Architecture of parallel adaptation to freshwater in multiple populations of threespine stickleback

Abstract

Threespine sticklebacks adapted to freshwater environments all over the Northern Hemisphere. This adaptation involved parallel recruitment of freshwater alleles in clusters of closely linked sites, or divergence islands (DIs). However, it is unclear to what extent the DIs involved in adaptation and the alleles within them coincide between populations adapting to similar environments. Here, we examine 10 freshwater populations of similar ages from the White Sea basin, and study the repeatability of patterns of adaptation in them. Overall, the 65 detected DIs tend to reside in regions of low recombination, underlining the role of reduced recombination in their establishment. Moreover, the DIs are clustered in the genome to the extent that is not explainable by the recombination rate alone, consistent with the divergence hitchhiking model. 21 out of the 65 DIs are universal; i.e., the frequency of freshwater alleles in them is increased in all analyzed populations. Universal DIs tend to have longer core region shared between populations, and the divergence between the marine and the freshwater haplotypes in them is higher, implying that they are older, also consistently with divergence hitchhiking. Within most DIs, the same set of sites distinguished the marine and the freshwater haplotypes in all populations; however, in some of the DIs, the genetic architecture of the freshwater haplotype differed between populations, suggesting that they could have been established by soft selective sweeps.