The role of epistasis on the evolution of recombination in host–parasite coevolution

Abstract

a b s t r a c tAntagonistic coevolution between hosts and parasites is known to affect selection on recombination in hosts. The Red Queen Hypothesis (RQH) posits that genetic shuffling is beneficial for hosts because it quickly creates resistant genotypes. Indeed, a large body of theoretical studies have shown that for many models of the genetic interaction between host and parasite, the coevolutionary dynamics of hosts and parasites generate selection for recombination or sexual reproduction. Here we investigate models in which the effect of the host on the parasite (and vice versa) depend approximately multiplicatively on the number of matched alleles. Contrary to expectation, these models generate a dynamical behavior that strongly selects against recombination/sex. We investigate this atypical behavior analytically and numerically. Specifically we show that two complementary equilibria are responsible for generating strong linkage disequilibria of opposite sign, which in turn causes strong selection against sex. The biological relevance of this finding stems from the fact that these phenomena can also be observed if hosts are attacked by two parasites that affect host fitness independently. Hence the role of the Red Queen Hypothesis in natural host parasite systems where infection by multiple parasites is the rule rather than the exception needs to be reevaluated.

Identifying the Molecular Basis of Host-Parasite Coevolution: Merging Models and Mechanisms

“…These models revealed that coevolution can generate diverse gene-frequency dynamics ranging from selective sweeps to sustained cycles. More recent work has refined the conditions under which coevolution favors sexual reproduction or recombination Agrawal 2006;Salathé et al 2008;Kouyos et al 2009), while other recent theory has expanded coevolution's reach by showing that it might drive other important evolutionary transitions. For instance, coevolution can generate selection for changes in ploidy levels Oswald and Nuismer 2007), patterns of mate choice Otto et al 2008), rates of mutation (M'Gonigle et al 2009), and even mating system (Agrawal and Lively 2001).…”

On the Causes of Selection for Recombination Underlying the Red Queen Hypothesis

“…Third, the interactions between host loci mediating parasite resistance need to be epistatic (Kouyos et al 2007) or display dominance (Agrawal & Otto 2006). In the absence of epistatic interactions among loci, strong LD of constant sign build up quickly which cause strong selection against recombination (Kouyos et al 2008). Data from plant and animal studies suggest that epistatic interactions among disease resistance loci are indeed prevalent (Kover & Caicedo 2001).…”

The genetics of infectious disease susceptibility: has the evidence for epistasis been overestimated?

“…(c) Multiplicative matching-alleles model. This model is presented as a counterpoint to the matching-allele model, as it does not implicitly involve epistatic interactions between resistance alleles at different loci [4,29]. Instead, the number of matched alleles determines host and parasite fitness in a multiplicative fashion, leading to intermediate, or partial, estimates of resistance.…”

“…While epistasis is an integral component of many models of disease resistance and antagonistic coevolution (but not all [4,29]; Figure 2), the contribution of epistatic variance to susceptibility remains difficult to evaluate using conventional QTL mapping methods. With the advent of next generation sequencing approaches, however, new insights can be generated into the genetic architecture of susceptibility [23,30].…”