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Spermatogenesis and lobular cyst type of testes organization in marine gastropod Littorina saxatilis (Olivi 1792)

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Abstract

Although individual stages of spermatogenesis in Littorina saxatilis are well studied at the electron microscopic level, the gonad structure and the spatial localization of gametes at different stages of maturation remain unclear. Using differential-interference contrast (DIC) for observations of fresh tissue we show that the mature testis consists of numerous ovoid lobules forming larger lobes. The lobules of intact mature testes of L. saxatilis are filled with randomly arranged multicellular cysts containing gametes at different stages of maturation. Gametes within a cyst are highly synchronized in respect of the differentiation degree. At the same time, no spatial gradient in the arrangement of cysts according to the maturation degree of gametes in them was observed in any of the studied lobules. The male gonads contain cysts with early spermatids, mid, late spermatids, and spermatozoa. Using silver-staining, DAPI, and chromomycin A3 (CMA3) staining, we identify 20 main types of nucleus organization in differentiating sperm. Premature and mature male gonads contain cysts with a mosaic arrangement as well as rare solitary cyst cells, goniablast cysts, or separate spermatogonia in between them. Our data indicate that the testis structure in L. saxatilis cannot be attributed to the tubular type, as previously thought. It corresponds to the lobular cyst type but individual lobules contain cysts with gametes at the same stage of development. It is similar to the testis structure of several fishes, amphibians, and Drosophila melanogaster. This type of the gonad organization has never been described in gastropods before.

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Acknowledgments

We thank the anonymous reviewers for critical comments and helpful advice on the previous version of the manuscript. We are grateful to Natalia Lentsman for linguistic corrections. The research was technically supported by the Center for Molecular and Cell Technologies and the Environmental Safety Observatory of St Petersburg State University.

Funding

This work was supported by the Russian Academy of Sciences (Molecular and Cell Biology Program of the Presidium of the Russian Academy of Sciences), the Russian Foundation for Basic Research (grant no. 18-54-20001-nor а), and the St Petersburg State University (grant no. 0.40.491.2017).

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Authors and Affiliations

  1. Institute of Cytology of the Russian Academy of Sciences, Tikhoretsky prospect, 4, St Petersburg, 194064, Russia

    Sergei Iu. Demin, Vera N. Stefanova & Natalia A. Mikhailova

  2. Department of Invertebrate Zoology, St Petersburg State University, Universitetskaya nab., 7/9, St Petersburg, 199034, Russia

    Andrey I. Granovitch & Natalia A. Mikhailova

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  1. Sergei Iu. Demin
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  2. Vera N. Stefanova
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  3. Andrey I. Granovitch
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  4. Natalia A. Mikhailova
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Correspondence to Natalia A. Mikhailova.

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Demin, S.I., Stefanova, V.N., Granovitch, A.I. et al. Spermatogenesis and lobular cyst type of testes organization in marine gastropod Littorina saxatilis (Olivi 1792). Cell Tissue Res 376, 457–470 (2019). https://doi.org/10.1007/s00441-019-03004-y

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