Complex adaptive architectures constrain the pace of adaptations sweeping across human gut microbiomes

Recent work has shown that commensal gut bacteria can evolve rapidly within hosts on short timescales of days to months, fueled by the enormous mutational input generated daily in the microbiome. Yet how rapidly adaptations spread across gut microbiomes of different hosts remains unclear. We address this question by estimating the number of independent origins of gene-specific sweeps spreading via recombination across bacterial populations. Multiple origins (soft sweeps) indicate that adaptive mutations arise rapidly whereas one origin (hard sweeps) indicate slower mutational input. Contrary to expectations of rapid adaptation, we find that many gene-specific sweeps have only one or a few origins. We show that this requires that sweeps arise from adaptive mutation rates orders of magnitude lower than single base pair mutation rates. This implies that gene-specific sweeps bear difficult-to-mutate complex adaptations such as structural or epistatic variants. Consistent with this interpretation, we find that identified sweep regions exhibit patterns of nucleotide diversity and linkage disequilibrium inconsistent with a single adaptive mutation rising to high frequency. We conclude that recombination across human gut microbiomes enables the spread of adaptations with complex genetic architectures that otherwise would require a long waiting time to generate de novo within an individual host.