The current study focuses on a symbiotic bacterium found in the slender pigeon louse, Columbicola columbae (Insecta: Phthiraptera). Molecular phylogenetic analyses indicated that the symbiont belongs to the gamma subdivision of the class Proteobacteria and is allied to Sodalis glossinidius, the secondary symbiont of tsetse flies (Glossina spp.) and also to the primary symbiont of grain weevils (Sitophilus spp.). Relative-rate tests revealed that the symbiont of C. columbae exhibits accelerated molecular evolution in comparison with the tsetse fly symbiont and the weevil symbiont. Whole-mount in situ hybridization was used to localize the symbiont and determine infection dynamics during host development. In first- and second-instar nymphs, the symbionts were localized in the cytoplasm of oval bacteriocytes that formed small aggregates on both sides of the body cavity. In third-instar nymphs, the bacteriocytes migrated to the central body and were finally located in the anterior region of the lateral oviducts, forming conspicuous tissue formations called ovarial ampullae. In adult females, the symbionts were transmitted from the ovarial ampullae to developing oocytes in the ovarioles. In adult males, the bacteriocytes often disappeared without migration. A diagnostic PCR survey of insects collected from Japan, the United States, Australia, and Argentina detected 96.5% (109/113) infection, with a few uninfected male insects. This study provides the first microbial characterization of a bacteriocyte-associated symbiont from a chewing louse. Possible biological roles of the symbiont are discussed in relation to the host nutritional physiology associated with the feather-feeding lifestyle.
