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

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.

Cheaper is not always worse: strongly protective isolates of a defensive symbiont are less costly to the aphid host.

Defences against parasites are typically associated with costs to the host that contribute to the maintenance of variation in resistance. This also applies to the defence provided by the facultative bacterial endosymbiont Hamiltonella defensa, which protects its aphid hosts against parasitoid wasps while imposing life-history costs. To investigate the cost-benefit relationship within protected hosts, we introduced multiple isolates of H. defensa to the same genetic backgrounds of black bean aphids, Aphis fabae, and we quantified the protection against their parasitoid Lysiphlebus fabarum as well as the costs to the host (reduced lifespan and reproduction) in the absence of parasitoids. Surprisingly, we observed the opposite of a trade-off. Strongly protective isolates of H. defensa reduced lifespan and lifetime reproduction of unparasitized aphids to a lesser extent than weakly protective isolates. This finding has important implications for the evolution of defensive symbiosis and highlights the need for a better understanding of how strain variation in protective symbionts is maintained.