Rapid and transient evolution of local adaptation to seasonal host fruits in an invasive fly

Both adaptive phenotypic plasticity and local adaptation can influence the match between phenotypic traits and local environmental conditions. Theory predicts that coarse-grained environments, which are stable for multiple generations, promote local adaptation, while fine-grained environments, in which individuals encounter more than one environment in their lifetime, favor adaptive phenotypic plasticity. When the heterogeneity of the environment is spatially and/or temporarily intermediate, with periods of environmental stability from one to only a few generations, the relative contributions of local adaptation and adaptive phenotypic plasticity in enabling individuals’ phenotypes to match the environments they encounter remains unclear. Here, we used Drosophila suzukii as a model system to evaluate the relative influence of genetic and plastic effects on this match in heterogeneous environments with an intermediate grain. This pest insect can develop within different fruits, and persists throughout the year in a given location on a succession of different host fruits, each one being available for only a few generations. Using reciprocal common environment experiments of natural D. suzukii populations collected from cherry, strawberry and blackberry, we found that both oviposition preference and offspring performance were higher on medium made with the fruit from which the population originated, than on media made with alternative fruits. This pattern remained after two generations in the laboratory, suggesting that genetic effects predominate over plastic effects. Our study demonstrates that spatially and temporally variable selection does not prevent the rapid evolution of local adaptation in natural populations. The speed and strength of adaptation may be facilitated by several mechanisms including a large effective population size and strong selective pressures imposed by host plants. Impact Summary Natural populations often exhibit good “fit” to the environment they are in. However, environments change over both time and space, and following change, the fit between a population and its environment may be poor. A question of long-standing interest to evolutionary biologists is, how do populations track changing environments to maintain fitness? Two main mechanisms are known: ( i ) plastic shifts, or adaptive phenotypic plasticity, in which traits immediately change in response to environmental change, and ( ii ) genetic shifts in the form of local adaptation, in which traits change over time through differences in fitness of individuals harboring different genetic variants. Plasticity is common when environments change over the course of an individual lifetime, while adaptation is common when environments change over the course of multiple generations. However, many environments change at an intermediate pace, and it is unclear whether plasticity or adaptation are more vital to maintaining fitness under such conditions. Drosophila suzukii is well-suited to evaluating the relative importance of plasticity and adaptation in response to an intermediate pace of environmental change. This species experiences an environment that shifts every 1-4 generations as host fruits change over time and space. Here, we studied natural populations of D. suzukii collected from different hosts. Using reciprocal common environment experiments, we evaluated their fitness on their source and alternative hosts. Drosophila suzukii populations were most fit on their source host, successfully tracking an intermediate pace of environmental change. We developed a new statistical method to quantify the contributions of adaptive plasticity and local adaptation in determining fitness. We found that fitness was maintained via local adaptation to each new host in succession. This study provides a novel statistical tool that can be applied to other systems, and highlights that spatially and temporally variable selection does not prevent local adaptation and, on the contrary, illustrates how rapid the adaptive process can be. ### Competing Interest Statement The authors have declared no competing interest.