Field surveys of APSE, a pea aphid (Acyrthosiphon pisum) defensive mutualist-associated bacteriophage

Symbiotic bacteria are responsible for host expansion, phenotypic diversity, and speciation events in insects. While obligate symbiosis ultimately produces bacterial genomes without mobile genetic elements, facultative and recently derived symbionts may retain mobile genetic elements, including bacteriophages. Hamiltonella defensa, a facultatively symbiotic bacterium found in pea aphids (Acyrthosiphon pisum), increases the likelihood that its host aphid will survive and reproduce after being attacked by the parasitoid wasp Aphidius ervi. H. defensa is itself infected by a bacteriophage called APSE, which is vital to the symbiosis: when not infected by bacteriophage APSE, H. defensa provides no protection from parasitism, and has a deleterious effect on aphid fecundity.  Two APSE variants have been identified in North American pea aphids.  The first, APSE-2 contains a cytolethal distending toxin homolog (cdtB), and provides aphids with a 30-40% post-parasitism survival rate; the other, APSE-3, contains a putative YD-repeat toxin and provides near-total parasitoid resistance.  Despite the far greater protection provided by APSE-3, more than eighty percent of H. defensa-infected field lines collected in the last two years contain the cdtB-bearing APSE-2 strain; the remainder do not amplify any known toxin. The prevalence of the moderately-protective strain may be due to population-level trade-offs between the stability and the strength of the defensive phenotype.  Relative to APSE-2s, APSE-3s are lost more frequently from aphid clonal lines and integrated into H. defensa genomes at lower rates.  Additionally, we identified a novel cdtB allele, which persists at moderate rates despite offering no anti-wasp protection.