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The unique uterine structure of the basal monogenean Chimaericola leptogaster (Monogenea: Polyopisthocotylea), an ectoparasite of the relictual holocephalan fish Chimaera monstrosa

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Abstract

Ultrastructural studies of the monogenean uterus are few in number and no non-polystomatid polyopisthocotyleans have been investigated. The uterus of Chimaericola leptogaster, a basal polyopisthocotylean monogenean, has several unusual features, including six reflexed loops comprising four ascending and three descending, longitudinally oriented, linear sections. At the ultrastructural level, three readily distinguishable uterine regions and other distinctive characteristics are apparent. One novel feature occurs in the proximal uterus, where the lining forms a so-called ‘single-layered multi-rowed cellular epithelium’, which includes two types of cells, tall (ca. 14–19 μm in height) and short (ca. 6–9 μm in height) cells, both lying on the basement membrane. Although known from other bilaterian groups, this is the first record of this type of epithelium in the Neodermata. The lining of the middle uterine region comprises a single regular layer of columnar glandular epithelial cells, which produce numerous rounded, electron-dense granules associated with Golgi complexes. The presence of the uterine glands in the middle region of the uterus is an unusual feature for a monogenean, having previously been described only for basal orders of the Cestoda, i.e. the Gyrocotylidea, Caryophyllidea and Spathebothriidea. Seen in cross-section, the epithelium of the distal uterus contains three areas of tall single-layered columnar epithelium (ca. 30 μm deep) interspersed by three areas of flattened epithelium (ca. 0.2–0.9 μm deep). Such a pattern is quite different from those reported for other monogeneans and, indeed, other neodermatan groups. The investigation has shown that the outer layer of the fully formed eggshell is assembled from epithelial secretions in the middle uterine lumen, but is modified in terms of its shape in the distal uterus. Possible phylogenetic implications arising from the unusual features described are discussed in relation to other neodermatan groups and recent molecular phylogenies of the Bilateria.

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Acknowledgements

The authors would like to thank the staff of the RV ‘Johan Ruud’, belonging to Tromsø University (Norway), for their invaluable help with the fishing. We are also grateful to the staff of the Centre of Electron Microscopy, I.D. Papanin Institute for Biology of Inland Waters (Borok, Russia) for technical assistance. The present study was supported by the Russian Foundation for Fundamental research (Project no.15-04-02890-a to LGP).

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Authors and Affiliations

  1. I. D. Papanin Institute for Biology of Inland Waters, Russian Academy of Sciences, 152742 Borok, Yaroslavl Province, Russia

    Larisa G. Poddubnaya

  2. Department of Arctic and Marine Biology, Faculty of Biosciences, Fisheries and Economics, University of Tromsø, 9037, Tromsø, Norway

    Willy Hemmingsen

  3. Department of Life Sciences, Natural History Museum, Cromwell Road, London, SW7 5BD, UK

    David I. Gibson

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  1. Larisa G. Poddubnaya
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Correspondence to Larisa G. Poddubnaya.

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Poddubnaya, L.G., Hemmingsen, W. & Gibson, D.I. The unique uterine structure of the basal monogenean Chimaericola leptogaster (Monogenea: Polyopisthocotylea), an ectoparasite of the relictual holocephalan fish Chimaera monstrosa . Parasitol Res 116, 2695–2705 (2017). https://doi.org/10.1007/s00436-017-5578-8

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