Parasitic wasp turns caterpillars into head-banging bodyguards

Bodyguards have a tough and risky job but they usually get paid for their trouble. But not the caterpillar of the geometer moth. Against its will, it is recruited to defend the developing young of a parasitic wasp, and the only 'reward' it gets for its trouble is to be eaten inside out by the larvae of its attacker.

The vast majority of wasps are "parasitoids", animals that practice the grisly art of body-snatching. They lay their eggs in the bodies of other living animals to provide their newly hatched grubs with a fresh supply of meat. Like HR Giger's alien, the full-grown larvae then burst through their host's skin, usually killing it in the process.

But the fate of one type of caterpillar Thyrinteina leucocerae doesn't end there. It is targeted by a Glyptapanteles wasp that, on a single pass, can lay as many as 80 eggs onto the hapless host. Two weeks later, the larvae burst through their host's skin. But despite its injuries, the caterpillar remains alive and stays near the hatched grubs as they spin their pupae and turn into adults. It never moves and it never feeds. All it does it violently swing its head in response to nearby movement. After the adult wasps fly off, it eventually dies.  

Amir Grosman from the University of Amsterdam  has found that the caterpillar's strange behaviour is all part of the manipulations of the wasp. Its last act is to defend the very grubs that spent the last two weeks killing it, playing the role of bodyguard as well as incubator.

Head-banging caterpillars

Together with Dutch and Brazilian colleages, Grosman showed that caterpillars that were incubating wasp grubs were just as active as unaffected ones. However, after the grubs hatched, the majority of the host caterpillars froze completely, stopped feeding and reared up onto their hind legs.

These zombie-like sentinels only moved in the presence of stinkbugs, which will eat both caterpillars and wasp pupae. When Grosman placed these predators near the caterpillars, almost all of the parasitized ones  lashed out with violent swings of their heads. These head butts are not a normal response, for only one of the 20 unaffected caterpillars reacted to stinkbugs in the same way. Even so, they are an effective defence. In about 60% of encounters with the head-swinging caterpillars, the bugs either give up or were knocked off their twigs.

In natural conditions, the caterpillar's vigil ensures that more wasp pupae survive. When Grosman removed these unwitting guardians, the death rate among the pupae doubled. Some were eaten and a few, in an ironic twist, became hosts themselves to other wasp grubs - a case of so-called "hyperparasitism".  Clearly, the young wasps benefit from their warden's actions but the caterpillars themselves get nothing. Every last one of them was dead within a week after the pupae opened and the adult wasps emerged.  

No grub left behind...

The ability to change the behaviour of its host is a common strategy in a parasite's playbook, and this is just one case among many. Another wasp, Hymenoepimecis argyraphaga, induces its spider host to spin a radically different type of web to support the wasp's cocoon. Snails infected with the Leucochloridium fluke neglect their shade-seeking instincts and crawl onto brightly lit leaves, where they are more likely to be eaten by the fluke's next host - birds.  One brain parasite, Toxoplasma gondii, makes rodent hosts less fearful of the smell of cats, which are its final host. It may even have affected human culture.

How does the wasp make the caterpillar change its behaviour so radically? The weird change only happens about two weeks after the female wasp originally filled the caterpillar with eggs, so she's unlikely to play any role in it. The hatching process isn't the trigger, because caterpillars that are artificially damaged don't behave in the same way. And the pupae don't secrete any mind-altering chemicals because placing them next to uninfected caterpillars has no effect.

The most likely scenario is altogether more amazing. When Grosman dissected guardian caterpillars, he found that not all the wasp larvae leave their hosts. One or two stay behind and are still active. Grosman thinks that its these hangers-on that manipulate the half-dead caterpillar. They effectively sacrifice themselves for the survival of their siblings.

Image by José Lino-Neto

Reference: Grosman, A.H., Janssen, A., de Brito, E.F., Cordeiro, E.G., Colares, F., Fonseca, J.O., Lima, E.R., Pallini, A., Sabelis, M.W., Raine, N.E. (2008). Parasitoid Increases Survival of Its Pupae by Inducing Hosts to Fight Predators. PLoS ONE, 3(6), e2276. DOI: 10.1371/journal.pone.0002276