Oogenesis in three species of Naidinae (Annelida, Clitellata) is extraovarian of the Stylaria type

Older observations, which were based solely on light microscopy, suggested that the main stages of oogenesis such as yolk uptake, take place outside the ovary, i.e. in the body or the ovisac cavity in some groups of clitellate annelids. Such extraovarian oogenesis was observed in naidines (Naidinae). Because there are no current data about the ovary organization and the course of oogenesis in Naidinae, we analyzed female gametogenesis in three common representatives of this taxon - Stylaria lacustris, Chaetogaster diaphanus and Ripistes parasita - using light, fluorescent and transmission electron microscopy. We found paired and inconspicuous ovaries only in S. lacustris. These ovaries were made up of four to five syncytial cysts that are composed of oogonia and germ cells, which are synchronously entering meiotic prophase I. The cysts were enveloped by thin somatic cells. No growing oocytes were observed within the ovaries. However, as many as five freely floating germ-line cysts, each clustering about 30 germ cells surrounded by flat somatic cells, were observed within the ovisacs in all three of the species studied. The germ-line cysts that were found in all of the naidines studied had an architecture that is typical for clitellate annelids, i.e. each germ cell was connected to a common and anuclear cytoplasmic mass, the cytophore, via one intercellular bridge. Within these cysts, two morphologically different categories of germ cells arose. One cell usually continued meiosis, gathered nutrients and became the oocyte, whereas the rest of cells did not continue meiosis and did not gather a yolk - these cells appear to supply the oocyte with cytoplasm and cell organelles and are regarded as nurse cells. Generally, as in other microdriles, the species studied produced large, yolky oocytes. The details of oogenesis and oocyte organization are similar to other oligochaetous clitellates that have been studied. Interestingly, peculiar organelles, which are called accessory nuclei, have been found within the perinuclear cytoplasm of Ch. diaphanus vitellogenic oocytes. However, their molecular composition, functions and fate are unknown. The results obtained unequivocally show that in the naidines studied, the majority of oogenesis takes place outside the ovary, i.e. most of oogenesis is extraovarian. For comparative purposes, we propose the term “an ovary of the Stylaria type” to describe the type of extraovarian oogenesis in which polarized germ-line cysts develop freely within the ovisac cavity.