Every cloud has a silver lining: Moderate plant water stress positively impacts development, immunity, and gut microbiota of a specialist herbivore

The ongoing global temperature rise has led to increasing frequency of drought events, negatively impacting vegetation and the living organisms relying on it. Extreme drought killing host plants can clearly reduce herbivore fitness, but the impact of moderate host plant water stress on insect herbivores can vary, and may even be beneficial. The Finnish Glanville fritillary butterfly ( Melitaea cinxia ) has faced reduced precipitation in recent years, which has impacted population dynamics. However, whether the negative effects depend on extreme desiccation killing the host plant or moderate drought impacting plant quality remains unclear. We assessed the performance of larvae fed on moderately water-stressed Plantago lanceolata in terms of growth, gut microbial composition and immune response. We found that larvae fed on water-stressed plants had better growth, a more heterogeneous bacterial community and a shifted fungal community in the gut, and up-regulated the expression of one candidate immune gene (pelle), whereas survival remained unaffected. Most of the measured traits showed considerable variation due to family structure. Our data suggest that in temperate regions moderate host plant water stress can positively shape resource acquisition of this specialized insect herbivore, potentially by increasing nutrient accessibility or concentration. Potentially, the better larval performance may be mediated by a shift of the microbiota on water-stressed plants, calling for further research especially on the understudied gut fungal community.