Evidence is accumulating that evolutionary changes are not only common during biological invasions but may also contribute directly to invasion success. The genomic basis of such changes is still largely unexplored. Yet, understanding the genomic response to invasion may help to predict the conditions under which invasiveness can be enhanced or suppressed. Here, we characterized the genome response of the spotted wing drosophila Drosophila suzukii during the worldwide invasion of this pest insect species, by conducting a genome-wide association study to identify genes involved in adaptive processes during invasion. Genomic data from 22 population samples were analyzed to detect genetic variants associated with the status (invasive versus native) of the sampled populations based on a newly developed statistic, we called C2, that contrasts allele frequencies corrected for population structure. We evaluated this new statistical framework using simulated data sets and implemented it in an upgraded version of the program BayPass. We identified a relatively small set of single-nucleotide polymorphisms that show a highly significant association with the invasive status of D. suzukii populations. In particular, two genes, RhoGEF64C and cpo, contained single-nucleotide polymorphisms significantly associated with the invasive status in the two separate main invasion routes of D. suzukii. Our methodological approaches can be applied to any other invasive species, and more generally to any evolutionary model for species characterized by nonequilibrium demographic conditions for which binary covariables of interest can be defined at the population level.

A better understanding of the factors affecting host plant use by spotted-wing drosophila (Drosophila suzukii) could aid in the development of efficient management tools and practices to control this pest. Here, proxies of both preference (maternal oviposition behavior) and performance (adult emergence) were evaluated for 12 different fruits in the form of purees. The effect of the chemical composition of the fruits on preference and performance traits was then estimated. We synthesized the literature to interpret our findings in the light of previous studies that measured oviposition preference and larval performance of D. suzukii. We show that fruit identity influences different parts of the life cycle, including oviposition preference under both choice and no-choice conditions, emergence rate, development time, and number of emerging adults. Blackcurrant was always among the most preferred fruit we used, while grape and tomato were the least preferred fruits. Larvae performed better in cranberry, raspberry, strawberry, and cherry than in the other fruits tested. We found that fruit chemical compounds can explain part of the effect of fruit on D. suzukii traits. In particular, oviposition preference under choice conditions was strongly influenced by fruit phosphorus content. In general, the consensus across studies is that raspberry, blackberry, and strawberry are among the best hosts while blackcurrant, grape and rose hips are poor hosts. Our results generally confirm this view but also suggest that oviposition preferences do not necessarily match larval performances. We discuss opportunities to use our results to develop new approaches for pest management.

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.

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Rapid environmental change presents a significant challenge to the persistence of natural populations. Rapid adaptation that increases population growth, enabling populations that declined following severe environmental change to grow and avoid extinction, is called evolutionary rescue. Numerous studies have shown that evolutionary rescue can indeed prevent extinction. Here, we extend those results by considering the demographic history of populations. To evaluate how demographic history influences evolutionary rescue, we created 80 populations of red flour beetle, Tribolium castaneum, with three classes of demographic history: diverse populations that did not experience a bottleneck, and populations that experienced either an intermediate or a strong bottleneck. We subjected these populations to a new and challenging environment for six discrete generations and tracked extinction and population size. Populations that did not experience a bottleneck in their demographic history avoided extinction entirely, while more than 20% of populations that experienced an intermediate or strong bottleneck went extinct. Similarly, among the extant populations at the end of the experiment, adaptation increased the growth rate in the novel environment the most for populations that had not experienced a bottleneck in their history. Taken together, these results highlight the importance of considering the demographic history of populations to make useful and effective conservation decisions and management strategies for populations experiencing environmental change that pushes them toward extinction.

Autophagy is an evolutionary conserved cellular self-degradation process considered as a major energy mobilizing system in eukaryotes. It has long been considered as a post-translationally regulated event, and the importance of transcriptional regulation of autophagy-related genes (atg) for somatic maintenance and homeostasis during long period of stress emerged only recently. In this regard, large changes in atg transcription have been documented in several species under diverse types of prolonged catabolic situations. However, the available data primarily concern atg mRNA levels at specific times and fail to capture the dynamic relationship between transcript production over time and integrated phenotypes. Here, we present the development of a statistical model describing the dynamics of expression of several atg and lysosomal genes in European glass eel (Anguilla anguilla) during long-term fasting at two temperatures (9 °C and 12 °C) and make use of this model to infer the effect of transcripts dynamics on an integrated phenotype – here weight loss. Our analysis shows long-term non-random fluctuating atg expression dynamics and reveals for the first time a significant contribution of atg transcripts production over time to weight loss. The proposed approach thus offers a new perspective on the long-term transcriptional control of autophagy and its physiological role.

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.

Adaptation to divergent environments can result in ecological specialization. The detection of trade-offs across environments (i.e., negative correlations in performance between different environments) is the hallmark of specialization. Although such trade-offs are predicted by theory, experimental evidence that trade-offs can readily evolve in the laboratory remains scarce. Here, we investigated the evolution of adaptation to distinct environments, including potential fitness trade-offs by maintaining populations of the generalist fruit pest, Drosophila suzukii, for 26 generations on media made with different fruits. We measured the performance and preference of each evolved population on the different fruits using reciprocal transplant experiments after five generations and at the end of our experiment. After five generations, experimental populations on most fruits had gone extinct, but they had adapted to three test fruit media, without exhibiting trade-offs. By generation 26 on these three fruits, specific adaptation to each fruit media had evolved, with trade-offs across media for some populations. The evolution of fruit-specific performance did not drive the evolution of corresponding preferences (i.e., preferences for the evolution fruit). This study suggests that ecological specialization can evolve in generalist species, even if only transiently, when hosts or habitats are heterogeneous over time and space.