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Ultrastructural aspects of spermatogenesis, testes, and vas deferens in the parthenogenetic tapeworm Atractolytocestus huronensis Anthony, 1958 (Cestoda: Caryophyllidea), a carp parasite from Slovakia

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Abstract

Spermatogenesis, testes, and vas deferens in the parthenogenetic monozoic tapeworm Atractolytocestus huronensis Anthony, 1958 (Cestoda: Caryophyllidea) from Slovakia, parasitizing the carp Cyprinus carpio L., have been investigated by means of transmission electron microscopy for the first time. The present results show that helminths with parthenogenetic and normal reproduction may share some common spermatology features, e.g., dense cytoplasm of the peripherally localized spermatogonia or a rosette type of spermatogenesis. In contrast to tapeworms with normal reproduction, the most prominent ultrastructural characteristic of the spermatocytes of A. huronensis is fragmentation of their nuclei. This clear feature of cell degeneration might be a consequence of the aberrant first meiotic division. Peripheral cortical microtubules and a single centriole, indicators of the ongoing spermiogenesis, were observed only very rarely in the early spermatids. Characteristics of normal spermiogenesis, i.e., apical dense material in the zone of differentiation in early stages of spermiogenesis, flagellar rotation, and proximo-distal fusion, were never found in the present study. The testes follicles are surrounded by a thin cytoplasmic sheath underlined by a basal lamina. Vas deferens is lined by flat epithelium with numerous surface lamellae and cilia. Mature, functional spermatozoa were not observed in the vas deferens of A. huronensis from Slovakia.

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References

  • Bruňanská M (2009) Spermatological characters of the caryophyllidean cestode Khawia sinensis Hsü, 1935, a carp parasite. Parasitol Res 105:1603–1610

    Article  PubMed  Google Scholar 

  • 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, New York, pp 327–354

    Google Scholar 

  • Bruňanská M, Poddubnaya LG, Dezfuli B (2005) Vitellogenesis in two spathebothriidean cestodes. Parasitol Res 96:390–397

    Article  PubMed  Google Scholar 

  • Bruňanská M, Drobníková P, Oros M (2009) Vitellogenesis in the cestode Atractolytocestus huronensis Anthony, 1958 (Caryophyllidea: Lytocestidae). Parasitol Res 105:647–654

    Article  PubMed  Google Scholar 

  • Cable RM (1971) Parthenogenesis in parasitic helminths. Am Zool 11:267–272

    Google Scholar 

  • Cannon LRG (1971) The life cycle of Bunodera sacculata and B. luciopercae (Trematoda: Allocreadiidae) in Algonquin Park, Ontario. Can J Zool 49:1417–1429

    Google Scholar 

  • Davydov VG, Poddubnaya LG, Kolesnikova GA (1994) Ultrastructure of genital system ducts of Caryophyllaeus laticeps (Cestoda, Caryophyllidea). Parazitologiya 28:501–509, In Russian

    Google Scholar 

  • Dobson MJ, Pearlman RE, Karaiskakis A, Spyropoulous B, Moens PB (1994) Synaptonemal complex proteins: occurrence, epitope mapping and chromosome disjunction. J Cell Sci 107:2749–2760

    CAS  PubMed  Google Scholar 

  • Fujino T, Ishii Y (1982) Ultrastructural studies on spermatogenesis in a parthenogenetic type of Paragonimus westermani (Kerbert 1878) proposed as P. pulmonalis (Baelz 1880). J Parasitol 68:433–441

    Article  CAS  PubMed  Google Scholar 

  • Grey AJ, Mackiewicz JS (1980) Chromosomes of caryophyllidean cestodes: diploidy, triploidy, and parthenogenesis in Glaridacris catostomi. Int J Parasitol 10:397–407

    Article  Google Scholar 

  • Halton DW, Hardcastle A (1976) Spermatogenesis in a monogenean, Diclidophora merlangi. Int J Parasitol 6:43–53

    Article  CAS  PubMed  Google Scholar 

  • Jones AW, Mackiewicz JS (1969) Naturally occurring triploidy and parthenogenesis in Atractolytocestus huronensis Anthony (Cestoidea: Caryophyllidea) from Cyprinus carpio L. in North America. J Parasitol 55:1105–1118

    Article  Google Scholar 

  • Jourdane J, Imbert-Establet D, Tchuem Tchuenté LA (1995) Parthenogenesis in Schistosomatidae. Parasitol Today 11:427–430

    Article  CAS  PubMed  Google Scholar 

  • Korneva ZV, Davydov VG (2001) Ultrastructure of the male reproductive system in three proteocephalidean cestodes. Zool Zh 80:921–928, In Russian

    Google Scholar 

  • Králová-Hromadová I, Štefka J, Špakulová M, Orosová M, Bombarová M, Hanzelová V, Bazsalovicsová E, Scholz T (2010) Intra-individual internal transcribed spacer 1 (ITS1) and ITS2 ribosomal sequence variation linked with multiple rDNA loci: a case of triploid Atractolytocestus huronensis, the monozoic cestode of common carp. Int J Parasitol 40:175–181

