Admixture between old lineages facilitated contemporary ecological speciation in Lake Constance stickleback

David A Marques,Ole Seehausen,Kay Lucek,Vitor C Sousa,Laurent Excoffier

doi:10.1038/s41467-019-12182-w

Abstract

Ecological speciation can sometimes rapidly generate reproductively isolated populations coexisting in sympatry, but the origin of genetic variation permitting this is rarely known. We previously explored the genomics of very recent ecological speciation into lake and stream ecotypes in stickleback from Lake Constance. Here, we reconstruct the origin of alleles underlying ecological speciation by combining demographic modelling on genome-wide single nucleotide polymorphisms, phenotypic data and mitochondrial sequence data in the wider European biogeographical context. We find that parallel differentiation between lake and stream ecotypes across replicate lake-stream ecotones resulted from recent secondary contact and admixture between old East and West European lineages. Unexpectedly, West European alleles that introgressed across the hybrid zone at the western end of the lake, were recruited to genomic islands of differentiation between ecotypes at the eastern end of the lake. Our results highlight an overlooked outcome of secondary contact: ecological speciation facilitated by admixture variation.

Highlights

Ecological speciation can sometimes rapidly generate reproductively isolated populations coexisting in sympatry, but the origin of genetic variation permitting this is rarely known
The models we compare are: (1) primary divergence in situ, in which lake and stream ecotypes have recently diverged from standing genetic variation in a single lineage that colonized Lake Constance; (2) ecological vicariance; (3) secondary contact, in which ecotypes correspond to West and East European lineages that have diverged in allopatry, recently met and sorted between lake and stream habitats with exchange of genes at the lake-stream boundaries; and (4) hybrid origin, in which one of the ecotypes has recently evolved through hybridization between divergent West and East European lineages or sorting of admixture variation following introgression from one divergent lineage into the other lineage
We identified five different mitochondrial DNA haplotypes in the Lake Constance catchment (Fig. 1b), all of them matching haplotypes that today can be found in four main European river catchments, draining respectively into the Baltic Sea, the North Sea, the Mediterranean Sea, and the Black Sea[12,22,26] (Fig. 1a)

Summary

Introduction

Ecological speciation can sometimes rapidly generate reproductively isolated populations coexisting in sympatry, but the origin of genetic variation permitting this is rarely known. The authors estimated that ecotypes have been diverging for ~4500 generations, translating to ~9000 years or an early post-glacial divergence Such a long time for ecological speciation corresponds to what has been reported in other well-studied cases of sympatric stickleback species[20], but is at odds with the historical ichthyological literature[15,16,17,18]. The models we compare are: (1) primary divergence in situ, in which lake and stream ecotypes have recently diverged from standing genetic variation in a single lineage that colonized Lake Constance; (2) ecological vicariance (outlined above); (3) secondary contact, in which ecotypes correspond to West and East European lineages that have diverged in allopatry, recently met and sorted between lake and stream habitats with exchange of genes at the lake-stream boundaries; and (4) hybrid origin, in which one of the ecotypes has recently evolved through hybridization between divergent West and East European lineages or sorting of admixture variation following introgression from one divergent lineage into the other lineage

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Conclusion