Shared Patterns of Genome-Wide Differentiation Are More Strongly Predicted by Geography Than by Ecology

Closely related populations often display similar patterns of genomic differentiation, yet it remains an open question which ecological and evolutionary forces generate these patterns. The leading hypothesis is that this similarity in divergence is driven by parallel natural selection. However, several recent studies have suggested that these patterns may instead be a product of the depletion of genetic variation that occurs as result of background selection (i.e., linked negative selection). To date, there have been few direct tests of these competing hypotheses. To determine the relative contributions of background selection and parallel selection to patterns of repeated differentiation, we examined 24 independently derived populations of freshwater stickleback occupying a variety of niches and estimated genomic patterns of differentiation in each relative to their common marine ancestor. Patterns of genetic differentiation were strongly correlated across pairs of freshwater populations adapting to the same ecological niche, supporting a role for parallel natural selection. In contrast to other recent work, our study comparing populations adapting to the same niche produced no evidence signifying that similar patterns of genomic differentiation are generated by background selection. We also found that overall patterns of genetic differentiation were considerably more similar for populations found in closer geographic proximity. In fact, the effect of geography on the repeatability of differentiation was greater than that of parallel selection. Our results suggest that shared selective landscapes and ancestral variation are the key drivers of repeated patterns of differentiation in systems that have recently colonized novel environments.