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

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.
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