Migratory immunity: parasite infection, host defense and fitness costs in monarch butterflies

Background/Question/Methods

Monarchs (Danaus plexippus) are a globally distributed insect 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 affects host-pathogen ecology; both parasite prevalence and virulence are highest in non-migratory monarch populations. Past work also revealed a high degree of variation among individual monarchs in their susceptibility to infection, and showed negative effects of infection on monarch survival and flight performance. Here I discuss collaborative studies aimed at three interrelated questions:  (1) To what degree do infected monarchs have lower migratory success than healthy butterflies, and could this be mediated through parasite impacts on host energy reserves and/or wing morphology?  (2) Do innate immune defense predict parasite resistance, and do monarchs experience fitness tradeoffs between immune defense, energy reserves, and other fitness traits?  (3) Do monarchs that enter reproductive diapause, a physiological state that precedes fall migration, show differential measures of immunity or parasite resistance? Results are based on a combination of field monitoring studies to quantify monarch lipid reserves and immune measures during fall migration, stable isotope work to examine migratory distances travelled by healthy and infected butterflies, and laboratory experiments to examine costs of innate immune defenses and effects of diapause induction on parasite resistance.

Results/Conclusions

Results showed significant effects of parasitism on monarch fall migration distances: among monarchs overwintering in Mexico, healthy butterflies on average travelled farther distances that infected monarchs. Moreover, healthy monarchs were larger and had greater lipid reserves than infected monarchs during the fall migration.  One measure of innate immunity predicted quantitative resistance to parasite infection, but laboratory studies and examination of wild migrating monarchs did not reveal strong fitness costs of immune defense. Finally, monarchs entering reproductive diapause (as precedes fall migration) showed slightly greater resistance to infection and slightly elevated immune defense relative to non-diapausing monarchs.  Collectively, these results underscore negative effects of parasitism on monarch migratory success, an effect that could keep prevalence low in wild populations. Although innate immune defense in monarchs does not appear to be costly under scenarios measured here, elevated defenses prior to fall migration could further reduce levels of parasitism in wild monarch populations.