Reproduction of trematodes in the molluscan host: an ultrastructural study of the germinal mass and brood cavity in daughter rediae of Tristriata anatis Belopolskaia, 1953 (Digenea: Notocotylidae)
- 51 Downloads
This study describes the fine structure of the germinal mass in daughter rediae of Tristriata anatis. The germinal mass consists of undifferentiated cells, germinal cells and supporting cells and contains numerous cercarial embryos up to tail bud stage. Supporting cells and their outgrowths form a tight meshwork of the germinal mass. In its basal part, this meshwork serves as scaffolding for undifferentiated and germinal cells, naked cell aggregates and early germinal balls. More mature embryos are located apically. The hypertrophied supporting tissue appears to be involved in an intensive transport of substances, as indicated by abundant gap junctions between cell outgrowths and numerous pinocytotic vesicles and microtubules in their cytoplasm. Germinal cells contain annulate lamellae and the nuage, typical organelles of animal oocytes. In young rediae containing embryonic cercariae at the tail bud stage, the supporting tissue starts to degenerate in the apical part of the germinal mass, and a primordial brood cavity emerges though it develops fully only in mature rediae containing late embryonic cercariae. An unusual feature of the germinal mass in T. anatis rediae is an enhancement of the embryo brooding function. At the same time, the performance of this function by the brood cavity is reduced. This is the first time such a redistribution of the embryo brooding function between the germinal mass and the brood cavity has been reported.
KeywordsTristriata anatis Reproduction of redia Ultrastructure Germinal mass Germinal cell Brood cavity
We are grateful to Natalia Lentsman for her help with the translation of the MS into English. We would like to thank the reviewers for their valuable comments and suggestions. Scientific research was performed using equipment of the “Taxon” Research Resource Center (http://www.ckp-rf.ru/ckp/3038/) of the Zoological Institute of the Russian Academy of Sciences (St. Petersburg).
This work was supported by the Russian Foundation for Basic Research (Grant No 16-04-00753) and by the programme of the Russian Academy of Sciences of the Zoological Institute No. АААА-А17-117030310322-3.
- Ataev GL (2017) Reproduction of trematode partenitae: review of main theories. Nauka, Saint PetersburgGoogle Scholar
- Cribb TH, Bray RA, DTJ L, Pichelin S, Herniou EA (2001) The Digenea. In: DTJ L, Bray RA (eds) Interrelationships of the Platyhelminthes. Taylor and Francis, London, pp 168–185Google Scholar
- Dobrovolskij AA, Ataev GL (2003) The nature of reproduction of trematodes rediae and sporocysts. In: Combes C, Jourdane J (eds) Taxonomy ecology and evolution of metazoan parasites, vol I. PUP, Perpignan, pp 249–272Google Scholar
- Dobrovolskij AA, Galaktionov KV, Muhamedov GK, Sinha BK, Tihomirov IA (1983) Parthenogenetic generations of trematodes. Trudy Leningradskogo obshchestva estestvoispytateleǐ (Transactions of the Leningrad Society of Naturalists) 82:1–108 (in Russian)Google Scholar
- Galaktionov KV (2016) Evolution and biological radiation of trematodes: a synopsis of ideas and opinions. In: Galaktionov KV (ed) Coevolution of parasites and hosts. (Proceedings of the Zoological Institute of the Russian Academy of Sciences, 320, Supl. 4). Zoological Institute Publ, St. Petersburg, pp 74–126 (in Russian)Google Scholar
- Hanna REB, Moffett D, Forster FI, Trudgett AG, Brennan GP, Fairweather I (2016) Fasciola hepatica: a light and electron microscope study of the ovary and of the development of oocytes within eggs in the uterus provides an insight into reproductive strategy. Vet Parasitol 221:93–103. https://doi.org/10.1016/j.vetpar.2016.03.011 CrossRefPubMedGoogle Scholar
- Isakova NP (2011) Germinal mass of the rediae of Trematoda. Parazitologiya 45:358–366 (In Russian)Google Scholar
- Littlewood DTJ (2006) The evolution of parasitism in flatworms. In: Maule AG, Marks NJ (eds) Parasitic flatworms: molecular biology, biochemistry, immunology and physiology. CAB International, Wallingford, pp 1–36Google Scholar
- Littlewood DTJ, Bray RA, Waeschenbach A (2015) Phylogenetic patterns of diversity in cestodes and trematodes. In: Morand S, Krasnov BR, DTJ L (eds) Parasite diversity and diversification: evolutionary ecology meets phylogenetics. Cambridge University Press, Cambridge, pp 304–319CrossRefGoogle Scholar
- Morozova KN, Gubanova NV, Kiseleva EV (2005) Structural organization and possible functions of annulate lamellae. Tsitologiya 47:667–678 (In Russian)Google Scholar
- Podvyaznaya IM, Galaktionov KV (2008) An ultrastructural study of the early cercarial development in Prosorhynchoides borealis (Digenea: Bucephalidae) with special reference to formation of the primitive epithelium. J Helminthol 82(2):101–108. https://doi.org/10.1017/S0022149X08890803 CrossRefPubMedGoogle Scholar
- Podvyaznaya IM, Galaktionov KV (2014) Trematode reproduction in the molluscan host: an ultrastructural study of the germinal mass in the rediae of Himasthla elongata (Mehlis, 1831) (Digenea: Echinostomatidae). Parasitol Res 113:1215–1224. https://doi.org/10.1007/s00436-014-3760-9 CrossRefPubMedGoogle Scholar
- Pollard TD, Earnshaw WC, Lippincott-Schwartz J, Johnson GT (2017) Cell biology. 3rd edn. Elsevier, PhiladelphiaGoogle Scholar
- Stunkard HW (1966) The morphology and life-history of Notocotylus atlanticus n. sp., a digenetic trematode of eider ducks, Somateria mollissima, and the designation, Notocotylus duboisi nom. nov., for Notocotylus imbricatus (Looss, 1893) Szidat, 1935. Biol Bull 131:501–515. https://doi.org/10.2307/1539989 CrossRefPubMedGoogle Scholar
- Wang B, Collins JJ, Newmark PA (2013) Functional genomic characterization of neoblast-like stem cells in larval Schistosoma mansoni. elife. https://doi.org/10.7554/eLife.00768
- Žd’árská Z (1995) Ultrastructure of the primitive epithelium of Echinostoma revolutum (Digenea: Echinostomatidae) cercaria. Folia Parasitol 42:266–268Google Scholar