Mutualism promotes insect fitness by fungal nutrient compensation and facilitates fungus propagation by mediating insect oviposition preference

Abstract Penicillium and Bactrocera dorsalis (oriental fruit fly, Hendel) are major pathogens and pests of citrus fruits, as both of them can cause detrimental losses in citrus production. However, their interaction in the cohabitation of citrus fruits remains elusive. In this study, we revealed a mutualistic relationship between Penicillium and B. dorsalis. We found that insect behaviors can facilitate the entry of fungal pathogens into fruits, and fungal pathogens promote the fitness of insects in return. More specifically, Penicillium could take advantage of the openings left by ovipositors of flies, and adult flies contaminated with Penicillium could spread the fungus to new sites. Moreover, the volatile emissions from fungi could attract gravid flies to the infected site for egg laying. The fungus and B. dorsalis were able to establish mutual interaction, as revealed by the presence of Penicillium DNA in intestinal tracts of flies throughout all larval stages. The fungal partner seemed to promote the emergence rate and shorten the emergence duration of the flies by providing pyridoxine, one of the B group vitamins. Different from previously reported scenarios of strong avoidance of Drosophila and attraction of Aedes aegypti toward Penicillium, our findings unveil a hitherto new paradigm of the mutualism between Penicillium and B. dorsalis, by which both insect and fungus earn benefits to facilitate their propagation.