Elevational disease distribution in a natural plant–pathogen system: insights from changes across host populations and climate

Abstract

Understanding the factors determining the distribution of parasites and pathogens in natural systems is essential for making predictions about the spread of emerging infectious disease. Here, we report the distribution of the fungal anther‐smut disease, caused by Microbotryum spp., on populations of the European wildflower Silene vulgaris over a range of elevations. A survey of several geographically distinct mountains in the southern French alps found that anther‐smut disease was restricted to high elevations, rarely observed below 1300 m despite availability of hosts below this elevation. Anther smut causes host‐sterility, and is recognized as a model system for natural host–pathogen interactions, sharing common features with vector‐borne and sexually‐transmitted disease in animals. In such systems, many biotic and abiotic factors likely to change over ecological gradients can influence disease epidemiology, including host spatial structure, pathogen infectivity, host resistance, and vector behavior. Here, we tested whether host population size, density, or connectivity also declined across elevation, and whether these epidemiologically relevant factors explained the observed disease distribution. We found that while none of these factor means changed across elevation, disease was significantly more likely to occur at both higher elevations and in larger populations, the majority of which were found above 1300 m. The break in disease incidence was also associated with an apparent scarcity of these larger host populations between 1000 and 1300 m in elevation. Examining variation in climatic factors among host populations, we also showed that the probability of disease was higher in areas with historically colder, wetter, and more stable conditions. The restricted distribution of anther‐smut disease in high‐elevation S. vulgaris provides an opportunity for empirical study on range limits and disease distribution in natural alpine communities that are considered particularly sensitive to the effects of climate change.

Sympatry and interference of divergent Microbotryum pathogen species

“…It remains to be determined whether S. vulgaris is predisposed to receiving host‐shifts due to its susceptibility or whether the ecology of being weedy and very widespread creates more opportunities for host‐shifts to occur and to be observed. Moreover, in the current and previous studies (Abbate & Antonovics, ; Abbate et al, ; Bucheli, Gautschi, & Shykoff, ; Le Gac et al, ), S. vulgaris from high elevations (>ca. 1,300 m) was found infected by multiple distinct, endemic, and apparently self‐sustaining lineages of Microbotryum , which is also consistent with a greater propensity for host‐shifts and perhaps new disease emergence onto this 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.…”

“…The time interval between nonendemic and endemic inoculations was varied as second treatments of 7 or 10 days, and the proportions of plants diseased by the endemic pathogen for all treatments were compared to paired sets of plants initially treated with water as a control followed by the endemic pathogen at the same time intervals. After low disease rates in the first run of the experiment, which is usual for this host species (Abbate & Antonovics, ), an independent second run of the experiment was performed and combined with the first (following test of run significance, below). All treatments totaled between 107 and 140 plants surviving to flower that were randomized for positions in the greenhouse.…”

“…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, ).…”

Host resistance and pathogen infectivity in host populations with varying connectivity

“…For example, the yearly average temperature decreases and precipitation increases going from the High coast, to the inland, and alpine regions of Northern Sweden (SMHI ,b). This might affect disease development in different areas, as found in surveys of the host Silene vulgaris and its anther‐smut disease in the French Alps where the probability of disease was higher in areas with colder and wetter conditions (Abbate and Antonovics ). However, if differences in disease incidence and prevalence seen among V. alpina populations were primarily due to climate variation, then one would predict a gradual change in disease incidence and prevalence from the High coast, to the inland, and alpine populations that clearly contrasts with the patterns observed (Carlsson‐Granér and Thrall ).…”