Temperature overrides nutritional cues for optimal oviposition decision in a polyphagous invasive insect

Polyphagous insects often rely on multiple cues to select oviposition sites, including substrate temperature and nutritional resources. Optimal conditions do not always align, however, and a thermally optimal oviposition site can be nutritionally suboptimal, and vice versa. Our study evaluated the ability of females to make optimal oviposition site decisions under such mismatch between thermal and nutritional conditions in an invasive polyphagous fly species, Drosophila suzukii. We also tested if symbiotic Wolbachia bacteria modulate oviposition choice. First, we quantified the performance of D. suzukii (i.e., number of eggs laid, offspring development time, survival and mass) on four different fruit purees at three ambient temperatures. Second, we investigated how oviposition choice was affected by substrate temperature or nutritional cues separately. Finally, we designed a multiple-scenario oviposition experiment, forcing females to make choices when temperature and nutrition do not align, to explore which of the two factors are most influential for decision making. While temperature and fruit quality both influenced offspring performance, females consistently prioritised temperatures that were optimal for larval development, resulting in oviposition on less preferred fruits. This choice was in line with the preference-performance hypothesis as temperature had a larger effect than fruit quality on performance in the no-choice experiments. Infection by Wolbachia resulted in higher survival and faster development of offspring. Wolbachia also influenced female oviposition decision, modifying fruit preference and leading to more evenly distributed eggs in complex scenarios, but without altering the preference for thermally favourable oviposition sites. These results support the hypothesis that the invasive success of D. suzukii is in part explained by its ability to select optimal oviposition sites. More generally, this study highlights that animal behaviour needs to be examined under suboptimal conditions to infer the importance of behavioural flexibility for individual fitness and population biology under environmental change.