Integrating circadian activity and gene expression profiles to predict chronotoxicity of Drosophila suzukii response to insecticides

Native to Southeast Asia, Drosophila suzukii is a recent invader that infests ripe and ripening fruit, leading to significant crop losses. Since current D. suzukii management strategies rely on insecticide usage, and insecticide detoxification gene expression is under circadian regulation in the closely related Drosophila melanogaster, we set out to determine if integrative analysis of daily activity patterns and detoxification gene expression can predict chronotoxicity of D. suzukii to insecticides. Locomotor assays, detoxification gene expression analysis, and acute insecticide contact bioassays were performed under conditions that approximate a typical summer day in Watsonville, California, where D. suzukii was first detected in North America. Summer is also the cropping season, when most insecticide applications occur. We observed that D. suzukii assumed a bimodal activity pattern, with maximum activity occurring at dawn and dusk. Five of the six genes tested exhibited rhythmic expression over a circadian day, with the majority showing peak expression at dawn (ZT0, 6am). We observed significant differences in the chronotoxicity of D. suzukii towards malathion, with highest susceptibility at ZT0 (6am), corresponding to peak expression of cytochrome P450s that may be involved in bioactivation of malathion. High activity levels were not found to consistently correlate with high insecticide susceptibility as initially hypothesized. Chronobiology and chronotoxicity of D. suzukii provide valuable insights for monitoring and control efforts, because insect activity as well as insecticide timing and efficacy are crucial considerations for pest management. However, field research is necessary for extrapolation to agricultural settings.