Spermiogenesis and sperm ultrastructure in Calicotyle affinis Scott, 1911 (Platyhelminthes, Monogenea, Monopisthocotylea, Monocotylidae)

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Summary

Spermatological characteristics of Calicotyle affinis Scott, 1911, an endoparasitic monocotylid monogenean from the cloaca of a holocephalan fish Chimaera monstrosa L, have been investigated by means of transmission electron microscopy for the first time. Spermiogenesis exhibits features basically similar to those of the congeneric Calicotyle kroyeri and Calicotyle australiensis, but there are some new findings with respect to the formation and fine structure of the spermatozoon including the remarkable complex end-piece (EP). Morphogenesis of the EP, which is located at the anterior (proximal) region of the late spermatid, includes two stages: (1) the centriolar region is continuous with a cytoplasmic mass of the zone of differentiation, the electron-dense surface of the spermatid undergoes significant changes in the sculpturing and the inner core of developing spermatid is electron-lucent; (2) after central fusion of the arching membranes a definitive structure of the EP is subsequently evolved, finally comprising 3 – 4 electron-dense discs attached to a central common electron-lucent column. The EP is considered as a synapomorphy of the genera Calicotyle + Dictyocotyle. The mature spermatozoon of C. affinis comprises the EP, two parallel axonemes of almost equal lengths with the 9 + “1” trepaxonematan pattern, mitochondrion, nucleus, and a reduced number of parallel cortical microtubules (1 – 3). The posterior (distal) extremity of the mature spematozoon contains a single tapering axoneme. Ultrastructural characteristics of the mature spermatozoon of C. affinis coincide mostly with those of congeneric C. australiensis. Variations of the spermatological characters within the genus Calicotyle, between Calicotyle and enigmatic Dictyocotyle as well as other monocotylid monogeneans are discussed.

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  • Bakhoum A.J.S. Miquel J. Ndiaye P.I. Justine J.-L. Falchi A. Bâ C.T. Marchand B. Quilichini Y. (2017): Advances in spermatological characters in the Digenea: review and proposal of spermatozoa models and their phylogenetic importance. Adv. Parasitol. 98: in press.

  • Bruňanská M. (2010): Recent insights into spermatozoa development and ultrastructure in the Eucestoda. In: Lejeune T. Delvaux P. (Eds) Human spermatozoa: maturation capacitation and abnormalities. Nova Science Publishers Inc. New York pp. 327 – 354

  • Bruňanská M. Bílý T. Nebesářová J. (2015): Nippotaenia mogurndae Yamaguti et Myiata 1940 (Cestoda Nippotaeniidea): first data on spermiogenesis and sperm ultrastructure. Parasitol. Res. 114: 1443 – 1453. DOI: 10.1007/s00436-015-4327-0

  • Bruňanská M. Mackiewicz J.S. Poddubnaya L.G. (2017): Spermatological characteristics of the enigmatic monogenean Dictyocotyle coeliaca Nybelin 1941 (Monopisthocotylea: Monocotylidae) reveal possible adaptation to endoparasitism. Acta Parasitol. 62: 110 – 120. DOI: 10.1515/ap-2017-0013

  • Bruňanská M. Poddubnaya L.G. Xylander W.E.R. (2012): Spermatozoon cytoarchitecture of Amphilina foliacea (Platyhelminthes Amphilinidea). Parasitol. Res. 111: 2063 – 2069. DOI: 10.1007/s00436-012-3053-0

  • Chisholm L.A. Wheeler T.A. Beverley-Burton M. (1995): A phylogenetic analysis and revised classification of the Monocotylidae Taschenberg 1879 (Monogenea). Syst. Parasitol. 32: 159 – 191. DOI: 10.1007/BF00008827

  • Chisholm L.A. Hansknecht T.J. Whittington I.D. Overstreet R.M. (1997): A revision of the Calicotylinae Monticelli 1903 (Monogenea: Monocotylidae). Syst. Parasitol. 38: 159 – 183. DOI: 10.1023/A:1005844306178

  • Chisholm L.A. Morgan J.A.T. Adlard R.D. Whittington I.D. (2001): Phylogenetic analysis of the Monocotylidae (Monogenea) inferred from 28S rDNA sequences. Int. J. Parasitol. 31: 1537 – 1547. DOI: 10.1016/S0020-7519(01)00313-7

  • Ehlers U. (1985): Phylogenetic relationship within the Platyhelminthes. In: Conway Morris S. George J.D. Gibson R. Platt H.M. (Eds) The origin and relationships of lower invertebrates. Oxford University Press Oxford pp. 143 – 158

  • Hoberg E.P. Mariaux J. Brooks D.R. (2001): Phylogeny among the orders of the Eucestoda (Cercomeromorphae): integrating morphology molecules and total evidence. In: Littlewood D.T.J. Bray R.A. (Eds) Interrelationships of the Platyhelminthes. Taylor and Francis London New York pp. 112 – 126

  • Justine J.L. (1991a): Cladistic study in the Monogenea (Platyhelminthes) based upon a parsimony analysis of spermiogenetic and spermatozoal ultrastructural characters. Int. J. Parasitol. 21: 821 – 838

