Rapid Molecular Evolution of Symbionts of

is a genus of whose members include plant pathogens, insect pathogens and endosymbionts of animals. phenotypes have been repeatedly observed to be spontaneously lost in cultures, and several studies have documented a high genomic turnover in symbionts and plant pathogens. These observations suggest that evolves quickly in comparison to other insect symbionts. Here, we systematically assess evolutionary rates and patterns of , a natural symbiont of . We analysed genomic evolution of Hy within flies, and Mel within culture over several years. We observed that substitution rates are among the highest reported for any bacteria, and around two orders of magnitude higher compared with other inherited arthropod endosymbionts. The absence of mismatch repair loci and is conserved across , and likely contributes to elevated substitution rates. Further, the closely related strains Mel and Hy (>99.5 % sequence identity in shared loci) show extensive structural genomic differences, which potentially indicates a higher degree of host adaptation in Hy, a protective symbiont of . Finally, comparison across diverse lineages confirms previous reports of dynamic evolution of toxins, and identifies loci similar to the male-killing toxin Spaid in several lineages and other endosymbionts. Overall, our results highlight the peculiar nature of genome evolution, which may explain unusual features of its evolutionary ecology.