Overwintering drives rapid adaptation in Drosophila with potential costs to insecticide resistance

Abstract Winter is a formidable challenge for ectotherms that inhabit temperate climates. The extent to which winter conditions drive rapid adaptation, and separately, how selection from novel stressors affects adaptation to winter, remain poorly understood. Here we use replicate populations of Drosophila melanogaster in a field experiment to test i) whether winter conditions drive rapid adaptation and ii) for trade-offs between insecticide resistance and overwintering survival. Following a longitudinal field experiment investigating the evolution of insecticide resistance, we tracked subsequent evolution during an overwintering period. In unexposed control populations, we detected parallel evolutionary shifts indicative of adaptation to winter conditions in multiple traits, including body size and fecundity. Additionally, populations that had evolved insecticide resistance during the growing season were more likely to go extinct than control populations. Further, both control and resistant populations showed patterns of lower resistance following the winter period, suggestive of a trade-off between overwintering success and insecticide resistance. Rapid evolutionary responses to winter conditions, and potential costs of resistance, provide important context for understanding overwintering performance in temperate insects with implications for pest management and ecosystem services.