Differential Tolerance to Direct and Indirect Density-Dependent Costs of Viral Infection in Arabidopsis thaliana

Population density and costs of parasite infection may condition the capacity of organisms to grow, survive and reproduce, i.e. their competitive ability. In host–parasite systems there are different competitive interactions: among uninfected hosts, among infected hosts, and between uninfected and infected hosts. Consequently, parasite infection results in a direct cost, due to parasitism itself, and in an indirect cost, due to modification of the competitive ability of the infected host. Theory predicts that host fitness reduction will be higher under the combined effects of costs of parasitism and competition than under each factor separately. However, experimental support for this prediction is scarce, and derives mostly from animal–parasite systems. We have analysed the interaction between parasite infection and plant density using the plant-parasite system of Arabidopsis thaliana and the generalist virus Cucumber mosaic virus (CMV). Plants of three wild genotypes grown at different densities were infected by CMV at various prevalences, and the effects of infection on plant growth and reproduction were quantified. Results demonstrate that the combined effects of host density and parasite infection may result either in a reduction or in an increase of the competitive ability of the host. The two genotypes investing a higher proportion of resources to reproduction showed tolerance to the direct cost of infection, while the genotype investing a higher proportion of resources to growth showed tolerance to the indirect cost of infection. Our findings show that the outcome of the interaction between host density and parasitism depends on the host genotype, which determines the plasticity of life-history traits and consequently, the host capacity to develop different tolerance mechanisms to the direct or indirect costs of parasitism. These results indicate the high relevance of host density and parasitism in determining the competitive ability of a plant, and stress the need to simultaneously consider both factors to understand the selective pressures that drive host–parasite co-evolution.Author Summary: Parasites are a potent selective force, as they reduce the fitness of their hosts through a direct cost of infection, due to parasitism itself, and an indirect cost, due to modification of the competitive ability of the infected host. Theory predicts that fitness reduction will be higher under the combined effects of costs of parasitism and host population density than under each factor separately, but experimental support for this prediction is scarce, and derives mostly from animal–parasite systems. We have analysed the combined effects of host density and costs of infection using the plant virus Cucumber mosaic virus and its host plant Arabidopsis thaliana. The interaction between these factors may result in a reduction or an increase of plant competitive ability, depending on host genotype, which determines the plasticity of life-history traits and consequently, different tolerance mechanisms to the combined effects of plant density and direct or indirect cost of parasitism. These tolerance mechanisms are associated with resource reallocation. Our results stress the relevance of the interaction between host and parasite traits in determining the outcome of infection contributing to understand the selective pressures that drive host–parasite co-evolution.