Symbiont-mediated protection varies with wasp genotype in the Drosophila melanogaster-Spiroplasma interaction

The ability of an insect to survive attack by natural enemies can be modulated by the presence of defensive symbionts. Study of aphid-symbiont-enemy interactions has indicated that protection may depend on the interplay of symbiont, host and attacking parasite genotypes. However, the importance of these interactions are poorly understood outside of this model system. Here, we study interactions within a Drosophila model system, in which Spiroplasma protect their host against parasitoid wasps and nematode attack. We examine whether the strength of protection conferred by Spiroplasma to its host, Drosophila melanogaster varies with strain of attacking Leptopilina heterotoma wasp. We perform this analysis in the presence and absence of ethanol, an environmental factor that also impacts the outcome of parasitism. We observed that Spiroplasma killed all strains of wasp. However, the protection produced by Spiroplasma following wasp attack depended on attacking wasp strain. A composite measure of protection, including both the chance of the fly surviving attack and the relative fecundity/fertility of the survivors, varied from a <4% positive effect of the symbiont following attack of the fly host by the Lh14 strain of wasp to 21% for the Lh-Fr strain in the absence of ethanol. Variation in protection provided was not associated with differences in the oviposition behaviour of the different wasp strains. We observed that environmental ethanol altered the pattern of protection against wasp strains, with Spiroplasma being most protective against the Lh-Mad wasp strain in the presence of ethanol. These data indicate that the dynamics of the Spiroplasma-Drosophila-wasp tripartite interaction depend upon the genetic diversity within the attacking wasp population, and that prediction of symbiont dynamics in natural systems will thus require analysis across natural enemy genotypes and levels of environmental ethanol.Impact SummaryNatural enemies – predators, parasites and pathogens – are a common source of mortality in animals, and this has driven the evolution of an array of mechanisms for preventing and surviving attack. Recently it has been observed that microbial symbionts form a component of insect defence against attack by pathogens and parasites. Whether an individual fly dies or lives following wasp attack, for instance, is partly determined by the presence or absence of Spiroplasma bacteria in the fly blood. The evolutionary biology of these ‘protective symbioses’ will in part depend on the specificity of defence – does Spiroplasma defend against all wasp strains equally, or does defence vary between wasp strains? We investigated this in the model insect, Drosophila melanogaster. We observed that the defensive symbiont killed all strains of wasps tested. However, the capacity of the symbiont to rescue the fly varied – Spiroplasma rescued the flies for some attacking wasp strains, but not for others. These data mean that the degree to which symbionts protect their host will depend on the wasp strains circulating in nature. Our results are important in terms of understanding the forces that promote symbiont mediated protection and understanding the origins of diversity of circulating wasp strains. Further, these data indicate enemy diversity and their interaction with protective symbionts should be included in evaluation of the efficiency of biocontrol programmes involving natural enemies.