Migratory trade-offs: Do monarch butterflies sacrifice immune defense for lipid storage?

Background/Question/Methods

The annual migration of the monarch butterfly is one of nature’s most captivating phenomena, yet little is known about the physiological changes that enable such long distance flight. Along their migratory pathway, monarchs forage extensively to accrue lipids that fuel flight and sustain the butterflies during the five month overwintering period in Mexico. Investment in lipid storage and other flight-related tissue is costly, and potentially diverts resources away from other processes, such as immune defense.  Whether or not monarchs face this energetic trade-off between lipid storage and immunity might depend on the distance they travel to reach the overwintering sites.  We collected 200 adult monarchs overwintering in Michoacán, Mexico and quantified their lipid stores and immune function. Immunity was assayed in two ways: total hemocyte (immune cell) counts and phenoloxidase activity (PO). We also sampled wing tissue for analyses of stable hydrogen isotopes (δD) to estimate the natal origins where monarchs fed as larvae prior to migration, and thus to infer the distance each monarch migrated.

Results/Conclusions

We found a weak negative relationship between two measures of immune defense (hemocyte counts and PO) and lipid mass for all monarchs combined after correcting for size and sex.  After accounting for the level of hydrogen isotope depletion as an indicator of migratory distance, a strong negative relationship between immunity and lipids emerged for the subset of monarchs estimated to have travelled the farthest distances. Our results suggest that monarchs do sacrifice immune defense in favor of lipid storage, and this is especially so for individuals that make the longest distance flights. More generally, our results underscore how long-distance migration can alter host-pathogen interactions by mediating changes in immune investment. As many migratory species are known to harbor infectious diseases that can infect humans and domesticated animals, this issue has far-reaching consequences for animal and human health.