Bacterial endosymbionts protect aphids in the field and alter parasitoid community composition

Abstract

It has become increasingly evident that many organisms rely on microbial symbionts for defense against natural enemies, but the ecological importance of defensive symbionts for natural communities still needs to be investigated. A well-known example is Hamiltonella defensa, a heritable endosymbiotic bacterium commonly found in aphids. Laboratory experiments have shown that H. defensa strongly protects aphids against parasitic wasps (parasitoids), although this protection is not equally effective against different species of parasitoids, or even different genotypes of the same species. These results suggest that H. defensa plays an important role in reducing aphid mortality by parasitoids and presumably affects the community composition of parasitoids relying on aphids as a resource. However, there is little evidence that this is indeed the case under natural conditions. We tested this in a field experiment with black bean aphids (Aphis fabae) by setting up replicated field plots with genetically identical aphids that did or did not harbor H. defensa and following their colonization by natural enemies over a growing season. We observed a clear reduction in parasitism of symbiont-protected aphids, particularly by the parasitoids posing the highest risk. However, protected aphids did not develop larger populations than unprotected ones, possibly reflecting the balancing effect of costs associated with harboring H. defensa. We also observed shifts in the parasitoid species composition on aphids protected by H. defensa, showing that defensive symbionts have the potential to alter the diversity and structure of food webs, with likely consequences for their function and stability.

Cascading effects of herbivore protective symbionts on hyperparasitoids

“…In addition, inbreeding in parasitoids can significantly influence their biology, including host selection behaviour (Sepúlveda et al, 2016) and it is possible that outbred individuals may respond differently to endosymbiont defence or to hyperparasitoid attack. However, field experiments suggest that aphids are protected by symbionts against natural parasitoid populations in a similar manner to that observed in the laboratory Rothacher et al, 2016), and it is likely that the results reported in this study will also pertain in natural conditions.…”

“…No laboratory or field cage experiments previously undertaken in the aphid symbiont system have yet included hyperparasitoids, although they can be an extremely important source of parasitoid mortality in the field (Müller et al, 1999). A previous field experiment has shown no differences between aphids with and without symbionts in their rates of secondary parasitism Rothacher et al, 2016), although hyperparasitoid sample sizes were small. The fact that the relative benefits of a symbiont can vary depending on the wider community present shows that we need to consider the food web context when seeking to explain the patterns of symbiont distribution we observe in nature (Ferrari et al, 2012;Russell et al, 2013).…”

“…Aphids provide an excellent experimental model to explore how microbial symbiosis affects food web ecology (Rothacher et al, 2016) because their protective symbionts and their natural enemy complex (van Veen et al, 2006) have been well characterised. Aphids are attacked by a broad suite of natural enemies, including fungal pathogens and hymenopteran parasitoids.…”

“…Hamiltonella defensa strains vary considerably in the protection they provide , and there is evidence of both parasitoid-species and parasitoid-genotype specificity (Rouchet & Vorburger, 2012;Asplen et al, 2014;McLean & Godfray, 2015). A recent population cage experiment using a model aphid-parasitoid food web demonstrated that the presence or absence of H. defensa in one of the aphid species can affect community stability and dynamics (Rothacher et al, 2016;Sanders et al, 2016).…”

Nine facultative endosymbionts in aphids. A review

“…Symbionts, aphids, plants, natural enemies and the environment are all directly or indirectly associated with each other composing a reticular structure (Figure 2) and the defensive symbionts may have the potential to alter the food web structure and dynamics (Rothacher et al, 2016;Hrček et al, 2016).…”