The legacy of past climate warming: strong local adaptation in rear-edge populations

Improving forecasts of species responses to climate change has become a central challenge in ecology and evolution as species distributions are increasingly disrupted by ongoing climate warming. Insight into this challenge may be gained through a better understanding of evolutionary responses to past climate change. The rear edges of species distributions are typically relict populations persisting in former glacial refugia at warmer range limits. As such, they form natural laboratories to study the evolutionary outcomes of past climate warming. Three such outcomes have been proposed for rear-edge populations: maintenance of high diversity due to long-term persistence, strong genetic drift following habitat decline, and strong local adaptation allowing persistence despite environmental change. Empirical studies rarely explicitly test these alternate outcomes limiting our understanding of evolutionary responses to warming climates. We tested all three evolutionary outcomes at the rear edge of the North American herb Campanula americana, by assessing genetic variation in a genome-wide population genetic study, drift load as measure of fitness decline due to drift in a controlled crossing study, and local adaptation in a transplant study. Rear-edge populations exhibited reduced genetic diversity within populations and high differentiation among populations, typically interpreted as evidence of genetic drift, yet show limited drift load. Instead, these populations expressed strong local adaptation, thriving in rear-edge habitats that were unsuitably warm for populations in the expanded range. This indicates that warm-edge populations may persist under warming climates by gradually adapting, even in the face of genetic erosion. Our findings highlight the importance of explicitly testing for all evolutionary outcomes, and particularly going beyond measures of genetic variation, when inferring evolutionary history. More broadly, these findings identify rear-edge populations not as relics of decline, but as underappreciated models for studying successful adaptation under long-term climate change.