Spermiogenesis and sperm ultrastructure of Valipora mutabilis Linton, 1927 (Cestoda, Cyclophyllidea, Gryporhynchidae)
Abstract
This is the first ultrastructural study of the spermiogenesis and the mature spermatozoon of a cyclophyllidean cestode of the family Gryporhynchidae. The spermiogenesis of Valipora mutabilis begins with the formation of a differentiation zone delimited by arching membranes and containing two centrioles. One of the centrioles develops an axoneme that grows directly into the cytoplasmic protrusion. The other centriole remains situated in a cytoplasmic bud and is subsequently aborted (type IV of cestode spermiogenesis). The mature spermatozoon of V. mutabilis is a filiform cell, tapered at both extremities and lacks mitochondria. The anterior extremity is characterised by the presence of an apical cone and a single helicoidal crested body. The axoneme is of 9 + ‘1’ trepaxonematan pattern, with a periaxonemal sheath. The cortical microtubules are twisted at an angle of about 45° to the spermatozoon axis. The nucleus is electron dense and spirally coiled around the axoneme. The cytoplasm is electron lucent and contains numerous granules of electron-dense material. In contrast to a recent opinion for close phylogenetic relationships, these ultrastructural data demonstrate the distant position between gryporhynchids and the family Taeniidae. The most similar pattern in the ultrastructure of the spermiogenesis and the mature spermatozoon has been described for dilepidids, some hymenolepidids and some anoplocephalids.
Keywords
Mature Spermatozoon Cortical Microtubule Anterior Extremity Sperm Ultrastructure Cytoplasmic ProtrusionNotes
Acknowledgements
We are grateful to Dr. S.R. Stoitsova (Institute of Microbiology, Bulgarian Academy of Sciences) for kindly providing fixed and embedded specimens of V. mutabilis and to Dr P. Zekhtindzhiev (Institute of Zoology, Bulgarian Academy of Sciences) for his help in the field studies. This study was supported by the National Science Fund, Ministry of Education and Science of the Republic of Bulgaria, grant B-1539/05. The collaborative research was facilitated by the cooperation agreement between the Bulgarian Academy of Sciences and the Polish Academy of Sciences.
References
- Bâ A, Bâ CT, Marchand B (2000) Ultrastructure of spermiogenesis and the spermatozoon of Sudarikovina taterae (Cestoda, Cyclophyllidea, Anoplocephalidae) intestinal parasite of Tatera gambiana (Rodentia, Gerbillidae). J Submicrosc Cytol Pathol 32:137–144PubMedGoogle Scholar
- Bâ CT, Marchand B (1992a) Reinvestigation of the ultrastructure of spermiogenesis and the spermatozoon of Hymenolepis nana (Cestoda, Cyclophyllidea), parasite of the small intestine of Rattus rattus. Mol Reprod Dev 33:39–45PubMedCrossRefGoogle Scholar
- Bâ CT, Marchand B (1992b) Ultrastructural particularities of the spermatozoon of Stilesia globipunctata (Cestoda) parasite of the small intestine of sheep and goats in Senegal. J Submicrosc Cytol Pathol 24:29–34Google Scholar
- Bâ CT, Marchand B (1994a) Ultrastructure of spermiogenesis and the spermatozoon of Aporina delafondi (Cyclophyllidea, Anoplocephalidae) intestinal parasite of turtle-doves in Senegal. Int J Parasitol 24:225–235PubMedCrossRefGoogle Scholar
- Bâ CT, Marchand B (1994b) Ultrastructure of spermiogenesis and the spermatozoon of Raillietina (Raillietina) tunetensis (Cyclophyllidea, Davaineidae) intestinal parasite of turtle doves in Senegal. Int J Parasitol 24:237–248PubMedCrossRefGoogle Scholar
