Tolerance-conferring defensive symbionts and the evolution of parasite virulence

Abstract

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 yet to be explored theoretically. 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.

The impact of sterility-mortality tolerance and recovery-transmission trade-offs on host–parasite coevolution

“…In fact, it can cause the parasite to also branch, which does not occur when the parasite evolves in isolation. This aligns with the findings of a recent theoretical study exploring the coevolution of parasite virulence and host mortality tolerance through a defensive symbiont [65]. They discovered that the defensive symbiont can cause the parasite to split into two subpopulations, resulting in the coexistence of strains with low and high virulence.…”

Hyperparasitism and the evolution of parasite virulence

“…Although models of hyperparasitism are relatively rare, especially in an evolutionary context, some of our key findings are mirrored in models of other tripartite systems. For example, multiple studies have found that introducing an additional species to a host-parasite system can lead to evolutionary branching in the host (Best 2018) or the parasite (Kisdi, Geritz, and Boldin 2013; Best 2018; Smith and Ashby 2022; Morozov and Best 2012) populations. In a related study that also has relevance to biocontrol, Smith and Ashby (2022) explore how the introduction of a tolerance-conferring defensive symbiont affects the evolution of parasite virulence.…”

“…For example, multiple studies have found that introducing an additional species to a host-parasite system can lead to evolutionary branching in the host (Best 2018) or the parasite (Kisdi, Geritz, and Boldin 2013; Best 2018; Smith and Ashby 2022; Morozov and Best 2012) populations. In a related study that also has relevance to biocontrol, Smith and Ashby (2022) explore how the introduction of a tolerance-conferring defensive symbiont affects the evolution of parasite virulence. They show that even if the defensive symbiont is initially beneficial to the host population, in the long-term it is costly because it always selects for higher parasite virulence.…”

Incomplete immunity in a natural animal-microbiota interaction boosts pathogen virulence

“…These pathogens had the highest virulence in naïve immunocompetent hosts relative to other evolved pathogens, but lower virulence in naïve immune-compromised hosts. Collectively, our phenotypic findings demonstrate that the immediate benefits of increased survival and pathogen tolerance conferred by the microbiota can ultimately lead to extremely negative impacts on the host 25 .…”