Parasitic wasp responses to symbiont-based defense in aphids

Abstract

Background 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. 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 s econdary e ndosymbiont). 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. Results We 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. Conclusions Here 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.

Survival to Parasitoids in an Insect Hosting Defensive Symbionts: A Multivariate Approach to Polymorphic Traits Affecting Host Use by Its Natural Enemy

“…Discrepancy between aphid hospitality to the A. ervi wasp vs. hospitality to its progeny, where extra eggs are invested to balance immature mortality, is an important finding that emerges from this study (see also [33] who independently observed the same mechanism). In order to exploit a ‘multifaceted’ polymorphic and clonally reproducing host such as A. pisum , the A. ervi wasps and immatures must balance their differential capacity to use hosts with divergent hospitality occurring together in mixed host populations.…”

“…Host susceptibility to A. ervi in A. pisum is clonally variable, depending behaviorally on aphid body color ([29] and references therein), and physiologically on host defensive anti-parasitoid bacterial symbionts. In particular, Hamiltonella defensa bacteria can kill or stop development of A. ervi immature stages, thus acting as a symbiotic form of host resistance (reviewed in [30]; see also [29], [31], [32], [33]). With host defensive bacteria, the Aphidius -aphid host system thus comprises three players associated in a tripartite trophic, symbiotic, and parasitic interaction.…”

Heat Stress Affects Facultative Symbiont-Mediated Protection from a Parasitoid Wasp

“…[25,40,41]). It is possible that the parasitoid exhibited different oviposition behavior in the different treatments, but typically this is observed in choice rather than no-choice assays [25,40,42,43]. …”

Experimental Models to Study the Role of Microbes in Host-Parasite Interactions

“…Aphids are thus ideal experimental models to understand the impact of defensive symbionts on the evolution of their hosts and parasites. For instance, it is employed to study the cost of defensive symbionts (Vorburger et al, 2013; Polin et al, 2014; Cayetano et al, 2015), their population dynamics (Oliver et al, 2008), their role in parasitoid community composition (Rothacher et al, 2016), the specificity of symbiont-associated defense (Martinez et al, 2016b), and to demonstrate that host symbiont’s role in defense imposes new selection pressure on parasites (Oliver et al, 2012). Another biological system worth mentioning is the role of Wolbachia against viruses.…”