Barbronia weberi (Clitellata, Hirudinida, Salifidae) has ovary cords of the Erpobdella type

Abstract

The organization of the ovaries in representative of the Salifidae (Hirudinida, Erpobdelliformes) was studied at the ultrastructural level for the first time. Like in other leeches, the ovaries of Barbronia weberi are composed of an outer envelope (i.e., an ovisac made up of two coelomic epithelia, muscle cells, and connective tissue) and several internal units, which are broadly similar to the ovary cords found in representatives of the Erpobdellidae. There are usually 6-8 ovary cords that are twisted or cambered with a narrow apical part and a broader, irregularly shaped distal end in each ovisac of B. weberi. Each ovary cord is built from somatic and germ-line cells and the latter tend to form multicellular cysts that are equipped with a central cytoplasmic core (cytophore). There are two morphologically different subpopulations of germ-line cells: oocytes and more numerous nurse cells. Growing oocytes form protuberances on the ovary cord surface and eventually detach from the cord and float freely in the ovisac lumen, whereas the other components of germ-line cysts (i.e., nurse cells and cytophore) degenerate. It should be pointed out that there is a prominent gradient of germ-cell development along the long axis of the cord. The somatic cells form the ovary cord envelope (the so-called spongiosa cells) and also penetrate the spaces between germ-line cells. Both kinds of the somatic cells, that is, those forming the cord envelope and the somatic cells that are associated with oocytes (follicular cells) have a well-developed system of intercellular channels. Additionally, one prominent somatic cell, the apical cell, was found at the apical tip of each ovary cord. Because the aforementioned features of ovary cords found in B. weberi are very similar (with a few minor exceptions) to the ovary cords that have been described in Erpobdella octoculata and E. johanssoni, we propose the term "ovary cords of the Erpobdella type" for them. Our results support a close phylogenetic relationship between Salifidae and Erpobdellidae.

Description of ovary organization and oogenesis in a phreodrilid clitellate

“…We summarize that Insulodrilus bifidus possess female germ‐line cysts of the same composition and form as others clitellate annelids, that is, each germ line cell has one RC connecting it with the central cytophore and the fate of interconnected cell are different, that is, the majority function as NCs and only one or sometimes more become oocytes. To date, germline cysts have been described in numerous clitellates, including several families of leeches including Glossiphoniidae (Aisenstadt, ; Damas, ; Świątek, ), Hirudinidae and Haemopidae (Świątek, ; Ben Ahmed, Fuchs, Tekaya, Harrath & Świątek, ), Erpobdellidae (Świątek, Krok & Bielecki, ) and Salifidae (Urbisz, Lai, & Świątek, ) and microdrile taxa such as Lumbriculidae (Urbisz & Świątek, ), Tubificinae (Urbisz, Krodkiewska & Świątek, ; Urbisz, Chajec & Świątek, ), Limnodriloidinae (Urbisz, Chajec, Ito & Ito, ), Enchytraeidae (Paschma, ; Dumont, ; Urbisz et al, ), Naidinae (Gorgoń, Wardas, Krodkiewska & Świątek, ) and Propappidae (Gorgoń, Krodkiewska & Świątek, ). Moreover, cysts equipped with a cytophore have been noticed in such earthworms as Eisenia foetida (Chapron & Relexans, ) and Dendrobaena veneta (Siekierska, ).…”

“…Salifidae (Urbisz, Lai, & Świątek, 2014) and microdrile taxa such as Lumbriculidae (Urbisz & Świątek, 2013), Tubificinae (Urbisz, Krodkiewska & Świątek, 2010;Urbisz, Chajec & Świątek, 2015), Limnodriloidinae (Urbisz, Chajec, Ito & Ito, 2018), Enchytraeidae (Paschma, 1962;Dumont, 1969;Urbisz et al, 2017), Naidinae (Gorgo n, Wardas, Krodkiewska & Świątek, 2017) and Propappidae (Gorgo n, Krodkiewska & Świątek, 2015). Moreover, cysts equipped with a cytophore have been noticed in such earthworms as Eisenia foetida (Chapron & Relexans, 1971) and Dendrobaena veneta (Siekierska, 2003).…”

The Ovary of Tubifex tubifex (Clitellata, Naididae, Tubificinae) Is Composed of One, Huge Germ-Line Cyst that Is Enriched with Cytoskeletal Components

“…Studies of ovary organization and oogenesis in clitellate annelids have shown that the formation of germ-line cysts is a conserved phase of gametogenesis. In all of the clitellate annelids that have been studied to date, as a rule, each germ cell is connected to the common cytoplasmic mass (cytophore) by only one stable cytoplasmic bridge [ 24 – 28 , 30 , 31 , 33 – 38 ]. Despite that general rule, the cyst morphology varies substantially between different clitellate taxa with respect to the number of germ cells, the level of cytophore development and the ratio of nurse cells to oocytes.…”

“…Despite that general rule, the cyst morphology varies substantially between different clitellate taxa with respect to the number of germ cells, the level of cytophore development and the ratio of nurse cells to oocytes. In the majority of clitellate annelids (Tubificinae, Lumbricida, Lumbriculida, Branchiobdellida, Acanthobdellida, Glossiphoniidae, Erpobdelliformes and Hirudiniformes) ovaries are composed of irregularly shaped and multicellular cysts, however, the exact number of cysts in an ovary and germ-cells in a cyst has not yet been determined [ 24 – 26 , 28 , 31 , 35 , 37 , 38 ]. In contrast, spherical cysts that are composed of a low number of cells occur only in the whiteworm Enchytraeus albidus (Enchytraeidae) and in fish leeches (Piscicolidae) (see Table 2 ) ([ 33 , 34 , 39 ], our unpublished results).…”

“…Recently, the gross morphology of the female germ-cell cysts in some clitellate annelids has been described in several taxa e.g., in leeches [ 26 , 28 ], and in oligochaetous clitellates [ 27 , 31 ]. These studies revealed that there is a great deal of variety in the cyst morphology in these animals (for more details see Discussion , [ 32 ] and references herein).…”