- Bâ CT, Marchand B (1994c) Comparative ultrastructure of the spermatozoa of Inermicapsifer guineensis and I. madagascariensis (Cestoda, Anoplocephalidae, Inermicapsiferinae), intestinal parasites of rodents in Senegal. Can J Zool 72:1633–1638CrossRefGoogle Scholar
- Bâ CT, Marchand B (1994d) Ultrastructure of spermiogenesis and the spermatozoon of Mathevotaenia herpestis (Cestoda) intestinal parasite of Atelerix albiventris in Senegal. Acta Zool (Stockh) 75:167–175CrossRefGoogle Scholar
- Bâ CT, Marchand B (1994e) Similitude ultrastructurale des spermatozoïdes de quelques Cyclophyllidea. Parasite 1:51–55PubMedGoogle Scholar
- Bâ CT, Marchand B (1995) Spermiogenesis, spermatozoa and phyletic affinities in the Cestoda. Mém Mus Natl Hist Nat 166:87–95Google Scholar
- Bâ CT, Marchand B (1998) Ultrastructure of spermiogenesis and the spermatozoon of Vampirolepis microstoma (Cestoda, Hymenolepididae), intestinal parasite of Rattus rattus. Microsc Res Tech 42:218–225PubMedCrossRefGoogle Scholar
- Bâ CT, Marchand B, Mattei X (1991) Demonstration of the orientation of the Cestodes spermatozoon illustrated by the ultrastructural study of spermiogenesis of a Cyclophyllidea: Thysaniezia ovilla, Rivolta, 1874. J Submicrosc Cytol Pathol 23:606–612Google Scholar
- Bâ CT, Bâ A, Marchand B (2005a) Ultrastructure of the spermatozoon of Raillietina (Raillietina) baeri (Cyclophyllidea, Davaineidae) an intestinal parasite of the multimammate rat, Mastomys huberti (Rodentia, Muridae). Parasitol Res 97:173–178PubMedCrossRefGoogle Scholar
- Bâ CT, Bâ A, Marchand B (2005b) Ultrastructure of the spermatozoon of Paroniella reynoldsae (Cyclophyllidea, Davaineidae) an intestinal parasite of Corvus albus (Aves, Corvidae). Acta Parasitol 50:208–214Google Scholar
- Barrett NJ, Smyth JD (1983) Observation of the structure and ultrastructure of sperm development in Echinococcus multilocularis, both in vitro and in vivo. Parasitology 87:1iGoogle Scholar
- Bona FV (1994) Family Dilepididae Railliet & Henry, 1909. In: Khalil LF, Jones A, Bray RA (eds) Keys to the cestode parasites of vertebrates. CAB International, Wallingford, pp 443–554Google Scholar
- Bruňanská M, Scholz T, Dezfuli BS, Poddubnaya L (2006) Spermiogenesis and sperm ultrastructure of Cyathocephalus truncatus (Pallas, 1781) Kessler, 1868 (Cestoda: Spathebothriidea). J Parasitol 92:884–892PubMedCrossRefGoogle Scholar
- Chomicz L, Świderski Z (1992) Spermiogenesis and ultrastructure of the spermatozoon of the cestode Dicranotaenia coronula (Dujardin, 1845) (Cyclophyllidea, Hymenolepididae). In: Proceedings of the 5th Asia-Pacific Electron Microscopy Conference. Beijing, pp 324–325Google Scholar
- Eira C, Miquel J, Vingada J, Torres J (2006) Spermiogenesis and spermatozoon of the cestode Mosgovoyia ctenoides (Cyclophyllidea: Anoplocephalidae), an intestinal parasite of Oryctolagus cuniculus (Lagomorpha, Leporidae). J Parasitol 92:708–718PubMedCrossRefGoogle Scholar
- Euzet L, Świderski Z, Mokhtar-Maamouri F (1981) Ultrastructure comparée du spermatozoїde des Cestodes. Relations avec la phylogénèse. Ann Parsitol (Paris) 56:247–259Google Scholar
- Featherston DW (1971) Taenia hydatigena III. Light and electron microscopy study of spermiogenesis. Z Parasitenkd 37:148–168PubMedCrossRefGoogle Scholar
- Hidalgo C, Miquel J, Torres J, Marchand B (2000) Ultrastructural study of a spermiogenesis and the spermatozoon in Catenotaenia pusilla, an intestinal parasite of Mus musculus. J Helminthol 74:73–81PubMedGoogle Scholar
