Wolbachia springs eternal: symbiosis in Collembola is associated with host ecology

Wolbachia are endosymbiotic alpha-proteobacteria infecting a wide range of arthropods and nematode hosts with diverse interactions, from reproductive parasites to obligate mutualists. Their taxonomy is defined by lineages called supergroups (labelled by letters of the alphabet), while their evolutionary history is complex, with multiple horizontal transfers and secondary losses. One of the least recently derived, supergroup E, infects springtails (Collembola), widely distributed hexapods, with sexual and/or parthenogenetic populations depending on species. To better characterize the diversity of Wolbachia infecting springtails, the presence of Wolbachia was screened in 58 species. Eleven (20%) species were found to be positive, with three Wolbachia genotypes identified for the first time in supergroup A. The novel genotypes infect springtails ecologically and biologically different from those infected by supergroup E. To root the Wolbachia phylogeny, rather than distant other Rickettsiales, supergroup L infecting plant-parasitic nematodes was used here. We hypothesize that the ancestor of Wolbachia was consumed by soil-dwelling nematodes, and was transferred horizontally via plants into aphids, which then infected edaphic arthropods (e.g. springtails and oribatid mites) before expanding into most clades of terrestrial arthropods and filarial nematodes.

Automated summary

Wolbachia, an endosymbiotic bacteria, infects diverse arthropods and nematode hosts and has various interactions. The taxonomy of Wolbachia is defined by supergroups, while its evolutionary history involves horizontal transfers and secondary losses. In this study, the diversity of Wolbachia infecting springtails was characterized, and new genotypes were identified. The phylogeny of Wolbachia was rooted using a different group infecting plant-parasitic nematodes. It is hypothesized that the ancestor of Wolbachia was consumed by soil-dwelling nematodes and was then transferred to aphids and subsequently infected edaphic arthropods before expanding to other terrestrial arthropods and filarial nematodes.