Evolution of barrier loci at an intermediate stage of speciation with gene flow

Abstract

Understanding the origin of new species is a central goal in evolutionary biology. Diverging lineages often evolve highly heterogeneous patterns of differentiation; however, the underlying mechanisms are not well understood. We used an integrated approach to investigate evolutionary processes governing genetic differentiation between the hybridizing campions (Silene dioica (L.) Clairv. and S. latifolia Poiret). Demographic modeling indicated that the two species diverged with continuous gene flow. The best-supported scenario with heterogeneity in both migration rate and effective population size suggested that 5% of the loci evolved without gene flow. Differentiation (FST) and sequence divergence (dXY) were correlated and both tended to peak in the middle of most linkage groups, consistent with reduced gene flow at highly differentiated loci. Highly differentiated loci further exhibited signatures of selection and differentiation was significantly elevated around previously identified QTLs associated with assortative mating. In between-species population pairs, isolation by distance was stronger for genomic regions with low between-species differentiation than for highly differentiated regions that may contain barrier loci. Moreover, differentiation landscapes within and between species were only weakly correlated suggesting that the interplay of background selection and conserved genomic features is not the dominant determinant of genetic differentiation in these lineages. Instead, our results suggest that divergent selection drove the evolution of barrier loci played and the genomic landscape of differentiation between the two species, consistent with predictions for speciation in the face of gene flow.