The Origin of Centrosomes in Parthenogenetic Hymenopteran Insects

A longstanding enigma has been the origin of maternal centrosomes that facilitate parthenogenetic development in Hymenopteran insects. In young embryos, hundreds of microtubule-organizing centers (MTOCs) are assembled completely from maternal components. Two of these MTOCs join the female pronucleus to set up the first mitotic spindle in unfertilized embryos and drive their development. These MTOCs appear to be canonical centrosomes because they contain gamma-tubulin, CP190, and centrioles and they undergo duplication. Here, we present evidence that these centrosomes originate from accessory nuclei (AN), organelles derived from the oocyte nuclear envelope. In the parasitic wasps Nasonia vitripennis and Muscidifurax uniraptor, the position and number of AN in mature oocytes correspond to the position and number of maternal centrosomes in early embryos. These AN also contain high concentrations of gamma-tubulin. In the honeybee, Apis mellifera, distinct gamma-tubulin foci are present in each AN. Additionally, the Hymenopteran homolog of the Drosophila centrosomal protein Dgrip84 localizes on the outer surfaces of AN. These organelles disintegrate in the late oocyte, leaving behind small gamma-tubulin foci, which likely seed the formation of maternal centrosomes. Accessory nuclei, therefore, may have played a significant role in the evolution of haplodiploidy in Hymenopteran insects.