Comparative organization of follicle, accessory cells and spawning anlagen in dynamic semelparous clutch manipulators, the urochordate Oikopleuridae

Abstract

The urochordate appendicularians play a key trophic role in marine ecosystems and are the second largest component of zooplankton after copepods. Part of their success is due to their ability to undergo rapid population blooms in response to changes in primary productivity. Nonetheless, the reproductive biology of this important group remains poorly understood. In the present study, we investigated the organization of male and female germ and accessory somatic cells in the Oikopleuridae. We found that the structure of the ovary had been previously misconstrued as consisting of germ and accessory 'cells' interspersed together, whereas, in fact, the germline exists as a giant transparent syncytium. Somatic follicle cells, integral to regulation of the temporal progression of gametogenesis, could be classified into three types in females and two in males, and we characterized functional gap junctions between follicle cells and the germline syncytium in both sexes. The number of follicle cells per oocyte produced was much reduced in comparison with many commonly studied model organisms. We further identified a novel anlagen that permits spawning of the animal via rupture of the gonad wall, which is obligatory for the release of oocytes, but optional for the release of sperm that usually occurs via the spermiduct. The organization of the female germline in the Oikopleuridae shares some features of meroistic oogenesis with the arthropod Drosophila, but the process of synchronous oogenesis in these semelparous organisms remains quite distinctive with respect to that previously characterized in the animal kingdom and certainly within the chordate phylum.