Wolbachia-induced delay of paternal chromatin condensation does not prevent maternal chromosomes from entering anaphase in incompatible crosses of Drosophila simulans

Abstract

The behavior of parental chromosomes during the first mitosis of Drosophila simulans zygotes obtained from unidirectional incompatible crosses is described and it is demonstrated that the condensation of parental chromatin complements was asynchronous. The timing of paternal chromatin condensation appeared to be delayed in these embryos, so that condensed maternal chromosomes and entangled prophase-like paternal fibers congressed in the equatorial plane of the first metaphase spindle. At anaphase the maternal chromosomes migrated to opposite poles of the spindle, whereas the paternal chromatin lagged in the midzone of the spindle. This resulted in dramatic errors in paternal chromatin inheritance leading to the formation of embryos with aneuploid or haploid nuclei. These observations suggest that the anaphase onset of maternal chromosomes is unaffected by the improper alignment of the paternal complement. Since the first metaphase spindle of the Drosophila zygote consists of twin bundles of microtubules each holding one parental complement, we suspect that each half spindle regulates the timing of anaphase onset of its own chromosome set. In normal developing embryos, the fidelity of chromosome transmission is presumably ensured by the relative timing required to prepare parental complements for the orderly segregation that occurs during the metaphase-anaphase transition.