Rapid molecular evolution ofSpiroplasmasymbionts ofDrosophila

Spiroplasmaare a group of Mollicutes whose members include plant pathogens, insect pathogens, and endosymbionts of animals.Spiroplasmaphenotypes have been repeatedly observed to be spontaneously lost inDrosophilacultures, and several studies have documented a high genomic turnover inSpiroplasmasymbionts and plant pathogens. These observations suggest thatSpiroplasmaevolves quickly in comparison to other insect symbionts. Here, we systematically assess evolutionary rates and patterns ofSpiroplasma poulsonii, a natural symbiont ofDrosophila. We analysed genomic evolution ofsHy within flies, andsMel withinin vitroculture over several years. We observed thatS. poulsoniisubstitution 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 locimutSandmutLis conserved acrossSpiroplasmaand likely contributes to elevated substitution rates. Further, the closely related strainssMel andsHy (>99.5% sequence identity in shared loci) show extensive structural genomic differences, which potentially indicates a higher degree of host adaptation insHy, a protective symbiont ofDrosophila hydei. Finally, comparison across diverseSpiroplasmalineages confirms previous reports of dynamic evolution of toxins, and identifies loci similar to the male-killing toxin Spaid in severalSpiroplasmalineages and other endosymbionts. Overall, our results highlight the peculiar nature ofSpiroplasmagenome evolution, which may explain unusual features of its evolutionary ecology.