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An ultrastructural study of the ovary cord organization and oogenesis in the amphibian leech Batracobdella algira (Annelida, Clitellata, Hirudinida)

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Abstract

This study reveals the ovary micromorphology and the course of oogenesis in the leech Batracobdella algira (Glossiphoniidae). Using light, fluorescence, and electron microscopies, the paired ovaries were analyzed. At the beginning of the breeding season, the ovaries were small, but as oogenesis progressed, they increased in size significantly, broadened, and elongated. A single convoluted ovary cord was located inside each ovary. The ovary cord was composed of numerous germ cells gathered into syncytial groups, which are called germ-line cysts. During oogenesis, the clustering germ cells differentiated into two functional categories, i.e., nurse cells and oocytes, and therefore, this oogenesis was recognized as being meroistic. As a rule, each clustering germ cell had one connection in the form of a broad cytoplasmic channel (intercellular bridge) that connected it to the cytophore. There was a synchrony in the development of the clustering germ cells in the whole ovary cord. In the immature leeches, the ovary cords contained undifferentiated germ cells exclusively, from which, previtellogenic oocytes and nurse cells differentiated as the breeding season progressed. Only the oocytes grew considerably, gathered nutritive material, and protruded at the ovary cord surface. The vitellogenic oocytes subsequently detached from the cord and filled tightly the ovary sac, while the nurse cells and the cytophore degenerated. Ripe eggs were finally deposited into the cocoons. A comparison of the ovary structure and oogenesis revealed that almost all of the features that are described in the studied species were similar to those that are known from other representatives of Glossiphoniidae, which indicates their evolutionary conservatism within this family.

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Acknowledgments

We would like to express our sincere thanks to Dr. Danuta Urbańska-Jasik and Dr. Łukasz Chajec (University of Silesia in Katowice, Poland) for their invaluable assistance in preparing the material for the analyses in light and transmission electron microscopies.

Funding

This research was supported financially as part of the statutory activities of the University of Silesia in Katowice and was also supported by the Tunisian Ministry of Higher Education and Scientific Research (LR18ES41).

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Correspondence to Raja Ben Ahmed.

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Highlights

The evidence presented here shows that:

1. The ovary cords in B. algira are elongated and non-polarized structures that are composed of multicellular germ-line cysts that have a well-developed cytophore.

2. These cysts are surrounded by a somatic envelope and are enclosed within the ovary sac.

3. Oogenesis is meroistic, as was indicated by the differentiation of the germ cells into nurse cells and oocytes and has a synchronous character (all of the developing oocytes were in the same phase of oogenesis).

4. The large vitellogenic oocytes detached from the ovary cords and filled the ovarian sac.

5. Several yolky egg cells were formed at a given time, and they were then laid into the cocoons.

6. The strong similarities of the ovary organization and oogenesis between B. algira and other Glossiphoniidae suggests their conservative character among this family, and therefore, B. algira ovaries should be regarded as being a “Glossiphonia” type.

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Ahmed, R.B., Urbisz, A.Z. & Świątek, P. An ultrastructural study of the ovary cord organization and oogenesis in the amphibian leech Batracobdella algira (Annelida, Clitellata, Hirudinida). Protoplasma 258, 191–207 (2021). https://doi.org/10.1007/s00709-020-01560-7

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