The microbial symbionts of eukaryotes influence disease resistance in many host-parasite systems. Symbionts show substantial variation in both genotype and phenotype, but it is unclear how natural selection maintains this variation. It is also unknown whether variable symbiont genotypes show specificity with the genotypes of hosts or parasites in natural populations. Genotype by genotype interactions are a necessary condition for coevolution between interacting species. Uncovering the patterns of genetic specificity among hosts, symbionts, and parasites is therefore critical for determining the role that symbionts play in host-parasite coevolution. Here, we show that the strength of protection conferred against a fungal pathogen by a vertically transmitted symbiont of an aphid is influenced by both host-symbiont and symbiont-pathogen genotype by genotype interactions. Further, we show that certain symbiont phylogenetic clades have evolved to provide stronger protection against particular pathogen genotypes. However, we found no evidence of reciprocal adaptation of co-occurring host and symbiont lineages. Our results suggest that genetic variation among symbiont strains may be maintained by antagonistic coevolution with their host and/or their host's parasites.

Department of Zoology University of Oxford Oxford OX1 3PS United Kingdom

Department of Zoology University of Oxford Oxford OX1 3PS United Kingdom Current Address Department of Biology University of Rochester Rochester NY 14627 USA

Department of Zoology University of Oxford Oxford OX1 3PS United Kingdom Current Address Institute of Entomology Biology Centre CAS Branisovska 31 Ceske Budejovice 37005 Czech Republic