Abstract
The impact of infectious diseases in natural ecosystems is strongly influenced by the degree of pathogen specialization and by the local assemblies of potential host species. This study investigated anther‐smut disease, caused by fungi in the genus Microbotryum, among natural populations of plants in the Caryophyllaceae. A broad geographic survey focused on sites of the disease on multiple host species in sympatry. Analysis of molecular identities for the pathogens revealed that sympatric disease was most often due to co‐occurrence of distinct, host‐specific anther‐smut fungi, rather than localized cross‐species disease transmission. Flowers from sympatric populations showed that the Microbotryum spores were frequently moved between host species. Experimental inoculations to simulate cross‐species exposure to the pathogens in these plant communities showed that the anther‐smut pathogen was less able to cause disease on its regular host when following exposure of the plants to incompatible pathogens from another host species. These results indicate that multi‐host/multi‐pathogen communities are common in this system and they involve a previously hidden mechanism of interference between Microbotryum fungi, which likely affects both pathogen and host distributions.
Highlights
Infectious diseases have a major influence on natural communities, and both positive and negative effects on biodiversity have been re‐ corded (Benítez, Hersh, Vilgalys, & Clark, 2013; Johnson, Roode, & Fenton, 2015; Mordecai, 2011; Seabloom et al, 2015; Young, Parker, Gilbert, Sofiea Guerra, & Nunn, 2017)
The exceptions to this trend of disease on two host species being the result of sympatry between host‐specific Microbotryum lineages were several samples collected from S. vulgaris that resulted from cross‐species disease transmission
In a broadly distributed multi‐host/multi‐pathogen system, this study revealed the co‐occurrence of anther‐smut diseases on sym‐ patric host species and significant pathogen interactions that may impact disease and host distributions in natural populations
Summary
Anther‐smut disease, caused by fungi in the genus Microbotryum, is one of the most studied host–pathogen associations in natural sys‐ tems (Figure 1) This disease has been used as a model for pathogen speciation, pollinator‐mediated dispersal, multiple infection, biolog‐ ical invasion, and competition (Abbate & Antonovics, 2014; Bruns, Antonovics, & Hood, 2018; Fontaine, Gladieux, Hood, & Giraud, 2013; Giraud, Gladieux, & Gavrilets, 2010; Gold, Giraud, & Hood, 2009; Kemler et al, 2013; Le Gac, Hood, Fournier, & Giraud, 2007; Vercken et al, 2010). This study helps to reveal a complex source of interactions between relatively specialized pathogens on multiple host species and their potential impact on the occurrence of disease in natural populations
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