    Article  PubMed  Google Scholar 

  • Liu G, He L (1989) G-banding of chromosomes and G-bands quantitative analysis of Spirometra mansoni with microscope photometer. Hereditas 11:12–15, in Chinese, abstract in English

    Google Scholar 

  • Mackiewicz JS (1981) Caryophyllidea (Cestoidea): evolution and classification. Adv Parasitol 19:139–206

    Article  Google Scholar 

  • Olson PD, Poddubnaya LG, Littlewood DTJ, Scholz T (2008) On the position of Archigetes and its bearing on the early evolution of the tapeworms. J Parasitol 94:898–904

    Article  CAS  PubMed  Google Scholar 

  • Oros M, Hanzelová V, Scholz T (2004) The cestode Atractolytocestus huronensis (Caryophyllidea) continues to spread in Europe: new data on the helminth parasite of the common carp. Dis Aquat Org 62:115–119

    Article  CAS  PubMed  Google Scholar 

  • Petkevičiūtė R, Kuperman BI (1992) Karyological investigations of Caryophyllaeus laticeps (Pallas, 1781) (Cestoda: Caryophyllidea). Folia Parasitol 39:115–121

    PubMed  Google Scholar 

  • Poddubnaya LG (2002) Ultrastructure of the male reproductive ducts in Diphyllobothrium latum (Cestoda, Pseudophyllidea). Zool Zh 81:394–405, In Russian

    Google Scholar 

  • Poddubnaya LG, Mackiewicz JS, Bruňanská M, Dezfuli BS (2005) Fine structure of the male reproductive ducts, vagina and seminal receptacle of Cyathocephalus truncatus (Cestoda: Spathebothriidea). Folia Parasitol 52:241–250

    PubMed  Google Scholar 

  • Protasova EN, Kuperman BI, Roytman VA, Poddubnaya LG (1990) Caryophyllids of the fauna in SSSR. Nauka, Moscow, p 238, In Russian

    Google Scholar 

  • Robinson JM, Bogitsch BJ (1978) A morphological and cytochemical study of sperm development in Hymenolepis diminuta. Z Parasitenkd 56:81–92

    Article  Google Scholar 

  • Rohde K, Watson N (1986) Ultrastructure of the sperm ducts of Austramphilina elongata (Platyhelminthes, Amphilinidae). Zool Anz 217:23–30

    Google Scholar 

  • Sakaguchi Y, Nakagawa C (1975) A note on the chromosomes of the common liver fluke (Fasciola sp.) from Japan. Chromosome Inf Serv 19:20–21

    Google Scholar 

  • Sakaguchi Y, Yoneda W (1976) A further chromosome study of the common liver fluke (Fasciola sp.) from Japan. Chromosome Inf Serv 20:25–26

    Google Scholar 

  • Sasada K (1978) Studies on the chromosomes of parasitic helminths (II). Triploidy and cytological mechanism of parthenogenesis in Diphyllobothrium erinacei (Cestoda: Diphyllobothriidae). Jpn J Parasitol 27:547–560

    Google Scholar 

  • Swiderski Z, Mackiewicz JS (2002) Ultrastructure of spermatogenesis and spermatozoa of the caryophyllidean cestode Glaridacris catostomi Cooper, 1920. Acta Parasitol 47:83–104

    Google Scholar 

  • von Wettstein D (1977) The assembly of the synaptonemal complex. Phil Trans R Soc Lond Ser B 277:235–243

    Article  Google Scholar 

  • von Wettstein D, Rasmussen SW, Holm PB (1984) The synaptonemal complex in genetic segregation. Annu Rev Genet 18:331–431

    Article  Google 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 45:311–325

    Article  CAS  PubMed  Google Scholar 

  • Watson NA (1999) Platyhelminthes. In: Adiyodi KG, Adiyodi RG, Jamieson BGM (eds) Reproductive biology of invertebrates. Volume IX, part A. Progress in male gamete ultrastructure and phylogeny. Oxford IBH, New Delhi, pp 97–142

    Google 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 19:897–905

    Article  Google Scholar 

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Acknowledgments

We are grateful to Professor J.S. Mackiewicz who kindly provided valuable constructive comments on an earlier version of the manuscript and edited this text. The help of Dr. Borislav Kostič with the preparation of the plates with figures is thankfully acknowledged. Thanks to the staff of the Laboratory of Electron Microscopy, Institute of Parasitology BC AS CR, České Budějovice, Czech Republic for technical assistance. This study was supported by the Grant Agency of the Slovak Republic VEGA (project no. 2/0018/08).

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Correspondence to Magdaléna Bruňanská.

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Bruňanská, M., Nebesářová, J. & Oros, M. Ultrastructural aspects of spermatogenesis, testes, and vas deferens in the parthenogenetic tapeworm Atractolytocestus huronensis Anthony, 1958 (Cestoda: Caryophyllidea), a carp parasite from Slovakia. Parasitol Res 108, 61–68 (2011). https://doi.org/10.1007/s00436-010-2038-0

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