Abstract
BackgroundRecent findings indicate that several insect lineages receive protection against particular natural enemies through infection with heritable symbionts, but little is yet known about whether enemies are able to discriminate and respond to symbiont-based defense. The pea aphid, Acyrthosiphon pisum, receives protection against the parasitic wasp, Aphidius ervi, when infected with the bacterial symbiont Hamiltonella defensa and its associated bacteriophage APSE (Acyrthosiphon pisum secondary endosymbiont). Internally developing parasitoid wasps, such as A. ervi, use maternal and embryonic factors to create an environment suitable for developing wasps. If more than one parasitoid egg is deposited into a single aphid host (superparasitism), then additional complements of these factors may contribute to the successful development of the single parasitoid that emerges.ResultsWe performed experiments to determine if superparasitism is a tactic allowing wasps to overcome symbiont-mediated defense. We found that the deposition of two eggs into symbiont-protected aphids significantly increased rates of successful parasitism relative to singly parasitized aphids. We then conducted behavioral assays to determine whether A. ervi selectively superparasitizes H. defensa-infected aphids. In choice tests, we found that A. ervi tends to deposit a single egg in uninfected aphids, but two or more eggs in H. defensa-infected aphids, indicating that oviposition choices may be largely determined by infection status. Finally, we identified differences in the quantity of the trans-β-farnesene, the major component of aphid alarm pheromone, between H. defensa-infected and uninfected aphids, which may form the basis for discrimination.ConclusionsHere we show that the parasitic wasp A. ervi discriminates among symbiont-infected and uninfected aphids, and changes its oviposition behavior in a way that increases the likelihood of overcoming symbiont-based defense. More generally, our results indicate that natural enemies are not passive victims of defensive symbionts, and that an evolutionary arms race between A. pisum and the parasitoid A. ervi may be mediated by a bacterial symbiosis.
Highlights
Recent findings indicate that several insect lineages receive protection against particular natural enemies through infection with heritable symbionts, but little is yet known about whether enemies are able to discriminate and respond to symbiont-based defense
We examined the effects of superparasitism on a range of experimental lines that varied in aphid genotype, infection status and H. defensa strain (Table 1)
We found that superparasitism resulted in higher rates of successful parasitism compared to single parasitism in all lines infected with H. defensa (Table 2C, Figure 1A, B)
Summary
Recent findings indicate that several insect lineages receive protection against particular natural enemies through infection with heritable symbionts, but little is yet known about whether enemies are able to discriminate and respond to symbiont-based defense. In addition to carrying the obligate nutritional symbiont, Buchnera aphidicola, this aphid is often infected with additional facultative bacteria, called ‘secondary’ symbionts, which have been found to mediate important ecological interactions These effects include thermal tolerance [20,21], resistance to fungal pathogens [9] and parasitoid wasps [14]. In the latter case, A. pisum acquires partial to complete immunity to parasitism by the common parasitoid wasp Aphidius ervi via infection with the g-proteobacterial symbiont Hamiltonella defensa [14,22]. A. pisum lacking H. defensa (or those carrying H. defensa that lack APSE) are highly susceptible to parasitism by A. ervi, while lines carrying APSE-infected H. defensa receive partial to complete protection depending on H. defensa strain and associated phage haplotype [22,23,24]
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