The Asian vinegar fly Drosophila suzukii (spotted wing Drosophila [SWD]) has emerged as a major invasive insect pest of small and stone fruits in both the Americas and Europe since the late 2000s. While research efforts have rapidly progressed in Asia, North America, and Europe over the past 5 years, important new insights may be gained in comparing and contrasting findings across the regions affected by SWD. In this review, we explore common themes in the invasion biology of SWD by examining (1) its biology and current pest status in endemic and recently invaded regions; (2) current efforts and future research needs for the development of predictive models for its geographic expansion; and (3) prospects for both natural and classical (=importation) biological control of SWD in invaded habitats, with emphasis on the role of hymenopteran parasitoids. We conclude that particularly fruitful areas of research should include fundamental studies of its overwintering, host-use, and dispersal capabilities; as well as applied studies of alternative, cost-effective management techniques to complement insecticide use within the integrated pest management framework. Finally, we emphasize that outreach efforts are critical to effective SWD management by highlighting successful Communicated by M. Traugott. Electronic supplementary materialThe online version of this article (strategies and insights gained from various geographic regions.Keywords Biological control Á Drosophila Á Frugivore Á Integrated pest management Á Invasion biology Key message• Spotted wing Drosophila (SWD) is a major invasive pest of soft fruits in the Americas and Europe. • We review the current global distribution and economic impacts of SWD, develop models for predicting its further spread, and discuss the prospects for biological control of this pest. • The following research areas into SWD biology appear particularly promising: its biology at low temperatures, the dispersal and migratory abilities of adults, and exploration in Asian regions for potential classical biological control agents.

In August 2008, the first detection of the spotted wing drosophila, Drosophila suzukii, to the North America mainland in California caused great concern, as the fly was found infesting a variety of commercial fruits. Subsequent detections followed in Oregon, Washington, Florida and British Columbia in 2009; in Utah, North Carolina, South Carolina, Michigan, and Louisiana in 2010; and in Virginia, Montana, Wisconsin, Pennsylvania, New Jersey, Maryland and Mexico in 2011. In Europe, it has been detected in Italy and Spain in 2009 and in France in 2010. Economic costs to the grower from D. suzukii include the increased cost of production (increased labor and materials for chemical inputs, monitoring and other management tools) and crop loss. An effective response to the invasion of D. suzukii requires proper taxonomic identification at the initial phase, understanding basic biology and phenology, developing management tools, transferring information and technology quickly to user groups, and evaluating the impact of the research and extension program on an economic, social, and environmental level. As D. suzukii continues to expand its range, steps must be initiated in each new region to educate and inform the public as well as formulate management tactics suitable for the crops and growing conditions in each.

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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.

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