Microorganization of ovaries and oogenesis of Haplotaxis sp. (Clitellata: Haplotaxidae)

Abstract

Ovaries of Haplotaxis sp. were studied in active and nonactive states, that is, in a sexually mature specimen and in specimens outside of the reproductive period. Two pairs of ovaries were found in segments XI and XII. Especially in the nonactive state, they were in close contact with copulatory glands. Each ovary was composed of germ cells interconnected with syncytial cysts, which were enveloped by a layer of somatic cells. Within cysts each germ cell had one ring canal connecting it to the common anuclear cytoplasmic mass called a cytophore. During oogenesis clustering germ cells differentiated into nurse cells and oocytes; thus, the oogenesis was recognized as meroistic. Vitellogenic oocytes were detached from the ovaries and continued yolk absorption within the body cavity. Because recent studies have shown the variety of ovaries and germ line cyst organization in clitellates and suggest their evolutionary conservatism at the family or subfamily level, the data presented here can be valid in understanding the phylogenetic relationships among Clitellata. In this context, ovaries found in Haplotaxis sp. resembled those of the "Tubifex" type. "Tubifex" ovaries are characteristic for numerous microdrile taxa (tubificines, limnodriloidines, propappids, lumbriculids, and leech-like branchiobdellids) and can be regarded as the primary character for these Clitellata in which germ-line cysts are formed during early oogenesis. As the family Haplotaxidae is currently considered to be paraphyletic and the species studied here belongs to Haplotaxidae sensu stricto, our results support the close relationship of Haplotaxidae sensu stricto to the clade consisting of Lumbriculidae, Branchiobdellida, and Hirudinida, in which lumbriculids are sister to the latter two.

Ovary micromorphology and oogenesis in a rhyacodriline oligochaete (Clitellata: Naididae, Rhyacodrilinae)

“…Concerning the cytological aspects of oogenesis that have been described in P. montanus , they are in line with the descriptions of this process in other microdriles (reviewed in Jamieson, 1981, 1992; and discussed recently in Gorgoń et al, 2017; Świątek et al, 2020; Urbisz et al, 2017; Urbisz et al, 2021). Briefly, similar to other microdriles, P. montanus produces yolk‐rich oocytes, and the yolk is mainly gathered due to heterosynthesis (the intensive absorption of the yolk precursors during vitellogenesis).…”

“…These ovaries are called the “Tubifex” type and were described in taxa such as Tubificinae, Limnodriloidinae, Propappidae, Lumbriculidae and Haplotaxidae ( Haplotaxis sp .) (Świątek & Urbisz, 2019; Urbisz et al, 2021). The germ‐line cysts interconnect a relatively small number of cells (from 16 to 32), which are initially at the same developmental stage, that is, the cells develop synchronously within a given cyst until the oocytes and NCs appear, but the ovaries are composed of a dozen or so small cysts; the ovaries are usually inconspicuous and conically shaped.…”

“…However, there are substantial differences between the taxa in the detailed cyst organization that determine the ovary structure and functioning. In order to avoid a too detailed discussion, we only concentrated on the microdriles, for more details of the ovary organization in the leech‐like taxa and earthworms, see Świątek and Urbisz (2019), Świątek et al (2020) and Urbisz et al (2021). Generally, three kinds of ovary organization can be observed among the microdriles (reviewed in detail in Świątek & Urbisz, 2019): No germ‐line cysts, the ovary has a chain‐like form with gradually developing oocytes, the so‐called “Capilloventer” ovary type (Świątek et al, 2016).…”

“…During the last 20 years, our knowledge about the organization of the ovaries and oogenesis in annelid clitellates has increased considerably. Special attention has been paid to leeches (Hirudinida) and their allies (Acanthobdellida, Branchiobdellida) and certain taxa of microdrile clitellates, for example, Capilloventridae, Phreodrilidae, Enchytraeidae, Propappidae, Lumbriculidae, Naididae and Haplotaxidae (summarized in Świątek & Urbisz, 2019; Urbisz et al, 2021). Together with older descriptions (reviewed in Świątek & Urbisz, 2019), these studies showed that the ovaries of clitellate annelids are composed of germ cells that are joined into syncytial cysts that are enveloped by thin somatic cells.…”

“…In Naidinae, the ovaries are inconspicuous and are composed of four to five cysts, which unite about 30 cells each (Gorgoń et al, 2017). Moreover, oocytes can be retained within the ovary until the beginning of the yolk absorption phase (vitellogenesis), and then they can detach from the ovary and finalize the yolk accumulation in the coelom as in Tubificinae, Enchytraeidae and Haplotaxidae (Urbisz et al, 2010; Urbisz et al, 2017; Urbisz et al, 2021). Alternatively, whole germ‐line cysts can detach from the ovaries before the growth phase (i.e., in previtellogenesis), and then oogenesis occurs in the coelom as was found in Naidinae (the so‐called extraovarian oogenesis, Gorgoń et al, 2017).…”