The Evolution of Mutualism in Gut Microbiota Via Host Epithelial Selection

Abstract

The human gut harbours a large and genetically diverse population of symbiotic microbes that both feed and protect the host. Evolutionary theory, however, predicts that such genetic diversity can destabilise mutualistic partnerships. How then can the mutualism of the human microbiota be explained? Here we develop an individual-based model of host-associated microbial communities. We first demonstrate the fundamental problem faced by a host: The presence of a genetically diverse microbiota leads to the dominance of the fastest growing microbes instead of the microbes that are most beneficial to the host. We next investigate the potential for host secretions to influence the microbiota. This reveals that the epithelium-microbiota interface acts as a selectivity amplifier: Modest amounts of moderately selective epithelial secretions cause a complete shift in the strains growing at the epithelial surface. This occurs because of the physical structure of the epithelium-microbiota interface: Epithelial secretions have effects that permeate upwards through the whole microbial community, while lumen compounds preferentially affect cells that are soon to slough off. Finally, our model predicts that while antimicrobial secretion can promote host epithelial selection, epithelial nutrient secretion will often be key to host selection. Our findings are consistent with a growing number of empirical papers that indicate an influence of host factors upon microbiota, including growth-promoting glycoconjugates. We argue that host selection is likely to be a key mechanism in the stabilisation of the mutualism between a host and its microbiota. © 2012 Schluter, Foster.