Evil parasites are the stuff of horror movies, bursting out of unsuspecting victims in the most ghoulish fashion possible. However, it seems that even parasites are not immune to parasites of their own. Anne Duplouy, Saskya van Nouhuys and Minna Kohonen from the University of Helsinki, Finland, describe how Hyposoter horticola parasitic wasps, which exclusively target Granville fritillary butterfly caterpillars – on the Åland Islands off Finland – are susceptible in turn to Mesochorus cf. stigmaticus hyperparasitic wasps, which hijack H. horticola larvae as incubators for their own offspring. However, Duplouy had also noticed previously that H. horticola populations had lower levels of M. cf. stigmaticus infection where H. horticola had high rates of infection by the symbiotic Wolbachia bacteria (doi: 10.1371/journal.pone.0134843). Explaining that Wolbachia infections are often beneficial to their hosts in order to maintain their welcome, Duplouy wondered whether the bacteria also boosted the resistance of H. horticola to M. stigmaticus hyperparasitic lodgers – consequently reducing M. cf. stigmaticus infection rates when Wolbachia infection rates are high. However, there was an alternative explanation for low levels of M. cf. stigmaticus infection: if Wolbachia reduced the resistance of H. horticola to M. cf. stigmaticus, this would allow M. stigmaticus to kill off Wolbachia-infected H. horticola to keep their numbers down when M. cf. stigmaticus infection rates were high.
Intrigued by both possibilities, the team investigated whether Wolbachia-infected H. horticola were better at evading M. cf. stigmaticus infections or became more susceptible to the tenacious hyperparasite. First, they had to produce H. horticola-infected Granville fritillary caterpillars that they could place in the environment, where half of the caterpillars were carrying H. horticola that were infected with Wolbachia and the other half were Wolbachia free.
Duplouy and colleagues collected parasitized fritillary larvae from the Åland Islands and waited for the adult H. horticola wasps to emerge. Knowing that only 50% of the parasitic wasps carried Wolbachia, they then offered clutches of butterfly eggs to the H. horticola wasp mothers for them to lay their eggs in. After nurturing the butterfly eggs as they developed into caterpillars, the team checked that some individuals from each clutch were carrying H. horticola wasp larvae and then transferred the parasitized caterpillars onto potted plants, where they spun silky nests for overwintering; the team finally transferred the plants and their parasitised caterpillars to Åland Islands to measure the impact that Wolbachia infection had on the rate of M. cf. stigmaticus infestation of H. horticola larvae.
Retrieving the caterpillar nests from the islands several weeks later and comparing the number of butterfly nests that had been targeted by the M. cf. stigmaticus hyperparasites, the team found that 74% of the H. horticola larvae that carried Wolbachia were infested by M. cf. stigmaticus larvae, in contrast to the Wolbachia-free H. horticola, which only suffered a 40% M. stigmaticus infestation rate. So, Wolbachia infections seem to make H. horticola larvae more vulnerable to parasitic infection, which poses the question of why H. horticola maintains the close relationship with symbiotic bacteria that increase its vulnerability in some circumstances. ‘In order to persist in the host population, [Wolbachia] must have a positive effect on the fitness of infected parasitic wasps that could outweigh the costly burden of susceptibility to widespread parasitism’, says Duplouy and colleagues, who suspect that bacteria may contribute to H. horticola’s resistance to other parasitic infections instead.