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Russian Journal of Marine Biology

, Volume 40, Issue 2, pp 71–81 | Cite as

The origin of nematode sperm: Progenesis at the cellular level

  • V. V. Yushin
  • V. V. Malakhov
Review the Biology of Individual Development

Abstract

Analysis of the development and structure of aberrant sperm of nematodes and other metazoans with internal insemination showed that these spermatozoa have several unusual, but shared features: (1) the absence of a flagellum and an axoneme, an unusual arrangement of centrioles; (2) an amoeboid shape and amoeboid motility due to cytoskeleton components; (3) the poor condensation of nuclear chromatin, which may be diffuse, thread-like, and discrete; (4) the absence of a nuclear envelope; (5) multiple unmodified mitochondria; (6) the absence of an acrosome; (7) unique membranous components derived from the Golgi complex; and (8) the large size of spermatozoa due to prominent cytoplasm filled with a great number of components. These shared features of aberrant spermatozoa may be explained by the conservation of a number of features that are characteristic of the primitive undifferentiated cell (the predecessor of all specialized gametes). The primitive cell features of numerous versions of aberrant sperm reflect the arrest of cytoplasm specialization of male gametes at an early stage of development. This pattern of gamete evolution is quite consistent with the conception of progenesis (retention of juvenile characters by precocious, sexually mature morphologically juvenile stage). Thus, the origin of the aberrant sperm of nematodes and many other metazoans may be interpreted as progenesis at the cellular level.

Keywords

acrosome axoneme spermatogenesis flagellum membranous organelles fibrous bodies mitochondria progenesis pseudopodia centrioles cytoskeleton nuclear envelope 

