Genetic variation changes the interactions between the parasitic plant-ecosystem engineer Rhinanthus and its hosts

<jats:p> Within-species genetic variation is a potent factor influencing between-species interactions and community-level structure. Species of the hemi-parasitic plant genus <jats:italic>Rhinanthus</jats:italic> act as ecosystem engineers, significantly altering above- and below-ground community structure in grasslands. Here, we show the importance of genotypic variation within a single host species (barley— <jats:italic>Hordeum vulgare</jats:italic> ), and population-level variation among two species of parasite ( <jats:italic>Rhinanthus minor</jats:italic> and <jats:italic>Rhinanthus angustifolius</jats:italic> ) on the outcome of parasite infection for both partners. We measured host fitness (number of seeds) and calculated parasite virulence as the difference in seed set between infected and uninfected hosts (the inverse of host tolerance). Virulence was determined by genetic variation within the host species and among the parasite species, but <jats:italic>R. angustifolius</jats:italic> was consistently more virulent than <jats:italic>R. minor</jats:italic> . The most tolerant host had the lowest inherent fitness and did not gain a fitness advantage over other infected hosts. We measured parasite size as a proxy for transmission ability (ability to infect further hosts) and host resistance. Parasite size depended on the specific combination of host genotype, parasite species and parasite population, and no species was consistently larger. We demonstrate that the outcome of infection by <jats:italic>Rhinanthus</jats:italic> depends not only on the host species, but also on the underlying genetics of both host and parasite. Thus, genetic variations within host and parasite are probably essential components of the ecosystem-altering effects of <jats:italic>Rhinanthus</jats:italic> . </jats:p>