A cryptic host–parasitoid interaction reduces the impact of heatwaves on Drosophila host populations

Laboratory measures of thermal tolerance are used to predict population responses to climate extremes, but rarely account for co-occurring biotic stressors associated with consumers and resources. Among consumers, parasitoids have especially intimate interactions with hosts that likely both depend on and alter host physiology. However, the context-dependent interplay between host reactions to parasitism and heat remains understudied. We applied a factorial design of heatwave, parasitism and nutrition treatments on three rainforest Drosophila species to test whether parasitoid infection reduces host heat tolerance, particularly under nutritional deficiency. We found that high-yeast diets increased the resistance of Drosophila to parasitoids but decreased their survival during heatwaves. Surprisingly, exposure to parasitoids reduced the susceptibility of host populations to heatwaves compared to null models accounting for combined mortality effects; this reduction was observed under yeast-rich diets and independent of host susceptibility to their native parasitoids. We reveal that parasitoids exert cryptic effects on hosts they cannot successfully develop within, with positive fitness consequences for hosts under extreme heat. This consistent positive interactive effect across native hosts suggests a general crosstalk between physiological pathways for immunity and heat tolerance—a critical consideration for predicting population-dynamic responses to climate change within community networks of closely interacting species.