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References

  1. 1.
    Gilbert, S., Developmental Biology, New York: Plenum, 1991, vol. 1.Google Scholar
  2. 2.
    Drozdov, A.L., On a prototype of spermatozoa of multicellular animals, Tsitologiya, 1984, vol. 26, pp. 759–766.Google Scholar
  3. 3.
    Drozdov, A.L. and Ivankov, V.N., Morfologiya gamet zhivotnykh (Morphology of the Animal Gametes), Moscow: Kruglii God, 2000.Google Scholar
  4. 4.
    Ivanova-Kazas, O.M., Neoteny as a special modus of evolution, 1: Neoteny in lower Metazoa, polychets and mollusks, Zool. Zh., 1997, vol. 76, no. 11, pp. 1235–1243.Google Scholar
  5. 5.
    Reunov, A.A., About plesiomorphism and apomorphism of spermatogenic cells of multicellular animals, Usp. Sovrem. Biol., 2005, vol. 125, no. 4, pp. 360–372.Google Scholar
  6. 6.
    Reunov, A.A., Problem of terminology in the characteristics of spermatozoa of multicellular animals, Ontogenesis, 2005, vol. 36, no. 6, pp. 403–421.Google Scholar
  7. 7.
    Reunov, A.A., Spermatogenez mnogokletochnykh zhivotnykh (Spermatogenesis of Multicellular Animals), Moscow: Nauka, 2005.Google Scholar
  8. 8.
    Reunov, A.A. and Malakhov, V.V., Evolution of structure of spermatozoa in invertebrates, Usp. Sovrem. Biol., 1993, vol. 113, pp. 3–16.Google Scholar
  9. 9.
    Smirnov, S.V., Pedomorphosis as a mechanism of evolutionalry transformations, in Sovremennaya evolutsionnaya morfologiya (Recent Evolutionary Morphology), Kiev: Naukova Dumka, 1991, pp. 88–103.Google Scholar
  10. 10.
    Yushin, V.V. and Malakhov, V.V., Spermatozoa of Nematodes of the Order Enoplida have a nuclear membrane, Dokl. Ross. Akad. Nauk, Ser. Biol., 1999, vol. 367, pp. 718–720.Google Scholar
  11. 11.
    Adrianov, A.V. and Malakhov, V.V., Kinorhyncha, in Reproductive Biology of Invertebrates, vol. 9, part A: Progress in Male Gamete Ultrastructure and Phylogeny, New Delhi: Oxford Publ., 1999, pp. 193–211.Google Scholar
  12. 12.
    Afanasiev-Grigoriev, A.G. and Yushin, V.V., Electron microscopic study of spermiogenesis in the free-living marine nematode Leptosomatides marinae Platonova 1976 (Enoplida: Leptosomatidae), Russ. J. Mar. Biol., 2009, vol. 35, pp. 156–163.CrossRefGoogle Scholar
  13. 13.
    Afanasiev-Grigoriev, A.G., Zograf, J.K., and Yushin, V.V., Nuclear envelope in the spermatozoa of the leptosomatid nematode Leptosomatides marinae (Enoplida, Leptosomatidae), Russ. J. Nematol., 2006, vol. 14, pp. 119–125.Google Scholar
  14. 14.
    Alberti, G., Comparative spermatology of Chelicerata: review and perspective, Mém. Mus. Natl. Hist. Nat., 1995, vol. 166, pp. 203–230.Google Scholar
  15. 15.
    Alberti, G., Double spermatogenesis in Chelicerata, J. Morphol., 2005, vol. 266, pp. 281–297.PubMedCrossRefGoogle Scholar
  16. 16.
    Alberti, G. and Coons, L.B. Acari mites, in Microscopic Anatomy of Invertebrates, Vol. 8C: Chelicerate Arthropoda, New York: Wiley, 1999, pp. 515–1265.Google Scholar
  17. 17.
    Alvestad-Graebner, I. and Adam, H., Gnathostomulida, in Reproductive Biology of Invertebrates, Vol. 2: Spermatogenesis and Sperm Function, Chichester: Wiley, 1983, pp. 171–180.Google Scholar
  18. 18.
    Baccetti, B., Evolution of the sperm cell, in Biology of Fertilization, New York: Academic, 1985, pp. 3–58.CrossRefGoogle Scholar
  19. 19.
    Baccetti, B. Spermatozoa, in Microscopic Anatomy of Invertebrates, Vol. 11C: Insecta, New York: Wiley, 1998, pp. 843–894.Google Scholar
  20. 20.
    Baccetti, B. and Afzelius, B.A., The Biology of the Sperm Cell, Basel: Karger, 1976.Google Scholar
  21. 21.
    Baccetti, B., Dallai, R., Bernini, F., and Mazzini, M., The spermatozoon of Arthropoda, XXIV: Sperm metamorphosis in the diplopod Polyxenus, J. Morphol., 1974, vol. 143, pp. 187–246.PubMedCrossRefGoogle Scholar
  22. 22.
    Baccetti, B., Dallai, R., Grimaldi, de Zio S., and Marinari, A., The evolution of the nematode spermatozoon, Gamete Res., 1983, vol. 8, pp. 309–323.CrossRefGoogle Scholar
  23. 23.
