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 × 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 × G × 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 × 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 × 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 × G × 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.
Highlights
Whether the encounter between a host and a parasite leads to infection or not is often determined by the distinct combination of their respective genotypes
While the initial number of nymphs exposed to the wasps differed between plants (Beta 15.6 ± 7.2 SD, Chenopodium 13.8 ± 6.0, Vicia: 17.3 ± 6.7), we did not include this value in the final model, since it had no significant effect on parasitism rates when aphid line and host plant were included (Table S1), suggesting that parasitoids were host limited in our assays
Genotype-by-genotype interactions between the parasitoid L. fabarum and the aphid-protective endosymbiont H. defensa have been observed in multiple laboratory experiments (Cayetano and Vorburger, 2015; Schmid et al, 2012) and are assumed to be an important driver of the coevolutionary dynamics in this
Summary
Whether the encounter between a host and a parasite leads to infection or not is often determined by the distinct combination of their respective genotypes. Apart from experimental evidence, modelling approaches support the potential influence of environmental changes on host– parasite coevolution through three-way interactions (Mostowy & Engelstädter, 2011) Taken together, these references underline the importance of incorporating environmental variability into classical G × G interaction studies, prior to generalizing conclusions to more complex natural systems. While the influence of the host plant on insect interactions is striking in many systems, actual studies of G × G × E interactions with host plant as the environmental variable are rare Investigating such interactions requires a study system where specific genotype combinations can be replicated, as is the case for the A. fabae/H. defensa/L. fabarum system. Our results support earlier studies, suggesting that in our model system, coevolution between aphids and parasitoids is largely symbiont- mediated and governed by genotype-specific interactions, which remain remarkably stable across different environments
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