A Whole-Genome Scan for Association With Invasion Success in the Fruit Fly Drosophila Suzukii Using Contrasts of Allele Frequencies Corrected for Population Structure

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

New set of microsatellite markers for the spotted-wing <em>Drosophila suzukii</em> (Diptera: Drosophilidae): a promising molecular tool for inferring the invasion history of this major insect pest

International audienceHistorical and observational data for invasive species are often sparse and incomplete, so molecular genetic markers are increasingly used and have proved to be efficient tools to make inferences about invasion histories. Here, we report the development of 28 polymorphic microsatellite markers in the invasive spotted-wing drosophila, Drosophila suzukii (Matsumura, 1931) (Diptera: Drosophilidae) designed from recent genomics resources, and their cross-amplification in closely related Drosophila species of the suzukii subgroup. The markers, located on autosomal chromosomes, were characterized in two distinct invasive populations from France and Hawaii (USA), and in four sister species of the suzukii subgroup. They all showed substantial polymorphism as well as revealing strong genetic differentiation between the two genotyped populations. These markers represent a promising molecular tool for population genetic studies on D. suzukii, more especially in order to reconstruct the pathways and demographic processes of the world-wide invasion in this major insect pest

Deciphering the Routes of invasion of Drosophila suzukii by Means of ABC Random Forest.

Deciphering invasion routes from molecular data is crucial to understanding biological invasions, including identifying bottlenecks in population size and admixture among distinct populations. Here, we unravel the invasion routes of the invasive pest Drosophila suzukii using a multi-locus microsatellite dataset (25 loci on 23 worldwide sampling locations). To do this, we use approximate Bayesian computation (ABC), which has improved the reconstruction of invasion routes, but can be computationally expensive. We use our study to illustrate the use of a new, more efficient, ABC method, ABC random forest (ABC-RF) and compare it to a standard ABC method (ABC-LDA). We find that Japan emerges as the most probable source of the earliest recorded invasion into Hawaii. Southeast China and Hawaii together are the most probable sources of populations in western North America, which then in turn served as sources for those in eastern North America. European populations are genetically more homogeneous than North American populations, and their most probable source is northeast China, with evidence of limited gene flow from the eastern US as well. All introduced populations passed through bottlenecks, and analyses reveal five distinct admixture events. These findings can inform hypotheses concerning how this species evolved between different and independent source and invasive populations. Methodological comparisons indicate that ABC-RF and ABC-LDA show concordant results if ABC-LDA is based on a large number of simulated datasets but that ABC-RF out-performs ABC-LDA when using a comparable and more manageable number of simulated datasets, especially when analyzing complex introduction scenarios