A very hungry caterpillar munches on a cabbage leaf and sets off an alarm. The plant releases chemicals into the air, signalling that it is under attack. This alarm is intercepted by a wasp, which stings the caterpillar and implants it with eggs. When they hatch, the larval wasps devour their host from the inside, eventually bursting out to spin cocoons and transform into adults. The cabbage (and those around it) are saved, and the wasp—known as a parasitoid because of its fatal body-snatching habits—raises the next generation.
But that’s not the whole story.
Some parasitic wasps are “hyperparasitoids”—they target other parasitoid wasps. And they also track the cabbage’s alarm chemicals, so they can find infected caterpillars. When they do, they lay their eggs on any wasp grubs or pupae that they find. Their young devour the young of the other would-be parasites, in a tiered stack of body-snatching. It’s like a cross between the films Alien and Inception.
Erik Poelman from Wageningen University in the Netherlands studied one of these grisly networks: the caterpillars of the small cabbage white butterfly are attacked by two parasitoid wasps—Cotesia rubecula and Cotesia glomerata—which in turn are attacked by the hyperparasitoid Lysibia nana.
L.nana lays one egg in every wasp grub or pupa that it finds. C.rubecula produces a huge grub, but it only lays one in each caterpillar. C.glomerata is the better choice for a host—its smaller larvae offer less room for L.nana’s own progeny, but it implants around 20 to 40 of these into the same unfortunate caterpillar. If L.nana can find one of these clusters, it can parasitise an huge brood of wasp larvae in one visit. And it can find them thanks to the cabbage.
As parasitoid grubs grow in a caterpillar, they suppress their host’s immune system and control its growth and metabolism for their own benefit. As a side effect, they also change the chemicals in the caterpillar’s spit. C.glomerata does this far more than C.rubecula, and the cabbage reacts to the distinct salivary cocktails by releasing different blends of alarm chemicals. The blend produced in response to a C.glomerata-parasitised caterpillar shares only 40 percent of its ingredients with that produced in response to a C.rubecula-parasitised one.
And L.nana can smell the difference between them. In lab experiments, Poelman found that it was particularly attracted to the smell of cabbages that had been attacked by C.glomerata-parasitised caterpillars—its preferred host.
In the field, the C.glomerata grubs had an even rougher time. Over three years, Poelman collected thousands of cocoons of both parasitoids from a field of cabbage plants. Four species of hyperparasitoid targeted these wasps. Collectively, they laid eggs in 5 to 15 percent of C.rubecula’s brood, but a huge 20 to 55 percent of C.glomerata’s. That’s a pretty astonishing range—up to half of this parasite’s young are lost to another parasite!
It’s possible that C.rubecula goes relatively undetected, because it has a stealth mode. Perhaps it has evolved so that it barely alters the salivary chemicals of its caterpillars, “to not reveal itself to hyperparasitoids,” says Poelman. This is still a hypothesis, and one that Poelman wants to test. But there’s a piece of evidence for it: C.rubecula has been accidentally introduced into the United States from Europe, and there, it gets hyperparasitised far more regularly. Perhaps it hasn’t had time to evolve inconspicuousness in North American caterpillars.
And what of the cabbage? Poelman writes that it’s caught between a rock and a hard place. By releasing chemicals that summon parasitoids, which can do away with its pesky caterpillar problems, it also summon hyperparasitoids, which can do away with its helpful bodyguards!
It remains to be seen how these competing evolutionary pressures affects the deployment of its chemical alarms, and it’s important that we find out. After all, some agricultural scientists are trying to use plant alarm chemicals to lure in parasitic wasps that can help them to control pest insects. But this strategy might fail if it attracts too many hyperparasitoids are about.
And it only gets more complicated. After all, some hyperparasitoids lay their eggs in other hyperparasitoids! “A common enemy of a hyperparasitoid therefore is another hyperparasitoid. This can include other females of the same species,” says Poelman. A caterpillar may play host to two, three, maybe even four tiers of parasites.
Reference: Poelman, Bruinsma, Zhu, Weldegergis, Boursault, Jongema, van Loom, Vet, Harvey & Dicke. 2012. Hyperparasitoids Use Herbivore-Induced Plant Volatiles to Locate Their Parasitoid Host. PLoS Biol http://dx.doi.org/10.1371/journal.pbio.1001435