Punch in the gut: Parasite tolerance of phytochemicals reflects host diet

Abstract

Gut parasites of plant-eating insects are exposed to antimicrobial phytochemicals that can reduce infection. Trypanosomatid gut parasites infect insects of diverse nutritional ecologies as well as mammals and plants, raising the question of how host diet-associated phytochemicals shape parasite evolution and host specificity. To test the hypothesis that phytochemical tolerance of trypanosomatids reflects the chemical ecology of their hosts, we compared related parasites from honey bees and mosquitoes--hosts that differ in phytochemical consumption--and contrasted our results with previous studies on phylogenetically related, human-parasitic Leishmania. We identified one bacterial and ten plant-derived substances with known antileishmanial activity that also inhibited honey bee parasites associated with colony collapse. Bee parasites exhibited greater tolerance of chrysin--a flavonoid found in nectar, pollen, and plant resin-derived propolis. In contrast, mosquito parasites were more tolerant of cinnamic acid--a product of lignin decomposition present in woody debris-rich larval habitats. Parasites from both hosts tolerated many compounds that inhibit Leishmania, hinting at possible trade-offs between phytochemical tolerance and mammalian infection. Our results implicate the phytochemistry of host diets as a potential driver of insect-trypanosomatid associations, and identify compounds that could be incorporated into colony diets or floral landscapes to ameliorate infection in bees. ORIGINALITY AND SIGNIFICANCETrypanosomatid parasites of insects pose threats to beneficial insects, crop plants, and human health. Elucidation of the environmental factors that determine host-parasite specificity and transmission of trypanosomatids is essential to predict the spread and spillover potential of trypanosomatids in wild and agricultural ecosystems. Our comparisons between trypanosomatids of bees and mosquitoes implicate the phytochemical composition of host diets as a potential determinant of insect-trypanosomatid associations. To our knowledge, this is the first comparative study of phytochemical tolerance in insect trypanosomatids. As the first characterization of phytochemical tolerance among honey bee-associated trypanosomatids, our results also identify compounds that could ameliorate infection of managed bees with parasites of concern to wild pollinators and associated with colony collapse.