Is there a disease‐free halo at species range limits? The codistribution of anther‐smut disease and its host species

Abstract

While disease is widely recognized as affecting host population size, it has rarely been considered to play a role in determining host range limits. Many diseases may not be able to persist near the range limit if host population density falls below the critical threshold level for pathogen invasion. However, in vector‐ and sexually transmitted diseases, pathogen transmission may be largely independent of host density and theory demonstrates that diseases with frequency‐dependent transmission may persist in small populations near the range limit. Empirical studies of disease at species range limits have lagged behind the theory, and to date, no previous study has tested the hypothesis that vector or sexually transmitted diseases can be maintained at host range limits. We studied the distribution of anther‐smut disease, a sterilizing pollinator‐transmitted disease, on four alpine plant species to determine whether disease was present at the host range limits. We found that host abundance declined towards the elevational range limits, and disease extended to the most extreme elevational range limits in three of the four host species. Maximum likelihood estimation of the magnitude of the disease‐free halo showed that it was small or nonexistent for all host species. Moreover, disease prevalence within populations was often higher nearer the host's range limit than in the range centre and was independent of host density. Synthesis. Our results show that diseases where transmission is frequency‐dependent have the potential to affect host distributions not just in theory, but also in real world populations.

The role of infectious disease in the evolution of females: Evidence from anther‐smut disease on a gynodioecious alpine carnation*

“…These surveys were part of an ongoing project to map host and pathogen distribution with respect to range margins (Bruns et al. ). Populations were surveyed every 50 m in elevation along 13 transects in the Maritime Alps (Fig.…”

“…To determine if there is a positive correlation between disease prevalence and female frequency, we surveyed D. pavonius populations throughout the broader Maritime Alps region. These surveys were part of an ongoing project to map host and pathogen distribution with respect to range margins (Bruns et al 2018). Populations were surveyed every 50 m in elevation along 13 transects in the Maritime Alps (Fig.…”

Anther smut disease caused by Microbotryum on berry campion Silene baccifera: endemic pathogen or host shift?

“…Moreover, a search of two localities in Germany where the disease had been recorded within the past 10 years failed to find the disease, suggesting the disease is not self‐sustaining. Nor was the disease ever found on S. baccifera in the southern Piemonte region of Italy which was a focal area for the present study of the distribution of anther smut and where the disease has previously been found on over 20 other species (Bruns et al ., ).…”

Sympatry and interference of divergent Microbotryum pathogen species

“…For example, the typical proportions of disease within host populations are between 0.10 and 0.30 for S. latifolia (Antonovics, ), ca. 0.30 for S. vuglaris in upper elevations (Abbate & Antonovics, ), or even >0.50 for Dianthus furcatus or Dianthus pavonius (Bruns et al, ). Therefore, the potential for frequent contact between Microbotryum species on separate host species is high.…”

“…Anther‐smut disease, caused by fungi in the genus Microbotryum , is one of the most studied host–pathogen associations in natural systems (Figure ). This disease has been used as a model for pathogen speciation, pollinator‐mediated dispersal, multiple infection, biological invasion, and competition (Abbate & Antonovics, ; Bruns, Antonovics, & Hood, ; Fontaine, Gladieux, Hood, & Giraud, ; Giraud, Gladieux, & Gavrilets, ; Gold, Giraud, & Hood, ; Kemler et al, ; Le Gac, Hood, Fournier, & Giraud, ; Vercken et al, ). Research has shown that the fungi formerly grouped under the Microbotryum violaceum epithet represent a large species complex, consisting of many independent lineages, each specific (i.e., endemic) to only one or a very small number of host species (Kemler et al, ; Le Gac et al, ; Lutz et al, ; Piątek, Lutz, & Kemler, ; de Vienne, Hood, & Giraud, ).…”