ANOTHER TOOL IN THE TOOLBOX:Wolbachia-mediated protection against a specialized fungal pathogen of aphids

Abstract

AbstractAphids harbor nine heritable facultative symbionts, most mediating one or more ecological interactions. However, one aphid symbiont,Wolbachia, has eluded functional characterization despite being well-studied in other arthropods. InPentaloniaaphids, global pests of banana,Wolbachiawas hypothesized to function as a co-obligate symbiont alongside the traditional obligateBuchnera, but subsequent genomic analyses failed to support this role. Sampling across multiple aphid populations, we found that > 80% ofPentaloniaaphids carried a M-supergroup strain ofWolbachianamedwPni. While the lack of fixation confirms thatWolbachiais not a co-obligate symbiont, the high infection frequencies in these entirely asexual aphids strongly suggestedWolbachiaconfers net fitness benefits. Finding no correlation betweenWolbachiaand aphid food plants use, we challengedWolbachia-infected aphids with common natural enemies. WhileWolbachiadid not protect aphids against parasitoids, this symbiont conferred significant protection against the specialized fungal pathogen,Pandora neoaphidis,and improved aphid fitness in the absence of enemy challenge. Thus, we identified a new phenotype for the multifacetedWolbachiaand highlight a system that provides unique opportunities to merge key models of heritable symbiosis to better understand infection dynamics in nature and mechanisms underpinning symbiont-mediated phenotypes.IMPORTANCE:Wolbachiasymbionts spread and persist in a wide range of arthropods and nematodes by using a range of functional strategies, including reproductive manipulation, providing protection against viral and bacterial pathogens or by provisioning nutrients. Despite being one of the best-studied symbionts, little is known about the strains that infect aphids. In this study, we characterized the functional role of a Supergroup MWolbachiastrain infecting strictly asexual aphids of the genusPentalonia. We report for the first time that this symbiont also defends against fungal entomopathogens and expand on the range of phenotypes conferred by this multifaceted symbiont.