Strong genotype-by-genotype interactions between aphid-defensive symbionts and parasitoids persist across different biotic environments

Abstract

The dynamics of coevolution between hosts and parasites are influenced by their genetic interactions. Highly specific interactions, where the outcome of an infection depends on the precise combination of host and parasite genotypes (G x G interactions), have the potential to maintain genetic variation by inducing negative frequency-dependent selection. The importance of this effect also rests on whether such interactions are consistent across different environments or modified by environmental variation (G x G x E interaction). In the black bean aphid, Aphis fabae, resistance to its parasitoid Lysiphlebus fabarum is largely determined by the possession of a heritable bacterial endosymbiont, Hamiltonella defensa, with strong G x G interactions between H. defensa and L. fabarum. A key environmental factor in this system is the host plant on which the aphid feeds. Here, we exposed genetically identical aphids harbouring three different strains of H. defensa to three asexual genotypes of L. fabarum and measured parasitism success on three common host plants of A. fabae, namely Vicia faba, Chenopodium album and Beta vulgaris. As expected, we observed the pervasive G x G interaction between H. defensa and L. fabarum, but despite strong main effects of the host plants on average rates of parasitism, this interaction was not altered significantly by the host plant environment (no G x G x E interaction). The symbiont-conferred specificity of resistance is thus likely to mediate the coevolution of A. fabae and L. fabarum, even when played out across diverse host plants of the aphid.