Do highly divergent loci reside in genomic regions affecting reproductive isolation? A test using next-generation sequence data in Timema stick insects

Background: Genetic divergence during speciation with gene flow is heterogeneous across the genome, with some regions exhibiting stronger differentiation than others. Exceptionally differentiated regions are often assumed to experience reduced introgression, i.e., reduced flow of alleles from one population into another because such regions are affected by divergent selection or cause reproductive isolation. In contrast, the remainder of the genome can be homogenized by high introgression. Although many studies have documented variation across the genome in genetic differentiation, there are few tests of this hypothesis that explicitly quantify introgression. Here, we provide such a test using 38,304 SNPs in populations of Timema cristinae stick insects. We quantify whether loci that are highly divergent between geographically separated (‘allopatric’) populations exhibit unusual patterns of introgression in admixed populations. To the extent this is true, highly divergent loci between allopatric populations contribute to reproductive isolation in admixed populations. Results: As predicted, we find a substantial association between locus-specific divergence between allopatric populations and locus-specific introgression in admixed populations. However, many loci depart from this relationship, sometimes strongly so. We also report evidence for selection against foreign alleles due to local adaptation. Conclusions: Loci that are strongly differentiated between allopatric populations sometimes contribute to reproductive isolation in admixed populations. However, geographic variation in selection and local adaptation, in aspects of genetic architecture (such as organization of genes, recombination rate variation, number and effect size of variants contributing to adaptation, etc.), and in stochastic evolutionary processes such as drift can cause strong differentiation of loci that do not always contribute to reproductive isolation. The results have implications for the theory of ‘genomic islands of speciation’