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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., (© 2024 The Author(s). Environmental Microbiology published by John Wiley & Sons Ltd.)

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 bacterium Hamiltonella defensa correlates with strength of defence against parasitoids. However, co-inheritance creates difficulties for partitioning their relative contributions to aphid defence. Here we identified isolates of H. defensa that were nearly identical except for APSE type. When holding H. defensa genotype constant, protection levels corresponded to APSE virulence module type. Results further indicated that APSEs move repeatedly within some H. defensa clades providing a mechanism for rapid evolution in anti-parasitoid defences. Strain variation in H. defensa also correlates with the presence of a second symbiont Fukatsuia 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., (© 2023 The Authors. Environmental Microbiology published by Applied Microbiology International and John Wiley & Sons Ltd.)

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 endosymbiont Hamiltonella defensa confers protection against the parasitoid, Aphidius ervi, and Regiella insecticola protects against aphid-specific fungal pathogens, including Pandora neoaphidis. Here, we investigated whether these two common aphid symbionts protect against a specialized virus A. 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 housing H. defensa. In contrast, APV titres were significantly reduced and costs to APV infection were largely eliminated in aphids with R. insecticola. To our knowledge, R. insecticola is 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 either R. insecticola or H. 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., (© 2022 The Authors. Molecular Ecology published by John Wiley & Sons Ltd.)

Ecologically relevant symbioses are widespread in terrestrial arthropods but based on recent findings these specialized interactions are likely to be especially vulnerable to climate warming. Importantly, empirical data and climate models indicate that warming is occurring asynchronously, with night-time temperatures increasing faster than daytime temperatures. Daytime (DTW) and night-time warming (NTW) may impact ectothermic animals and their interactions differently as DTW results in greater daily temperature variation and moves organisms nearer to their thermal limits, while NTW avoids thermal limits and may relieve constraints of cooler night-time temperatures; a nuance that has largely been ignored in the literature. In laboratory experiments, we investigated how the timing of warming influences a widespread defensive mutualism involving the pea aphid Acyrthosiphon pisum, and its heritable symbiont, Hamiltonella defensa, which protects against an important natural enemy, the parasitic wasp Aphidius ervi. Three aphid sublines were experimentally created from single aphid genotype susceptible to A. ervi: one line infected with a highly protective H. defensa strain, one infected with a moderately protective strain and one without any facultative symbiont. We examined aphid fitness in the presence and absence of parasitoids and when exposed to an average 2.5°C increase occurring across three warming scenarios (night-time vs. daytime vs. uniform) relative to no-warming controls. An increase of 2.5°C, as predicted to occur by the IPCC before 2100, was sufficient to disable the aphid defensive mutualism regardless of the timing of warming; a surprising result given that the daily maxima for control and NTW scenarios were identical. We also found that warming negatively impacted (a) symbiont-mediated interactions between host and parasitoid more than symbiont-free ones; (b) species interactions (host-parasitoid) more than each participant independently and (c) aphids more than parasitoids even though higher trophic levels are generally predicted to be more affected by warming. Here we show that 2.5°C warming, regardless of timing, negatively impacted a common microbe-mediated defensive mutualism. While this was a laboratory-based study, results suggest that temperature increases predicted in the near-term may disrupt the many ecological symbioses present in terrestrial ecosystems., (© 2020 British Ecological Society.)