Dynamics of a bacteriophage required in a heritable defensive symbiosis

Facultative bacteria associated with insects can provide ecologically important phenotypes, including defense from natural enemies.  A bacteriophage, APSE, provides an effector molecule to a bacterial symbiont, Hamiltonella defensa, which in turn provides the bacterium’s host, the pea aphid, Acyrthosiphon pisum, with protection from a parasitoid wasp, Aphidius ervi.  When not infected with bacteriophage APSE, H. defensa provides no known benefits to its aphid host, and has a deleterious effect on aphid fitness.  Several variants of APSE have previously been identified in A. pisum, and more have been found in other aphid species.  Each known phage variant contains one of three toxins in a variable cassette region: this is putatively the source of anti-parasitoid protection.  In North American pea aphids, two APSE variants have been identified.  APSE-2 contains a cytolethal distending toxin homolog, and provides aphids with a 30-40% post-parasitism survival rate.  APSE-3, which contains a putative YD-repeat toxin, provides near-total parasitoid resistance.  Despite the far greater protection provided by APSE-3, APSE-2 is prevalent in many field populations.  In lab-held lines, the more protective APSE-3s have been lost from aphid populations held long-term, leaving aphids with non-protective H. defensa infections; no loss of APSE-2 has ever been reported.  This suggests potential population-level trade-offs between stability and strength of the defensive phenotype.  We have characterized structural genes and the variable toxin region in geographically diverse APSEs to improve our understanding of phage-level variation in this tripartite defensive symbiosis.