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Licensed Unlicensed Requires Authentication Published by De Gruyter December 28, 2016

Spermatological characteristics of the enigmatic monogenean Dictyocotyle coeliaca Nybelin, 1941 (Monopisthocotylea: Monocotylidae) reveal possible adaptation to endoparasitism

Magdaléna Bruňanská, John S. Mackiewicz and Larisa G. Poddubnaya
From the journal Acta Parasitologica

Abstract

Spermatological characters of Dictyocotyle coeliaca Nybelin, a unique endoparasitic monogenean from the body cavity of the ray Amblyraja radiata (Elasmobranchii: Rajidae), was investigated by means of scanning and transmission electron microscopy for the first time. The process of the spermatozoon formation begins with the appearance of the differentiation zone which contains two centrioles. Subsequently developed two free flagella rotate to lie parallel before their fusing. After fusion, both the mitochondrion and nucleus migrate alongside the axonemes. Spermatids are formed within parallel cytoplasmic canals. During late spermiogenesis, an electron-dense spiral end-piece is formed proximally to the centriolar region of some spermatids. At the end of spermiogenesis, this end-piece is separated by a plasma membrane from the late spermatid and remains in the residual cytoplasm when spermatozoa are released into the testis lumen. The mature spermatozoon of D. coeliaca contains two parallel axonemes with the 9 + “1” trepaxonematan pattern, mitochondrion, nucleus, parallel cortical microtubules, and electron-dense granules. Especially the presence of electron-dense granules, occurring frequenly in the spermatozoa of endoparasitic flatworms, may indicate an adaptation to endoparasitic lifestyle in D. coeliaca. The anterior extremity of the male gamete contains one centriolar derivative, a small component of the second centriolar derivative and anterior extremity of the mitochondrion. The posterior extremity of the mature spematozoon exhibits tubular elements of the disorganized axoneme. Variations of the spermatozoon ultrastructural characters within monocotylid monogeneans and possible evolutionary significance of glycogen in sperm to the endoparasitic habit are discussed.

Acknowledgements

The authors would like to specially thank Dr. Willy Hemmingsen, University of Troms⊘ (Norway), and the staff of the RV ‘Johan Ruud’, of the University for their help with the fishing and material collection. The authors are grateful to the staff of the Centre of Electron Microscopy, I.D. Papanin Institute for the Biology of Inland Waters, Russian Academy of Sciences, Borok, Russia, for technical assistance. We thank an anonymous reviewer for reference to A. paronaperugiae. The present study was supported by the Russian Foundation for Fundamental Research (Project no. 15-04-02890a to LGP) and the Grant Agency of the Slovak Republic VEGA (Project no. 2/0104/16 to MB). The work was realized within a frame of Centre of Excellence for Parasitology (Code ITMS: 26220120022) based on the support of the Operational Programme “Research & Development” funded from the European regional Development Fund (rate 0.4).

References

Anderson W.A., Personne P. 1970. The localization of glycogen in the spermatozoa of various invertebrate and vertebrate species. The Journal of Cell Biology, 44, 29–51. 10.1083/ jcb.44.1.29Search in Google Scholar

Bakhoum A.J.S., Quilichini Y., Justine J.L., Bray R.A., Miquel J., Feliu C., Bâ C.T., Marchand B. 2015. First spermatological study in the Atractotrematidae (Digenea, Haploporoidea): the case of Atractotrema sigani, intestinal parasite of Siganus lineatus. Parasite, 22, 26. http://dx.doi.org/10.1051/parasite/2015026Search in Google Scholar

Brinkmann A. Jr. 1952. Fish trematodes from Norwegian waters. The history of fish trematode investigations in Norway and the Norwegian species of the order Monogenea. Universitetet i Bergen Årbok, Naturvitenskapelig Rekke 1, 1–134Search in Google Scholar

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

Bruňanská M., Brázová T., Zhokhov A.E., Poddubnaya L.G. 2014. Ultrastructural features of the spermatozoon and its differentiation in Brandesia turgida (Brandes, 1888) (Digenea, Microphalloidea, Pleurogenidae). Parasitology Research, 113, 2483–2491. 10.1007/s00436-014-3897-6Search in Google Scholar

Bruňanská M., Poddubnaya L.G., Xylander W.E.R. 2012. Spermatozoon cytoarchitecture of Amphilina foliacea (Platyhelminthes, Amphilinidea). Parasitology Research, 111, 2063–2069. 10.1007/s00436-012-3053-0Search in Google Scholar

Bruňanská M., Poddubnaya L.G., Xylander W.E.R. 2013. A reinvestigation of spermiogenesis in Amphilina foliacea (Platyhelminthes: Amphilinidea). Folia Parasitologica, 60, 43–50. 10.14411/fp.2013.006Search in Google Scholar

Burton P.R. 1972. Fine structure of the reproductive system of a frog lung-fluke. III. The spermatozoon and its differentiation. Journal of Parasitology, 58, 68–8310.2307/3278243Search in Google Scholar

