Abstract
To our knowledge, this paper describes the first ultrastructural results on spermiogenesis and the spermatozoon of a Digenea belonging to the family Deropristidae, Deropristis inflata. Spermiogenesis follows the usual pattern found in the digeneans, but a single noteworthy characteristic concerns the centriole, which presents a “prominent pear-shaped electron-dense region.” Spermiogenesis in D. inflata begins with the formation of a differentiation zone. The two centrioles give rise to flagella. These two flagella undergo a rotation of 90° and fuse with the median cytoplasmic process. The proximo-distal fusion occurs at the level of attachment zones. The mature spermatozoon of D. inflata possesses five regions and presents all the features found in the digenean gamete. However, several characteristics allow us to distinguish the spermatozoon of D. inflata from other digenetic trematoda, namely the external ornamentations of the plasmic membrane, the anterior and posterior extremities. Furthermore, the distal part of the nucleus in front of those of the mitochondria appears such a distinctive criterion in the spermatozoon of this species. Our ultrastructural investigations produce new data on the reproduction of D. inflata, which may be useful for the understanding of the phylogenetic relationships in the Deropristidae family.
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Agostini S, Miquel J, Ndiaye P, Marchand B (2005) Dicrocoelium hospes Looss, 1907 (Digenea, Dicrocoeliidae): spermiogenesis, mature spermatozoon and ultrastructural comparative study. Parasitol Res 96:38–48
Bâ CT, Marchand B (1995) Spermiogenesis, spermatozoa and phyletic affinities in the Cestoda. Mem Mus Natl Hist Nat 166:87–95
Baptista-Farias MFD, Kohn A, Cohen SC (2001) Ultrastructure of spermatogenesis and sperm development in Saccocoeliodes godoyi Kohn & Froes, 1896 (Digenea, Haploporidae). Mem Inst Oswaldo Cruz 96:61–70
Brooks DR (1989) A summary of the database pertaining to the phylogeny of the major groups of parasitic platyhelminths, with a revised classification. Can J Zool 67:714–720
Brooks DR, O’Grady RT, Glen DR (1985) The phylogeny of the Cercomeria, Brooks, 1982 (Platyhelminthes). Proc Helminthol Soc Wash 52:1–20
Brooks DR, Bandoni SM, Macdonald CA, O’Grady RT (1989) Aspects of the phylogeny of the Trematoda Rudoplphi, 1808 (Platyhelminthes: Cercomeria). Can J Zool 67:2609–2624
Burton PR (1972) Fine structure of the reproductive system of a frog lung fluke. III. The spermatozoon ands its differentiation. J Parasitol 58:68–83
Carranza S, Baguñà J, Riutort M (1997) Are the Platyhelminthes a monophyletic primitive group? An assessment using 18S rDNA sequences. Mol Biol Evol 14:485–497
Castilho F, Barandela T (1990) Ultrastructural study on the spermiogenesis and spermatozoon of the metacercaraie of Microphallus primas (Digenea), a parasite of Carcinus maenas. Mol Reprod Dev 25:140–146
Choudhury A, Dick TA (1998) Systematics of the Deropristiidae Cable and Hunninen, 1942 (Trematoda) and biogeographical associations with sturgeons (Osteichthyes: Acipenseridae). Syst Parasitol 41:21–39
Cifrian B, Garcia-Corrales P, Martinez Alos S (1993) Ultrastructural study of the spermatogenesis and mature spermatozoa of Dicrocoelium dendriticum (Plathelminthes, Digenea). Parasitol Res 79:204–212
Cribb TH, Bray RA, Olson PD, Littlewood DTJ (2003) Life cycle evolution in the Digenea: a new perspective from phylogeny. Adv Parasitol 54:197–254
Ehlers U (1984) Phylogenetisches system der Plathelminthes. Verh Nat Wiss Ver Hamburg 27:291–294
Ehlers U (1986) Comments on a phylogenetic system of the Platyhelminthes. Hydrobiologia 132:1–12
Erwin BE, Halton DW (1983) Fine structural observations on spermatogenesis in a progenetic Trematode, Bucephaloides gracilescens. Int J Parasitol 13:413–426
Fujino T, Ishii Y, Mori T (1977) Ultrastructural studies on the spermatozoa and spermatogenesis in Paragonimus and Eurytrema (Trematoda: Digenea). Jap J Parasitol 26:240–255
