Pichia occidentalis volatiles elicit divergent behavioral responses in Drosophila suzukii and Drosophila melanogaster

ABSTRACT Drosophila suzukii (spotted-wing drosophila) is an invasive pest that infests ripe, market-ready fruit, posing a significant threat to fruit production. To develop alternatives to conventional chemical control, environmentally derived fungi (EF) were evaluated for their potential to modulate D. suzukii behavior and viability. Pichia occidentalis , isolated from Drosophila melanogaster oral and fecal secretions, exhibited species-specific repellency in D. suzukii . In D. suzukii , exposure to P. occidentalis reduced survival, most pronounced in males, and significantly inhibited female oviposition. In contrast, D. melanogaster showed no reduction in survival and increased oviposition in the presence of the fungus. Solid-phase microextraction coupled with gas chromatography–mass spectrometry (SPME GC-MS) identified volatile metabolites produced by P. occidentalis . Subsequent cafeteria-style assays of individual volatiles revealed that several of these compounds elicited aversive responses in D. suzukii while remaining attractive to D. melanogaster , highlighting species-specific olfactory effects. Isoamyl butanoate, 2-phenyl-1-propanal, and benzyl alcohol demonstrated consistent repellent activity with superior efficacy compared to established D. suzukii repellents (2-pentylfuran, 1-octen-3-ol, and geosmin). Collectively, these findings demonstrate that EF metabolites can differentially influence closely related species and may be leveraged as targeted, behavior-based tools for managing D. suzukii . IMPORTANCE Drosophila suzukii is a major invasive pest that damages fresh fruit by laying eggs in ripening crops, leading to significant agricultural losses. Current control strategies rely heavily on chemical insecticides, which provide incomplete control and can harm non-target organisms. Here, we show that volatile metabolites produced by the environmental yeast Pichia occidentalis differentially influence closely related Drosophila species, decreasing oviposition and longevity in D. suzukii while stimulating oviposition in D. melanogaster . This species-specific divergence highlights the potential of microbial volatiles as precision tools for pest management, further supporting a behavior-based approach that selectively disrupts pest reproduction while minimizing ecological impact.