Abstract

This paper examines a mathematical model for the coevolution of parasite virulence and host resistance under a multilocus gene-for-gene interaction. The degrees of parasite virulence and host resistance show coevolutionary cycles for sufficiently small costs of virulence and resistance. Besides these coevolutionary cycles of a longer period, multilocus genotype frequencies show complex fluctuations over shorter periods. All multilocus genotypes are maintained within host and parasite classes having the same number of resistant/virulent alleles and their frequencies fluctuate with approximately equally displaced phases. If either the cost of virulence or the number of resistance loci is larger then a threshold, the host maintains the static polymorphism of singly (or doubly or more, depending on the cost of resistance) resistant genotypes and the parasite remains universally avirulent. In other words, host polymorphism can prevent the invasion of any virulent strain in the parasite. Thus, although assuming an empirically common type of asymmetrical gene-for-gene interaction, both host and parasite populations can maintain polymorphism in each locus and retain complex fluctuations. Implications for the red queen hypothesis of the evolution of sex and the control of multiple drug resistance are discussed.

Highlights

  • Host– parasite coevolution, the process of reciprocal adaptive genetic changes in host and parasites [1], shapes levels of diversity [2,3,4,5], accelerates the pace of evolution [6], and may drive the evolution of sexual reproduction [7,8,9] or elevated mutation rate [10 –12]. These effects crucially depend on the mode of coevolution: ‘arms race dynamics’ (ARD), where selection is directional and results in escalation of host defence and parasite counter-defence, or ‘fluctuating selection dynamics’ (FSD; known as Red Queen dynamics), with frequency-dependent selection for rare host and parasite genotypes

  • We investigated the presence and properties of coevolution between the dinoflagellate A. minutum—the most abundant dinoflagellate species at the time of study in the two river estuaries we sampled—and its local endoparasites during the short time span of blooms

  • (iv) We detected no local adaptation in P. infectans, as the dominant signal was the lower infectivity of Rance parasites

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Summary

Introduction

Host– parasite coevolution, the process of reciprocal adaptive genetic changes in host and parasites [1], shapes levels of diversity [2,3,4,5], accelerates the pace of evolution [6], and may drive the evolution of sexual reproduction [7,8,9] or elevated mutation rate [10 –12]. We answered these questions by monitoring the abundance of the host A. minutum and its parasites, isolating and culturing monoclonal strains of both the host and microeukaryotic parasites at several time points in these two estuaries, and conducting a large number of crossinoculation experiments over time and space to characterize the coevolutionary process. For each species and location, we sampled three to five time points, and one to seven parasite strains per time point These parasite strains were cross-inoculated with 115 strains of A. minutum (eight dates of isolation with 10–18 strains per date, electronic supplementary material, table S2). Under FSD, parasite infectivity and host resistance do not necessarily change with time, which is why it was originally proposed to use time-shift experiments to reveal FSD coevolution [19]. We tested for effects of date host and date parasite using a simpler one-way analysis of variance for the resistance of host by date (when averaged over all parasite strains), and for the infectivity of the parasite by date (when averaged over all host strains)

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