Microbiome diversity promotes the evolution of host selection

Background/Question/Methods

Host-associated microbiomes are characterized by a large diversity of microbial species, many of which are involved in mutualistic interactions with the host organism. This diversity can potentially promote the competitive exclusion of microbial mutualists by non-mutualists (i.e., “cheaters”) that are capable of reaping the benefits of the mutualistic interaction without enduring any of the costs. Active regulation of the microbiome by the host through the selection of mutualists and the imposition of sanctions against cheaters are the main mechanisms assumed to maintain microbial-host mutualisms within holobionts. The question is how such mutualisms can evolve when naïve hosts are unable to initially distinguish between mutualists and cheaters. In systems such as plant roots housing nitrogen-fixing bacteria, modular spatial structure within the host has been suggested as a critical feature enabling the host to target localized microbial colonies dominated by mutualists for rewards and those dominated by cheaters for sanctions. Here we use a mathematical adaptive dynamics approach within a metacommunity framework to study the evolution of host selection strategies and their effects on host-microbial mutualisms.

Results/Conclusions

We demonstrate that the modular spatial structure of the host alone will only allow for the evolution of weak regulation due to the high fitness costs associated with keeping the rapid growth of the cheater in check. However, the presence of numerous non-mutualistic weak cheater strategies in the host microbiome can help drive the evolution of a stronger, more robust host regulation of the microbiome by lowering the fitness costs associated with the imposition of sanctions on more strongly disruptive cheaters. Thus for holobiont species, competition within a diverse microbiome, in addition to a modular spatial structure within the host, may be a necessary requirement for the evolution of host selection and the persistence of mutualism.