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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 While genome sequencing has expanded our knowledge of symbiosis, role assignment within multi-species microbiomes remains challenging due to genomic redundancy and the uncertainties of in vivo impacts. We address such questions, here, for a specialized nitrogen (N) recycling microbiome of turtle ants, describing a new genus and species of gut symbiont—Ischyrobacter davidsoniae (Betaproteobacteria: Burkholderiales: Alcaligenaceae)—and its in vivo physiological context. A re-analysis of amplicon sequencing data, with precisely assigned Ischyrobacter reads, revealed a seemingly ubiquitous distribution across the turtle ant genus Cephalotes, suggesting ≥50 million years since domestication. Through new genome sequencing, we also show that divergent I. davidsoniae lineages are conserved in their uricolytic and urea-generating capacities. With phylogenetically refined definitions of Ischyrobacter and separately domesticated Burkholderiales symbionts, our FISH microscopy revealed a distinct niche for I. davidsoniae, with dense populations at the anterior ileum. Being positioned at the site of host N-waste delivery, in vivo metatranscriptomics and metabolomics further implicate I. davidsoniae within a symbiont-autonomous N-recycling pathway. While encoding much of this pathway, I. davidsoniae expressed only a subset of the requisite steps in mature adult workers, including the penultimate step deriving urea from allantoate. The remaining steps were expressed by other specialized gut symbionts. Collectively, this assemblage converts inosine, made from midgut symbionts, into urea and ammonia in the hindgut. With urea supporting host amino acid budgets and cuticle synthesis, and with the ancient nature of other active N-recyclers discovered here, I. davidsoniae emerges as a central player in a conserved and impactful, multipartite symbiosis. 

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.