Transmission and temporal dynamics of anther‐smut disease (Microbotryum) on alpine carnation (Dianthus pavonius)

Abstract

Summary Theory has shown that sterilizing diseases with frequency‐dependent transmission (characteristics shared by many sexually transmitted diseases) can drive host populations to extinction. Anther‐smut disease (caused by Microbotryum sp.) has become a model plant pathogen system for studying the dynamics of vector‐ and sexually transmitted diseases: infected individuals are sterilized, producing spores instead of pollen, and the disease is spread between reproductive individuals by insect pollinators. We investigated anther‐smut disease in a heavily infected population of Dianthus pavonius (alpine carnation) over an 8‐year period to determine disease impacts on host population dynamics. Over the 8 years, disease prevalence remained consistently high (>40%), while the host population numbers declined by over 50%. The observed rate of vector transmission to reproductive, adult hosts was inadequate to explain the high disease prevalence. Additional density‐dependent aerial transmission to highly susceptible juveniles, indicated from experimental field and greenhouse studies, is likely to play a key role in maintaining the high disease prevalence. Epidemiological models that accounted for the mixed transmission mode predicted an eventual decline in disease. Synthesis. Our results demonstrate that high prevalence of a sterilizing disease does not necessarily drive host populations towards extinction and also highlights the importance of demographic studies for establishing the presence of alternative transmission modes.

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

“…Vector transmission is typically frequency‐dependent (Antonovics, Iwasa, & Hassell, ; McCallum, Barlow, & Hone, ), so disease establishment and persistence should not depend on a threshold host density (Getz & Pickering, ; Lloyd‐Smith et al., ). Detailed marked‐plant studies of the transmission within a single large population of D. pavonius in the range centre have shown that transmission is actually a mixture of frequency‐dependent pollinator‐transmission and density‐dependent wind transmission (Bruns et al., ). However, theoretical models of mixed frequency and density‐dependent transmission have shown that even small levels of frequency‐dependent transmission increase the conditions for disease persistence and reduce the threshold density for disease invasion (Ryder, Miller, White, Knell, & Boots, ).…”

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

“…Overall disease prevalence in this area has been close to 40% for the entire time (Bruns et al. ), but there is significant heterogeneity in host and pathogen density at a more fine‐scale local level (J. Antonovics et al., unpubl. data).…”

“…In D. pavonius , the disease is systemic, affecting all flowers on the plant, and recovery is extremely rare (Bruns et al. ). Pollinators are the main route for spore dispersal, although localized aerial dispersal also occurs (Bruns et al.…”

“…Pollinators are the main route for spore dispersal, although localized aerial dispersal also occurs (Bruns et al. ). We have observed a wide range of insects on D. pavonius flowers including bees, skipper butterflies, syrphid flies, bee flies, and small anthophilid flies.…”

“…To quantify sex‐specific differences in inflorescence production in the field, we analyzed flowering data from a long‐term census study of the Garelli population (Bruns et al. ). In July 2015, all the flowering plants in a 10 × 20 m plot were counted, and the total number of flowering stems (regardless of whether they were in bud, flower, or fruit stage) for each plant was recorded.…”