Parallel evolution of similar traits by independent populations in similar environments is considered strong evidence for adaptation by natural selection. Often, however, replicate populations in similar environments do not all evolve in the same way, thus deviating from any single, predominant outcome of evolution. This variation might arise from non-adaptive, population-specific effects of genetic drift, gene flow or limited genetic variation. Alternatively, these deviations from parallel evolution might also reflect predictable adaptation to cryptic environmental heterogeneity within discrete habitat categories. Here, we show that deviations from parallel evolution are the consequence of environmental variation within habitats combined with variation in gene flow. Threespine stickleback (Gasterosteus aculeatus) in adjoining lake and stream habitats (a lakestream pair) diverge phenotypically, yet the direction and magnitude of this divergence is not always fully parallel among 16 replicate pairs. We found that the multivariate direction of lakestream morphological divergence was less parallel between pairs whose environmental differences were less parallel. Thus, environmental heterogeneity among lakestream pairs contributes to deviations from parallel evolution. Additionally, likely genomic targets of selection were more parallel between environmentally more similar pairs. In contrast, variation in the magnitude of lakestream divergence (independent of direction) was better explained by differences in lakestream gene flow; pairs with greater lakestream gene flow were less morphologically diverged. Thus, both adaptive and non-adaptive processes work concurrently to generate a continuum of parallel evolution across lakestream stickleback population pairs.
Yoel E Stuart, Thor Veen, Jesse N Weber, Dieta Hanson, Mark Ravinet, Brian K Lohman, Cole J Thompson, Tania Tasneem, Andrew Doggett, Rebecca Izen, Newaz Ahmed, Rowan DH Barrett, Andrew P Hendry, Catherine L Peichel, Daniel I Bolnick. (2017). Contrasting effects of environment and genetics generate a continuum of parallel evolution. Nature Ecology & Evolution, 1(6)