Ecological stability masks rapid, convergent evolution within the honey bee worker microbiome

While ecological dynamics within host-associated microbiomes are well-documented, how evolutionary processes unfold within them remains poorly understood. Using longitudinal metagenomics, we quantified ecological and evolutionary dynamics across over 1,000 bacterial genomes from honey bee worker microbiomes sampled across 12 colonies. We show that microbial community composition is strongly tied to colony identity and diverges continuously over time, rather than through discrete seasonal shifts. Despite this ecological turnover, most bacterial populations are stable, harboring extensive genetic variation shaped by strong purifying selection. Against this constrained backdrop, we identify thousands of rapid shifts in allele frequency that cannot be explained by strain replacement, population abundance, or genetic drift. Nonsynonymous variants exhibit localized signatures of selection at neighboring synonymous sites and independently recur within homologous proteins shared by phylogentically distant taxa found across independent colonies. Altogether, our findings demonstrate that ecological persistence can mask rapid evolutionary dynamics, revealing recurrent genetic signatures consistent with adaptive evolution across diverse bacteria.