Another tool in the toolbox: Aphid-specific Wolbachia protect against fungal pathogens

Abstract

Aphids harbor nine common facultative symbionts, most mediating one or more ecological interactions. Wolbachia pipientis, well-studied in other arthropods, remains poorly characterized in aphids. In Pentalonia nigronervosa and P. caladii, global pests of banana, Wolbachia was initially hypothesized to function as a co-obligate nutritional symbiont alongside the traditional obligate Buchnera. However, genomic analyses failed to support this role. Our sampling across numerous populations revealed that more than 80% of Pentalonia aphids carried an M-supergroup strain of Wolbachia (wPni). The lack of fixation further supports a facultative status for Wolbachia, while high infection frequencies in these entirely asexual aphids strongly suggest Wolbachia confers net fitness benefits. Finding no correlation between Wolbachia presence and food plant use, we challenged Wolbachia-infected aphids with common natural enemies. Bioassays revealed that Wolbachia conferred significant protection against a specialized fungal pathogen (Pandora neoaphidis) but not against generalist pathogens or parasitoids. Wolbachia also improved aphid fitness in the absence of enemy challenge. Thus, we identified the first clear benefits for aphid-associated Wolbachia and M-supergroup strains specifically. Aphid-Wolbachia systems provide unique opportunities to merge key models of symbiosis to better understand infection dynamics and mechanisms underpinning symbiont-mediated phenotypes.