Disentangling site-specific and shared local adaptation in a classic system of repeated evolution

Abstract

Repeated divergence across contrasting habitats is widely used to infer natural selection and adaptation. However, such inferences remain inherently correlative and capture only adaptation shared among populations from the same habitat type, thereby missing site-specific adaptation unique to individual populations. Field transplant experiments test adaptation more directly by measuring fitness in nature, but they are typically limited to pairwise reciprocal exchanges between populations and therefore cannot separate shared habitat-level and unique site-specific adaptation. Here we extend the typical transplant framework to include multiple populations from both within and across habitat types, allowing fitness variation to be partitioned into shared habitat-level and unique site-specific components. We apply this framework to lake-stream stickleback, a classic system for studying adaptation via repeated divergence. Specifically, we transplanted laboratory-reared fish from a panmictic lake population and four independent stream populations across one lake and two stream sites. Stream fish outperformed lake fish in streams and vice versa, demonstrating adaptive lake-stream divergence. However, at both stream sites, local stream fish also outperformed foreign stream fish. Strikingly, this site-specific advantage was twice as large as the advantage of foreign stream fish over lake fish, reflecting the fitness benefit of shared stream adaptation. These results show that most fitness-relevant evolutionary variation in this system is unique to individual populations and therefore invisible to approaches that rely on repeated evolution to infer adaptation. More broadly, our work underscores the importance of ecological scale for understanding adaptation and evolutionary predictability. Significance statementRepeated evolutionary responses to similar environments commonly serve as evidence for adaptation. However, such comparative approaches do not directly measure fitness or resolve whether variation among populations from the same nominal habitat reflects adaptation to site-specific conditions. Using laboratory-raised lake and stream stickleback transplanted both within and across habitat types, we separated the fitness effects of shared adaptation to the same nominal habitat and site-specific adaptation unique to individual populations. Site-specific adaptation explained two-thirds of the total fitness variation, exceeding the contribution of adaptation shared among populations from the same habitat type. Our study highlights that natural selection generates fitness-relevant divergence at finer ecological scales than comparative approaches can resolve, underscoring the irreplaceable value of field experiments for understanding evolution.