Influence of Multiple Infection and Relatedness on Virulence: Disease Dynamics in an Experimental Plant Population and Its Castrating Parasite

Abstract

The level of parasite virulence, i.e., the decrease in host's fitness due to a pathogen, is expected to depend on several parameters, such as the type of the disease (e.g., castrating or host-killing) and the prevalence of multiple infections. Although these parameters have been extensively studied theoretically, few empirical data are available to validate theoretical predictions. Using the anther smut castrating disease on Silene latifolia caused by Microbotryum lychnidis-dioicae, we studied the dynamics of multiple infections and of different components of virulence (host death, non-recovery and percentage of castrated stems) during the entire lifespan of the host in an experimental population. We monitored the number of fungal genotypes within plants and their relatedness across five years, using microsatellite markers, as well as the rates of recovery and host death in the population. The mean relatedness among genotypes within plants remained at a high level throughout the entire host lifespan despite the dynamics of the disease, with recurrent new infections. Recovery was lower for plants with multiple infections compared to plants infected by a single genotype. As expected for castrating parasites, M. lychnidis-dioicae did not increase host mortality. Mortality varied across years but was generally lower for plants that had been diseased the preceding year. This is one of the few studies to have empirically verified theoretical expectations for castrating parasites, and to show particularly i) that castrated hosts live longer, suggesting that parasites can redirect resources normally used in reproduction to increase host lifespan, lengthening their transmission phase, and ii) that multiple infections increase virulence, here in terms of non-recovery and host castration.

Strong phylogeographic co‐structure between the anther‐smut fungus and its white campion host

“…However, another factor may limit pathogen migration and contribute to the relative isolation among geographically‐circumscribed genetic clusters of the anther‐smut fungus. A competitive exclusion of distantly related genotypes by resident genotypes has been shown previously to occur in M. lychnidis‐dioicae (Hood, ; López‐Villavicencio et al ., , ; Buono et al ., ). This relatedness‐dependent competitive exclusion may prevent long‐distance migrants to establish in genetically different clusters.…”

Transmission and temporal dynamics of anther‐smut disease (Microbotryum) on alpine carnation (Dianthus pavonius)

“…These fitness losses are much higher than those reported for anther‐smut on S. latifolia , where complete sterilization was less common (0–60% of all infections; Buono et al . ), and overwinter recovery was high (>60% Biere & Antonovics ). Indeed Rausher () calculated that the total loss in lifetime fitness of S. latifolia as a result of anther‐smut infection approximated the cost of resistance.…”

Multiple infections, relatedness and virulence in the anther‐smut fungus castrating Saponaria plants

“…latifolia plants. The spatial structure found in populations (Giraud, ) would not explain the high relatedness among fungal strains within plants found in experimental inoculations (Buono, Lopez‐Villavicencio, Shykoff, Snirc, & Giraud, ; Koskella et al., ; López‐Villavicencio et al., ) but could still play a role in nature in increasing further relatedness within plants (Lopez‐Villavicencio et al., ).…”

“…Virulence was found to be higher for multiply infected plants than for singly infected ones, with more spores produced (and thus likely more host resource uptake by the pathogen), lower recovery probability and greater castration (Buono et al., ; Hood, ; López‐Villavicencio et al., ). However, higher castration rates in multiple infections were mitigated by greater relatedness (Buono et al., ; López‐Villavicencio et al., ). This indicated that the fungus behaved differently when competing with a close versus a distant relative within the same host plant.…”