On the evolutionary origins of host–microbe associations

Animals can provide benefits to their associated microbes—}and these can, in turn, positively affect their hosts. But how do such mutually beneficial associations arise in the first place? In particular, when animal and microbe initially have independent lifestyles, this is not clear. By developing a model of animal and microbial life cycles on patchy habitats, we show how their overlapping ecologies of development and dispersal can lead to the enrichment of certain microbes in the dispersing animals, even in the absence of specific mutualistic benefits. This enrichment can then set the stage for the evolution of more specific host{–}microbe associations, which also implies that host enrichment per se is not an indicator of a beneficial host{–}microbe symbiosis.Many microorganisms with high prevalence in host populations are beneficial to the host and maintained by specialized transmission mechanisms. Although microbial promotion of host fitness and specificity of the associations undoubtedly enhance microbial prevalence, it is an open question whether these symbiotic traits are also a prerequisite for the evolutionary origin of prevalent microbial taxa. To address this issue, we investigate how processes without positive microbial effects on host fitness or host choice can influence the prevalence of certain microbes in a host population. Specifically, we develop a theoretical model to assess the conditions under which particular microbes can become enriched in animal hosts even when they are not providing a specific benefit to a particular host. We find increased prevalence of specific microbes in a host when both show some overlap in their lifecycles, and especially when both share dispersal routes across a patchy habitat distribution. Our results emphasize that host enrichment per se is not a reliable indicator of beneficial host{–microbe interactions. The resulting increase in time spent associated with a host may nevertheless give rise to new selection conditions, which can favor microbial adaptations toward a host-associated lifestyle, and, thus, it could be the foundation for subsequent evolution of mutually beneficial coevolved symbioses.A Python implementation of the model underlying the results in this paper has been deposited in GitHub (https://github.com/misieber/patchbiota)