In the pea aphid, Acyrthosiphon pisum, infection with the heritable bacterial symbiont, Hamiltonella defensa, confers protection against an important natural enemy, the parasitoid wasp Aphidius ervi. Typically, female wasps deposit a single egg into the aphid hemocoel, which subsequently develops within a living aphid before pupating and eventually killing the aphid host. Aphids infected with Hamiltonella, however, survive and reproduce when wasps are killed before completing development. In the absence of parasitism, Hamiltonella infection is not required for aphid survival or reproduction and surveys of natural pea aphid populations indicate intermediate infection frequencies. It is well known that herbivorous insects have developed strategies to overcome plant defenses such as secondary metabolites, so we wanted to discover whether wasp have developed strategies aimed at circumventing symbiont-based defense against parasitism. Specifically, we sought to determine 1) if wasps can distinguish Hamiltonella-infected aphids from uninfected ones?, 2) is superparasitism (depositing more than one egg in an aphid) a strategy that wasps can use to increase rates of successful parasitism?,  and if so, 3) do wasps selectively superparasitize Hamiltonella-infected aphids more than uninfected aphids?

Results/Conclusions

1) In Y-tube choice tests, we found that wasps can distinguish between honeydew collected from Hamiltonella-infected aphids and uninfected aphids. Using gas chromatography, we were unable to identify volatile differences in honeydew between infected and uninfected lines.

2) In bioassays, we found that superparasitism led to significantly higher rates of successful parasitism in Hamiltonella-infected aphids compared to singly-parasitized controls.

3) In choice tests, we found that female wasps tended to lay a single egg in uninfected aphids while depositing more than one egg in Hamiltonella-infected aphids, indicating that wasps are capable of selectively superparasitizing Hamilonella-infected hosts. Gas chromatography of whole-aphid extracts revealed significant differences in the quantity of trans-beta-farnesene (aphid alarm pheromone), which potentially explains the wasp's ability to discriminate.

Together these results indicate that A. ervi has likely developed strategies, including selective superparasitism, to overcome the symbiont-based defense deployed by the pea aphid.