The three-spined stickleback (Gasterosteus aculeatus) is a model system to study parallel adaptation due to its repeated evolution of similar phenotypes in numerous independent colonisations of freshwater habitats. Most of this parallelism stems from parallel selection on alleles that are identical by descent and are maintained in low frequencies in marine populations. Recent evidence suggests that degrees of parallel evolution in sticklebacks are geographically heterogeneous and constrained by demographic history. Since previous genetic research on European sticklebacks was biased towards high-latitude regions, we investigated southern populations thought to stem from a lineage which subsequently colonised the rest of Europe after the last glaciation. As southern marine populations are believed to have gone extinct, the spread of alleles between different southern European populations has been highly unlikely, potentially limiting parallel evolution. We compared levels of genetic differentiation and genetic parallelism of 19 Adriatic and Iberian stickleback populations to Pacific, Atlantic and Caspian counterparts, where gene flow between freshwater populations across extant marine populations is still possible. Ours results support previous findings that southern populations are highly differentiated and of low genetic diversity. Linkage disequilibrium network analyses revelead unexpectedly high levels of genetic parallelism in southern European freshwater populations, which is a likely relic of freshwater adaptation prior to the extinction of marine sticklebacks. Weakening parallelism signatures with latitude likely reflect the diversity loss at the frontiers of the last colonisation wave towards northern Europe, highlighting the importance of demographic history in shaping contemporary patterns of parallel adaptation.
Parallel evolution despite low genetic diversity in Europe's ancient sticklebacks