Dissecting the invasion history of Spotted-Wing Drosophila (Drosophila suzukii) in Portugal using genomic data

Abstract Background The invasive pest Spotted-Wing Drosophila, Drosophila suzukii (Matsumura), causes extensive damage and production losses of soft-skinned fruits. Native to Asia, the species has now spread worldwide, with first reports in Portugal in 2012. In this study, we focus on the genomic signatures of the recent Portuguese invasion, in the context of worldwide patterns established in previous works. We analyzed whole genome pool sequencing data from three Portuguese populations (N = 240) sampled in 2019 and 2021. Results The correlation of allele frequencies suggested that Portuguese populations are related to South European ones, indicating a Mediterranean invasion route. While two populations exhibited levels of genetic variation comparable to others in the invasive range, a third showed low levels of genetic diversity, which may result from a recent colonization of the region. Genome-wide analyses of natural selection identified ten genes previously associated with D. suzukii’s invasive capacity, which may have contributed to the species’ success in Portugal. Additionally, we pinpointed six genes evolving under positive selection across Portuguese populations but not in European ones, which is indicative of local adaptation. One of these genes, nAChRalpha7, encodes a nicotinic acetylcholine receptor, which are known targets for insecticides widely used for D. suzukii control, such as neonicotinoids and spinosyns. Although spinosyn resistance has been associated with mutations in the nAChRalpha6 in other Drosophila species, the putative role of nAChRalpha7 in insecticide resistance and local adaptation in Portuguese D. suzukii populations encourages future investigation. Conclusions Our results highlight the complex nature of rapid species invasions and the role of rapid local adaptation in determining the invasive capacity of these species.