Bychowsky B.E. 1957. Monogenetic trematodes, their classification and phylogeny. Izdatel’stvo Academiya Nauk SSSR, Moscow-Leningrad, 509 pp. (in Russian)Search in Google Scholar

Chisholm L.A., Wheeler T.A., Beverley-Burton M. 1995. A phylogenetic analysis and revised classification of the Monocotylidae Taschenberg, 1879 (Monogenea). Systematic Parasitology, 32, 159–191. 10.1007/BF00008827Search in Google Scholar

Chisholm L.A., Hansknecht T.J., Whittington I.D., Overstreet R.M. 1997. A revision of the Calicotylinae Monticelli, 1903 (Monogenea: Monocotylidae). Systematic Parasitology, 38, 159–183. 10.1023/A:1005844306178Search in Google Scholar

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. International Journal of Parasitology, 31, 1537–1547. 10.1016/S0020-7519(01) 00313-7Search in Google Scholar

Dawes B. (Ed.)1946. The Trematoda, with special reference to British and other European forms. Cambridge University Press, Cambridge, pp. 613Search in Google Scholar

Dawes B., Griffiths I. 1958. The enigmatical trematode "Dictyocotyle coeliaca". Nature, 182, 1033–1034. DOI:10.1038/1821033a010.1038/1821033a0Search in Google Scholar PubMed

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

Euzet E., Combes C. 1998. The selection of habitats among the monogenea. International Journal of Parasitology, 28, 1645–1652. 10.1016/S0020-7519(98)00062-9Search in Google Scholar

Fournier A. 1976. The tegument of Euzetrema knoepffleri, endoparasitic Monogenean of an amphibian: ultrastructure and evolution during the life cycle. Annales de Parasitologie Humaine et Comparée,51, 15–2610.1051/parasite/1976511015Search in Google Scholar

Fournier A., Justine J.L. 1994. Ultrastructure of spermiogenesis and spermatozoa in Euzetrema knoepffleri (Platyhelminthes, Monogenea). Parasite, 7, 123–12610.1051/parasite/1994012123Search in Google Scholar

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

Justine J. L. 1991a. Cladistic study in the Monogenea (Platyhelminthes), based upon a parsimony analysis of spermiogenetic and spermatozoal ultrastructural characters. International Journal for Parasitology, 21, 821–83810.1016/0020-7519(91)90151-VSearch in Google Scholar

Justine J. L. 1991b. Phylogeny of parasitic Platyhelminthes: a critical study of synapomorphies proposed on the basis of the ultrastructure of spermiogenesis and spermatozoa. Canadian Journal of Zoology, 69, 1421–144010.1139/z91-203Search in Google Scholar

Justine J.L. 1993. Phylogénie des Monogènes basée sur une analyse de parcimonie des caractères de l’ultrastructure de la spermiogenèse et des spermatozoϊdes incluant les résultats récents. Bulletin français de la pêche et de la pisciculture, 328, 137–155 ( In Franch)10.1051/kmae:1993018Search in Google Scholar

Justine J.L. 1998. Spermatozoa as phylogenetic characters for the Eucestoda. Journal of Parasitology, 84, 385–40810.2307/3284502Search in Google Scholar

Justine J.L. 2001. Spermatozoa as phylogenetic characters for the Platyhelminthes. In: (Eds. D.T.J. Littlewood and R.A. Bray) Interrelationships of the Platyhelminthes. Taylor and Francis, London, New York, 231–238Search in Google Scholar

Justine J.L., Mattei X. 1983a. Comparative ultrastructural study of spermiogenesis in Monogeneans (Flatworms). 2. Heterocotyle (Monopisthocotylea: Monocotylidae). Journal of Ultrastructure Research, 84, 213–22310.1016/S0022-5320(83)80002-1Search in Google Scholar

Justine J.L., Mattei X. 1983b. Comparative ultrastructural study of spermiogenesis in Monogeneans (Flatworms). 3. Two species of Amphibdelloides (Monopisthocotylea: Amphibdellatidae). Journal of Ultrastructure Research, 84, 224–23710.1016/S0022-5320(83)80003-3Search in Google Scholar

Justine J.L., Mattei X. 1984. Comparative ultrastructural study of spermiogenesis in Monogeneans (Flatworms). 3. Diplectanum (Monopisthocotylea: Diplectanidae). Journal of Ultrastructure Research, 88, 77–9110.1016/S0022-5320(84)90183-7Search in Google Scholar

Justine J.L., Mattei X. 1985. A spermatozoon with undulating membrane in a parasitic Flatworm, Gotocotyla (Monogenea, Polyopisthocotylea, Gotocotylidae). Journal of Ultrastructure Research, 90, 163–17110.1016/0889-1605(85)90106-5Search in Google Scholar

Justine J.L., Mattei X. 1988. Bending of 9 + “1” axonemes of flatworm spermatozoa in hypotonic media: an experimental study. Journal of Ultrastructure and Molecular Structure Research, 100, 31–3810.1016/0889-1605(88)90056-0Search in Google Scholar

Justine J.L., Lambert A., Mattei X. 1985. Spermatozoon ultrastructure and phylogenetic relationships in the Monogenea (Platyhelminthes). International Journal for Parasitology, 15, 601–60810.1016/0020-7519(85)90004-9Search in Google Scholar

