific phenotypic traits

Summary

Introduction

The question of how and why populations split and diverge into new species is foundational to the field of evolutionary biology. Speciation driven by divergent natural selection and by ecologically-mediated sexual selection, termed ‘ecological speciation’ [2], has come into the focus of speciation genomics This is because genomic data allows us to make inferences on the relationship between individual phenotype and genotype, to detect targets of selection and to infer past and present gene flow among emerging species. Other barrier loci conferring intrinsic post-zygotic or pre-zygotic reproductive isolation can have similar effects These genomic regions resistant to gene flow have been called ‘genomic islands of differentiation’ [5,8,9]. Some models predict further that islands would grow in size due to a local ‘spill over’ effect of strong selection reducing effective gene flow at nearby, weakly selected mutations [5,22]

Results

Discussion

Conclusion