Oikos 123: 1126–1136, 2014 doi: 10.1111/oik.01001 © 2014 Th e Authors. Oikos © 2014 Nordic Society Oikos Subject Editor: Anna-Liisa Laine. Accepted 14 February 2014 Elevational disease distribution in a natural plant – pathogen system: insights from changes across host populations and climate Jessica L. Abbate and Janis Antonovics J. L. Abbate ([email protected]), Centre d ’ É cologie Fonctionelle et É volutive (CEFE), UMR 5175, CNRS, 1919 route de Mende, FR-34293, Montpellier, France. – J. Antonovics, Dept of Biology, Univ. of Virginia, Charlottesville, VA 22904, USA. 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 wildfl ower 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 infl uence 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 signifi cantly more likely to occur at both higher elevations and in larger populations, the majority of which were found above 1300 m. Th e 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. Th e 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 eff ects of climate change. Once marginalized in classical ecology textbooks, parasitic stability (Harvell et al. 2002, IPCC 2007, Laff erty 2009). organisms are now understood to play a major role in However, the determinants of disease distribution in natural structuring biological communities, population dynamics, systems have been relatively under-studied, limiting species evolution and global biodiversity (Anderson and our understanding of the full consequences of current and May 1981, Altizer et al. 2003, Guernier et al. 2004, future ecosystem perturbations. Hudson et al. 2006). Understanding how parasites and Anther smut is a naturally-occurring endemic disease pathogens are distributed in space and time is essential of fl owering plants in the pink family, Caryophyllaceae, for guiding vaccination programs (Real and Biek 2007), caused by host-specifi c lineages of the obligate basidiomy- setting quarantine guidelines, managing wildlife and cete, Microbotryum spp. Th e disease has large advantages nature reserves (Monz ó n et al. 2011), selecting agricultural for distributional studies because it is easily observable in cultivars (Wolfe 1985), and making predictions about dis- the fi eld without the need for special equipment, and it ster- ease emergence (Jones et al. 2008). Th e concurrent map- ilizes rather than kills its host, thereby facilitating assessment ping of species distributions and habitat features can off er of disease prevalence and occurrence not only in the powerful insight into ecological requirements and factors fi eld (Antonovics et al. 2002) but also using herbarium spec- potentially important for survival, reproduction, or disper- imens (Hood et al. 2010). As a pollinator-transmitted sal (Shea and Chesson 2002). For host – pathogen systems, sterilizing disease, anther smut shares characteristics these factors can aff ect the spread and persistence of disease with sexually-transmitted diseases in animals (Lockhart (Anderson and May 1981). With rapid climate change, this et al. 1996), and has been investigated with regard to knowledge is particularly important for anticipating the many broader ecological and evolutionary topics such as timing and intensity of endemic and epidemic diseases genome evolution, metapopulation dynamics, and speciation which may threaten human health, food supply and social (Bernasconi et al. 2009). Because its hosts are generally 1126 abundant and economically unimportant, it is a disease density and frequency of disease (prevalence) have complex whose natural distribution can be studied without the need impacts on sexual and vector-mediated transmission, and for quarantine or intervention, in contrast to many animal reduced transmission within populations can reduce or agricultural systems, whose study in unperturbed condi- spread and persistence in the metapopulation (Antonovics tions is diffi cult for logistic, economic or ethical reasons. et al. 1995, Biere and Honders 1998, Carlsson-Gran é r and Anther-smut disease of the Caryophyllaceae is distributed Th rall 2002, Essenberg 2012). Additionally, delayed host world-wide, with disease generally occurring throughout phenology at higher elevations could further restrict the native range of each particular host (Hood et al. the availability of hosts if fl owering seasons do not overlap, 2010). However, in one particularly wide-spread host spe- and such temporal avoidance of disease within populations cies, Silene vulgaris , natural history observations suggested is associated with anther-smut resistance in S. latifolia that host-specifi c endemic disease on this species was (Biere and Antonovics 1996). restricted to high elevation populations above ca 2000 m Here, we conducted systematic surveys of Silene across much of its natural geographic range (Hood et al. vulgari s and its anther-smut disease to quantify disease dis- 2010, Antonovics and M. Hood unpubl.). Below this eleva- tribution across elevational transects within the host ’ s tion, diseased S. vulgaris had been documented only in sym- native range in the French Alps. We tested whether concur- patry with diseased congener Silene latifolia , and molecular rent changes in host population size, density, or connectiv- markers showed that the disease on S. vulgaris at these low ity suffi ciently explained the observed pattern of disease elevations was caused by cross-species transmission from the incidence, and whether elevation was still important after S. latifolia -specifi c fungal lineage (Hood et al. 2003). Th ough these host spatial factors were considered. We then used common occurrence of anther-smut disease in high-elevation these survey localities and dates to explore the contribution S. vulgaris was noted as early as 1957 (Marsden-Jones of climate and host phenology, two ecological factors that and Turrill 1957), its incidence had never explicitly could aff ect disease spread in this system and are commonly been studied. Furthermore, despite the general extent of known to correlate with elevation. S. vulgaris distribution (Jalas and Suominen 1986), few details on the availability of host populations across the region were known. Methods High-elevation species distributions typically point to abiotic environmental explanations, particularly for plants Study species (K ö rner 2003). In disease systems, both temperature and rainfall can have varying eff ects on pathogen viability, Silene vulgaris host resistance and disease transmission (Harvell et al. Silene vulgaris (commonly known as ‘ bladder campion ’ ) is a 2002, Strange 2003, Kutz et al. 2009). A few studies on gynodioecious perennial member of the Caryophyllaceae, Microbotryum species infecting S. latifolia have noted that widely distributed across and native to Eurasia. Th e species is temperatures can alter fungal spore germination, mating, easily identifi ed by the infl ated hanging calyx with a and development of infectious hyphae (Hood and crown of fi ve deeply-notched petals, the dichasial infl ores- Antonovics 1998) as well as in planta infection success of cence, and opposing simple oblong-shaped leaves protrud- teliospore inocula (Sch ä fer et al. 2010). Whereas these two ing from each swollen node along the stem. Each plant can studies showed reduced activity under colder temperatures, have a large number of stems arising from a single taproot, Alexander and Maltby (1990) noted delayed disease allowing for counts of discrete individuals. S. vulgaris is expression after an incubator overheated to above 30° C for found from sea level to roughly 2400 m, largely in meadows, over 48 h in the weeks prior to fl owering. However, in this mown or grazed fi elds, and along steep embankments system, it is neither clear how climatic changes would or other land features prone to disturbance. aff ect epidemiological parameters, nor is it clear that climate Silene vulgaris is morphologically variable and several factors are the only important changes occurring across