Immune defenses are suppressed by reproductive development and mating activity in monarch butterflies
Animals frequently face trade-offs between reproduction and immunity. Past work showed that when immunity is up-regulated, reproductive output decreases, and vice versa. These shifts in immune allocation can determine host susceptibility to pathogens. Many aspects of reproduction can be costly to immunity, and a crucial open question involves how different components (e.g., copulation, egg production) contribute to immune costs. Monarch butterflies show tremendous generational differences in the timing of reproductive development. Adult monarchs emerging in fall have low levels of juvenile hormone (JH), resulting in a prolonged migratory state termed reproductive diapause. This generation of monarchs does not mate and reproduce until the following spring. Summer generations have high levels of JH and reproduce immediately following adult emergence. To understand how monarch immunity depends on hormonal activation and mating activity, we manipulated environmental conditions (temperature and daylength) that induce reproductive diapause during larval development, exposed a subset of adults to a JH-analog to reverse diapause, and varied access to mating opportunities. We tested how environmental conditions, JH treatment, and mating activity influenced the investment in two components of immunity (hemocyte concentration and phenoloxidase activity).
Diapause induction did not affect the initial measures of monarch immunity upon adult emergence, but the change in immune measures (over two weeks) depended on both diapause induction and mating activity. Monarchs raised in “fall” environmental conditions maintained higher levels of immunity from the first to the second timepoint than reproductive monarchs (raised in “summer” conditions or raised in “fall” conditions and treated with JH). Male monarchs prevented from mating also maintained higher defenses than monarchs that mated when provided access to conspecifics. In female monarchs, those that mated and also laid eggs showed greater reductions in immunity than those that were unmated or that mated but did not lay eggs. Further, there was a negative relationship between the frequency of mating in females and the degree of reduction in hemocyte concentration. Cumulatively, these results suggest that wild monarchs that are reproductively active (spring and summer) are less well defended than monarchs during the fall migratory generation, and that among reproductively active individuals, those that mate more frequently or invest in higher fecundity are especially immunocompromised. Our results indicate that seasonal shifts in reproduction and immune investment could alter host-pathogen interactions by mediating changes in host susceptibility to infection.