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

Strong partial immunity in recovered hosts is predicted to favour more virulent pathogens upon re-infection in the population. We present empirical evidence that the incomplete immunity generated by commensal host microbiota can similarly select for higher pathogen virulence. We tracked the evolutionary trajectories of a widespread pathogen (Pseudomonas aeruginosa) experimentally passaged through populations of nematode hosts which had been immune-primed by a natural commensal. Immune protection selected for pathogens more than twice as likely to kill the nematode as those evolved in non-primed or immune-compromised animals. Despite the higher virulence that emerged, pathogen molecular evolution in immune-primed hosts was slower and more constrained compared to evolution in immune-compromised hosts, where substantial genetic differentiation was exhibited. These findings directly attribute the partial protective immunity provided by host-microbiome interactions as a significant selective force shaping the virulence and evolutionary dynamics of novel infectious diseases.