  • Justine J.L. (1991b): 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 J.L. (1993): Phylogénie des Monogènes basée sur une analyse de parcimonie des caractères de l’ultrastructure de la spermiogenèse et des spermatozoïdes incluant les résultats récents. [Phylogeny of the Monogenea based upon a parsimony analysis of characters of spermiogenesis and spermatozoon ultrastructure including recent results]. Bull. Fr. Pêche Pisci 328: 137 – 155 (In French)

  • Justine J.L. (1998): Spermatozoa as phylogenetic characters for the Eucestoda. J. Parasitol. 84: 385 – 408

  • Justine J.L. (2001): Spermatozoa as phylogenetic characters for the Platyhelminthes. In: Littlewood D.T.J. Bray R.A. (Eds) Interrelationships of the Platyhelminthes. Taylor and Francis London pp. 231 – 238

  • Justine J.L. Mattei X. (1983a): Etude ultrastructurale comparée de la spermiogenèse des Monogènes. I. Megalocotyle (Monopisthocotylea Capsalidae). [Comparative ultrastructural study of spermiogenesis in Monogeneans (Flatworms). I. Megalocotyle (Monopisthocotylea Capsalidae)]. J. Ultrastr. Res. 82: 296 – 308 (In French)

  • Justine J.L. Mattei X. (1983b): Comparative ultrastructural study of spermiogenesis in Monogeneans (Flatworms). 2. Heterocotyle (Monopisthocotylea: Monocotylidae). J. Ultrastr. Res. 84: 213 – 223

  • Justine J.L. Mattei X. (1983c): Comparative ultrastructural study of spermiogenesis in Monogeneans (Flatworms). 3. Two species of Amphibdelloides (Monopisthocotylea Amphibdellatidae). J. Ultrastr. Res. 84: 224 – 237

  • Justine J.L. Mattei X. (1984): Comparative ultrastructural study of spermiogenesis in monogeneans (Flatworms). 3. Diplectanum (Monopisthocotylea: Diplectanidae). J. Ultrastr. Res. 88: 77 – 91

  • Justine J.L. Mattei X. (1986): Comparative ultrastructural study of spermiogenesis in monogeneans (Flatworms). 5. Calceostoma (Monopisthocotylea: Calceostomatidae). J. Ultrastr. Mol. Str. Res. 96 : 54 – 63

  • Justine J.L. Mattei X. (1987): Phylogenetic relationships between the families Capsalidae and Dionchidae (Platyhelminthes Monogenea Monopisthocotylea) indicated by the comparative ultrastructural study of spermiogenesis. Zool. Scr. 16: 111 – 116

  • Justine J.L. Lambert A. Mattei X. (1985): Spermatozoon ultrastructure and phylogenetic relationships in the Monogenea (Platyhelminthes). Int. J. Parasitol. 15: 601 – 608

  • Kearn G. Whittington I. (2015): Sperm transfer in monogenean (platyhelminth) parasites. Acta Parasitol. 60: 567 – 599. DOI: 10.1515/ap-2015-0082

  • Levron C. Miquel J. Oros M. Scholz T. (2010): Spermatozoa of tapeworms (Platyhelminthes Eucestoda): advances in ultrastructural and phylogenetic studies. Biol. Rev. 85: 523 – 543. DOI: 10.1111/j.1469-185X.2009.00114.x

  • Rohde K. (1988): Phylogenetic relationship of free-living and parasitic Platyhelminthes on the basis of ultrastructural evidence. In: Ax P. Ehlers U. (Eds) Free-living and symbiotic Platyhelminthes. Gustav Fischer Verlag Stuttgart New York pp. 353 – 357

  • Rohde K. Watson N. (1986): Ultrastructure of spermatogenesis and sperm of Austramphilina elongata (Platyhelminthes Amphilinidea). J. Submicrosc. Cytol. 18: 361 – 374

  • Sproston N.G. (1946): A synopsis of the monogenetic trematodes. Trans. Zool. Soc. London 25: 185 – 600

  • Tappenden T. Kearn G.C. (1991): Spermiogenesis and sperm ultrastructure in the monocotylid monogenean Calicotyle kroyeri. Int. J. Parasitol. 21: 57 – 63. DOI:10.1016/0020-7519(91)90120-V

  • Watson N.A. (1997): Spermiogenesis and sperm ultrastructure in Troglocephalus rhinobatidisNeoheterocotyle rhinobatidis and Merizocotyle australensis (Platyhelminthes Monogenea Monopisthocotylea Monocotylidae). Int. J. Parasitol. 27: 389 – 401. DOI: 10.1016/S0020-7519(96)00203-2

  • Watson N.A. Chisholm L.A. (1998): Spermatozoa and spermiogenesis in the monocotylid Heterocotyle capricornensis (Platyhelminthes Monogenea Monopisthocotylea) including observations of aberrant folding and fusing of spermatozoa in one individual. Folia Parasitol. 45: 211 – 220

  • Watson N.A. Rohde K. (1994): Ultrastructure of sperm and spermiogenesis in the monocotylid monogeneans Monocotyle helicophallus and Calicotyle australiensis (Platyhelminthes). Int. J. Parasitol. 24: 1019 – 1030. DOI:10.1016/0020-7519(94)90168-6

  • Yamaguti S. (1963): Systema helminthum. Monogenea and Aspidocotylea vol IV. Interscience Publishers New York 699 pp.

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