Architecture and Life History of Female Germ-Line Cysts in Clitellate Annelids

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Phreodrilidae is a small family uniting about 50 species of minute freshwater clitellate annelids inhabiting mainly the Southern hemisphere. Other than the male and spermathecal genitalia, their internal organization is poorly known. Here, we present results of our study of the ovaries and oogenesis in Insulodrilus bifidus, a phreodrilid from Western Australia using light and electron microscopy. The ovaries are paired and located in segment XII. They are inconspicuous and composed of several (10–12) spherical germ‐line cysts loosely interconnected by flattened somatic cells. The cysts usually comprise 32 germ cells and each cell is connected via a cytoplasmic bridge (ring canal) to the central cytoplasmic mass (the cytophore). In ovaries, germ cells in a given cyst develop in full synchrony. However, there is no synchrony among cysts, so there is a developmental gradient of cysts (from oogonial to early meiotic) along the longitudinal ovary axis. Within the cysts that are located in the distal end of the ovary the synchrony is finally lost and interconnected cells diversify into two morphologically distinct categories: an oocyte and 31 nurse cells. Such cysts detach from the ovaries and further development occurs within the body cavity. The oocyte gathers nutrients, mainly in form of yolk spheres, whereas nurse cells grow slightly and do not gather yolk. Organelles such as ribosomes, mitochondria and endoplasmic reticulum pass freely through the ring canals and are present within the cytophore, which suggests cytoplasmic transfer towards the oocyte. The formation of female germ‐line cysts equipped with cytophore and cells differentiated into oocyte and nurse cells matches the general pattern of oogenesis found in clitellates. In details, the ovary organization and oogenesis found in I. bifidus resembles the situation described in some representatives of Naidinae and Enchytraeidae.

Section: Resultsmentioning

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Section: Resultsmentioning

confidence: 95%

Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

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Section: Introductionmentioning

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Description of ovary organization and oogenesis in a phreodrilid clitellate

Świątek

Pinder²,

Gajda

2019

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

Urbisz

Martin

Lagnika

et al. 2020

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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)

Świątek

Rodríguez

Małota

et al. 2022

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The main goal of the article is to describe the ovary organization and oogenesis in Peristodrilus montanus, an aquatic oligochaete of the subfamily Rhyacodrilinae. The presented analysis will not only enrich the knowledge about how eggs are formed but, because of the suggested conservatism of ovary organization in clitellate annelids, can contribute to disentangling the complex phylogenetic relationships of the rhyacodrilines within Naididae. The paired, conically shaped ovaries are located in segment XI. They are composed of a dozen or so syncytial germ‐line cysts, which are associated with somatic cells. Each germ cell in a cyst has one intercellular bridge that joins it to a central and anuclear cytoplasmic mass, the cytophore. This pattern of cyst organization is typical for all clitellates that have been studied to date. Initially, the germ cells in a cyst undergo a synchronous development, however, there is no synchrony between cysts, and therefore there is a developmental gradient (oogonia, pre‐diplotene germ cells, germ cells in diplotene) of oogenesis along the long ovary axis. The cysts are composed of a maximum of 32 cells. Cysts with cells in diplotene detach from the ovaries and the extraovarian phase of oogenesis begins. The developmental synchrony is lost, one cell (an oocyte) per cyst starts to gather cell components and yolk and grows considerably. The remaining cells grow to some extent and function as nurse cells. Like in other microdriles, P. montanus oocytes are rich in yolk; other features of oogenesis are also similar to those that are known from other microdrile taxa. The system of ovary organization found in the studied species is broadly similar to the corresponding features known from Naidinae and Phreodrilidae and, to some extent, in Enchytraeidae. However, this system is different from the one that is known in Tubificinae, Limnodriloidinae and Branchiurinae.