UC Santa Cruz

A broad array of endosymbionts ensure their spread through host populations via vertical transmission, yet much remains unknown concerning the type and number of cellular mechanisms underlying reliable transmission. Wolbachia are the most common endosymbionts in nature, but their prevalence varies greatly in host populations due to imperfect transmission. To better understand the cellular basis of Wolbachia transmission, this project explored the cellular distributions of Wolbachia diverged up to 40 million years in the oocytes of 18 divergent Drosophila species. This analysis revealed three cellular distributions: 1) a tight clustering of Wolbachia at the posterior pole plasm (the site of germline formation); 2) a concentration at the posterior pole plasm, but with a significant population of Wolbachia distributed throughout the oocyte; 3) and a distribution of Wolbachia throughout the oocyte, with none or very few located at the posterior pole plasm. Examination of this latter class reveal Wolbachia access the posterior pole plasm during the interval between late oogenesis and the blastoderm formation. Wolbachia in this class concentrate in the posterior somatic follicle cells that encompass the pole plasm of the developing oocyte suggesting these are the source of that ultimately occupy the germline. In contrast, strains in which Wolbachia concentrate in the posterior pole plasm, no or few Wolbachia are found in the follicle cells associated with the pole plasm. Phylogenomic analysis indicates that closely related Wolbachia tend to exhibit similar patterns of posterior localization, suggesting that diverse localization strategies are a function of Wolbachia-associated factors. Previous studies revealed that endosymbionts rely on one of two distinct routes of vertical transmission: continuous maintenance in the germline (germline-to-germline) and a more circuitous route via the soma (germline-to-soma-to-germline). This work demonstrates that Wolbachia maintains the diverse arrays of cellular mechanisms necessary for both of these distinct transmission routes. This characteristic may account for its ability to infect and spread globally through a vast range of host insect species.