Rapid evolution of symbiont‐mediated resistance compromises biological control of aphids by parasitoids

Abstract

There is growing interest in biological control as a sustainable and environmentally friendly way to control pest insects. Aphids are among the most detrimental agricultural pests worldwide, and parasitoid wasps are frequently employed for their control. The use of asexual parasitoids may improve the effectiveness of biological control because only females kill hosts and because asexual populations have a higher growth rate than sexuals. However, asexuals may have a reduced capacity to track evolutionary change in their host populations. We used a factorial experiment to compare the ability of sexual and asexual populations of the parasitoid Lysiphlebus fabarum to control caged populations of black bean aphids (Aphis fabae) of high and low clonal diversity. The aphids came from a natural population, and one‐third of the aphid clones harbored Hamiltonella defensa, a heritable bacterial endosymbiont that increases resistance to parasitoids. We followed aphid and parasitoid population dynamics for 3 months but found no evidence that the reproductive mode of parasitoids affected their effectiveness as biocontrol agents, independent of host clonal diversity. Parasitoids failed to control aphids in most cases, because their introduction resulted in strong selection for clones protected by H. defensa. The increasingly resistant aphid populations escaped control by parasitoids, and we even observed parasitoid extinctions in many cages. The rapid evolution of symbiont‐conferred resistance in turn imposed selection on parasitoids. In cages where asexual parasitoids persisted until the end of the experiment, they became dominated by a single genotype able to overcome the protection provided by H. defensa. Thus, there was evidence for parasitoid counteradaptation, but it was generally too slow for parasitoids to regain control over aphid populations. It appears that when pest aphids possess defensive symbionts, the presence of parasitoid genotypes able to overcome symbiont‐conferred resistance is more important for biocontrol success than their reproductive mode.

The price of protection: a defensive endosymbiont impairs nymph growth in the bird cherry‐oat aphid, Rhopalosiphum padi

“…B), the fittest genotypes still performed better on this host than the least fit genotypes. In summary, these findings suggest that plant resistance factors will favor the fittest R. padi genotypes, but symbiont‐infected individuals will be favored when parasitoids are abundant (Käch et al ., ), although these aphids might not achieve optimal performance on a poor quality host plant. While the consequences of symbiont‐conferred parasitoid resistance for aphid biocontrol are increasingly recognized (Vorburger, ), symbiont‐mediated fitness trade‐offs that interact with plant defensive traits have received relatively little attention until recently (e.g., Frago et al ., ; Karley et al ., ) and should be taken into account when deploying crop resistance and natural enemies for integrated management of crop pests.…”

“…Additionally, the cowpea aphid, Aphis craccivora (Koch), is attacked by a number of Braconid wasps, including Binodoxys communis (Gahan), B. koreanus (Stary), L. orientalis (Stary & Rakhshani), and A. colemani; H. defensa infection did not protect aphids against L. orientalis or A. colemani, but did provide resistance to B. communis and B. koreanus (Asplen et al, 2014). The authors hypothesized that differential protection conferred by endosymbionts against particular parasitoid species might be linked to particular H. defensa-APSE combinations, and recent work provides evidence for specificity of symbiont defense in relation to APSE strain and aphid and parasitoid genotype (Dennis et al, 2017;Käch et al, 2018;Martinez et al, 2018). These factors could explain why H. defensa provided protection to R. padi against A. colemani (this study) and to Ap.…”

“…The APSE genome has been reported to undergo rapid recombination resulting in strain-dependent variation in the identity of toxins and their protective effects (Degnan & Moran, 2008a,b;Dennis et al, 2017), which might also explain differences between wasp genera in their susceptibility to symbiont-APSE-mediated protection (Käch et al, 2018). Other studies have highlighted the existence of aphid-encoded resistance to parasitism irrespective of endosymbiont presence in M. euphorbiae and Ac.…”

The role of defensive symbionts in host–parasite coevolution

“…In the green peach aphid ( Myzus persicae ) or the black bean aphid ( Aphis fabae ), for example, clones harbouring defensive symbionts are much more resistant than the most‐resistant clones lacking these symbionts (von Burg et al ., ; Vorburger et al ., ). Laboratory experiments indeed confirmed that clones possessing heritable defensive symbionts are under strong positive selection in the presence of parasitoids (Herzog, Müller & Vorburger, ; Oliver et al ., ; Käch et al ., ).…”

Defensive symbionts mediate species coexistence in phytophagous insects

“…At least four species of facultative symbionts, namely Hamiltonella defensa, Serratia symbiotica, Regiella insecticola (Moran, Russell, Koga, & Fukatsu, 2005) and a symbiont referred to as X-type (Guay, Boudreault, Michaud, & Cloutier, 2009), include strains that increase aphid resistance to parasitoid wasps (Heyworth & Ferrari, 2015;Oliver, Russell, Moran, & Hunter, 2003;Vorburger, Gehrer, & Rodriguez, 2010). Parasitoids are important natural enemies of aphids (Schmidt et al, 2003), hence the possession of resistance-conferring symbionts can be under strong positive selection (Herzog et al, 2007;Käch, Mathé-Hubert, Dennis, & Vorburger, 2018;Oliver et al, 2008). However, this selective advantage may be lost or even reversed in the absence of parasitoids, because the possession of defensive symbionts can also entail costs to the host.…”