Abstract
This ultrastructural study of the female reproductive system of Calicotyle affinis, a monogenean without a uterus, demonstrates, for the first time in a monogenean, the presence of accessory cells located in the peripheral region of the ovary and a single large cell whose surface is penetrated by deep invaginations which restrict the passage of oocytes through the lumen of the distal extremity of the ovary. The cytoarchitecture of the epithelial lining of the two vaginae is a syncytium formed by an anucleate epithelial lining with sunken epithelial perykaria. The wall of the seminal receptacle is an enlarged prolongation of the vaginal epithelial lining. Fertilization occurs in the fertilization chamber and fertilized oocytes retain cortical granules within their cytoplasm, a characteristic known to occur in free-living flatworms. Our study also highlights concentrations of two distinct groups of Mehlis’ gland cell ducts on either side of the proximal end of the ootype distinguished by ultrastructural characteristics of their secretory granules. The epithelial wall of the ootype is formed by a single layer of regular, columnar, glandular epithelial cells; these cells are closely adjacent, conjoined towards their apical region by septate junctions and produce rounded, electron-dense granules which are discharged into the ootype lumen via a merocrine or holocrine mechanism. Released granules concentrate around the eggshell and form an additional fibrous coat. The morphological diversity observed in the female reproductive system of the Monogenea is commented on it relation to clarifying patterns in monogenean evolution and for understanding the phylogeny of the Neodermata.
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References
Arafa SZ, El-Naggar MM, Kearn GC (2014) On some ultrastructural features of the monogenean parasite Macrogyrodactylus congolensis from Clarias gariepinus inhabiting the River Nile in Egypt. Acta Parasitol 59:238–246. https://doi.org/10.2478/s11686-014-0236-0
Brinkmann A Jr (1940) Contribution to our knowledge of the monogenetic trematodes. Årbok Bergen Mus, Naturvit Rekke 1:1–117
Bullard SA, Overstreet RM (2000) Calicotyle californiensis n. sp. and Calicotyle urobati n. sp. (Monogenea: Calicotylinae) from elasmobranchs in the Gulf of California. J Parasitol 86:939–944. https://doi.org/10.2307/3284801
Cable J, Tinsley RC (1991) Intra-uterine larval development of the polystomatid monogeneans, Pseudodiplorchis americanus and Neodiplorchis scaphiopodis. Parasitology 103:253–266. https://doi.org/10.1017/s0031182000059539
Cable J, Harris PD, Tinsley RC (1996) Ultrastructural adaptations for viviparity in the female reproductive system of gyrodactylid monogeneans. Tissue Cell 28:515–526. https://doi.org/10.1016/s0040-8166(96)80054-1
Chisholm LA, Hansknecht TJ, Whittington ID, Overstreet RM (1997) A revision of the Calicotylinae Monticelli, 1903 (Monogenea: Monocotylidae). Syst Parasitol 38:159–183. https://doi.org/10.1023/a:100584-4306178
Colhoun LM, Fairweather I, Brennan GP (1998) Observations on the mechanism of eggshell formation in the liver fluke, Fasciola hepatica. Parasitology 116:555–567. https://doi.org/10.1017/s0031182098002662
Conn DB (1993) Ultrastructure of the gravid uterus of Hymenolepis diminuta (Platyhelminthes: Cestoda). J Parasitol 79:583–590. https://doi.org/10.2307/3283386
