Explaining the microbial diversity conundrum: can microbiome composition be crucial for host fitness, while highly divergent among healthy individuals?

Abstract

Recent empirical studies offer conflicting findings regarding the relation between host fitness and the composition of its microbiome, a conflict which we term the microbial {beta} - diversity conundrum: it has been shown that the microbiome is crucial for host wellbeing and survival. At the same time, different healthy individuals microbiome compositions, even in the same population, often differ dramatically, contrary to the notion that a vital trait should be highly conserved. Moreover, gnotobiotic individuals exhibit highly deleterious phenotypes, supporting the notion that the microbiome is paramount to host fitness. However, the introduction of almost arbitrarily selected microbiota into the system often achieves a significant rescue effect of the deleterious phenotypes, even microbiota from soil or phylogenetically distant host species, highlighting an apparent paradox. Here we suggest several solutions to the paradox using a computational framework, simulating the population dynamics of hosts and their microbiomes over multiple generations. The answers, relating to factors such as host population size, the specific mode of contribution of the microbes to host fitness, and the typical microbiome richness, offer solutions to the conundrum by creating scenarios where even when a hosts fitness is determined in full by its microbiome composition, this composition has little or no effect on the natural selection dynamics of the population.