Almost all organisms are attacked by parasites. Recent studies have shown that many animals, from butterflies to chimpanzees, can protect themselves against parasites through self-medication (the use of anti-parasitic substances or diets). However, the mechanisms by which medication behaviors reduce parasite infection and disease remain poorly understood. This project focuses on monarch butterflies and their protozoan parasites. Monarch caterpillars are specialist feeders on milkweed plants, and milkweeds vary in their concentrations and toxicity of chemicals called cardenolides. When feeding on toxic milkweed, monarchs become less sick, and infected female butterflies preferentially lay their eggs on toxic milkweed to reduce disease in their offspring. This project will determine whether toxic milkweeds reduce disease by directly killing parasites, by increasing the immune response of monarchs, or by providing monarchs with a gut flora that prevents parasite infection. Beyond monarch butterflies, this project has broad relevance to other animals, many of which use medicinal plants. The parasites studied here are related to parasites causing disease in agricultural animals and humans, thus elucidating the anti-parasitic activity of milkweed chemicals could have future applications for treating disease. The project will also integrate research with education, by training graduate and undergraduate students, including those from underrepresented groups in science. The researchers will also develop lesson modules with the Wylde Center, an Atlanta-based non-profit organization that teaches environmental awareness through community-garden based outdoor programs. As part of this, the project will directly contribute to the science education of thousands of K-12 students.
Hosts have evolved a range of defenses against their parasites, including behavioral and microbial defenses. Such defenses may have important consequences for the evolution of physiological immunity, but research on the interplay between physiological immunity, behavioral immunity and microbial protection remains scarce. This project will study the interaction between monarch butterflies, their milkweed host plants and their protozoan parasites to address three hypotheses: (1) behavioral use of medicinal milkweeds directly decreases parasite infection, rendering physiological immunity superfluous and reducing investment in such immune mechanisms; (2) medicinal milkweeds do not reduce monarch immunity but instead exert their protective effects by enhancing physiological immune responses; and (3) medicinal milkweeds modulate monarch midgut microbiota to a state that confers resistance to parasite infection. These hypotheses will be addressed by elucidating immune responses differentially mounted upon infection of butterflies from resistant and susceptible populations, comparing anti-parasite immune responses in monarchs fed on medicinal and non-medicinal milkweed plants, and by analyzing the effects of milkweed secondary and nutritional chemicals on monarch immunity and resistance. In addition, comparison of the midgut microbiota of monarchs reared on medicinal and non-medicinal milkweeds will be coupled with experiments manipulating gut microbiota to test for the effect of medicinal milkweed microbial communities on monarch resistance to infection. The researchers will use a combination of fieldwork, controlled experiments and next generation sequencing technology, including the use of RNASeq to quantify differential immune responses and MiSeq to quantify bacterial and fungal caterpillar gut communities.
