Virulence and community dynamics of fungal species with vertical and horizontal transmission on a plant with multiple infections

The virulence evolution of multiple infections of parasites from the same species has been modeled widely in evolution theory. However, experimental studies on this topic remain scarce, particularly regarding multiple infections by different parasite species. Here, we characterized the virulence and community dynamics of fungal pathogens on the invasive plant Ageratina adenophora to verify the predictions made by the model. We observed that A. adenophora was highly susceptible to diverse foliar pathogens with mixed vertical and horizontal transmission within leaf spots. The transmission mode mainly determined the pathogen community structure at the leaf spot level. Over time, the pathogen community within a leaf spot showed decreased Shannon diversity; moreover, the vertically transmitted pathogens exhibited decreased virulence to the host A. adenophora, but the horizontally transmitted pathogens exhibited increased virulence to the host. Our results demonstrate that the predictions of classical models for the virulence evolution of multiple infections are still valid in a complex realistic environment and highlight the impact of transmission mode on disease epidemics of foliar fungal pathogens. We also propose that seedborne fungi play an important role in structuring the foliar pathogen community from multiple infections within a leaf spot. Author summary A growing number of examples indicate that many plant diseases are caused by multiple taxa of microbes. Therefore, how virulence evolves in the context of multiple infections by different species with both vertical and horizontal transmission modes represents an important area of pathogen ecology and evolution, but there is a lack of experimental study. Here, we employ a naturally occurring host-parasite system, the invasive plant Ageratina adenophora and its foliar pathogens, to verify that theoretical predictions of classical models for virulence evolution are still valid in a complex realistic environment, i.e., the transmission mode determines the dynamics of the virulence and pathogen community under multiple infections. Moreover, we propose that seedborne fungi are important in structuring the foliar pathogen community consisting of multiple infections within a leaf spot. Our findings provide valuable information for understanding how multiple infections affect the key components, i.e., the virulence evolution and pathogen community dynamics, of host-pathogen interactions in the field.

Automated summary

This study analyzed fungal pathogens on the invasive plant Ageratina adenophora to verify predictions made by models regarding virulence evolution in multiple infections. It was found that the transmission mode determined the dynamics of virulence and pathogen community under multiple infections, highlighting the impact of transmission mode on disease epidemics. Additionally, the role of seedborne fungi in shaping the pathogen community from multiple infections within a leaf spot was proposed.