Gene-specific selective sweeps are pervasive across human gut microbiomes

The human gut microbiome is composed of a highly diverse consortia of
species that are continually evolving within and across hosts. The ability
to identify adaptations common to many human gut microbiomes would not
only reveal shared selection pressures across hosts, but also key drivers
of functional differentiation of the microbiome that may affect community
structure and host traits. However, the extent to which adaptations have
spread across human gut microbiomes is relatively unknown. Here, we
develop a novel selection scan statistic named the integrated Linkage
Disequilibrium Score (iLDS) that can detect sweeps of adaptive alleles
spreading across host microbiomes via migration and horizontal gene
transfer. Specifically, iLDS leverages signals of hitchhiking of
deleterious variants with a beneficial variant. Application of the
statistic to ~30 of the most prevalent commensal gut species from 24 human
populations around the world revealed more than 300 selective sweeps
across species. We find an enrichment for selective sweeps at loci
involved in carbohydrate metabolism, indicative of adaptation to host
diet, and we find that the targets of selection significantly differ
between industrialized and non-industrialized populations. One of these
sweeps is at a locus known to be involved in the metabolism of
maltodextrin, a synthetic starch that has recently become a widespread
component of industrialized diets. In summary, our results indicate that
recombination between strains fuels pervasive adaptive evolution among
human gut commensal bacteria, and strongly implicate host diet and
lifestyle as a critical selection pressures.