Drosophilid fruit flies have provided science with striking cases of behavioral adaptation and genetic innovation. A recent example is the invasive pest Drosophila suzukii, which, unlike most other Drosophila, lays eggs and feeds on undamaged, ripening fruits. This not only poses a serious threat for fruit cultivation but also offers an interesting model to study evolution of behavioral innovation. We developed genome and transcriptome resources for D. suzukii. Coupling analyses of these data with field observations, we propose a hypothesis of the origin of its peculiar ecology. Using nuclear and mitochondrial phylogenetic analyses, we confirm its Asian origin and reveal a surprising sister relationship between the eugracilis and the melanogaster subgroups. Although the D. suzukii genome is comparable in size and repeat content to other Drosophila species, it has the lowest nucleotide substitution rate among the species analyzed in this study. This finding is compatible with the overwintering diapause of D. suzukii, which results in a reduced number of generations per year compared with its sister species. Genome-scale relaxed clock analyses support a late Miocene origin of D. suzukii, concomitant with paleogeological and climatic conditions that suggest an adaptation to temperate montane forests, a hypothesis confirmed by field trapping. We propose a causal link between the ecological adaptations of D. suzukii in its native habitat and its invasive success in Europe and North America.

Drosophila suzukii Matsumura, an endemic pest in southeast Asia, has invaded Europe and the U.S.A. Unlike most of its closely related sibling species, the serrated ovipositor of D. suzukii permits ovipositing in undamaged fresh fruits. In the present study, volatiles are identified from host plants that are potentially involved in D. suzukii host recognition and oviposition behaviour. It is shown that mated females are attracted to volatiles emitted from intact fruits. The antennally‐active suite of compounds released from the fresh fruits is identified by gas chromatography coupled with electroantennographic detection, as well as gas chromatography‐mass spectrometry. In olfactometer bioassays, mated females are significantly attracted to an electroantennographically active volatile, isoamyl acetate, when tested at 10 µg of synthetic compound in a rubber septa, which has a release rate comparable to that of fresh fruits. In addition, a genomic survey shows that D. suzukii not only possesses the full repertoire of genes encoding odorant receptors activated by isoamyl acetate in D. melanogaster, but also that one of the genes, OR67a, is represented by five duplicated copies. These results indicate that D. suzukii uses olfactory cues to select oviposition sites. The identification of volatiles emitted by host fruits that attract D. suzukii may aid in the development of a selective and efficient synthetic lure for monitoring this pest. As a close relative of Drosophila melanogaster, D. suzukii provides a unique opportunity for understanding the physiological mechanisms involved in the shift of this species from use of rotten to ripe fruits for oviposition.

Summary The highly invasive spotted wing Drosophila Drosophila suzukii is a key pest of soft fruit and berries in Europe and North America, and development of control techniques is an urgent research challenge. Drosophila suzukii is widely associated with the yeast Hanseniaspora uvarum. Yeasts are symbionts of drosophilid flies and communicate with insects through volatile metabolites for spore dispersal. Accordingly, yeasts and behaviour‐modifying chemicals produced by yeasts are prospective tools for environmentally sound insect management. We first bioassayed flight attraction, feeding and oviposition of D. suzukii females in response to H. uvarum yeast and blueberries, which are a preferred host fruit. We then investigated the combined effect of yeast and insecticide on adult female oviposition behaviour and mortality towards the development of a yeast‐based control method. Following mating, attraction of female flies to blueberry and yeast odour cues was strongly enhanced. Yeast feeding significantly increased in mated females, while yeast did not increase oviposition on blueberries. This observation suggests that mated flies become attracted to yeast for feeding and to fruit for egg laying. A combined feeding–oviposition assay demonstrated different roles and interference between yeast and fruit stimuli: during the day after mating, females laid fewer eggs when yeast was available. The post‐mating yeast‐feeding response is an opportunity for the development of an attract‐and‐kill technique for population control of D. suzukii. Exposing flies to a blend of yeast and insecticide reduced oviposition and greatly enhanced adult fly mortality compared with an insecticide treatment alone. Synthesis and applications. Mated females are the key life stage for Drosophila suzukii population control. Egg‐laying females perforate fruit skin and fungal infestations ensue, even when eggs and larvae are killed off by insecticide sprays. Behaviour‐modifying chemicals, including yeast metabolites, enable environmentally safe insect management via manipulation of olfactory‐mediated reproductive behaviour. Our results highlight that yeast and yeast semiochemicals hold potential for D. suzukii management and that response modulation to olfactory stimuli following mating is a vital element for the development of D. suzukii control methods. Yeast feeding is enhanced in mated D. suzukii females, and this change in post‐mating behaviour can be exploited by an attract‐and‐kill strategy, combining a fly‐associated yeast with an insecticide. Furthermore, using the D. suzukii yeast mutualist, H. uvarum, may reduce non‐target effects and increase species specificity, which further contributes to the development of an efficient and safe control method.

A high reproductive potential is one reason for the rapid spread of Drosophila suzukii in Europe and in the United States. In order to identify mechanisms that mediate mating and reproduction in D. suzukii we studied the fly’s reproductive behavior, diurnal mating activity and sexual maturation. Furthermore, we studied the change of female cuticular hydrocarbons (CHCs) with age and conducted a preliminary investigation on the role of female-derived chemical signals in male mating behavior. Sexual behavior in D. suzukii is characterized by distinct elements of male courtship leading to female acceptance for mating. Time of day and age modulate D. suzukii mating activity. As with other drosophilids, female sexual maturity is paralleled by a quantitative increase in CHCs. Neither female CHCs nor other olfactory signals were required to induce male courtship, however, presence of those signals significantly increased male sexual behavior. With this pilot study we hope to stimulate research on the reproductive biology of D. suzukii, which is relevant for the development of pest management tools.

How the evolution of olfactory genes correlates with adaption to new ecological niches is still a debated topic. We explored this issue in Drosophila suzukii, an emerging model that reproduces on fresh fruit rather than in fermenting substrates like most other Drosophila. We first annotated the repertoire of odorant receptors (ORs), odorant binding proteins (OBPs), and antennal ionotropic receptors (aIRs) in the genomes of two strains of D. suzukii and of its close relative Drosophila biarmipes. We then analyzed these genes on the phylogeny of 14 Drosophila species: whereas ORs and OBPs are characterized by higher turnover rates in some lineages including D. suzukii, aIRs are conserved throughout the genus. Drosophila suzukii is further characterized by a non-random distribution of OR turnover on the gene phylogeny, consistent with a change in selective pressures. In D. suzukii, we found duplications and signs of positive selection in ORs with affinity for short-chain esters, and loss of function of ORs with affinity for volatiles produced during fermentation. These receptors—Or85a and Or22a—are characterized by divergent alleles in the European and American genomes, and we hypothesize that they may have been replaced by some of the duplicated ORs in corresponding neurons, a hypothesis reciprocally confirmed by electrophysiological recordings. Our study quantifies the evolution of olfactory genes in Drosophila and reveals an array of genomic events that can be associated with the ecological adaptations of D. suzukii.