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Spiroplasma(classMollicutes) is a diverse wall-less bacterial genus whose members are strictly dependent on eukaryotic hosts (mostly arthropods and plants), with which they engage in pathogenic to mutualistic interactions.Spiroplasmaare generally fastidious to culturein vitro, especially those that are vertically transmitted by their hosts, which include flies in the genusDrosophila.Drosophilahas been invaded by at least three independent clades ofSpiroplasma: Poulsonii (the best studied, contains reproductive manipulators and defensive mutualists associated with two major clades ofDrosophilaand has amongst the highest substitution rates within bacteria), Citri (restricted to therepletagroup ofDrosophila) and Ixodetis. We report the first genome drafts ofDrosophila-associated Citri cladeSpiroplasma: strainsMoj fromDrosophila mojavensis, strainsAld-Tx fromDrosophila aldrichifrom Texas (newly discovered; also associated withDrosophila mulleri) and strainsHy2 fromDrosophila hydei(the onlyDrosophilaspecies known to naturally also harbour a Poulsonii clade strain, thereby providing an arena for horizontal gene transfer). Compared to their Poulsonii clade counterparts, we infer that the three Citri clade strains have the following: (1) equal or worse DNA repair abilities; (b) more limited metabolic capacities, which may underlie their comparatively lower titres and transmission efficiency; and (c) similar content of toxin domains, including at least one ribosome-inactivating protein, which is implicated in the Poulsonii-conferred defence against natural enemies. As a byproduct of our phylogenomic analyses and exhaustive search for certain toxin domains in public databases, we document the toxin repertoire in close relatives ofDrosophila-associatedSpiroplasma, and in a very divergent newly discovered lineage (i.e. ‘clade X’). Phylogenies of toxin-encoding genes or domains imply substantial exchanges between closely and distantly related strains. Surprisingly, despite encoding several toxin genes and achieving relatively high prevalences in certain natural populations (sAld-Tx in this study;sMoj in prior work), fitness assays ofsMoj (this study) andsAld-Tx (prior work) in the context of wasp parasitism fail to detect a beneficial effect to their hosts. Thus, how Citri clade strains persist in theirDrosophilahost populations remains elusive.