Gracenea M, Ferrer JR, Gonzalez-Moreno O, Trullols M (1997) Ultrastructural study of spermatogenesis and the spermatozoon in Postorchigenes gymnesicus (Trematoda, Lecithodendriidae). J Morphol 234:223–232
Gracenea M, Ferrer JR, Gonzalez-Moreno O (2000) The spermatogenesis and the spermatozoon in Brachylaima sp. (Digenea): ultrastructural study. Acta Parasitol 45:169
Grant WC, Harkema R, Muse KE (1976) Ultrastructure of Pharyngostomoides procyonis Harkema 1942 (Diplostomatidae). I. Observations on the male reproductive system. J Parasitol 62(1):39–49
Hendow HT, James BL (1988) Ultrastructure of spermatozoon and spermatogenesis in Maritrema linguilla (Digenea: Microphallidae). Int J Parasitol 18:53–63
Iomini C, Justine JL (1997) Spermatozoon and spermiogenesis of Echinostoma caproni (Platyhelminthes: Digenea): transmission and scanning electron microscopy, and tubulin immunocytochemistry. Tissue Cell 29:107–118
Iomini C, Mollaret I, Albaret JL, Justine JL (1997) Spermatozoon and spermiogenesis in Mesocoelium monas (Platyhelminthes: Digenea): ultrastructure and epifluorescence microscopy of labelling of tubulin and nucleus. Folia Parasitol 44:26–32
Jamieson BGM, Daddow LYM (1982) The ultrastructure of the spermatozoon of Neochasmus sp. (Cryptogonimidae, Digenea, Trematoda) and its phylogenetic significance. Int J Parasitol 12:547–559
Jones A, Bray RA, Gibson DI (2005) Keys to the trematoda. CABI publishing and the Natural History Museum, UK, London, p 768
Justine JL (1991) Phylogeny of parasitic Platyhelminthes: a critical study of synapomorphies proposed on the basis of the ultrastructure of spermiogenesis and spermatozoa. Can J Zool 69:1421–1440
Justine JL (1995) Spermatozoal ultrastructure and phylogeny in the parasitic Platyhelminthes. Mem Mus Natl Hist Nat 166:55–86
Justine JL (1997) La classification générale des Plathelminthes parasites: changements récents et utilisation des caractères ultrastructuraux, en particulier des spermatozoïdes. Bull Soc Zool Fr 122:269–277
Justine JL (1999) Spermatozoa of Platyhelminthes: comparative ultrastructure, tubulin immunocytochemistry and nuclear labeling. In: Gagnon C (ed) The male gamete: from basic science to clinical applications. Cache River, Vienna, Illinois, pp 351–362
Justine JL (2001) Spermatozoa as phylogenetic characters for the Platyhelminthes. In: Littlewood DTJ, Bray RA (eds) Interrelationships of the platyhelminthes. Taylor and Francis, London, pp 231–238
Justine JL, Mattei X (1981) Etude ultrastructurale du flagelle spermatique des Schistosomes (Trematoda: Digenea). J Ultrastruct Res 76:89–95
Justine JL, Mattei X (1982a) Etude ultrastructurale de la spermiogénèse et du spermatozoïde d’un Plathelminthe: Gonapodasmius (Trematoda: Didymozoidae). J Ultrastruct Res 79:350–365
Justine JL, Lambert A, Mattei X (1985) Spermatozoon ultrastructure and phylogenetic relationships in the monogeneans (Platyhelminthes). Int J Parasitol 15:601–608
Levron C, Ternengo S, Marchand B (2003) Ultrastructure of spermiogenesis and the spermatozoon of Helicometra fasciata (Digenea, Opecoelidae), a parasite of Labrus merula (Pisces, Teleostei). Acta Parasitol 48:255–264
Levron C, Ternengo S, Marchand B (2004a) Ultrastructure of spermiogenesis and the spermatozoon of Monorchis parvus (Digenea, Opecoelidae), a parasite of Diplodus annularis (Pisces, Teleostei). Parasitol Res 93(2):102–110
Levron C, Ternengo S, Marcahnd B (2004b) Spermiogenesis and sperm ultrastructure of Poracanthium furcatum (Trematoda, Digenea, Opecoelidae), a parasite of Mullus surmuletus (Pisces, Teleostei). Acta Parasitol 49(3):190–200
Levron C, Ternengo S, Marchand B (2004c) Spermiogenesis and sperm ultrastructure of Diphterostomum brusinae (Digenea, Zoogonidae), a parasite of Diplodus annularis (Pisces, Teleostei). Parasitol Res 94(2):147–154
Littlewood DTJ, Rohde K, Clough KA (1999) The interrelationships of all major groups of Platyhelminthes: phylogenetic evidence from morphology and molecules. Biol J Linn Soc 66:75–114