    Balsamo, M., Guidi, L., Pierboni L., et al., Living without mitochondria: spermatozoa and spermatogenesis in two species of Urodasys (Gastrotricha, Macrodasyida) from dysoxic sediments, Invertebr. Biol., 2007, vol. 126, pp. 1–9.CrossRefGoogle Scholar
  24. 24.
    Birkhead, T.R., Giusti, F., Immler, S., and Jamieson, B.G.M., Ultrastructure of the unusual spermatozoon of the Eurasian bullfinch (Pyrrhula pyrrhula), Acta Zool. (Stockholm), 2007, vol. 88, pp. 119–128.CrossRefGoogle Scholar
  25. 25.
    Boone, M., Willems, M., Claeys, M., and Artois, T., Spermatogenesis and the structure of the testes in Isodiametra pulchra (Isodiametridae, Acoela), Acta Zool. (Stockholm), 2011, vol. 92, pp. 101–108.CrossRefGoogle Scholar
  26. 26.
    Buckland-Nicks, J. and Sheltema, A., Was internal fertilization an innovation of early Bilateria? Evidence from sperm structure of a mollusc, Proc. R. Soc. B, 1995, vol. 261, pp. 11–18.CrossRefGoogle Scholar
  27. 27.
    Clement, P. and Wurdak, E., Rotifera, in Microscopic Anatomy of Invertebrates, Vol. 4: Aschelminthes, New York: Wiley, 1991, pp. 219–297.Google Scholar
  28. 28.
    Coil, W.H., Plathelminthes: Cestoidea, in Microscopic Anatomy of Invertebrates, Vol. 3: Plathelminthes and Nemertinea, New York: Wiley, 1991, pp. 211–283.Google Scholar
  29. 29.
    Crompton, D.W.T., Acanthocephala, in Reproductive Biology of Invertebrates, Vol. 2: Spermatogenesis and Sperm Functio, Chichester: Wiley, 1983, pp. 257–267.Google Scholar
  30. 30.
    De Ley, P. and Blaxter, M., Systematic position and phylogeny, in The Biology of Nematodes, London: Taylor and Francis, 2002, pp. 1–30.CrossRefGoogle Scholar
  31. 31.
    Foor, W.E., Nematoda, in Reproductive Biology of Invertebrate, Vol. 2: Spermatogenesis and Sperm Function, Chichester: Wiley, 1983, pp. 221–256.Google Scholar
  32. 32.
    Franzen, E., On spermiogenesis, morphology of the spermatozoon and biology of fertilization among invertebrates, Zool. Bidr. Uppsala, 1956, vol. 31, pp. 355–482.Google Scholar
  33. 33.
    Franzen, Å., Spermatogenesis, in Reproduction of Marine Invertebrates, Vol. 9: General Aspects: Seeking Unity in Diversity, Palo Alto: Blackwell, 1987, pp. 1–47.Google Scholar
  34. 34.
    Hendelberg, J., Platyhelminthes-Turbellaria, in Reproductive Biology of Invertebrates, vol. 2: Spermatogenesis and Sperm Function, Chichester: Wiley, 1983, pp. 75–104.Google Scholar
  35. 35.
    Hodda, M., Phylum Nematoda, Zootaxa, 2007, vol. 1668, pp. 265–293.Google Scholar
  36. 36.
    Jamieson, B.G.M. and Tudge, C.C., Crustacea-Decapoda, in Reproductive Biology of Invertebrates, Vol. 9, part C: Progress in Male Gamete Ultrastructure and Phylogeny, Chichester: Wiley, 1999, pp. 1–95.Google Scholar
  37. 37.
    Justine, J.-L., The spermatozoa of the schistosomes and the concept of progenetic spermiogenesis, in Comparative Spermatology 20 Years after, Serono Symposia, vol. 75, New York: Raven Press, 1991, pp. 977–979.Google Scholar
  38. 38.
    Justine, J.-L., Spermatozoal ultrastructure and phylogeny in the parasitic Platyhelminthes, Mem. Mus. Natl. Hist. Nat., 1995, vol. 166, pp. 55–86.Google Scholar
  39. 39.
    Justine, J.-L., Male and female gametes and fertilization, The Biology of Nematodes, London: Taylor and Francis, 2002, pp. 73–119.Google Scholar
  40. 40.
    Justine, J.-L. and Jamieson, B.G.M., Nematoda, in Reproductive Biology of Invertebrates, vol. 9, part B: Progress in Male Gamete Ultrastructure and Phylogeny, New Delhi: Oxford Publ., 1999, pp. 183–266.Google Scholar
  41. 41.
    Kruger, J.C. de W., Ultrastructure of sperm development in the plant parasitic nematode Xiphinema theresiae, J. Morphol., 1991, vol. 210, pp. 163–174.CrossRefGoogle Scholar
  42. 42.
    Lanfranchi, A. and Falleni, A., Ultrastructural observations on the male gametes in Austrognathia sp. (Gnathostomulida, Bursavaginoidea), J. Morphol., 1998, vol. 237, pp. 165–176.CrossRefGoogle Scholar
  43. 43.
    Mansir, A. and Justine, J.-L., Centrioles with ten singlets in spermatozoa of the parasitic nematode Heligmosomoides polygirus, Mém. Mus. Natl. Hist. Nat., 1995, vol. 166, pp. 119–128.Google Scholar
  44. 44.
