Paternal chromosome segregation during the first mitotic division determines Wolbachia-induced cytoplasmic incompatibility phenotype

The most common Wolbachia-induced phenotype in insects is cytoplasmic incompatibility (CI), which occurs when sperm from infected males fertilize eggs from uninfected females. CI produces distinct phenotypes in three closely related haplo-diploid species of the genus Nasonia: mortality in N. longicornis and N. giraulti, and conversion to male development in N. vitripennis. We demonstrate that the majority of CI-induced mortality occurs during embryogenesis and that the pattern of paternal chromosome segregation during the first mitosis is a good predictor of CI phenotype. In N. giraulti and N. longicornis, the paternal chromosomes mis-segregate, producing abnormal nuclei connected by chromatin bridges. Consequently, these embryos arrest development with very few and abnormal nuclei. In contrast, the paternal genome in N. vitripennis is either not segregated or mis-segregates to one of the two daughter nuclei. Consequently, these embryos continue development utilizing the maternally derived haploid nuclei, resulting in male offspring. The latter class is the first documented example of asymmetric mitotic segregation of abnormal chromosomes. We conclude that in haplo-diploids, CI-induced embryonic lethality occurs only when abnormal paternal genome segregation affects both products of the first mitotic division. This is the first study to associate differences in types of CI with specific cytological defects.