The contributions of host diet and genetic background to shaping parasite infection outcomes in monarch butterflies across natural populations

Highly specialized insect—parasite interactions can vary greatly between populations, which can be attributed to differences in evolutionary history and contemporary ecological differences. Understanding how this variation arises and persists across insect—parasite populations requires knowledge of both genetic and ecological factors. Dietary variation across subpopulations in an insect's rage is among the most important ecological factors that can shape interactions with their parasites. However, the roles of dietary and genetic differences in shaping insect–parasite interactions are understood in only a handful of systems, mostly pest, managed or common model species. Given that genetic and dietary differences often covary, disentangling their effects requires experimentation to complement the observational data on which our understanding of many systems is based. Here, we experimentally tested the roles of diet and genetic background in shaping monarch butterfly resistance to its protozoan parasite Ophryocystis elektroscirrha using monarchs from mainland North America, Puerto Rico and hybrids of these two populations. By factorially manipulating host diet and genetic background, we found that parasite resistance conferred by a toxic host plant to mainland North American monarchs did not provide resistance to Puerto Rican monarchs. Instead, resistance in Puerto Rican monarchs was conferred by their genetic background, which was partially passed to hybrids of mainland North American–Puerto Rican monarchs. We then assessed cuticular melanin, a proxy for immune competency, as a potential explanation for the increased resistance observed in Puerto Rican monarchs. Although we found support for melanin‐associated immune competency across populations, we did not find support for this hypothesis within populations. Overall, these findings add to a growing body of unique case studies that lend insight into the complex ecological and evolutionary dynamics of highly specialized host–parasite interactions.