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The ecological and evolutionary mechanisms behind the persistence of highly virulent pathogens: plague as a case study




Buhnerkempe, Michael G., author
Webb, Colleen T., advisor
Poff, N. LeRoy, committee member
Eisen, Rebecca J., committee member
Hoeting, Jennifer A., committee member

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The persistence of emerging infectious diseases is the result of eco-evolutionary feedbacks between a pathogen and its novel host. Spatial structure both within and between host populations (i.e., a metapopulation) in particular can have a large effect on the establishment and subsequent coevolution of a host and pathogen. Here, my colleagues and I explore how differing metapopulation structures in a host and pathogen affect the coevolutionary maintenance of high virulence and low resistance in an emerging infectious disease. We use the relatively recent emergence of plague, caused by the bacterium Yersinia pestis, in North America as a case study to both understand how spatial structure in the pathogen may differ from that of its host and how these differences may affect coevolutionary trajectories. Host responses to Y. pestis infection are highly variable with some species, like black-tailed prairie dogs (Cynomys ludovicianus), experiencing massive population declines upon introduction of the plague bacterium (i.e., epizootics), while others, like the California ground squirrel (Spermophilus beecheyi), exhibit enzootic maintenance of Y. pestis. These species in particular have markedly different spatial structures, but it is unclear how regional transmission of plague may structure the pathogen population. To understand transmission more fully, we developed a mechanistic model of plague infection in a single population that incorporated multiple routes of transmission and parameterized the model for the two species mentioned above. We found that transmission in the epizootic system is driven largely through on-host cycling of fleas (i.e., a booster-feed infection cycle). In contrast, enzootics are driven by an off-host, questing flea reservoir. The potential for off-host fleas to drive plague dynamics reveals the potential for non-overlapping host and pathogen metapopulation structures. The effect of such a structure on coevolution is not well-understood, particularly for quantitative traits where no theoretical methods exist to study coevolution in a metapopulation. Consequently, we also developed a novel theoretical framework for studying quantitative trait coevolution in a metapopulation. This new framework reveals that coevolutionary outcomes for resistance and virulence depend on the interaction between host and pathogen dispersal strategies with local reproduction and transmission dynamics favoring a diversity of resistance-virulence combinations. Host-pathogen coevolution is also affected by the shape of life-history trade-offs for both the host and the pathogen. We predicted coevolutionary outcomes under different host and pathogen dispersals assuming three different trade-off functions when resistance comes at the cost of reproduction and virulence increases transmission while decreasing the infectious period: accelerating, linear, and decelerating costs. We found that selection on resistance is most sensitive to concave trade-off functions, and selection on virulence was most sensitive to convex functions, although coevolutionarily stable strategies were only predicted when both resistance and virulence had accelerating cost trade-off functions. Predictions from the model also differ from those observed in well-mixed and spatially structured single populations indicating that eco-evolutionary dynamics do not scale directly with space. Implications for future models of plague coevolution are also discussed.


2013 Spring.
Includes bibliographical references.

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Yersinia pestis
pathogen persistence
disease ecology


Associated Publications