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.

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 SummaryNatural 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.

Polyphagous insect pests that infest many host plants are responsible for important economic losses in agriculture (Oerke, 2006).Hence, elucidating the mechanisms that drive patterns of host use by polyphagous insects is an important goal in ecological entomology. Oviposition preference, one of the main traits that determines host use in polyphagous insects, varies widely among host fruits and

1. The broad variation in host use among polyphagous insects is well documented but still poorly understood. In numerous pest insects, the proximate mechanisms responsible for variation in oviposition preference among host plants remain to be elucidated Drosophila suzukii is an invasive crop pest that attacks a wide range of host fruits. Females prefer ovipositing on particular fruit media (blackberry, cherry, blackcurrant) that are rich in phosphorus. As phosphorus is known to be involved in female reproduction in insects and Drosophila, phosphorus concentration could drive oviposition preference in D. suzukii. 2. To test the effect of phosphorus on oviposition, we measured the egg-laying preferences of D. suzukii in a choice environment containing 12 media with different concentrations of phosphoric acid (the main molecule that contains phosphorus within fruits). 3. In our assay, D. suzukii female did not prefer ovipositing in media with high phosphorus concentrations. As an experimental control, we verified the previous result of a higher female preference for media made of fruits rich in phosphorus. 4. Two alternative hypotheses could explain our results. A molecule containing phosphorus, but other than phosphoric acid, could drive the preference for phosphorus-rich fruits. Alternatively, one or more molecules that do not contain phosphorus could be responsible for the preference for these fruits. Studying the proximate mechanisms driving host use will ultimately help improve the management of any crop pest.

Organophosphate and carbamate insecticides have largely been used worldwide to control mosquito populations. As a response, the same amino acid substitution in the ace-1 gene (G119S), conferring resistance to both insecticides, has been selected independently in many mosquito species. In Anopheles gambiae, it has recently been shown that the G119S mutation is actually part of homogeneous duplications that associate multiple resistance copies of the ace-1 gene. In this study, we showed that duplications of resistance copies of the ace-1 gene also exist in the Culex pipiens species complex. The number of copies is variable, and different numbers of copies are associated with different phenotypic trade-offs: we used a combination of bioassays and competition in population cages to show that having more resistance copies conferred higher resistance levels, but was also associated with higher selective disadvantage (or cost) in the absence of insecticide. These results further show the versatility of the genetic architecture of resistance to organophosphate and carbamate insecticides around the ace-1 locus and its role in fine-tuned adaptation to insecticide treatment variations. Graphical Abstract