Tolerance-conferring defensive symbionts and the evolution of parasite virulence

A bstract Defensive symbionts in the host microbiome can confer protection from infection or reduce the harms of being infected by a parasite. Defensive symbionts are therefore promising agents of biocontrol that could be used to control or ameliorate the impact of infectious diseases. Previous theory has shown how symbionts can evolve along the parasitism-mutualism continuum to confer greater or lesser protection to their hosts, and in turn how hosts may coevolve with their symbionts to potentially form a mutualistic relationship. However, the consequences of introducing a defensive symbiont for parasite evolution and how the symbiont may coevolve with the parasite have received relatively little theoretical attention. Here, we investigate the ecological and evolutionary implications of introducing a tolerance-conferring defensive symbiont into an established host-parasite system. We show that while the defensive symbiont may initially have a positive impact on the host population, parasite and symbiont evolution tend to have a net negative effect on the host population in the long-term. This is because the introduction of the defensive symbiont always selects for an increase in parasite virulence and may cause diversification into high- and low-virulence strains. Even if the symbiont experiences selection for greater host protection, this simply increases selection for virulence in the parasite, resulting in a net negative effect on the host population. Our results therefore suggest that tolerance-conferring defensive symbionts may be poor biocontrol agents for population-level infectious disease control. L ay S ummary Defensive symbionts – microbes that confer protection to a host against a harmful parasite – are found throughout the natural world and represent promising candidates for biological control to combat infectious diseases. Symbionts can protect their hosts through a variety of mechanisms that may prevent infection (resistance) or increase survival following infection (tolerance), yet our understanding of the ecological and evolutionary impact of defensive symbionts on parasites is limited. Moreover, few theoretical predictions exist for how defensive symbionts are likely to evolve in the presence of parasites, and for the net effect on the host population. Using a mathematical model where defensive symbionts reduce parasite virulence (harm to the host), we investigate the impact of their introduction on the evolution of parasite virulence, how selection increases or decreases host protection, and whether such symbionts are beneficial for the host population. We find that this form of defensive symbiosis always selects for higher parasite virulence and that it can cause the parasite to diversify into high and low virulence strains which specialise on different host subpopulations. Crucially, we show that the introduction of a defensive symbiont will always lead to a long-term reduction in host population size even if they are beneficial in the short-term. Together, our results show that defensive symbionts can have a strong impact on the evolution of virulence and that this form of host protection is not robust, indicating that tolerance-conferring symbionts are likely to be poor candidates for biological control of infectious diseases at the population level.

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