Wolbachia action in the sperm produces developmentally deferred chromosome segregation defects during the Drosophila mid-blastula transition

Abstract

Wolbachia, a vertically transmitted endosymbiont infecting many insects, spreads rapidly through uninfected populations by a mechanism known as Cytoplasmic Incompatibility (CI). In CI, embryos from crosses between Wolbachia-infected males and uninfected females fail to develop due to the immediate action of Wolbachia-produced factors in the first zygotic division. In contrast, viable progeny are produced when the female parent is infected. Here, we find [~]1/3 of embryos from CI crosses in Drosophila simulans develop normally beyond the first and subsequent pre-blastoderm divisions. Developing CI-derived embryos then exhibit chromosome segregation errors during the mid-blastula transition and gastrulation. Single embryo PCR and whole genome sequencing reveal a large percentage of the developed CI-derived embryos bypass the first division defect. Using fluorescence in situ hybridization, we find increased chromosome segregation errors in gastrulating CI-derived embryos that had avoided the first division defect. Thus, Wolbachia in the sperm induces independent immediate and developmentally deferred defects. Like the initial immediate defect, the delayed defect is rescued through crosses to infected females.