Microbial protection favors parasite tolerance and alters host-parasite coevolutionary dynamics

Coevolution between hosts and parasites is a major driver of rapid evolutionary change1 and diversification.2,3 However, direct antagonistic interactions between hosts and parasites could be disrupted4 when host microbiota form a line of defense, a phenomenon widespread across animal and plant species.5,6 By suppressing parasite infection, protective microbiota could reduce the need for host-based defenses and favor host support for microbiota colonization,6 raising the possibility that the microbiota can alter host-parasite coevolutionary patterns and processes.7 Here, using an experimental evolution approach, we co-passaged populations of nematode host (Caenorhabditis elegans) and parasites (Staphylococcus aureus) when hosts were colonized (or not) by protective bacteria (Enterococcus faecalis). We found that microbial protection during coevolution resulted in the evolution of host mortality tolerance—higher survival following parasite infection—and in parasites adapting to microbial defenses. Compared to unprotected host-parasite coevolution, the protected treatment was associated with reduced dominance of fluctuating selection dynamics in host populations. No differences in host recombination rate or genetic diversity were detected. Genomic divergence was observed between parasite populations coevolved in protected and unprotected hosts. These findings indicate that protective host microbiota can determine the evolution of host defense strategies and shape host-parasite coevolutionary dynamics. •Microbial protection resulted in the evolution of host mortality tolerance•Parasites adapted to counter microbial defenses within hosts•Protective microbes reduced fluctuating selection dynamics•Microbial protection did not impact host genetic diversity or recombination rates Protective microbes are widespread across host species and likely play a key role in mediating host interactions with parasites. Rafaluk-Mohr et al. show that microbial protection against infection can influence the host defense strategies that evolve, as well as the patterns and processes of host-parasite coevolution.