Phage loss and the breakdown of a defensive symbiosis in aphids

Terrestrial arthropods are often infected with heritable bacterial symbionts which may themselves be infected by bacteriophages. However, what role, if any, bacteriophages play in the regulation and maintenance of insect-bacteria symbioses is largely unknown. Infection of the aphid Acyrthosiphon pisum by the bacterial symbiont Hamiltonella defensa confers protection against parasitoid wasps, but only when H. defensa is itself infected by the phage APSE. Here we use a controlled genetic background and correlation-based assays to show that loss of APSE produces up to seven- fold increases in the intra-aphid abundance of H. defensa. APSE loss is also associated with severe deleterious effects on aphid fitness: aphids infected with H. defensa lacking APSE have a significantly delayed onset of reproduction, lower weight at adulthood, and half as many total offspring as aphids infected with phage-harbouring H. defensa, indicating that phage loss can rapidly lead to the breakdown of the defen...