- Hoberg EP, Mariaux J, Justine J-L, Brooks DR, Weekes PJ (1997) Phylogeny of the Eucestoda (Cercomeromorphae) based on comparative morphology: historical perspectives and a new working hypothesis. J Parasitol 83:1128–1147PubMedCrossRefGoogle Scholar
- Hoberg EP, Jones A, Bray RA (1999) Phylogenetic analysis among the families of the Cyclophyllidea (Eucestoda) based on comparative morphology, with new hypotheses for co-evolution in vertebrates. Syst Parasitol 42:51–73PubMedCrossRefGoogle Scholar
- Hoberg EP, Mariaux J, Brooks DR (2001) Phylogeny among the orders of the Eucestoda (Cercomeromorphae): Integrating morphology, molecules and total evidence. In: Littlewood DTJ, Bray RA (eds) Interrelationships of the Platyhelminthes. Taylor and Francis, London, pp 112–126Google Scholar
- Justine J-L (1991) Phylogeny of parasitic Platyhelminthes: a critical study of synapomorphies proposed on the basis of the ultrastructure of spermiogenesis and spermatozoa. Can J Zool 69:1421–1440CrossRefGoogle Scholar
- Justine J-L (1998) Spermatozoa as phylogenetic character for the Eucestoda. J Parasitol 84:385–408PubMedCrossRefGoogle Scholar
- Justine J-L (2001) Spermatozoa as phylogenetic characters for the Platyhelminthes. In: Littlewood DTJ, Bray RA (eds) Interrelationships of the Platyhelminthes. Taylor and Francis, London, pp 231–238Google Scholar
- Kelsoe GH, Ubelaker JE, Allison VF (1977) The fine structure of spermiogenesis in Hymenolepis diminuta (Cestoda) with a description of the mature spermatozoon. Z Parasitenkd 54:175–187PubMedCrossRefGoogle Scholar
- Li H-Y, Brennan JP, Halton DW (2003) Spermatogenesis, spermiogenesis and spermatozoon in the cestode (Moniezia expansa) (Cyclophyllidea, Anoplocephalidae). Acta Zool Sin 49:370–379Google Scholar
- Mariaux J (1998) A molecular phylogeny of the Eucestoda. J Parasitol 84:114–124PubMedCrossRefGoogle Scholar
- McKerr G (1985) The fine structure and physiology of a trypanorhynch tapeworm Grillotia erinaceus. Ph.D. Thesis, The Queen’s University of BelfastGoogle Scholar
- Miquel J, Marchand B (1997) Ultrastructure of the spermatozoon of Dipylidium caninum (Cestoda, Cyclophyllidea, Dilepididae) an intestinal parasite of Canis familiaris. Parasitol Res 83:349–355PubMedCrossRefGoogle Scholar
- Miquel J, Marchand B (1998) Ultrastructure of spermiogenesis and the spermatozoon of Anoplocephaloides dentata (Cestoda, Cyclophyllidea, Anoplocephalidae) intestinal parasite of Arvicolidae rodents. J Parasitol 84:1128–1136PubMedCrossRefGoogle Scholar
- Miquel J, Świderski Z (2006) Ultrastructure of the spermatozoon of Dollfusiella spinulifera (Beveridge and Jones, 2000) Beveridge, Neifar and Euzet, 2004 (Trypanorhyncha, Eutetrarhynchidae). Parasitol Res 99:37–44PubMedCrossRefGoogle Scholar
- Miquel J, Bâ CT, Marchand B (1997) Ultrastructure of the spermatozoon of Skrjabinotaenia lobata (Cyclophyllidea, Catenotaeniidae), intestinal parasite of Apodemus sylvaticus (Rodentia, Muridae). J Submicrosc Cytol Pathol 29:521–526Google Scholar
- Miquel J, Bâ CT, Marchand B (1998) Ultrastructure of spermiogenesis of Dipylidium caninum (Cestoda, Cyclophyllidea, Dipylidiidae) an intestinal parasite of Canis familiaris. Int J Parasitol 28:1453–1458PubMedCrossRefGoogle Scholar
- Miquel J, Feliu C, Marchand B (1999) Ultrastructure of spermiogenesis and the spermatozoon of Mesocestoides litteratus (Cestoda, Mesocestoididae). Int J Parasitol 29:499–510PubMedCrossRefGoogle Scholar
- Miquel J, Hidalgo C, Feliu C, Marchand B (2000) Sperm ultrastructure of Taenia mustelae (Cestoda, Taeniidae), an intestinal parasite of the weasel, Mustela nivalis (Carnivora). Invert Reprod Dev 38:43–51Google Scholar
