DistinctWolbachialocalization patterns in oocytes of diverse host species reveal multiple strategies of maternal transmission

Abstract

A broad array of endosymbionts radiate through host populations via vertical transmission, yet much remains unknown concerning the cellular basis, diversity and routes underlying this transmission strategy. Here we address these issues, by examining the cellular distributions ofWolbachiastrains that diverged up to 50 million years ago in the oocytes of 18 divergentDrosophilaspecies. This analysis revealed threeWolbachiadistribution patterns: 1) a tight clustering at the posterior pole plasm (the site of germline formation); 2) a concentration at the posterior pole plasm, but with a significant bacteria population distributed throughout the oocyte; 3) and a distribution throughout the oocyte, with none or very few located at the posterior pole plasm. Examination of this latter class revealsWolbachiaaccesses the posterior pole plasm during the interval between late oogenesis and the blastoderm formation. We also find that oneWolbachiastrain in this class concentrates in the posterior somatic follicle cells that encompass the pole plasm of the developing oocyte, suggesting these are the source ofWolbachiathat ultimately occupy the germline. In contrast, strains in whichWolbachiaconcentrate at the posterior pole plasm generally exhibit no or fewWolbachiain the follicle cells associated with the pole plasm. Phylogenomic analysis indicates that closely relatedWolbachiastrains tend to exhibit similar patterns of posterior localization, suggesting that specific localization strategies are a function ofWolbachia-associated factors. Previous studies revealed that endosymbionts rely ononeof two distinct routes of vertical transmission: continuous maintenance in the germline (germline-to-germline) or a more circuitous route via the soma (germline-to-soma-to-germline). Here we demonstrate thatWolbachiastrains infectingDrosophilaspecies maintain the diverse arrays of cellular mechanisms necessary forbothof these distinct transmission routes. This characteristic may account for its ability to infect and spread globally through a vast range of host insect species.