Dubinina MN (1982) Parasitic worms of the class Amphilinida (Plathelminthes). Trudy Akad Nauk SSSR 10:1–143 (in Russian)
El-Naggar MM, Khidr AA, Kearn GC (1990) Ultrastructural observations on the oviduct, Mehlis’ glands and ootype of the monogenean Cichlidogyrus halli typicus (Price & Kirk, 1967) Paperna, 1979. Int J Parasitol 20:203–209. https://doi.org/10.1016/0020-7519(90)90102-s
Glennon V, Chislolm L, Whittington ID (2006) A redescription of Calicotyle australis Johnston, 1934 (Monogenea: Monocotylidae) from the type-host Trygonorrhina fasciata (Rhinobatidae) off Adelaide, South Australia, including descriptions of live and silver stained larvae. Syst Parasitol 63:29–40. https://doi.org/10.1007/s11230-005-5501-z
Goto S (1894) Studies on the ectoparasitic trematodes of Japan. J Coll Sci Imp Univ Tokyo 8:1–273
Gremigni V (1983) Platyhelminthes – Turbellaria. In: Adiyodi KG, Adiyodi RG (eds) Reproductive biology of invertebrates, vol 1. Oogenesis, oviposition and oosorption. John Wiley & Sons Ltd, Chichester, pp 67–107
Gresson RAR (1964) Oogenesis in the hermaphroditic Digenea (Trematoda). Parasitology 54:409–421. https://doi.org/10.1017/s0031182000082469
Guraya SS, Parshad VR (1988) Platyhelminthes. In: Adiyodi KG, Adiyodi RG (eds) Reproductive biology of invertebrates, vol 3. Accessory sex glands. John Wiley & Sons, Chichester, pp 1–49
Halton DW (2004) Microscopy and the helminth parasite. Micron 35:361–390. https://doi.org/10.1016/j.micron.2003.12.001
Halton DW, Stranock SD, Hardcastle A (1976) Fine structural observations on oocyte development in monogeneans. Parasitology 73:13–23. https://doi.org/10.1017/S0031182000051283
Hathway RP, Herlevich JC (1976) A histochemical study of egg shell formation in the monogenetic trematode Octomacrum lanceatum Mueller, 1934. Proc Helminthol Soc Wash 43:203–206
Holy JM, Wittrock DD (1986) Ultrastructure of the female reproductive organs (ovary, vitellaria, and Mehlis’ gland) of Halipegus eccentricus (Trematods: Derogenidae). Can J Zool 64:2203–2212. https://doi.org/10.1139/z86-334
Jones MK, Ernst I, Whittington ID (1998) The uterine epithelium of Gyrodactylus kobayashii (Monogenea: Gyrodactylidae): ultrastructure of basal matrices, cytoplasmic membranes and the birth plug, and comparison with other reproductive epithelia. Int J Parasitol 28:1805–1815. https://doi.org/10.1016/s0020-7519(98)00120-9
Justine J-L, Mattei X (1986) Ultrastructural observations on fertilization in Dionchus remorae (Platyhelminthes, Monogenea, Dionchidae). Acta Zool 67:97–101. https://doi.org/10.1111/j.1463-6395.1986.tb00853.x
Justine J-L, Mattei X, Euzet L (1994) Ultrastructure of Tetraonchoides (Platyhelminthes, Monogenea): tegument, tegumentary receptors, oocytes and mineralous corpuscles. Ann Sci Nat, Zool, Paris 15:151–161
Kearn GC (1986) The eggs of monogeneans. Adv Parasitol 25:175–273. https://doi.org/10.1016/S0065-308X(08)60344-9
Kitamura A, Ogawa K, Shimizu T, Kurashima A, Mano N, Taniuchi T, Hirose H (2010) A new species of Calicotyle Diesing, 1850 (Monogenea: Monocotylidae) from the shortspine spurdog Squalus mitsukurii Jordan & Snyder and the synonymy of Gymnocalicotyle Nybelin, 1941 with this genus. Syst Parasitol 75:117–124. https://doi.org/10.1007/s11230-009-9228-0
Korneva JV (2001) Ultrastructure of the female genital system in Proteocephalus torulosus and P. exiguus (Cestoda: Proteocephalidea). Helminthologia 38:67–74