- Miquel J, Świderski Z, Marchand B (2005a) Spermatological characters in the Dipylidiidae Stiles, 1896 (Cestoda, Cyclophyllidea). Acta Parasitol 50:65–73Google Scholar
- Miquel J, Świderski Z, Młocicki D, Eira C, Marchand B (2005b) Ultrastructure of spermatogenesis of the anoplocephalid cestode Gallegoides arfaai (Mobedi et Ghadirian, 1977) Tenora et Mas-Coma, 1978. Acta Parasitol 50:132–144Google Scholar
- Miquel J, Eira C, Świderski Z, Conn DB (2007a) Mesocestoides lineatus (Goeze, 1782) (Mesocestoididae): new data on sperm ultrastructure. J Parasitol 93:545–552PubMedCrossRefGoogle Scholar
- Miquel J, Świderski Z, Neifar L, Eira C (2007b) Ultrastructure of the spermatozoon of Parachristianella trygonis Dollfus, 1946 (Trypanorhyncha, Eutetrarhynchidae). J Parasitol 93:1296–1302PubMedCrossRefGoogle Scholar
- Mokhtar-Maamouri F, Azzouz-Draoui N (1990) Spermatogenèse et ultrastructure du spermatozoïde de Nematotaenia chantalae Dollfus, 1957 (Cestoda, Cyclophyllidea, Nematotaeniidae). Ann Parasitol Hum Comp 65:221–228Google Scholar
- Morseth DJ (1969) Spermtail finestructure of Echinicoccus granulosus and Dicrocoelium dendriticum. Exp Parasitol 24:47–53PubMedCrossRefGoogle Scholar
- Ndiaye PI, Miquel J, Marchand B (2003a) Ultrastructure of spermiogenesis and spermatozoa of Taenia parva Baer, 1926 (Cestoda, Cyclophyllidea, Taeniidae), a parasite of the common genet (Genetta genetta). Parasitol Res 89:34–43PubMedCrossRefGoogle Scholar
- Ndiaye PI, Agostini S, Miquel J, Marchand B (2003b) Ultrastructure of spermiogenesis and the spermatozoon in the genus Joyeuxiella Fuhrmann, 1935 (Cestoda, Cyclophyllidea, Dipylidiidae): comparative analysis of J. echinorhynchoides (Sonsino, 1889) and J. pasqualei (Diamare, 1893). Parasitol Res 91:175–186PubMedCrossRefGoogle Scholar
- Pichelin S, Cribb TH, Bona FV (1998) Glossocercus chelodinae (MacCallum, 1921) n. comb. (Cestoda: Dilepididae) from freshwater turtles in Australia and a redefinition of the genus Bancroftiella Johnston, 1911. Syst Parasitol 39:165–181CrossRefGoogle Scholar
- Robinson JM, Bogitsh BJ (1978) A morphological and cytochemical study of sperm development in Hymenolepis diminuta. Z Parasitenkd 56:81–92CrossRefGoogle Scholar
- Rohde K, Watson N (1986) Ultrastructure of spermiogenesis and sperm of Austramphilina elongata (Platyhelminthe, Amphilinidea). J Submicrosc Cytol 18:361–374Google Scholar
- Scholz T, Salgado-Maldonado G (2001) Metacestodes of the family Dilepididae (Cestoda: Cyclophyllidea) parasitising fishes in Mexico. Syst Parsitol 49:23–40CrossRefGoogle Scholar
- Scholz T, Kuchta R, Salgado-Maldonado G (2002) Cestodes of the family Dilepididae (Cestoda: Cyclophyllidea) from fish-eating birds in Mexico: a survey of species. Syst Parasitol 52:171–182PubMedCrossRefGoogle Scholar
- Shi DZ, Liu DS, Wang SK, Craig PS (1994) The ultrastructure of Echinococcus multilocularis. Chin J Parasite Dis Control 7:40–41Google Scholar
- Spasskii AA (1983) [On the zoological system of the higher cestodes.] In: Fourth National Conference of Parasitology, Varna, 3–5 October 1983, Abstracts, Sofia, Publishing House of Bulgarian Academy of Sciences, pp 29–30. (In Russian)Google Scholar
- Spasskii AA (2002) [A sketch on the taxonomic system of the cyclophyllidean tapeworms.] In: V.D. Gulyaev (ed.), Parazitologicheskie Issledovaniya v Sibiri i na Dal’nem Vostoke. Institut Sistematiki i Ekologii Zhivotnykh SO RAN, Novosibirsk, pp 175–177. (In Russian)Google Scholar
