Abstract
BackgroundFew models of genetic hitchhiking in subdivided populations have been developed and the rarity of empirical examples is even more striking. We here provide evidences of genetic hitchhiking in a subdivided population of the marine mussel Mytilus edulis. In the Bay of Biscay (France), a patch of M. edulis populations happens to be separated from its North Sea conspecifics by a wide region occupied only by the sister species M. galloprovincialis. Although genetic differentiation between the two M. edulis regions is largely non-significant at ten marker loci (average FST~0.007), a strong genetic differentiation is observed at a single locus (FST = 0.25). We validated the outlier status of this locus, and analysed DNA sequence polymorphism in order to identify the nature of the selection responsible for the unusual differentiation.ResultsWe first showed that introgression of M. galloprovincialis alleles was very weak in both populations and did not significantly affect their differentiation. Secondly, we observed the genetic signature of a selective sweep within both M. edulis populations in the form of a star-shaped clade of alleles. This clade was nearly fixed in the North Sea and was segregating at a moderate frequency in the Bay of Biscay, explaining their genetic differentiation. Incomplete fixation reveals that selection was not direct on the locus but that the studied sequence recombined with a positively selected allele at a linked locus while it was on its way to fixation. Finally, using a deterministic model we showed that the wave of advance of a favourable allele at a linked locus, when crossing a strong enough barrier to gene flow, generates a step in neutral allele frequencies comparable to the step observed between the two M. edulis populations at the outlier locus. In our case, the position of the barrier is now materialised by a large patch of heterospecific M. galloprovincialis populations.ConclusionHigh FST outlier loci are usually interpreted as being the consequence of ongoing divergent local adaptation. Combining models and data we show that among-population differentiation can also dramatically increase following a selective sweep in a structured population. Our study illustrates how a striking geographical pattern of neutral diversity can emerge from past indirect hitchhiking selection in a structured population.NoteNucleotide sequences reported in this paper are available in the GenBank™ database under the accession numbers EU684165 – EU684228.
Highlights
Few models of genetic hitchhiking in subdivided populations have been developed and the rarity of empirical examples is even more striking
As M. galloprovincialis samples were here studied to control for introgression of galloprovincialis alleles in M. edulis populations, sample size does not need to be high for these samples and we present results obtained with HQ subsets
We have shown that, in a structured population, a selective sweep at a positively selected linked locus is a simple scenario to account for unusually high level of differentiation at a marker locus
Summary
Few models of genetic hitchhiking in subdivided populations have been developed and the rarity of empirical examples is even more striking. We here provide evidences of genetic hitchhiking in a subdivided population of the marine mussel Mytilus edulis. The detection of adaptive evolution at the molecular level has essentially relied on indirect inferences [1]. This is because genomes are very large and adaptive evolution probably occurs only at a few segregating mutations at a given time [2]. Adaptive evolution leaves a footprint on the pattern of neutral diversity [3], which widens both the genomic extent and the time scale on which adaptation can be detected. The recent development of genome scans allows appreciating how genomes seem crippled by numerous signatures of adaptive evolution [17,18]
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