Genomics of divergence along a continuum of parapatric population differentiation

The patterns of genomic divergence during ecological speciation are shaped by a combination of evolutionary forces. Processes such as genetic drift, local reduction of gene flow around genes causing reproductive isolation, hitchhiking around selected variants, variation in recombination and mutation rates are all factors that can contribute to the heterogeneity of genomic divergence. On the basis of 60 fully sequenced three-spined stickleback genomes, we explore these different mechanisms explaining the heterogeneity of genomic divergence across five parapatric lake and river population pairs varying in their degree of genetic differentiation. We find that divergent regions of the genome are mostly specific for each population pair, while their size and abundance are not correlated with the extent of genome-wide population differentiation. In each pair-wise comparison, an analysis of allele frequency spectra reveals that 25–55% of the divergent regions are consistent with a local restriction of gene flow. Another large proportion of divergent regions (38–75%) appears to be mainly shaped by hitchhiking effects around positively selected variants. We provide empirical evidence that alternative mechanisms determining the evolution of genomic patterns of divergence are not mutually exclusive, but rather act in concert to shape the genome during population differentiation, a first necessary step towards ecological speciation. Authors Summary A variety of evolutionary forces influence the genomic landscape of divergence during ecological speciation. Here we characterize the evolution of genomic divergence patterns based on 60 fully sequenced three-spined stickleback genomes, contrasting lake and river populations that differ in parasite abundance. Our comparison of the size and abundance of divergent regions in the genomes across a continuum of population differentiation suggests that selection and the hitchhiking effect on neutral sites mainly contributes to the observed heterogeneous patterns of genomic divergence. Additional divergent regions of the genome can be explained by a local reduction of gene flow. Our description of genomic divergence patterns across a continuum of population differentiation combined with an analysis of molecular signatures of evolution highlights how adaptation shapes the differentiation of sticklebacks in freshwater habitats