- Spasskii AA, Spasskaya LP (1973) [A new subfamily, Gryporhynchinae subfam. n. (Cestoda: Cyclophyllidea).] Izvestiya Akademii Nauk Moldavskoy SSR. Seriya Biologicheskikh i Khimicheskikh Nauk 5:56–58. (In Russian)Google Scholar
- Spasskii AA, Spasskaya LP (1980) [Taxonomic survey of the tribes of the Dilepididae.] Izvestiya Akademii Nauk Moldavskoy SSR. Seriya Biologicheskikh i Khimicheskikh Nauk 6:53–63. (In Russian)Google Scholar
- Świderski Z (1968) The fine structure of spermatozoon of sheep tapeworm, Moniezia expansa (Rud., 1810) (Cyclophyllidea, Anoplocephalidae). Zoologica Poloniae 18:47–48Google Scholar
- Świderski Z (1976) Fine structure of the spermatozoon of Lacistorhynchus tenuis (Cestoda, Trypanorhyncha). Proceedings of the 6th European congress on electron microscopy. Jerusalem, pp 309–310Google Scholar
- Świderski Z, Mackiewicz JS (2002) Ultrastructure of spermatogenesis and spermatozoa of the caryophyllidean cestode Glaridacris catostomi Cooper, 1920. Acta Parasitol 47:83–104Google Scholar
- Świderski Z, Salamatin RV, Tkach VV (2000) Electron microscopical study of spermatozoa of the cestode Dilepis undula (Cyclophyllidea, Dilepididae). Vest Zool 34:93–97Google Scholar
- Świderski Z, Salamatin RV, Kornyushin VV (2002) Ultrastructure of the spermatozoon of the dilepididae cestode Kowalewskiella glareola (Burt, 1940) Lopez-Neira, 1952. In: Proceedings of the 12th Conference of Ukrainian Society of Parasitologists, Sevastopol, pp 132Google Scholar
- Tian X, Yuan L, Huo X, Han X, Li Y, Xu M, Lu M, Dai J, Dong L (1998) Ultrastructural observations on the transformation of the spermatozoon in spermatogenesis of taeniid cestodes. ChinJ Parasitol Parasite Dis 16:269–273Google Scholar
- Waeschenbach A, Webster BL, Bray RA, Littlewood DTJ (2007) Added resolution among ordinal level relationships of tapeworms (Platyhelminthes: Cestoda) with complete small and large subunit nuclear ribosomal RNA genes. Mol Phylogenet Evol 45:311–325PubMedCrossRefGoogle Scholar
- Willms K, Caro JA, Robert L (2003) Ultrastructure of spermatogonia and spermatocyte lobules in Taenia solium strobilae (Cestoda, Cyclophyllidea, Taeniidae) from golden hamsters. Parasitol Res 90:479–488PubMedCrossRefGoogle Scholar
- Willms K, Robert L, Jimenez JA, Everhart M, Kuhn RE (2004) Ultrastructure of spermiogenesis and the spermatozoon in Taenia crassiceps strobilae WFU strain (Cestoda, Cyclophyllidea, Taeniidae) from golden hamsters. Parasitol Res 93:262–267PubMedCrossRefGoogle Scholar
- Xylander WER (1989) Ultrastructural studies on the reproductive system of Gyrocotylidea and Amphilinidea (Cestoda): spermatogenesis, spermatozoa, testes and vas deferens of Gyrocotyle. Int J Parasitol 19:897–905CrossRefGoogle Scholar
- Yoneva A, Georgieva K, Mizinska Y, Georgiev BB, Stoitsova SR (2006a) Ultrastructure of spermiogenesis and mature spermatozoon of Skrjabinoporus merops (Cyclophyllidea, Metadilepididae). Acta Parasitol 51:200–208CrossRefGoogle Scholar
- Yoneva A, Miquel J, Świderski Z, Georgieva K, Mizinska Y, Georgiev BB (2006b) Ultrastructure of spermiogenesis and mature spermatozoon of Angularella beema (Clerc, 1906) (Cestoda, Cyclophyllidea, Dilepididae). Acta Parasitol 51:264–272CrossRefGoogle Scholar
- Yoneva A, Georgieva K, Mizinska Y, Nikolov PN, Georgiev BB, Stoitsova SR (2008) Ultrastructure of spermiogenesis and mature spermatozoon of Anonchotaenia globata (von Linstow, 1879) (Cestoda, Cyclophyllidea, Paruterinidae). Acta Zool (Stockh) (in press)Google Scholar