Ovaries of Tubificinae (Clitellata, Naididae) resemble ovary cords found in Hirudinea (Clitellata)

Abstract

The ultrastructure of the ovaries and oogenesis was studied in three species of three genera of Tubificinae. The paired ovaries are small, conically shaped structures, connected to the intersegmental septum between segments X and XI by their narrow end. The ovaries are composed of syncytial cysts of germ cells interconnected by stable cytoplasmic bridges (ring canals) and surrounded by follicular cells. The architecture of the germ-line cysts is exactly the same as in all clitellate annelids studied to date, i.e. each cell in a cyst has only one ring canal connecting it to the central, anuclear cytoplasmic mass, the cytophore. The ovaries found in all of the species studied seem to be meroistic, i.e. the ultimate fate of germ cells within a cyst is different, and the majority of cells withdraw from meiosis and become nurse cells; the rest continue meiosis, gather macromolecules, cell organelles and storage material, and become oocytes. The ovaries are polarized; their narrow end contains mitotically dividing oogonia and germ cells entering the meiosis prophase; whereas within the middle and basal parts, nurse cells, a prominent cytophore and growing oocytes occur. During late previtellogenesis/early vitellogenesis, the oocytes detach from the cytophore and float in the coelom; they are usually enveloped by the peritoneal epithelium and associated with blood vessels. Generally, the organization of ovaries in all of the Tubificinae species studied resembles the polarized ovary cords found within the ovisacs of some Euhirudinea. The organization of ovaries and the course of oogenesis between the genera studied and other clitellate annelids are compared. Finally, it is suggested that germ-line cysts formation and the meroistic mode of oogenesis may be a primary character for all Clitellata.

An ultrastructural study of the ovary cord organization and oogenesis in Erpobdella johanssoni (Annelida, Clitellata: Hirudinida)

“…In this section, we concentrate on the details of the ovary cord composition and oogenesis in arhynchobdellid leeches (Table 1). A comparison between all of the groups of clitellate annelids studied to date was presented recently (Urbisz et al, 2010). As is summarized in Table 1, the general organization of ovaries and oogenesis in the arhynchobdellid leeches studied to date is similar; however, there are several differences.…”

“…These cysts have a characteristic spatial arrangement; each germ cell in a given cyst has only one RC connecting it to a common anuclear cytoplasmic mass -the cytophore. Numerous studies have shown that the formation of germline cysts with a central cytophore is a conserved phase of gametogenesis in Clitellata (Fernández et al, 1992;Ferraguti, 1999;Jamieson, 2006;Krüger et al, 2008;Spałek-Wołczyńska et al, 2008;Swiątek, 2005bSwiątek, , 2008Świątek et al, 2009Ben Ahmed et al, 2010) and should be regarded as a primary condition (Urbisz et al, 2010;Świątek et al, 2012). Similar germline cysts with a central cytoplasmic mass have been found during gametogenesis in some Polychaeta, Plathyhelmintes and Nematoda (Sawada, 1975;Hirsh et al, 1976;Foor, 1983;Gibert et al, 1984;Sopott-Ehlers, 1989).…”

“…These studies, and ovary analyses in other, non-leech Clitellata (Paschma, 1962;Dumont, 1969;Relaxans, 1971a, 1971b;Siekierska, 2003;Urbisz et al, 2010;Świątek et al, 2012) have shown that in clitellate annelids the ovaries are made up of germline cysts (clones, nests, clusters) of the conserved pattern of the organization associated with somatic cells. In all of the clitellate species studied to date, the germline cysts are composed of numerous cells, and as a rule, each one is connected to the central, anuclear cytoplasmic mass, termed the cytophore, via only one stable cytoplasmic bridge (ring canal, RC).…”

“…Usually all germ cells in a cyst (cystocytes) enter meiosis; however, only a few continue meiosis and become egg cells. The rest withdraw from meiosis and are regarded as nurse cells (Fernández et al, 1992;Świątek, 2005b, 2008Spałek-Wołczyńska et al, 2008;Ben Ahmed et al, 2010;Urbisz et al, 2010;Swiątek et al, 2012). The presence of two cell categories (nurse cell and oocytes) suggests ovary meroism in Clitellata; however, to date there has been only one experimental study showing the transport of macromolecules from nurse cells via the cytophore towards the growing oocytes (Aisenstadt et al, 1967).…”

“…The presence of two cell categories (nurse cell and oocytes) suggests ovary meroism in Clitellata; however, to date there has been only one experimental study showing the transport of macromolecules from nurse cells via the cytophore towards the growing oocytes (Aisenstadt et al, 1967). Despite the conserved pattern of the germline cysts architecture, the ovary morphology differs markedly in different clitellate taxa (for details, seeŚwiątek, 2008; Urbisz et al, 2010;Świątek et al, 2012).…”