Microbes that protect their hosts from pathogenic infection are widespread components of the microbiota of both plants and animals. It has been found that interactions between ‘defensive’ microbes and pathogens can be genotype-specific and even underlie the variation in host resistance to pathogenic infection. These observations suggest a dynamic coevolutionary association between pathogens and defensive microbes, but direct evidence of coevolution is lacking. We tested the hypothesis that defensive microbes and pathogens could coevolve within host populations by co-passaging a microbe with host-defensive properties (Enterococcus faecalis) and a pathogen (Staphylococcus aureus) within Caenorhabditis elegans nematodes. Using both phenotypic and genomic analyses across evolutionary time, we found patterns of pathogen local adaptation and defensive microbe-pathogen coevolution via fluctuating selection dynamics. Moreover, coevolution with defensive microbes resulted in more rapid and divergent pathogen evolution compared to pathogens evolved independently in host populations. Taken together, our results indicate the potential for defensive microbes and pathogens to coevolve, driving interaction specificity and pathogen evolutionary divergence in the absence of host evolution.
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