Monarch butterfly, Danaus plexippus. (Flickr: Martin LaBar)
Using specific compounds to cure disease seems like a fairly advanced behavior—it’s necessary to recognize that you’re sick, then know what to take to cure yourself, then go out and find it. You might be surprised to learn, then, that one of the best examples of self-medication behavior in a non-human animal isn’t another primate species, or even another vertebrate. It’s none other than monarch butterflies. Female monarchs infected with a particular parasite prefer to lay eggs on host plants that help their offspring resist the parasite [PDF].
(I first heard about this discovery at this spring’s Evolution meetings, and learned that the article had been published online last week via Bora Zivkovic‘s link to coverage by Scientific American.)
. A monarch caterpillar. (Flickr: Martin LaBar)
Most natural monarch butterfly populations are infected, at varying rates, with the protozoan parasite Ophryocystis elektroscirrha. Monarch larvae become infected when they eat parasite spores laying on the leaves of their food plants; the parasites reproduce inside the growing larvae form more spores while the larvae undergoes metamorphosis. Infected adults emerge from their chrysalises covered in O. elektroscirrha spores, which they spread to their mates and to their own offspring.
Infection reduces monarchs’ lifespans and damages their flight performance [PDF]. This creates a selective tradeoff that prevents the parasites from becoming too damaging—gimpy (or dead) monarchs are less effective at spreading spores [PDF]—but the butterflies are still better off if not infected at all. It’s convenient for monarchs, then, that the plants they prefer to eat can also fight Ophryocystis elektroscirrha.
Monarch caterpillars are well-known to eat milkweeds, which defend themselves by producing organic compounds in a class called cardenolides—literally “heart poisons.” These deter lots of insect herbivores, but monarch caterpillars have evolved physiological mechanisms to store up cardenolides without suffering ill effects, which in turn makes each caterpillar, and its later adult phase, toxic to predators. (Lots of specialist herbivores evolve tolerances to, or even preferences for, their host plants’ defensive chemistry.)
It turns out that cardenolides are also bad for monarchs’ parasites. In an experiment published in 2008, de Roode et al. raised monarch caterpillars on two milkweed species that produced differing amounts of cardenolides, Asclepias curassavica and A. incarnata. They found that infected caterpillars fed the more toxic A. curassavica suffered fewer ill effects of infection [PDF].
This result is remarkable enough on its own. It suggests that the effects of infection by Ophryocystis elektroscirrha might vary in natural monarch populations depending on something separate from the monarch-parasite interaction itself—the toxicity of the locally-available milkweed species. But what if monarchs could choose more toxic milkweed to fight infection?
A female monarch feeds on butterflyweed, Asclepias tuberosa. (Flickr: donsutherland1)
This possibility of self-medication by monarchs is the focus of the latest result in the monarch-parasite system. In the new study, a team of researchers at Emory University and the University of Michigan offered infected and uninfected monarch caterpillars leaf cuttings from both of the milkweed species used in the 2008 experiment. However, infected caterpillars showed no greater preference for the more toxic milkweed.
Caterpillars might not be well-suited to self-medication anyway; they’re not very mobile, and so stuck with the host plant patch in which they hatch. Adult female monarchs, on the other hand, can fly—and seek out a patch of parasite-fighting plants on which to lay their eggs. In a second experiment, the team offered infected and uninfected adult females the opportunity to lay eggs on a single plant of each milkweed species, placed at opposite ends of a flight cage. And, indeed, infected female monarchs looked out for the best interest of their offspring, laying a larger proportion of their eggs on the more toxic plant.
This sort of trans-generational self-medication raises some very interesting questions, particularly, how do infected monarchs know they’re infected? How does local diversity of milkweed species in natural populations alter the coevolution of monarchs with Ophryocystis elektroscirrha? There’s still a lot to learn about this fascinating behavior, which may be happening in backyards across North America.
To conclude, here’s a great video produced by Emory University, in which Principal Investigator Jaap de Roode talks about monarchs in general, and the new discovery in particular.
References
Bradley, C., & Altizer, S. (2005). Parasites hinder monarch butterfly flight: implications for disease spread in migratory hosts. Ecology Letters, 8 (3), 290-300 DOI: 10.1111/j.1461-0248.2005.00722.x
de Roode, J., Pedersen, A., Hunter, M., & Altizer, S. (2008). Host plant species affects virulence in monarch butterfly parasites. Journal of Animal Ecology, 77 (1), 120-6 DOI: 10.1111/j.1365-2656.2007.01305.x
de Roode, J., Yates, A., & Altizer, S. (2008). Virulence-transmission trade-offs and population divergence in virulence in a naturally occurring butterfly parasite. Proceedings of the National Academy of Sciences, 105 (21), 7489-94 DOI: 10.1073/pnas.0710909105
Lefèvre, T., Oliver, L., Hunter, M., & De Roode, J. (2010). Evidence for trans-generational medication in nature. Ecology Letters DOI: 10.1111/j.1461-0248.2010.01537.x
