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Prior adaptation of parasitoids improves biological control of symbiont-protected pests.

ABSTRACT: There is increasing demand for sustainable pest management to reduce harmful effects of pesticides on the environment and human health. For pest aphids, biological control with parasitoid wasps provides a welcome alternative, particularly in greenhouses. However, aphids are frequently infected with the heritable bacterial endosymbiont Hamiltonella defensa, which increases resistance to parasitoids and thereby hampers biological control. Using the black bean aphid (Aphis fabae) and its main parasitoid Lysiphlebus fabarum, we tested whether prior adaptation of parasitoids can improve the control of symbiont-protected pests. We had parasitoid lines adapted to two different strains of H. defensa by experimental evolution, as well as parasitoids evolved on H. defensa-free aphids. We compared their ability to control caged aphid populations comprising 60% unprotected and 40% H. defensa-protected aphids, with both H. defensa strains present in the populations. Parasitoids that were not adapted to H. defensa had virtually no effect on aphid population dynamics compared to parasitoid-free controls, but one of the adapted lines and a mixture of both adapted lines controlled aphids successfully, strongly benefitting plant growth. Selection by parasitoids altered aphid population composition in a very specific manner. Aphid populations became dominated by H. defensa-protected aphids in the presence of parasitoids, and each adapted parasitoid line selected for the H. defensa strain it was not adapted to. This study shows, for the first time, that prior adaptation of parasitoids improves biological control of symbiont-protected pests, but the high specificity of parasitoid counter-resistance may represent a challenge for its implementation.

SUBMITTER: Rossbacher S

PROVIDER: S-EPMC7463345 | biostudies-literature | 2020 Sep

REPOSITORIES: biostudies-literature

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Prior adaptation of parasitoids improves biological control of symbiont-protected pests.

Rossbacher Silvan S Vorburger Christoph C

Evolutionary applications 20200306 8

There is increasing demand for sustainable pest management to reduce harmful effects of pesticides on the environment and human health. For pest aphids, biological control with parasitoid wasps provides a welcome alternative, particularly in greenhouses. However, aphids are frequently infected with the heritable bacterial endosymbiont <i>Hamiltonella defensa</i>, which increases resistance to parasitoids and thereby hampers biological control. Using the black bean aphid (<i>Aphis fabae</i>) and ...[more]

PMID: 32908591

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Project description: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.

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Prior adaptation of parasitoids improves biological control of symbiont-protected pests.

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Prior adaptation of parasitoids improves biological control of symbiont-protected pests.

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