Evolution of mutualism and diversity in microbial-host (holobiont) systems

Background/Question/Methods

Host-associated microbial, or holobiont systems, such as corals, are characterized by a large diversity of microbial strains or species, many of which are involved in mutualistic or symbiotic interactions with the host organism. However, the high diversity of microorganisms in holobionts poses a potential evolutionary conundrum for the maintenance of mutualism: microbial strategies that provide mutualistic benefits are expected to be replaced by other non-mutualistic strategies (i.e., “cheaters”) over time, particularly when the mutualism entails competitive costs. At best, such mutualistic strategies are expected to be adaptively neutral in relation to other strains or strategies. Host selection for mutualistic microbes is the main mechanism purported to explain the stability and persistence of observed host-microbial mutualistic interactions. Given the metacommunity structure of holobiont systems, another simple explanation that has not been explored as extensively is the possibility that the microbial diversity of the holobiont itself may be involved in facilitating the evolution of mutualistic strategies. Here we use mathematical and simulation-based patch-dynamic metacommunity models to study the evolution of mutualistic strategies in a holobiont metacommunity.

Results/Conclusions

We demonstrate that mutualistic microbes that normally would be competitively excluded from the holobiont metacommunity by cheater strategies occupying the same niche can successfully invade when microbial diversity is sufficiently high so as to ensure an overlap between the cheater’s niche and that of microbes occupying adjacent niches. Under these circumstances, microbes in adjacent niches can exclude the cheaters or keep them from excluding mutualistic microbes without any host selection for mutualism. Furthermore, the presence of a microbial mutualist within a holobiont metacommunity can potentially shift or drive the evolution of weak cheaters in niche space so that they straddle just enough niche space to both reap the benefits offered by the host-mutualist interaction, and block the reinvasion of mutualist's niche by another cheater strategy. Overall, these results suggest that the metacommunity construct provides a compelling alternative to host selection for explaining the maintenance of (costly) mutualism in competitive microbial communities.