Coevolution between hosts and parasites may promote the maintenance of genetic variation in both antagonists by negative frequency-dependence if the host-parasite interaction is genotype-specific. Here we tested for specificity in the interaction between parasitoids (Lysiphlebus fabarum) and aphid hosts (Aphis fabae) that are protected by a heritable defensive endosymbiont, the c-proteobacterium Hamiltonella defensa. Previous studies reported a lack of genotype specificity between unprotected aphids and parasitoids, but suggested that symbiont-conferred resistance might exhibit a higher degree of specificity. Indeed, in addition to ample variation in host resistance as well as parasitoid infectivity, we found a strong aphid clone-by-parasitoid line interaction on the rates of successful parasitism. This genotype specificity appears to be mediated by H. defensa, highlighting the important role that endosymbionts can play in host-parasite coevolution.

Host-parasitoid interactions may lead to strong reciprocal selection for traits involved in host defense

BackgroundInsect parasitoids are under strong selection to overcome their hosts’ defences. In aphids, resistance to parasitoids is largely determined by the presence or absence of protective endosymbionts such as Hamiltonella defensa. Hence, parasitoids may become locally adapted to the prevalence of this endosymbiont in their host populations. To address this, we collected isofemale lines of the aphid parasitoid Lysiphlebus fabarum from 17 sites in Switzerland and France, at which we also estimated the frequency of infection with H. defensa as well as other bacterial endosymbionts in five important aphid host species. The parasitoids’ ability to overcome H. defensa-mediated resistance was then quantified by estimating their parasitism success on a single aphid clone (Aphis fabae fabae) that was either uninfected or experimentally infected with one of three different isolates of H. defensa.ResultsThe five aphid species (Aphis fabae fabae, A. f. cirsiiacanthoides, A. hederae, A. ruborum, A. urticata) differed strongly in the relative frequencies of infection with different bacterial endosymbionts, but there was also geographic variation in symbiont prevalence. Specifically, the frequency of infection with H. defensa ranged from 22 to 47 % when averaged across species. Parasitoids from sites with a high prevalence of H. defensa tended to be more infective on aphids possessing H. defensa, but this relationship was not significant, thus providing no conclusive evidence that L. fabarum is locally adapted to the occurrence of H. defensa. On the other hand, we observed a strong interaction between parasitoid line and H. defensa isolate on parasitism success, indicative of a high specificity of symbiont-conferred resistance.ConclusionsThis study is the first, to our knowledge, to test for local adaptation of parasitoids to the frequency of defensive symbionts in their hosts. While it yielded useful information on the occurrence of facultative endosymbionts in several important host species of L. fabarum, it provided no clear evidence that parasitoids from sites with a high prevalence of H. defensa are better able to overcome H. defensa-conferred resistance. The strong genetic specificity in their interaction suggests that it may be more important for parasitoids to adapt to the particular strains of H. defensa in their host populations than to the general prevalence of this symbiont, and it highlights the important role symbionts can play in mediating host-parasitoid coevolution.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-016-0811-0) contains supplementary material, which is available to authorized users.