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Morphological features of the testis of freshwater blood flukes of the genus Sanguinicola Plehn, 1905, with consideration of the testicular patterns in the Aporocotylidae

Abstract

This is the first detailed study assessing the morphological features of the testis and testicular sperm of members of the freshwater blood flukes Sanguinicola sp. from Leuciscus idus (Cyprinidae) and for S. volgensis from Pelecus cultratus (Cyprinidae), and the marine blood fluke Aporocotyle simplex from Hippoglossoides platessoides (Pleuronectidae). The present study reports a unique feature in the distribution of germinal cellular components in freshwater Sanguinicola sp., showing the presence of the individual spermatocytes or their clusters in the testicular lobes, and the gathering of spermatid rosettes and spermatozoa within middle testicular lumen, which extends along the entire length of the testis. In contrast, each testis of marine A. simplex contains the usual mixed distribution of germ cells at various stages of development. The first TEM data on spermatozoon character of studied species has shown, unusual for digenean sperm structure, the absence of cortical microtubules in sperm principal region. Moreover, a variation in axoneme patterns is revealed in the studied aporocotylids, belonging to the different aporocotylid lineages a 9 + 0 axonemal type observed for freshwater teleost-infective species, Sanguinicola sp. and S. volgensis, and a 9 + ‘1’ axonemal type revealed in spermatozoa of marine teleost-infective species A. simplex. The results discussed with the published data on the digenean sperm structure and the testicular patterns in the Aporocotylidae likely represent additional characteristics supporting the divergent evolutionary lineages of freshwater and marine aporocotylids. We anticipate future morphological studies of the sperm structure in aporocotylids of three lineages for an understanding of their phylogenetic relationships.

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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 help with fish capture in June 2017. We are also grateful to master’s students, Ben Hall and Jonathon McFall (University of Aberdeen, Scotland), for their help with dissection of the fishes and the collection of parasites at sea. Our thanks are due to the staff of the Centre of Electron Microscopy, I.D. Papanin Institute for the Biology of Inland Waters (Borok, Russia), for technical assistance in TEM investigations. We acknowledge Dr. David Gibson (UK) for providing us with LM photo of Aporocotyle simplex.

Funding

The results were obtained within the Russian Foundation for Basic Research, Research project No. 20–04-00086 ‘Evolutionary studies on a basal group of trematodes: detailed morphological and molecular genetic analyses of freshwater aporocotylids, with an evaluation of their phylogenetic relationships with marine members of the family’.

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Larisa G. Poddubnaya performed scanning and transmission electron microscopy, prepared figures, wrote manuscript, and approved the final draft. Alexander E. Zhokhov performed light microsopy of freshwater species. Willy Hemmingsen performed light microscopy of marine species and text review. Ken MacKenzie analyzed data, text review, and approved the final draft.

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Correspondence to Larisa G. Poddubnaya.

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Poddubnaya, L.G., Zhokhov, A.E., Hemmingsen, W. et al. Morphological features of the testis of freshwater blood flukes of the genus Sanguinicola Plehn, 1905, with consideration of the testicular patterns in the Aporocotylidae. Parasitol Res 121, 2945–2954 (2022). https://doi.org/10.1007/s00436-022-07622-4

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Keywords

  • Testis
  • Sperm pattern
  • TEM
  • Sanguinicola
  • Aporocotyle
  • Divergent evolutionary lineages