Littlewood DTJ, Waeschenbach A (2015) Evolution: a turn up for the worms. Curr Biol 25:R448–R469. https://doi.org/10.1016/j.cub.2015.04.012
Moczoń T, Świderski Z (2000) Schistosoma japonicum: cytochemistry of the Mehlis’ gland and the ootype wall. Acta Parasitol 45:22–28
Moczoń T, Świderski Z (2002) Schistosoma haematobium: cytochemistry of the Mehlis’ gland and the ootype wall. Acta Parasitol 47:280–287
Moczoń T, Świderski Z, Huggel H (1992) Schistosoma mansoni: the chemical nature of the secretions produced by the Mehlis’ gland and ootype as revealed by cytochemical studies. Int J Parasitol 22:65–73. https://doi.org/10.1016/0020-7519(92)90081-u
Orido Y (1987) Development of the ovary and the female reproductive cells of the lung fluke, Paragonimus ohirai (Trematoda, Troglotrematidae). J Parasitol 73:161–171. https://doi.org/10.2307/3282362
Poddubnaya LG, Hemmingsen W (2014) Cytoarchitecture of the vitellaria of two monogenean species, parasites of the holocephalan fish, Chimaera monstrosa L, with analysis of vitelline structure in the Neodermata. Parazitologiya 48:257–269 (In Russian)
Poddubnaya LG, Mackiewicz JS, Kuperman BI (2003) Ultrastructure of Archigetes sieboldi (Cestoda: Caryophyllidea): relationship between progenesis, development and evolution. Folia Parasitol 50:275–292. https://doi.org/10.14411/fp.2003.047
Poddubnaya LG, Mackiewicz JS, Bruňanská M, Scholz T (2005a) Ultrastructural studies on the reproductive system of progenetic Diplocotyle olrikii (Cestoda: Spathebothriidea): ovarian tissue. Acta Parasitol 50:199–207
Poddubnaya LG, Mackiewicz JS, Bruňanská M, Scholz T (2005b) Fine structure of the female reproductive ducts of Cyathocephalus truncatus (Cestoda: Spathebothriidea), from salmonid fish. Folia Parasitol 52:323–338. https://doi.org/10.14411/fp.2005.045
Poddubnaya LG, Mackiewicz JS, Šwiderski Z, Bruňanská M, Scholz T (2005c) Fine structure of egg-forming complex ducts, eggshell formation and supporting neuronal plexus in progenetic Diplocotyle olrikii (Cestoda, Spathebothriidea). Acta Parasitol 50:292–304
Poddubnaya LG, Gibson DI, Olson PD (2007) Ultrastructure of the ovary, ovicapt and oviduct of the spathebothriidean tapeworm Didymobothrium rudolphii (Monticelli, 1890). Acta Parasitol 52:127–134. https://doi.org/10.2478/s11686-007-0014-3
Poddubnaya LG, Kuchta R, Levron C, Gibson DI, Scholz T (2009) The unique ultrastructure of the uterus of the Gyrocotylidea Poche, 1926 (Cestoda) and its phylogenetic implications. Syst Parasitol 74:81–93. https://doi.org/10.1007/s11230-009-9195-5
Poddubnaya LG, Kuchta R, Scholz T, Xylander WER (2010) Ultrastructure of the ovarian follicles, oviducts and oocytes of Gyrocotyle urna (Neodermata: Gyrocotylidea). Folia Parasitol 57:173–184. https://doi.org/10.14411/fp.2010.024
Poddubnaya LG, Hemmingsen W, Gibson DI (2013) Ultrastructural characteristics of the vaginae of the basal monogenean Chimaericola leptogaster (Leuckart, 1830). Parasitol Res 112:4053–4064. https://doi.org/10.1007/s00436-013-3596-8
Poddubnaya LG, Hemmingsen W, Gibson DI (2017) 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. https://doi.org/10.1007/s00436-017-5578-8
Ramalingam K (1971) Studies on vitelline cells of Monogenea. IV. Presence of masked phenol and its significance. Acta Histochem 41:72–78
