[Abstract] Ecological theory predicts that disease incidence increases with increasing density of host networks, yet evolutionary theory suggests that host resistance increases accordingly. To test the combined effects of ecological and evolutionary forces on host-pathogen systems, we analyzed the spatiotemporal dynamics of a plant (Plantago lanceolata)–fungal pathogen (Podosphaera plantaginis)relationship for 12 years in over 4000 host populations. Disease prevalence at the metapopulation level was low, with high annual pathogen extinction rates balanced by frequent (re-)colonizations. Highly connected host populations experienced less pathogen colonization and higher pathogen extinction rates than expected; a laboratory assay confirmed that this phenomenon was caused by higher levels of disease resistance in highly connected host populations.
Contrary to expectations, highly connected populations can experience less impact from infectious disease than isolated groups. What happens to pathogens in natural populations has been poorly studied, because they rarely cause devastating disease outbreaks. Thanks to a long-term study of an inconspicuous fungal-plant disease system, we have now gained some surprising insights. During a 12-year study, Jousimo et al. discovered that clustered and linked host-plant patches showed lower levels of fungal damage and higher fungal extinction rates than more distant patches (see the Perspective by Duffy). This phenomenon is explained by high gene flow and rapid evolution of host resistance within the connected patches. Populations of the modest weed Plantago, growing on the Åland Islands in the Baltic, were less than 10% infected by the Podosphaera mildew fungus in any given year, but infection turnover was high. These findings have broad implications for ecology, disease biology, conservation, and agriculture.
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