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Coevolutionary epidemiology : a population genetic exploration of evolutionary interactions between hosts and their infectious pathogens MacPherson, Ailene

Abstract

Coevolution between hosts and their parasites is widespread with important emergent consequences for natural systems from across the tree of life. The Red Queen Hypothesis suggests coevolution should maintain genetic variation in hosts and favour the evolution of sexual reproduction. Mathematical models have demonstrated that coevolutionary dynamics and the resulting effects on genetic variation and evolution of sex depend fundamentally on the genetic basis and life-history of the host-parasite interaction. Our understanding of the interaction genetics in natural systems is, however, still limited. In Chapter 2 I develop a statistical method based on genome-wide association studies (GWAS) to identify the genetic interactions between hosts and their parasites, demonstrating that inference of these genetic interactions is essential for a robust understanding of epidemiological traits. Classic models, including the one used in Chapter 2, consider the interaction between hosts and their free-living pathogens. Many pathogens are, however, directly transmitted between hosts and hence subject to epidemiological dynamics. In the Chapter 3, I consider the effects of these epidemiological dynamics on coevolution. We find, that epidemiological dynamics disrupt classic “Red Queen allele frequency cycles” observed in free-living pathogens, a change in dynamics that may limit the ability of coevolution to favour the evolution of sexual reproduction. Chapters 4 and 5 extend this by exploring the effects of epidemiological dynamics on the maintenance of genetic variation. Chapter 4 develops a baseline for the effect, examining the stochastic dynamics of heterozyogsity in a free-living pathogen population of constant size. In contrast to existing hypotheses, we find that coevolution in this classic model does not maintain genetic variation. In Chapter 5 we show that epidemiology can maintain genetic variation in hosts of directly transmitted pathogens, due in part to associated changes in population sizes. My thesis, therefore, demonstrates that, like other aspects of host and pathogen life-history, disease epidemiology fundamentally affects coevolutionary dynamics with implications for the evolution of sexual reproduction and the maintenance of genetic variation. Supplementary materials available at: http://hdl.handle.net/2429/77298.

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