Effects of parasitism on aphid nutritional and protective symbioses

Insects often carry heritable symbionts that negotiate interactions with food plants or natural enemies. All pea aphids, Acyrthosiphon pisum, require infection with the nutritional symbiont Buchnera, and many are also infected with Hamiltonella, which protects against the parasitoid Aphidius ervi. Hamiltonella-based protection requires bacteriophages called APSEs with protection levels varying by strain and associated APSE. Endoparasitoids, including A. ervi, may benefit from protecting the nutritional symbiosis and suppressing the protective one, while the aphid and its heritable symbionts have aligned interests when attacked by the wasp. We investigated the effects of parasitism on the abundance of aphid nutritional and protective symbionts. First, we determined strength of protection associated with multiple symbiont strains and aphid genotypes as these likely impact symbiont responses. Unexpectedly, some A. pisum genotypes cured of facultative symbionts were resistant to parasitism and resistant aphid lines carried Hamiltonella strains that conferred no additional protection. Susceptible aphid clones carried protective strains. qPCR estimates show that parasitism significantly influenced both Buchnera and Hamiltonella titres, with multiple factors contributing to variation. In susceptible lines, parasitism led to increases in Buchnera near the time of larval wasp emergence consistent with parasite manipulation, but effects were variable in resistant lines. Parasitism also resulted in increases in APSE and subsequent decreases in Hamiltonella, and we discuss how this response may relate to the protective phenotype. In summary, we show that parasitism alters the within-host ecology of both nutritional and protective symbioses with effects likely significant for all players in this antagonistic interaction.