Littlewood DTJ, Cribb TH, Olson PD, Bray RA (2001) Platyhelminth phylogenetics—a key to understanding parasitism? Belg J Zool 131:35–46
Miquel J, Nourrisson C, Marchand B (2000) Ultrastructure of spermiogenesis and the spermatozoon of Opecoeloides furcatus (Trematoda, Digenea, Opecoelidae), a parasite of Mullus barbatus (Pisces, Teleostei). Parasitol Res 86:301–310
Mollaret I, Jamieson BGM, Adlard RD, Hugall A, Lecointre G, Chombard C, Justine JL (1997) Phylogenetic analysis of the Monogenea and their relationships with Digenea and Eucestoda inferred from 28S rDNA sequences. Mol Biochem Parasitol 90:433–438
Ndiaye PI, Miquel J, Bâ CT, Feliu C, Marchand B (2002) Spermiogenesis and sperm ultrastructure of Scaphiostomum palaearcticum Mas-Coma, Esteban et Valero, 1986 (Trematoda, Digenea, Brachylaimidae). Acta Parasitol 47(4):259–271
Ndiaye PI, Miquel J, Feliu C, Marchand B (2003a) Ultrastructure of spermiogenesis and spermatozoa of Notocotylus neyrai Gonzalez castro, 1945 (Digenea, Notocotylidae), intestinal parasite of Microtus agrestis (Rodentia: Arvicolidae) in Spain. Invertebr Reprod Dev 43:105–115
Ndiaye PI, Miquel J, Fons R, Marchand B (2003b) Spermiogenesis and sperm ultrastructure of the liver fluke Fasciola hepatica Linnaeus, 1758 (Digenea, Fasciolidae): transmission and scanning electron microscopy, and tubulin immunocytochemistry. Acta Parasitol 48:182–194
Ndiaye PI, Miquel J, Bâ CT, Marchand B (2004) Ultrastructure of spermiogenesis and the spermatozoon of the liver fluke Fasciola gigantica Cobbold, 1856 (Digenea, Fasciolidae), a parasite of cattle in Senegal. J Parasitol 90(1):30–40
Olson PD, Cribb TH, Tkach VV, Bray RA, Littlewood DTJ (2003) Phylogeny and classification of the Digenea (Platyhelminthes: Trematoda). Int J Parasitol 33:733–755
Orido Y (1988) Ultrastructure of spermatozoa of the lung fluke, Paragonimus ohirai (Trematoda: Troglotrematidae), in seminal receptacle. J Morphol 196:333–343
Pamplona-Basilio MC, Baptista-Farias MFD, Kohn A (2001) Spermatogenesis and spermiogenesis in Didymocystis wedli Ariola, 1902 (Didymozoidae, Digenea). Mem Inst Oswaldo Cruz 96:1153–1159
Quilichini Y, Foata J, Marchand B (2007) Ultrastructural study of spermiogenesis and the spermatozoon of Crepidostomum metoecus (Digenea, Allocridiidae), a parasite of Salmo trutta (Pisces, Teleostei). J Parasitol (in press)
Rees FG (1979) The ultrastructure of the spermatozoon and spermiogenesis in Cryptocotyle lingua (Digenea: Heterophyidae). Int J Parasitol 9:405–419
Reynolds ES (1963) The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol 17:208–212
Rohde K, Hefford C, Ellis JT, Baverstock PR, Johnson AM, Watson NA, Dittmann S (1993) Contributions to the phylogeny of Platyhelminthes based on partial sequencing of 18s ribosomal DNA. Int J Parasitol 23:705–724
Sharma PN, Rai N (1995) Ultrastructural study on spermatogenesis in Ganeo tigrinum, an intestinal trematode of Rana tigrina. J Helminthol 69:77–84
Stitt AW, Fairweather I (1990) Spermatogenesis and the fine structure of the mature spermatozoon of the liver fluke, Fasciola hepatica (Trematoda: Digenea). Parasitology 101:395–407
Tang J, Wang W, Wang G (1998) Studies on ultrastructure of spermatogenesis and sperm in Pseudorhipidocotyle elpichthys. Acta Hydrobiol Sin 22:168–173
Zd’arska Z, Soboleva TN, Sterba J, Valkounova J (1991) Ultrastructure of the male reproductive system of the trematode Brachylaimus aequans. Folia Parasitol 38:33–37
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We would like to thank the Biguglia reserve for providing us with eels.
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Foata, J., Quilichini, Y. & Marchand, B. Spermiogenesis and sperm ultrastructure of Deropristis Inflata Molin, 1859 (Digenea, Deropristidae), a parasite of Anguilla anguilla . Parasitol Res 101, 843–852 (2007). https://doi.org/10.1007/s00436-007-0550-7
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DOI: https://doi.org/10.1007/s00436-007-0550-7