Rieger RM (1981) Morphology of the Turbellaria at the ultrastructural level. Hydrobiologia 84:213–229. https://doi.org/10.1007/978-94-009-8668-8_29
Rohde K (1975) Fine structure of the Monogenea, especially Polystomoides Ward. Adv Parasitol 13:1–33. https://doi.org/10.1016/s0065-308x(08)60317-6
Schmidt J (1996) Complex carbohydrates in shell precursor globules of the vitellarium and at the eggshell of Hymenolepis microstoma (Cestoda). Parasitol Res 82:157–164. https://doi.org/10.1007/s004360050087
Sopott-Ehlers B (1986) Fine structural characteristics of female and male germ cells in Proseriata Otoplanidae (Platyhelminthes). Hydrobiologia 132:137–144. https://doi.org/10.1007/bf00046240
Stranock SD, Halton DW (1975) Ultrastructural observations on Mehlis’ gland in the monogeneans, Diplozoon paradoxum and Calicotyle kroyeri. Int J Parasitol 5:541–550. https://doi.org/10.1016/0020-7519(75)90047-8
Świderski Z, Conn DB (1999) Ultrastructural aspects of fertilization in Proteocephalus longicollis, Inermicapsifer madagascariensis, and Mesocestoides lineatus (Platyhelminthes, Cestoda). Acta Parasitol 44:19–30
Świderski Z, Xylander WER (2000) Vitellocytes and vitellogenesis in cestodes in relation to embryonic development, egg production and life cycle. Int J Parasitol 30:805–817. https://doi.org/10.1016/s0020-7519(00)00066-7
Świderski Z, Conn DB, Mique J, Młocicki D (2004) Fertilization in the cestode Gallegoides arfaai (Mobedi et Ghadirian, 1977) Tenora et Mas-Coma, 1978 (Cyclophyllidea, Anoplocephalidae). Acta Parasitol 49:108–115
Świderski Z, Miquel J, Azzouz-Maache S, Pètavy A-F (2016) Fertilization in the cestode Echinococcus multilocularis (Cyclophyllidea, Taeniidae). Acta Parasitol 61:84–92. https://doi.org/10.1515/ap-2016-0010
Tappenden T, Kearn GC, Evans-Gowing R (1993) Fertilization and the functional anatomy of the germarium in the monogenean Entobdella soleae. Int J Parasitol 23:901–911. https://doi.org/10.1016/0020-7519(93)90056-5
Threadgold LT, Irwin SWB (1970) Electron microscope studies of Fasciola hepatica. IX The fine structure of Mehlis’ gland. Z Parasitenkd 35:16–30. https://doi.org/10.1007/bf00259527
Timofeeva TA (1985) Morphological and ecological aspects of evolution in the Monocotylidae (Monogenea). Parazitol Sb 33:44–76 (In Russian)
Tinsley RC (1983) Ovoviviparity in platyhelminth life-cycles. Parasitology 86:161–196. https://doi.org/10.1017/s00311182000050885
Acknowledgements
The authors would like to thank the staff of RV “Johan Ruud,” belonging to Tromsø University (Norway), for their help with the fishing. We are also grateful to the staff of the Centre of Electron Microscopy, I.D. Papanin Institute for the Biology of Inland Waters (Borok, Russia), for the technical assistance.
Funding
This work was supported by program no. АААА-А18-118012690100-5 of the Russian Academy of Sciences Institute for Biology of Inland Waters.
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Section Editor: Guillermo Salgado-Maldonado
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Poddubnaya, L.G., Hemmingsen, W. & Gibson, D.I. The first ultrastructural observations of the egg-forming complex of Calicotyle affinis, an endoparasitic monocotylid monogenean which lacks a uterus. Parasitol Res 117, 4013–4025 (2018). https://doi.org/10.1007/s00436-018-6111-4
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DOI: https://doi.org/10.1007/s00436-018-6111-4