Background/Question/Methods   Monarch butterflies (Danaus plexippus) are a globally distributed insect species best known for undertaking a spectacular annual migration in parts of North America. In wild populations, monarchs are commonly infected with a specialist protozoan Ophryocystis elektroscirrha; this parasite can be transmitted both vertically and horizontally and causes debilitating infections. The monarch-parasite system has served as a model for understanding how long-distance migration influences host-pathogen ecology and for investigating mechanisms of virulence evolution. Past work has also revealed a high degree of variation among individual monarchs in their susceptibility to infection, but the mechanisms of resistance to this parasite, and their associated tradeoffs and constraints, remain largely unknown. Here we performed a series of experiments to examine whether larval age at exposure and innate immunity predict final parasite loads and host survival following infection. We also tested for costs of immunity on host fitness traits. In addition, because of the known relationships between body pigmentation and immunity in other insect species, we asked whether butterfly wing coloration, including orange hue and black pigmentation, was correlated with infection and innate immune defenses.

Results/Conclusions Results showed strong effects of larval age on both immune defenses and parasite infection; late-stage larvae had sharply higher measures of innate immunity and were almost completely refractory to parasite infection, as compared with young and middle-stage larvae. Among the subset of infected hosts, results supported a role for larval hemocyte concentrations, but not phenoloxidase activity, in lowering parasite loads. Monarch infection status and parasite loads had strong effects on host fitness; we found weak positive effects of larval immune measures on some but not all adult fitness measures. Finally, heavily infected monarchs had lighter-colored wings, and we found a negative relationship between phenoloxidase activity and adult wing pigmentation, indicating a possible trade-off between melanin production for immune defense versus wing coloration. Collectively, these results point to a narrow window of time early in the host’s life during which infection can occur, and suggest small but significant costs and benefits of generalized immune defenses for these butterfly hosts.