Population-specific effect of Wolbachia on the cost of fungal infection in spider mites.

Many studies have revealed the ability of the endosymbiotic bacterium Wolbachia to protect its arthropod hosts against diverse pathogens. However, as Wolbachia may also increase the susceptibility of its host to infection, predicting the outcome of a particular Wolbachia-host-pathogen interaction remains elusive. Yet, understanding such interactions and their eco-evolutionary consequences is crucial for disease and pest control strategies. Moreover, how natural Wolbachia infections affect artificially introduced pathogens for biocontrol has never been studied. Tetranychus urticae spider mites are herbivorous crop pests, causing severe damage on numerous economically important crops. Due to the rapid evolution of pesticide resistance, biological control strategies using entomopathogenic fungi are being developed. However, although spider mites are infected with various Wolbachia strains worldwide, whether this endosymbiont protects them from fungi is as yet unknown. Here, we compared the survival of two populations, treated with antibiotics or naturally harboring different Wolbachia strains, after exposure to the fungal biocontrol agents Metarhizium brunneum and Beauveria bassiana. To control for potential effects of the bacterial community of spider mites, we also compared the susceptibility of two populations naturally uninfected by Wolbachia, treated with antibiotics or not. In one population, Wolbachia-infected mites had a better survival than uninfected ones in absence of fungi but not in their presence, whereas in the other population Wolbachia increased the mortality induced by B. bassiana. In one naturally Wolbachia-uninfected population, the antibiotic treatment increased the susceptibility of spider mites to M. brunneum, but it had no effect in the other treatments. These results suggest that natural Wolbachia infections may not hamper and may even improve the success of biological control using entomopathogenic fungi. However, they also draw caution on the generalization of such effects, given the complexity of within-host-pathogens interaction and the potential eco-evolutionary consequences of the use of biocontrol agents for Wolbachia-host associations.