A test of specific adaptation to symbiont-conferred host resistance in natural populations of a parasitoid wasp.

Parasitoids are important natural enemies of insects, imposing strong selection for the evolution of resistance. In aphids, the heritable defensive endosymbiont Hamiltonella defensa is a key determinant of resistance, making symbiont-conferred defense a potential target for specific adaptation by parasitoids. We tested this hypothesis in the aphid parasitoid Lysiphlebus fabarum and four of its host species, Aphis fabae fabae, A. hederae, A. urticata, and A. ruborum. The parasitoids show host-associated genetic differentiation indicative of host specialization, and each of these aphid species harbors 1-3 distinct strains of H. defensa, with no shared strains. We introduced eight H. defensa strains from all four aphid species into a common host background (a laboratory strain of symbiont-free A. f. fabae) and then tested the ability of 35 field-collected L. fabarum lines from the same four hosts to parasitize the H. defensa-carrying aphids. The natural origin of symbionts was a key determinant of parasitism success, with strains from A. f. fabae and A. hederae conferring strong protection, and strains from A. urticata and A. ruborum providing virtually no protection. For one strain each from A. f. fabae and A. hederae, we found a signature of specific adaptation by parasitoids, as parasitoids able to overcome their protection mostly came from the same hosts as the symbiont strains. Two other strains were so strongly protective that they permitted very little parasitism independent of where parasitoids came from. While not fully conclusive, these results are consistent with specialized parasitoids adapting to certain defensive symbionts of their host species, supporting the notion of symbiont-mediated coevolution.