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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. InPentalonia nigronervosaandP. caladii, global pests of banana,Wolbachiawas initially hypothesized to function as a co‐obligate nutritional symbiont alongside the traditional obligateBuchnera. However, genomic analyses failed to support this role. Our sampling across numerous populations revealed that more than 80% ofPentaloniaaphids carried an M‐supergroup strain ofWolbachia(wPni). The lack of fixation further supports a facultative status forWolbachia, while high infection frequencies in these entirely asexual aphids strongly suggestWolbachiaconfers net fitness benefits. Finding no correlation betweenWolbachiapresence and food plant use, we challengedWolbachia‐infected aphids with common natural enemies. Bioassays revealed thatWolbachiaconferred significant protection against a specialized fungal pathogen (Pandora neoaphidis) but not against generalist pathogens or parasitoids.Wolbachiaalso improved aphid fitness in the absence of enemy challenge. Thus, we identified the first clear benefits for aphid‐associatedWolbachiaand M‐supergroup strains specifically. Aphid‐Wolbachiasystems provide unique opportunities to merge key models of symbiosis to better understand infection dynamics and mechanisms underpinning symbiont‐mediated phenotypes. 

Abstract Heritable, facultative symbionts are common in arthropods, often functioning in host defence. Despite moderately reduced genomes, facultative symbionts retain evolutionary potential through mobile genetic elements (MGEs). MGEs form the primary basis of strain‐level variation in genome content and architecture, and often correlate with variability in symbiont‐mediated phenotypes. In pea aphids (Acyrthosiphon pisum), strain‐level variation in the type of toxin‐encoding bacteriophages (APSEs) carried by the bacteriumHamiltonella defensacorrelates with strength of defence against parasitoids. However, co‐inheritance creates difficulties for partitioning their relative contributions to aphid defence. Here we identified isolates ofH. defensathat were nearly identical except for APSE type. When holdingH. defensagenotype constant, protection levels corresponded to APSE virulence module type. Results further indicated that APSEs move repeatedly within someH. defensaclades providing a mechanism for rapid evolution in anti‐parasitoid defences. Strain variation inH. defensaalso correlates with the presence of a second symbiontFukatsuia symbiotica. Predictions that nutritional interactions structured this coinfection were not supported by comparative genomics, but bacteriocin‐containing plasmids unique to co‐infecting strains may contribute to their common pairing. In conclusion, strain diversity, and joint capacities for horizontal transfer of MGEs and symbionts, are emergent players in the rapid evolution of arthropods.