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

Both local adaptation and adaptive phenotypic plasticity can influence the match between phenotypic traits and local environmental conditions. Theory predicts that environments stable for multiple generations promote local adaptation, whereas highly heterogeneous environments favor adaptive phenotypic plasticity. However, when environments have periods of stability mixed with heterogeneity, the relative importance of local adaptation and adaptive phenotypic plasticity is unclear. Here, we used Drosophila suzukii as a model system to evaluate the relative influence of genetic and plastic effects on the match of populations to environments with periods of stability from three to four generations. This invasive pest insect can develop within different fruits, and persists throughout the year in a given location on a succession of distinct 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, which remained after two generations in the laboratory, was analyzed using a statistical method we developed to quantify the contributions of local adaptation and adaptive plasticity in determining fitness. Altogether, we found that genetic effects (local adaptation) dominate over plastic effects (adaptive phenotypic plasticity). 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.

Adaptation and correlated fitness responses over two time scales in Drosophila suzukii populations evolving in different environments.

The process of local adaptation involves differential changes in fitness over time across different environments. Although experimental evolution studies have extensively tested for patterns of local adaptation at a single time point, there is relatively little research that examines fitness more than once during the time course of adaptation. We allowed replicate populations of the fruit pest Drosophila suzukii to evolve in one of eight different fruit media. After five generations, populations with the highest initial levels of maladaptation had mostly gone extinct, whereas experimental populations evolving on cherry, strawberry and cranberry media had survived. We measured the fitness of each surviving population in each of the three fruit media after five and after 26 generations of evolution. After five generations, adaptation to each medium was associated with increased fitness in the two other media. This was also true after 26 generations, except when populations that evolved on cranberry medium developed on cherry medium. These results suggest that, in the theoretical framework of a fitness landscape, the fitness optima of cherry and cranberry media are the furthest apart. Our results show that studying how fitness changes across several environments and across multiple generations provides insights into the dynamics of local adaptation that would not be evident if fitness were analysed at a single point in time. By allowing a qualitative mapping of an experimental fitness landscape, our approach will improve our understanding of the ecological factors that drive the evolution of local adaptation in D. suzukii.