    Mattei, X., Boisson, C., Mattei, C., and Reizer, C., Spermatozoïde aflagellés chez un poisson: Gymnarchus niloticus (Téléostéen, Gymnarchidae), Compt. Rend. Acad. Sci. Paris, 1967, vol. 265, pp. 2010–2012.Google Scholar
  45. 45.
    Mattei, X., Mattei, C., Reizer, C., and Chevalier, J.-L., Ultrastructure des spermatozoïdes aflagellés des mormyres (Poissons Téléostéens), J. Microsc., 1972, vol. 15, pp. 67–78.Google Scholar
  46. 46.
    Matzke-Karasz, R., Giant spermatozoon coiled in small egg: fertilization mechanisms and their implications for evolutionary studies on Ostracoda (Crustacea), J. Exp. Zool., Ser. B, 2005, vol. 304, pp. 129–149.CrossRefGoogle Scholar
  47. 47.
    McLaren, D.J., The structure and the development of the spermatozoon of Dipetelonema viteae (Nematoda: Filarioidea), Parasitology, 1973, vol. 66, pp. 447–463.PubMedCrossRefGoogle Scholar
  48. 48.
    Merlin, J., Goldstein, A., and Goldstein, P., Meiotic structures in the animal-parasitic nematode Ascaris megalocephala: synaptonemal complexes, recombination nodules, and centrioles, J. Nematol., 2003, vol. 35, pp. 223–227.PubMedCentralPubMedGoogle Scholar
  49. 49.
    Morrow, E.H., How the sperm lost its tail: the evolution of aflagellate sperm, Biol. Rev., 2004, vol. 79, pp. 795–814.PubMedCrossRefGoogle Scholar
  50. 50.
    Pitnick, S., Hosken D., and Birkhead T., Sperm morphological diversity, in Sperm Biology, an Evolutionary Perspective, New York: Academic, 2008, pp. 69–149.Google Scholar
  51. 51.
    Pochon-Masson, J., Arthropoda-Crustacea, in Reproductive Biology of Invertebrates, Vol. 2: Spermatogenesis and Sperm Function, Chichester: Wiley, 1983, pp. 407–448.Google Scholar
  52. 52.
    Poinar, G.O., Jr. and Hess-Poinar, R.T., The fine structure of Gastromermis sp. (Nematoda: Mermithidae) sperm, J. Submicrosc. Cytol. Pathol., 1993, vol. 25, pp. 417–431.PubMedGoogle Scholar
  53. 53.
    Reger, J.F. and Fitzgerald, M.E.C., Arthropoda-Myriapoda, in Reproductive Biology of Invertebrates, Vol. 2: Spermatogenesis and Sperm Function, Chichester: Wiley, 1983, pp. 451–475.Google Scholar
  54. 54.
    Roosen-Range, E.C., The Process of Spermatogenesis in Animals, Cambridge: Cambridge Univ. Press, 1977.Google Scholar
  55. 55.
    Rundell, R.J. and Leander, B.S., Masters of miniaturization: convergent evolution among interstitial eukaryotes, Bioessays, 2010, vol. 32, pp. 430–437.PubMedCrossRefGoogle Scholar
  56. 56.
    Schmidt-Rhaesa, A., Ultrastructural observations of the male reproductive system and spermatozoa of Gordius aquaticus L., 1758, Invertebr. Reprod. Devel., 1997, vol. 32, pp. 31–40.CrossRefGoogle Scholar
  57. 57.
    Schmidt-Rhaesa, A., The Evolution of Organ Systems, Oxford: Univ. Press, 2007.CrossRefGoogle Scholar
  58. 58.
    Scott, A.L., Nematode sperm, Parasitol. Today, 1996, vol. 12, pp. 425–430.PubMedCrossRefGoogle Scholar
  59. 59.
    Shepherd, A.M. and Clark, S.A., Spermatogenesis and the ultrastructure of the sperm and of the male reproductive tract of Aphelenchoides blastophthorus (Nematoda: Tylenchida, Aphelenchina), Nematologica, 1976, vol. 22, pp. 1–9.CrossRefGoogle Scholar
  60. 60.
    Shepherd, A.M. and Clark, S.A., Spermatogenesis and sperm structure in some Meloidogyne species (Heteroderoidea, Meloidogynidae) and a comparison with those in some cyst nematodes (Heteroderoidea, Heteroderidae), Rev. Nematol., 1983, vol. 6, pp. 17–32.Google Scholar
  61. 61.
    Snook, R.R., Sperm in competition: not playing by the numbers, Trends Ecol. Evol., 2005, vol. 20, pp. 46–53.PubMedCrossRefGoogle Scholar
  62. 62.
    Swallow, J.G. and Wilkinson, G.S., The long and short of sperm polymorphisms in insects, Biol. Rev., 2002, vol. 77, pp. 153–182.PubMedCrossRefGoogle Scholar
  63. 63.
    Takahashi, Y., Goto, C., and Kita, K.K., Ultrastructural study of Trichinella spiralis with emphasis on adult male reproductive organs, J. Helminthol., 1994, vol. 68, pp. 353–358.PubMedCrossRefGoogle Scholar
  64. 64.
    Watson, N.A. and Rhode, K., Sperm and spermiogenesis of the “Turbellaria” and implications for the phylogeny of the phylum Platyhelminthes, Mem. Mus. Natl. Hist. Nat., 1995, vol. 166, pp. 37–54.Google Scholar
  65. 65.
