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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 Insects often harbour heritable symbionts that provide defence against specialized natural enemies, yet little is known about symbiont protection when hosts face simultaneous threats. In pea aphids (Acyrthosiphon pisum), the facultative endosymbiontHamiltonella defensaconfers protection against the parasitoid,Aphidius ervi, andRegiella insecticolaprotects against aphid‐specific fungal pathogens, includingPandora neoaphidis. Here, we investigated whether these two common aphid symbionts protect against a specialized virusA. pisum virus(APV), and whether their antifungal and antiparasitoid services are impacted by APV infection. We found that APV imposed large fitness costs on symbiont‐free aphids and these costs were elevated in aphids also housingH. defensa. In contrast, APV titres were significantly reduced and costs to APV infection were largely eliminated in aphids withR. insecticola. To our knowledge,R. insecticolais the first aphid symbiont shown to protect against a viral pathogen, and only the second arthropod symbiont reported to do so. In contrast, APV infection did not impact the protective services of eitherR. insecticolaorH. defensa. To better understand APV biology, we produced five genomes and examined transmission routes. We found that moderate rates of vertical transmission, combined with horizontal transfer through food plants, were the major route of APV spread, although lateral transfer by parasitoids also occurred. Transmission was unaffected by facultative symbionts. In summary, the presence and species identity of facultative symbionts resulted in highly divergent outcomes for aphids infected with APV, while not impacting defensive services that target other enemies. These findings add to the diverse phenotypes conferred by aphid symbionts, and to the growing body of work highlighting extensive variation in symbiont‐mediated interactions. 

Abstract BackgroundMost phages infect free-living bacteria but a few have been identified that infect heritable symbionts of insects or other eukaryotes. Heritable symbionts are usually specialized and isolated from other bacteria with little known about the origins of associated phages.Hamiltonella defensais a heritable bacterial symbiont of aphids that is usually infected by a tailed, double-stranded DNA phage named APSE. MethodsWe conducted comparative genomic and phylogenetic studies to determine how APSE is related to other phages and prophages. ResultsEach APSE genome was organized into four modules and two predicted functional units. Gene content and order were near-fully conserved in modules 1 and 2, which encode predicted DNA metabolism genes, and module 4, which encodes predicted virion assembly genes. Gene content of module 3, which contains predicted toxin, holin and lysozyme genes differed among haplotypes. Comparisons to other sequenced phages suggested APSE genomes are mosaics with modules 1 and 2 sharing similarities withBordetella-Bcep-Xylostella fastidiosa-like podoviruses, module 4 sharing similarities with P22-like podoviruses, and module 3 sharing no similarities with known phages. Comparisons to other sequenced bacterial genomes identified APSE-like elements in other heritable insect symbionts (Arsenophonusspp.) and enteric bacteria in the familyMorganellaceae. ConclusionsAPSEs are most closely related to phage elements in the genusArsenophonusand other bacteria in theMorganellaceae. 

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. 

Abstract Most insects harbour influential, yet non‐essential heritable microbes in their hemocoel. Communities of these symbionts exhibit low diversity. But their frequent multi‐species nature raises intriguing questions on roles for symbiont–symbiont synergies in host adaptation, and on the stability of the symbiont communities, themselves. In this study, we build on knowledge of species‐defined symbiont community structure across US populations of the pea aphid,Acyrthosiphon pisum. Through extensive symbiont genotyping, we show that pea aphids' microbiomes can be more precisely defined at the symbiont strain level, with strain variability shaping five out of nine previously reported co‐infection trends. Field data provide a mixture of evidence for synergistic fitness effects and symbiont hitchhiking, revealing causes and consequences of these co‐infection trends. To test whether within‐host metabolic interactions predict common versus rare strain‐defined communities, we leveraged the high relatedness of our dominant, community‐defined symbiont strains vs. 12 pea aphid‐derived Gammaproteobacteria with sequenced genomes. Genomic inference, using metabolic complementarity indices, revealed high potential for cooperation among one pair of symbionts—Serratia symbioticaandRickettsiella viridis. Applying the expansion network algorithm, through additional use of pea aphid and obligateBuchnerasymbiont genomes,SerratiaandRickettsiellaemerged as the only symbiont community requiring both parties to expand holobiont metabolism. Through their joint expansion of the biotin biosynthesis pathway, these symbionts may span missing gaps, creating a multi‐party mutualism within their nutrient‐limited, phloem‐feeding hosts. Recent, complementary gene inactivation, within the biotin pathways ofSerratiaandRickettsiella, raises further questions on the origins of mutualisms and host–symbiont interdependencies.