Abstract
Understanding the coevolution of hosts and parasites is a long-standing goal of evolutionary biology. There is a well-developed theoretical framework to describe the evolution of host-parasite interactions under the assumption of direct, two-species interactions, which can result in arms race dynamics or sustained genotype fluctuations driven by negative frequency dependence (Red Queen dynamics). However, many hosts rely on symbionts for defence against parasites. Whilst the ubiquity of defensive symbionts and their potential importance for disease control are increasingly recognized, there is still a gap in our understanding of how symbionts mediate or possibly take part in host-parasite coevolution. Herein we address this question by synthesizing information already available from theoretical and empirical studies. First, we briefly introduce current hypotheses on how defensive mutualisms evolved from more parasitic relationships and highlight exciting new experimental evidence showing that this can occur very rapidly. We go on to show that defensive symbionts influence virtually all important determinants of coevolutionary dynamics, namely the variation in host resistance available to selection by parasites, the specificity of host resistance, and the trade-off structure between host resistance and other components of fitness. In light of these findings, we turn to the limited theory and experiments available for such three-species interactions to assess the role of defensive symbionts in host-parasite coevolution. Specifically, we discuss under which conditions the defensive symbiont may take over from the host the reciprocal adaptation with parasites and undergo its own selection dynamics, thereby altering or relaxing selection on the hosts' own immune defences. Finally, we address potential effects of defensive symbionts on the evolution of parasite virulence. This is an important problem for which there is no single, clear-cut prediction. The selection on parasite virulence resulting from the presence of defensive symbionts in their hosts will depend on the underlying mechanism of defence. We identify the evolutionary predictions for different functional categories of symbiont-conferred resistance and we evaluate the empirical literature for supporting evidence. We end this review with outstanding questions and promising avenues for future research to improve our understanding of symbiont-mediated coevolution between hosts and parasites.
Highlights
All organisms are under constant threat of attack by pathogens and parasites, and as a result have evolved diverse strategies to avoid infection, including complex behaviours and sophisticated immune systems
There is a well-developed theoretical framework to describe the evolution of host–parasite interactions under the assumption of direct, two-species interactions, which can result in arms race dynamics or sustained genotype fluctuations driven by negative frequency dependence (Red Queen dynamics)
In light of these findings, we turn to the limited theory and experiments available for such three-species interactions to assess the role of defensive symbionts in host–parasite coevolution
Summary
All organisms are under constant threat of attack by pathogens and parasites, and as a result have evolved diverse strategies to avoid infection, including complex behaviours and sophisticated immune systems. There is a large and sophisticated body of theory on host–parasite coevolution (reviewed in Woolhouse et al, 2002; Salathe, Kouyos & Bonhoeffer, 2008), but most models of host–parasite interactions assume a direct interaction between host and parasite, without any interference from host-associated symbionts. As our main concern is on the consequences of defensive symbioses for host–parasite coevolution, we limit our discussion to symbiont-mediated protection against infectious organisms (i.e. parasites and pathogens). We do not discuss symbionts that provide protection against predators, herbivores, and other grazers
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