Synthesizing selection mosaic theory and host-pathogen theory to explain large-scale pathogen coexistence.

Abstract

Selection mosaic theory explains observations of polymorphism in host-pathogen interactions in terms of spatially variable natural selection but does not account for population dynamics. In contrast, classical host-pathogen theory easily explains observations of population cycles, but does not explain the persistence of pathogen polymorphism. Here, we synthesize these two frameworks to understand the effects of population cycles on pathogen polymorphism. We show that geographic variation in the frequency of two morphotypes of a baculovirus that infects the Douglas-fir tussock moth (Orgyia pseudotsugata) depends on the frequency of Douglas-fir (Pseudotsuga menziesii), an important tussock moth host tree. The morphotype frequency data are best explained by host-pathogen models that combine a selection mosaic with population cycles. In our model, population cycles intensify pathogen competition across a selection mosaic, leading to a strong effect of Douglas-fir frequency on morphotype frequency that matches the data. Models without host-pathogen cycles or a selection mosaic project only weak effects of varying Douglas-fir frequency. Our model further projects that a biopesticide made up of both viral morphotypes would be more effective than the current single-morphotype biopesticide, demonstrating that our synthesis of selection mosaic theory and host-pathogen theory provides useful insights into pest management.