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.
Highlights
Evidence for impacts of the microbiome on host health is accumulating
The two distributions correspond to the community of commensal microbiota and pathogenic microbiota; the height of the two distributions reflects the number of individuals in each category corresponding to each value along the continuum
If there is overlap between the two distributions, drawing the line toward the middle of the plot inevitably misclassifies some individuals: some members of the commensal microbiota will be to the right of the line, and some members of the pathogenic microbiota to the left of it
Summary
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. This effect can be reversed when pathogens increase host mortality. 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.
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