    Westheide, W., Progenesis as a principle in meiofaunal evolution, J. Nat. Hist., 1987, vol. 21, pp. 843–854.CrossRefGoogle Scholar
  66. 66.
    White-Cooper, H. and Bausek, N., Evolution and spermatogenesis, Philos. Trans. R. Soc., B, 2010, vol. 365, pp. 1465–1480.CrossRefGoogle Scholar
  67. 67.
    Witalinski, W., Spermatogenesis in the free-living mite, Pergamasus viator Halas (Parasitidae, Mesostigmata), I: Fine structure of spermatozoa, Z. Mikr.-Anat. Forsch., 1975, vol. 89, pp. 1–17.PubMedGoogle Scholar
  68. 68.
    Witalinski, W., Spermatogenesis in the free-living mite, Pergamasus viator Halas (Parasitidae, Mesostigmata), II: Spermiogenesis, Z. Mikr.-Anat. Forsch., 1976, vol. 90, pp. 657–680.PubMedGoogle Scholar
  69. 69.
    Yurchenko, O.V., Comparative ultrastructural study of spermatozoa in some oyster species from the AsianPacific coast, Micron., 2012, vol. 43, pp. 365–373.PubMedCrossRefGoogle Scholar
  70. 70.
    Yushin, V.V., Ultrastructure of spermatogenesis in the free-living marine nematode Anticoma possjetica (Enoplida, Anticomidae), Nematology, 2003, vol. 5, pp. 777–788.CrossRefGoogle Scholar
  71. 71.
    Yushin, V.V. and Coomans, A., Ultrastructure of sperm development in the free-living marine nematodes of the family Chromadoridae (Chromadorida: Chromadorina), Nematology, 2000, vol. 2, pp. 285–296.CrossRefGoogle Scholar
  72. 72.
    Yushin, V.V. and Coomans, A., Ultrastructure of sperm development in the free-living marine nematode Metachromadora itoi (Chromadoria, Desmodorida), Acta Zool. (Stockholm), 2005, vol. 86, pp. 255–265.CrossRefGoogle Scholar
  73. 73.
    Yushin, V.V., Coomans, A., and Malakhov, V.V., Ultrastructure of spermatogenesis in the free-living marine nematode Pontonema vulgare (Enoplida, Oncholaimidae), Can. J. Zool., 2002, vol. 80, pp. 1371–1382.CrossRefGoogle Scholar
  74. 74.
    Yushin, V.V. and Kosaka, H., Sperm storage in the uterium of the insect parasitic nematode Sphaerularia vespae (Nematoda, Sphaerulariidae), Nematology, 2013, vol. 15, pp. 761–770.Google Scholar
  75. 75.
    Yushin, V.V., Kosaka, H., and Kusunoki, M., Ultrastructural evidence of sperm dimorphism in nematode Deladenus sp. (Tylenchomorpha, Sphaerularioidea, Allantonematidae), Nematology, 2007, vol. 9, pp. 397–404.CrossRefGoogle Scholar
  76. 76.
    Yushin, V.V. and Malakhov, V.V., Ultrastructure of sperm cells in the female gonoduct of free-living marine nematodes from genus Enoplus (Nematoda: Enoplida), Fund. Appl. Nematol., 1994, vol. 17, pp. 513–519.Google Scholar
  77. 77.
    Yushin, V.V. and Malakhov, V.V., Ultrastructure of sperm development in the free-living marine nematode Enoplus anisospiculus (Enoplida: Enoplidae), Fund. Appl. Nematol., 1998, vol. 21, pp. 213–225.Google Scholar
  78. 78.
    Yushin, V.V. and Malakhov, V.V., Spermatogenesis and nematode phylogeny, in Nematology Monographs and Perspectives, Vol. 2: Proc. of the Fourth International Congress of Nematology, June 2002, Tenerife, Spain, Leiden: Brill, 2004, pp. 655–665.Google Scholar
  79. 79.
    Yushin, V.V. and Ryss, A.Y., Sperm development and structure in Bursaphelenchus mucronatus (Nematoda: Aphelenchoidea: Aphelenchoididae), Nematology, 2011, vol. 13, pp. 395–407.CrossRefGoogle Scholar
  80. 80.
    Yushin, V.V., Yoshida, M., and Spiridonov, S.E., Riders on the sperm: sperm dimorphism and spermatozeugmata in nematodes from the genus Steinernema (Rhabditida: Steinernematidae), Nematology, 2007, vol. 9, pp. 61–75.CrossRefGoogle Scholar
  81. 81.
    Zograf, J.K., Astakhova, A.A., and Yushin, V.V., Ultrastructure of spermatozoa in the free-living marine nematode Monoposthia costata (Chromadoria, Desmodorida), Russ. J. Nematol., 2008, vol. 16, pp. 119–126.Google Scholar

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© Pleiades Publishing, Ltd. 2014

Authors and Affiliations

  1. 1.Zhirmunsky Institute of Marine Biology, Far East BranchRussian Academy of SciencesVladivostokRussia
  2. 2.Far Eastern Federal UniversityVladivostokRussia
  3. 3.Moscow State UniversityMoscowRussia

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