There are so many fascinating stories about parasitic wasps that they have become a regular feature in this blog. Usually, their prey come off poorly in these tales, with caterpillars being reduced to little more than living, paralysed larders for macabre wasp grubs. But not always - some hosts don't take the invasion of their bodies lying down. This post is an attempt to redress the balance between parasite and host, by telling the story of the caterpillar that fights back... with medicine.
One species of tiger moth, Grammia incorrupta, has a fuzzy caterpillar called the woolly bear. Like most other caterpillars, it's exploited by several species of parasitoids including flies and wasps. If these body-snatchers lay their eggs inside a caterpillar, its menu changes and it develops a preference for a group of plant toxins called pyrrolizidine alkaloids (PA).
These have no nutritional value and they clearly come at a cost, for woolly bears that eat a PA-rich diet grow more slowly than their peers. And yet, infected caterpillars gulp down these poisons by the leaf-ful. They are the medicine that the caterpillar uses to kill its unwanted hitchhikers.
Michael Singer from Wesleyan University discovered the benefits of the caterpillars' questionable diet by feeding them on plants that were either rich or poor in PA, and then exposing some of them to parasitic flies. If caterpillars weren't carrying fly eggs, their odds of survival fell by 16% if they ate PA-rich food. But if they were infected, those that munched on PA-rich plants were 17% more likely to survive than those that didn't. The toxic chemicals killed the developing flies, and far fewer of them made it to adulthood if their hosts were loaded with PA.
Singer found that parasitized caterpillars wolfed down more than twice as much PA-rich food than uninfected ones. But when he gave infected caterpillars a choice of food, he found that they have subtly different strategies for coping with parasites, depending on how many eggs they've been saddled with.
He infected caterpillars with anywhere from 0-3 fly eggs and gave them a choice a PA-rich diet with precious few other nutrients, or a nutritious block of food without any protection toxins. If the fly had laid just one, the caterpillars that survived were those that ate more of the nutritious food but not the PA-rich one. Wesleyan believes that in consuming more protein and carbohydrates, the caterpillars gave their immune systems the fuel they needed to fight off the invaders.
If individuals were laden with two eggs, those that survived used a different tactic, eating more of the PA-rich food and not the general nutritious variety. With the extra invader, a boosted immune system wasn't enough and extra medicine was needed. If there were three parasite eggs (which hardly ever happens in nature), nothing did any good. Neither eating more nutrients nor more PA improved the caterpillars' survival - this degree of infection overwhelmed both of their defences.
Singer's study is the first definitive example of an insect using medicine to treat its own infection, where it's clearly doing so to improve its chances of survival. There's only one possible other example - the caterpillars of another species of tiger moth (Platyprepia virginalis) switches from tasty bush lupine to poisonous hemlock when it's invaded by parasites.
However, in this case, the poisons seem to bestow the caterpillar with tolerance rather than resistance and in many cases, both it and its parasites survive. As such, it isn't clear whether the caterpillar is medicating itself, or whether it's all part of the parasite's manipulations.
Being simple invertebrates, Singer's woolly bears also divorce the practice of self-medication from its typical association with high intelligence. Many other animals, from chimps to sheep, can learn (or be trained) to use specific plants to treat poisons and parasites but the woolly bears show that learning isn't necessary.
They eat PA-rich plants as a matter of course; when parasites are afoot, all that changes is how much of this food they consume. Singer thinks that the caterpillar's immune system recognises the presence of parasites and changes its taste system to make it more responsive to the tang of PA. Indeed, other studies have found that parasitized woolly bears respond more strongly to the taste of PA than uninfected ones.
Reference: Singer, M., Mace, K., & Bernays, E. (2009). Self-Medication as Adaptive Plasticity: Increased Ingestion of Plant Toxins by Parasitized Caterpillars PLoS ONE, 4 (3) DOI: 10.1371/journal.pone.0004796
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