Abstract

There is typically considerable variation in the level of infectivity of parasites and the degree of resistance of hosts within populations. This trait variation is critical not only to the evolutionary dynamics but also to the epidemiology, and potentially the control of infectious disease. However, we lack an understanding of the processes that generate and maintain this trait diversity. We examine theoretically how epidemiological feedbacks and the characteristics of the interaction between host types and parasites strains determine the coevolution of host–parasite diversity. The interactions include continuous characterizations of the key phenotypic features of classic gene-for-gene and matching allele models. We show that when there are costs to resistance in the hosts and infectivity in the parasite, epidemiological feedbacks may generate diversity but this is limited to dimorphism, often of extreme types, in a broad range of realistic infection scenarios. For trait polymorphism, there needs to be both specificity of infection between host types and parasite strains as well as incompatibility between particular strains and types. We emphasize that although the high specificity is well known to promote temporal “Red Queen” diversity, it is costs and combinations of hosts and parasites that cannot infect that will promote static trait diversity.

Highlights

  • COPYRIGHT AND REUSE Open Research Exeter makes this work available in accordance with publisher policies

  • We assumed an equal probability of mutation for the host and parasite. These simulation methods have been successfully used to approximate the adaptive dynamics (AD) process but it should be noted that in this approximation, the epidemiological dynamics will not reach their attractor before a new mutation arises and in this way, the ecological and evolutionary time scales are not strictly separated. (Note that the results presented below are qualitatively similar if we relax the assumption of equal mutation rates for the host and parasite, if we allow the mutational step size to increase, and if we change the number of hosts types and parasite strains used in the simulations.)

  • We examined whether specificity could lead to diversity beyond dimorphism by assuming the infection matrix in Figure 2B, where particular parasite strains are relatively more infective against particular host types

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Summary

Introduction

COPYRIGHT AND REUSE Open Research Exeter makes this work available in accordance with publisher policies. The gene families that are part of the pathogen recognition pathways, such as the major histocompatibility complex (MHC) of mammals and R genes in plants, have loci with many diverse alleles, and phenotypically this leads to considerable variation in infection probability for different host–parasite combinations (Bergelson et al 2001; Penn et al 2002) This diversity has important implications for individuals but for the epidemiology of the disease (Longini 1983; Lively 2010a), the effective treatment and management of disease (Anderson and May 1991), and in particular for the evolution of both hosts and parasites (Schmid-Hempel 2011). Evolution published by Wiley Periodicals, Inc. on behalf of The Society for the Study of Evolution

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