Kearn G.C. 1994. Evolutionary expansion of the Monogenea. International Journal of Parasitology, 24, 1227–1271. 10.1016/0020-7519(94)90193-7Search in Google Scholar

Kearn G., Whittington I. 2015. Sperm transfer in monogenean (platyhelminth) parasites. Acta Parasitologica, 60, 567–599. 10.1515/ap-2015-0082Search in Google Scholar

Levron C., Miquel J., Oros M., Scholz T. 2010. Spermatozoa of tapeworms (Platyhelminthes, Eucestoda): advances in ultrastructural and phylogenetic studies. Biological Reviews, 85, 523–543. 10.1111/j.1469-185X.2009.00114.xSearch in Google Scholar

Lyons K.M. 1973. The epidermis and sense organs of the Monogenea and some related groups. Advances in Parasitology, 11, 193–23210.1016/S0065-308X(08)60187-6Search in Google Scholar

Quilichini Y., Foata J., Marchand B. 2009. Ultrastructural study of spermiogenesis and the spermatozoon of Microcotyle panceri (Monogenea: Polyopisthocotylea: Microcotylidae), parasite of meagre Argyrosomus regius (Pisces, Teleostei). Journal of Parasitology, 95, 261–270. http://dx.doi.org/10.1645/GE-1302.1Search in Google Scholar PubMed

Poddubnaya L.G., Hemmingsen W., Gibson D.I. 2016. Surface ultrastructural characteristics of Dictyocotyle coeliaca Nybelin, 1941 (Monopisthocotylea: Monocotylidae), an endoparasitic monogenean of rays. Parasitology Research, 115, 965–973. 10.1007/s00436-015-4823-2Search in Google Scholar PubMed

Poulin R. (Ed.) 2006. Evolutionary Ecology of Parasites. Princeton University Press, Princeton, New Jersey, pp.342Search in Google Scholar

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

Rohde K., Watson N. 1986. Ultrastructure of spermatogenesis and sperm of Austramphilina elongata (Platyhelminthes, Amphilinidea). Journal of Submicroscopic Cytology and Pathology, 18, 361–374Search in Google Scholar

Rohde K., Watson N.A. 1994. Ultrastructure of spermiogenesis and spermatozoa of Polylabroides australis (Platyhelminthes, Monogenea, Polyopisthocotylea, Microcotylidae). Parasite, 1, 115–122. http://dx.doi.org/10.1051/parasite/1994012115Search in Google Scholar

Schmahl G., Elwasila M. 1992. Fine structure of spermatogenesis in monopisthocotylean monogeneans (Macrogyrodactylus polypteri; Pseudodactylogyrus bini). Folia Parasitologica, 39, 19–31Search in Google Scholar

Sproston N.G. 1946. A synopsis of the monogenetic trematodes. Transactions of the Zoological Society of London, 25, 185–60010.1111/j.1096-3642.1946.tb00218.xSearch in Google Scholar

Tappenden T., Kearn G.C. 1990. Spermiogenesis and sperm ultrastructure in the Monogenean parasite Acanthocotyle lobianchi. International Journal of Parasitology, 20, 747–753. 10.1016/0020-7519(90)90008-BSearch in Google Scholar

Tappenden T., Kearn G.C. 1991. Spermiogenesis and sperm ultrastructure in the Monocotylid Monogenean Calicotyle kroyeri. International Journal of Parasitology, 21, 57–63. 10.1016/20-7519(91)90120-VSearch in Google Scholar

Watson N.A. 1997. Spermiogenesis and sperm ultrastructure in Troglocephalus rhinobatidis, Neoheterocotyle rhinobatidis and Merizocotyle australensis (Platyhelminthes, Monogenea, Monopisthocotylea, Monocotylidae). International Journal of Parasitology, 27, 389–401. 10.1016/S0020-7519(96) 00203-2Search in Google Scholar

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 Parasitologica, 45, 211–220Search in Google Scholar

Watson N.A., Rohde K. 1994. Ultrastructure of sperm and spermiogenesis in the monocotylid monogeneans Monocotyle helicophallus and Calicotyle australiensis (Platyhelminthes). International Journal of Parasitology, 24, 1019–1030. 10.1016/0020-7519(94)90168-6Search in Google Scholar

Williams H.H. 1958. The anatomy of the trematode Dictyocotyle coeliaca Nybelin, 1941, with a discussion of its relationships with species of the genus Calicotyle Diesing, 1850. Annals and Magazine of Natural History, 13, 1, 465–47810.1080/00222935808650970Search in Google Scholar

Yamaguti S. (Ed.)1963. Systema helminthum. Monogenea and Aspidocotylea, vol IV. John Wiley & Sons, Interscience Publishers, New York, pp. 699Search in Google Scholar

Received: 2016-9-12
Revised: 2016-10-10
Accepted: 2016-10-11
Published Online: 2016-12-28
Published in Print: 2017-3-1

© 2016 W. Stefański Institute of Parasitology, PAS