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.
Highlights
It is generally considered that a parasite’s optimal level of virulence, i.e., the decrease in host fitness induced by disease that maximizes parasite transmission, depends on several factors, such as mode of transmission, dormancy ability, host availability, and the frequency of occurrence within single hosts of multiple infections by different parasite genotypes [1,2]
The occurrence of multiple infections is theoretically predicted to be an important determinant of virulence evolution because when different parasites compete for limited resources within a single host, more rapid exploitation strategies should win over prudent strategies, selecting for parasites that cause greater damage and mortality [2]
We investigated multiple infections by the fungus Microbotryum violaceum, responsible for the anther smut disease on the plant Silene latifolia
Summary
It is generally considered that a parasite’s optimal level of virulence, i.e., the decrease in host fitness induced by disease that maximizes parasite transmission, depends on several factors, such as mode of transmission, dormancy ability, host availability, and the frequency of occurrence within single hosts of multiple infections by different parasite genotypes [1,2]. The occurrence of multiple infections is theoretically predicted to be an important determinant of virulence evolution because when different parasites compete for limited resources within a single host, more rapid exploitation strategies should win over prudent strategies, selecting for parasites that cause greater damage and mortality [2]. When related parasites share a host, kin selection should reduce between-genotype competition, resulting in shared host exploitation that is more cooperative [3]. This predicted consequence of kin selection among parasites has been supported by some empirical data [4,5,6,7]. Our understanding of parasite virulence evolution would benefit from measures of the frequency of multiple infections and the relatedness among parasite genotypes within hosts in natural populations.
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