Abstract
BackgroundThe degree of genetic differentiation among populations experiencing high levels of gene flow is expected to be low for neutral genomic sites, but substantial divergence can occur in sites subject to directional selection. Studies of highly mobile marine fish populations provide an opportunity to investigate this kind of heterogeneous genomic differentiation, but most studies to this effect have focused on a relatively low number of genetic markers and/or few populations. Hence, the patterns and extent of genomic divergence in high-gene-flow marine fish populations remain poorly understood.ResultsWe here investigated genome-wide patterns of genetic variability and differentiation in ten marine populations of three-spined stickleback (Gasterosteus aculeatus) distributed across a steep salinity and temperature gradient in the Baltic Sea, by utilizing >30,000 single nucleotide polymorphisms obtained with a pooled RAD-seq approach. We found that genetic diversity and differentiation varied widely across the genome, and identified numerous fairly narrow genomic regions exhibiting signatures of both divergent and balancing selection. Evidence was uncovered for substantial genetic differentiation associated with both salinity and temperature gradients, and many candidate genes associated with local adaptation in the Baltic Sea were identified.ConclusionsThe patterns of genetic diversity and differentiation, as well as candidate genes associated with adaptation, in Baltic Sea sticklebacks were similar to those observed in earlier comparisons between marine and freshwater populations, suggesting that similar processes may be driving adaptation to brackish and freshwater environments. Taken together, our results provide strong evidence for heterogenic genomic divergence driven by local adaptation in the face of gene flow along an environmental gradient in the post-glacially formed Baltic Sea.Electronic supplementary materialThe online version of this article (doi:10.1186/s12915-015-0130-8) contains supplementary material, which is available to authorized users.
Highlights
The degree of genetic differentiation among populations experiencing high levels of gene flow is expected to be low for neutral genomic sites, but substantial divergence can occur in sites subject to directional selection
Amongst the most salient findings of this study was the observation that the average levels of genetic differentiation among Baltic Sea three-spined stickleback populations were low by all standards, numerous genomic regions displayed a high degree of population differentiation
In summary, we discovered that genome-wide patterns of genetic diversity and differentiation among continuously distributed Baltic Sea three-spined stickleback populations – as assessed from polymorphisms in over 30,000 single nucleotide polymorphism (SNP) loci – varied widely across the genome
Summary
The degree of genetic differentiation among populations experiencing high levels of gene flow is expected to be low for neutral genomic sites, but substantial divergence can occur in sites subject to directional selection. Outlier detection methods have become popular in identifying population structuring and adaptive differentiation in marine fishes, which generally show very low levels of genetic differentiation in neutral marker genes [18,19,20,21,22] and in which common garden experiments are often logistically demanding, if not impossible, to conduct (but see [23,24,25,26,27]). High-throughput population genomic studies aimed at detecting adaptive differentiation in marine fishes are rare, especially those employing a comprehensive sampling scheme. The latter point is relevant in the context of seascape genetics, which aims to integrate environmental features with population genetic data to assess their impact on the genetic structure of marine populations [42,43]. In such approaches, sampling of multiple populations across environmental gradients becomes critical for inferences about genotype–environment associations
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