Competitive history shapes rapid evolution in a seasonal climate

Abstract

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 and 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.

Publication
Proceedings of the National Academy of Sciences
Date

Significance

Understanding species’ eco-evolutionary responses to novel competitive interactions and shifting thermal regimes has become essential under global change. However, we lack insight into these dynamics because experimental evolution studies often focus on populations of individual species. Using a large-scale field experiment with two competing species of drosophilid flies, we show that rapid evolution in response to competition can alter a species’ evolutionary trajectory when exposed to a seasonally changing climate. Our results demonstrate that interactions with competitors, including invasive species, can shape evolution when climatic conditions change. More broadly, we provide empirical, field-based evidence that a legacy of recent adaptation can shape subsequent evolutionary trajectories.