Evolutionary dynamics of bacteria in the gut microbiome within and across hosts

TLDR

Gut microbiota are shaped by ecological and evolutionary forces, yet the evolutionary dynamics of gut bacteria over time remain poorly understood. The authors introduce a model‑based framework that quantifies evolutionary dynamics within and across hosts using panels of metagenomic samples. They apply this framework to study evolution in approximately 40 prevalent human gut species. Between‑host diversity follows quasi‑sexual evolution and purifying selection, but novel genealogical patterns show that within‑host bacterial evolution is dominated by rapid sweeps of few mutations or gene changes—some recombination‑seeded—while over decades replacement by unrelated strains prevails, demonstrating that gut bacteria adapt on human‑relevant timescales and linking short‑term dynamics to long‑term evolution.

Abstract

Gut microbiota are shaped by a combination of ecological and evolutionary forces. While the ecological dynamics have been extensively studied, much less is known about how species of gut bacteria evolve over time. Here, we introduce a model-based framework for quantifying evolutionary dynamics within and across hosts using a panel of metagenomic samples. We use this approach to study evolution in approximately 40 prevalent species in the human gut. Although the patterns of between-host diversity are consistent with quasi-sexual evolution and purifying selection on long timescales, we identify new genealogical signatures that challenge standard population genetic models of these processes. Within hosts, we find that genetic differences that accumulate over 6-month timescales are only rarely attributable to replacement by distantly related strains. Instead, the resident strains more commonly acquire a smaller number of putative evolutionary changes, in which nucleotide variants or gene gains or losses rapidly sweep to high frequency. By comparing these mutations with the typical between-host differences, we find evidence that some sweeps may be seeded by recombination, in addition to new mutations. However, comparisons of adult twins suggest that replacement eventually overwhelms evolution over multi-decade timescales, hinting at fundamental limits to the extent of local adaptation. Together, our results suggest that gut bacteria can evolve on human-relevant timescales, and they highlight the connections between these short-term evolutionary dynamics and longer-term evolution across hosts.