Conventional wisdom on the coevolution of host resistance and parasite virulence predicts that hosts should generally develop better defense and parasites should become more benign. However, examples of highly virulent pathogens in almost wholly susceptible host populations abound in nature. In these systems, eco-epidemiological feedbacks (e.g., spatial structuring of host and parasite populations) may alter coevolutionary trajectories. Here, we hypothesized that asymmetries in host and pathogen dispersal (e.g., low host and high pathogen dispersal) provide a brake on coevolutionary pressures enabling highly virulent pathogens to persist in susceptible host populations. To test this hypothesis, we developed a novel theoretical framework of coevolution in metapopulations. This method combined a state-structured model with transient sensitivity analysis to calculate selection gradients for both host resistance and parasite virulence across a range of host and pathogen dispersal strategies.
Results/Conclusions
We found that resistance thresholds in the host prevent the evolution of highly resistant forms. These thresholds were modified by the dispersal strategies of the host and vector. In all cases, virulence was positively selected for indicating that highly virulent pathogens can be evolutionarily stable in metapopulations. These methods highlight the importance of ecological dynamics in understanding host and pathogen coevolution and also provide one of the first models of quantitative trait coevolution in a metapopulation.