Conservative character of the germ-line cyst organization within enchytraeids (Annelida: Clitellata) ovary – New proofs based on two Achaeta species

Abstract

Ovaries in a minute and mainly aquatic clitellates, collectively termed microdriles, are usually tiny paired gonads localized, depending on the family/subfamily, in segments VI, XI, XII, or XIII. Sometimes, two pairs of ovaries are present in consecutive segments, or ovaries are unpaired. Usually, accumulating yolk (vitellogenic) oocytes detach from ovaries and float in the coelom cavity. This study presents the microscopical analyses of unpaired ovaries found in two representatives of the genus Achaeta (family Enchytraeidae). The ovary is an inconspicuous organ composed of germ-line cysts uniting early meiotic cells. Cysts comprise 16 synchronously developing cells interconnected via cytoplasmic bridges to the central cytoplasmic mass, termed cytophore. Each interconnected cell has one bridge connecting it to the cytophore. Clustering germ cells are enveloped by elongated somatic cells. The developmental synchrony within cysts is lost when one cell per cyst forms prominent microvilli, gather vast amounts of nutrients (yolk), and becomes an oocyte. The remaining 15 cells do not form microvilli, grow slowly, and are regarded as nurse cells that supply the oocyte with organelles and probably macromolecules. Such cysts detach from the ovary and float freely in the segmental cavity. Nurse cells and vitellogenic oocyte are still connected to the ball-like cytophore. Vitellogenic oocytes gather vast amounts of reserve material, mainly protein spheres. Finally, oocytes lose contact with the cytophore, and nurse cells no longer accompany them. The ovary organization and oogenesis scenario observed in this study are broadly similar to that described for other enchytraeid species, such as Enchytraeus albidus and Grania postclitellochaeta, and have been classified as the “Enchytraeus” type of ovary. The obtained results show that despite the unpaired nature of the Achaeta ovary and some differences in ovary morphology and oogenesis between different enchytraeid taxa, the ovaries of these clitellates are consistently composed of 16-celled germ-line cysts equipped with cytophore. Moreover, the presence of cysts equipped with cytophore in the ovaries of the studied Achaeta specimens provides the subsequent evidence that the formation of such germ-line cysts is a conserved aspect of oogenesis within the Clitellata. This consistency in the ovarian and oogenic patterns underscores the evolutionary conservation of these reproductive traits within the Enchytraeidae and clitellate annelids.