Eco-evolutionary dynamics will play a critical role in determining species’ fates as climatic conditions change. Unfortunately, we have little understanding of how rapid evolutionary responses to climate play out when species are embedded in the competitive communities that they inhabit in nature. We tested the effects of rapid evolution in response to interspecific competition on subsequent ecological and evolutionary trajectories in a seasonally changing climate using a field-based evolution experiment with Drosophila melanogaster. Populations of D. melanogaster were either exposed, or not exposed, to interspecific competition with an invasive competitor, Zaprionus indianus, over the summer. We then quantified these populations’ ecological trajectories (abundances) and evolutionary trajectories (heritable phenotypic change) when exposed to a cooling fall climate. We found that competition with Z. indianus in the summer affected the subsequent evolutionary trajectory of D. melanogaster populations in the fall, after all interspecific competition had ceased. Specifically, flies with a history of interspecific competition evolved under fall conditions to be larger, have lower cold fecundity and faster development than flies without a history of interspecific competition. Surprisingly, this divergent fall evolutionary trajectory occurred in the absence of any detectible effect of the summer competitive environment on phenotypic evolution over the summer or population dynamics in the fall. This study demonstrates that competitive interactions can leave a legacy that shapes evolutionary responses to climate even after competition has ceased, and more broadly, that evolution in response to one selective pressure can fundamentally alter evolution in response to subsequent agents of selection.

We tested how rapid evolution in response to interspecific competition influences ecological and evolutionary dynamics in a seasonal climate using a large-scale experimental evolution study in the field with the vinegar fly Drosophila melanogaster and its invasive competitor Zaprionus indianus. We conducted our experimental evolution study with replicate fly populations on caged peach trees planted in an experimental orchard that mimics our focal species’ primary Northeastern U.S. habitat. These field mesocosms experience natural temperature fluctuations and contain many of the predators and microbes that co-occur with local natural populations of D. melanogaster. To examine the consequences of rapid evolution in response to interspecific competition on ecological and evolutionary dynamics in the fall, we first allowed replicate populations of D. melanogaster to grow and evolve in the presence or absence of Z. indianus for ~6 generations over the summer (Fig. 1). At the end of summer, we removed Z. indianus, equalized abundances of D. melanogaster across populations, and allowed these populations with or without a history of interspecific competition to continue their ecological and evolutionary dynamics throughout the fall (~3 generations). We quantified the ecological (population dynamic) consequences of the summer competitive environment with weekly censuses of fly abundance through the fall, after all competition with Z. indianus had ceased. We quantified the evolutionary consequences of our treatments by measuring ten key phenotypes on D. melanogaster collected at the end of summer and end of the fall and then reared for two generations in a common garden to remove any plastic responses to treatments or field conditions. The ten phenotypes were: body size (female and male), early life fecundity (warm [25°C] and cold [15°C] conditions) and larval development speed and egg viability, each under three different conditions (Behrman et al. 2015; Rudman et al. 2019) (details in SI Appendix). The three conditions for larval development speed and egg viability were (1) cold (15°C) low density (50 eggs), (2) warm (25°C) low density and (3) warm high density (500 eggs).