A Bacterium Targets Maternally Inherited Centrosomes to Kill Males in Nasonia

Male killing is caused by diverse microbial taxa in a wide range of arthropods. This phenomenon poses important challenges to understanding the dynamics of sex ratios and host-pathogen interactions. However, the mechanisms of male killing are largely unknown. Evidence from one case in Drosophila suggests that bacteria can target components of the male-specific sex-determination pathway. Here, we investigated male killing by the bacterium Arsenophonus nasoniae in the haplo-diploid wasp Nasonia vitripennis, in which females develop as diploids from fertilized eggs and males develop parthenogenetically as haploids from unfertilized eggs. We found that Arsenophonus inhibits the formation of maternal centrosomes, organelles required specifically for early male embryonic development, resulting in unorganized mitotic spindles and developmental arrest well before the establishment of somatic sexual identity. Consistent with these results, rescue of Arsenophonus-induced male lethality was achieved by fertilization with sperm bearing the supernumerary chromosome paternal sex ratio (PSR), which destroys the paternal genome but bypasses the need for maternal centrosomes by allowing transmission of the sperm-derived centrosome into the egg. These findings reveal a novel mechanism of male killing in Nasonia, demonstrating that bacteria have evolved different mechanisms for inducing male killing in the Arthropods.