Multiple Infections by the Anther Smut Pathogen Are Frequent and Involve Related Strains

Abstract

Population models of host–parasite interactions predict that when different parasite genotypes compete within a host for limited resources, those that exploit the host faster will be selected, leading to an increase in parasite virulence. When parasites sharing a host are related, however, kin selection should lead to more cooperative host exploitation that may involve slower rates of parasite reproduction. Despite their potential importance, studies that assess the prevalence of multiple genotype infections in natural populations remain rare, and studies quantifying the relatedness of parasites occurring together as natural multiple infections are particularly scarce. We investigated multiple infections in natural populations of the systemic fungal plant parasite Microbotryum violaceum, the anther smut of Caryophyllaceae, on its host, Silene latifolia. We found that multiple infections can be extremely frequent, with different fungal genotypes found in different stems of single plants. Multiple infections involved parasite genotypes more closely related than would be expected based upon their genetic diversity or due to spatial substructuring within the parasite populations. Together with previous sequential inoculation experiments, our results suggest that M. violaceum actively excludes divergent competitors while tolerating closely related genotypes. Such an exclusion mechanism might explain why multiple infections were less frequent in populations with the highest genetic diversity, which is at odds with intuitive expectations. Thus, these results demonstrate that genetic diversity can influence the prevalence of multiple infections in nature, which will have important consequences for their optimal levels of virulence. Measuring the occurrence of multiple infections and the relatedness among parasites within hosts in natural populations may be important for understanding the evolutionary dynamics of disease, the consequences of vaccine use, and forces driving the population genetic structure of parasites. Infections of one host individual by multiple genotypes of a parasite occur in many natural systems and have major consequences on the evolution of disease severity. Under such multiple infections, the parasite genotypes compete for the host's limited resources, and the faster exploiters will be advantaged over more prudent genotypes, selecting for parasites that cause greater damage and mortality, i.e., having higher virulence. However, when different parasite genotypes within a host are related, a reduction of competitive conflicts between them should lead to more cooperative host exploitation, and thus to lower severity of disease. The occurrence of multiple infections and the relatedness among parasite genotypes within hosts therefore are important to our understanding of diseases, but studies that assess these parameters in nature remain scarce. We investigated multiple infections by the fungus Microbotryum violaceum, responsible for the anther smut disease on the plant Silene latifolia. Multiple infections in natural populations were extremely frequent, with many different genotypes within single host plants. The fungal genotypes found in the different stems of single plants were, however, more related than expected by chance. Together with previous artificial inoculation experiments, these results suggest that M. violaceum actively excludes dissimilar genotypes while tolerating closely related competitors.