Protective microbiomes can limit the evolution of host pathogen defense

Abstract

The evolution of host immunity occurs in the context of the microbiome, but little theory exists to predict how resistance against pathogens might be influenced by the need to tolerate and regulate commensal microbiota. We present a general model to explore the optimal investment in host immunity under conditions in which the host can, versus cannot easily distinguish among commensal versus pathogenic bacteria, and when commensal microbiota can, versus cannot protect the host against the impacts of pathogen infection. We find that a loss of immune vigilance associated with innate immunity over evolutionary time can occur due to the challenge of discriminating between pathogenic and other microbe species. Further, we find the greater the protective effect of microbiome species, acting either directly or via competition with a pathogen, or the higher the costs of immunity, the more likely the loss of immune vigilance is. Conversely, this effect can be reversed when pathogens increase host mortality. Generally, the magnitude of costs of immunity required to allow evolution of decreased immune vigilance are predicted to be lowest when microbiome and pathogen species most resemble each other (in terms of host recognition), and when immune effects on the pathogen are weak. Our model framework makes explicit the core trade‐offs likely to shape the evolution of immunity in the context of microbiome/pathogen discrimination. We discuss how this informs interpretation of patterns and process in natural systems, including vulnerability to pathogen emergence.

The study of host–microbiome (co)evolution across levels of selection

“…[35,36]). Such rapid acquisition of defence has been predicted to hinder the evolution of host genetic defence [37,38], and lead to host dependence of particular microbial taxa, but see Hrcěk et al [39]. Such inter-dependencies could reinforce the specificity of the interaction, for example, by reshaping self/non-self recognition within the immune system [40], and lead to host adaptations to recruit particular taxa or functional groups.…”

The microbiome extends host evolutionary potential

“…Finally, it is important to consider that not all host phenotypes will be influenced by the microbiome, and not all microbes will influence host phenotypes (e.g., V G-MICRO = 0). Naturally, many host-microbiome interactions are also pathogenic, but such relationships have been studied theoretically and empirically in disease ecology 8 , 29 and could also be incorporated into our quantitative genetics framework. Here, however, we are primarily focusing on adaptive microbiomes.…”

Evolution of animal immunity in the light of beneficial symbioses

“…Finally, another approach is to leverage the power of modelling and simulation to shape evolutionary hypotheses. For example, a recently developed model predicts that a weakened immune system can evolve when distinguishing between pathogen and symbiont is difficult, when symbionts provide strong levels of protection and when immune costs are high [137]. All these approaches, taken together with development of additional systems, will play a role as we move forward.…”