Hostname: page-component-586b7cd67f-vdxz6 Total loading time: 0 Render date: 2024-11-23T13:54:38.008Z Has data issue: false hasContentIssue false
  • English
  • Français

Gametogenesis and fertilization in Dirofilaria immitis (Nematoda: Filarioidea)

Published online by Cambridge University Press:  06 April 2009

C. J. Delves ,
R. E. Howells  and
R. J. Post
C. J. Delves
Affiliation:
Departments of Parasitology and Entomology, Liverpool School of Tropical Medicine, Pembroke Place, Liverpool L3 5QA
R. E. Howells
Affiliation:
Departments of Parasitology and Entomology, Liverpool School of Tropical Medicine, Pembroke Place, Liverpool L3 5QA
R. J. Post
Affiliation:
Departments of Parasitology and Entomology, Liverpool School of Tropical Medicine, Pembroke Place, Liverpool L3 5QA
Get access Rights & Permissions [Opens in a new window]

Summary

Gametogenesis in Dirofilaria immitis has been studied principally by means of the aceto-orcein chromosomal squash technique, but with additional ultrastructural observations. A terminal germinative zone, in which a continuous and rapid division of germ cells occurs, has been identified in the gonoduct of both male and female worms. Approximately 20% of cells within these germinative zones were in arrested mitotic division following the incubation in vitro of excised gonads in 0·01% colchicine for 4 h. All primary spermatocytes within a 1–2 cm length of the testis proximal to the germinative zone were at the prophase of the 1st meiotic division. In the corresponding region of the ovary, the primary oocytes were similarly at the prophase of the 1st meiotic division in 75% of female worms examined but in the remaining 25% all primary oocytes possessed markedly less condensed, probably interphase nuclei. A possible hormonal control of the cyclical development of primary oocytes, but not primary spermatocytes in D. immitis is suggested. In most of the remaining length of the gonoducts beyond this region of cells at meiotic prophase, the chromatin material of both primary spermatocytes and oocytes is decondensed. Recondensation of chromosomes in the spermatocytes is observed just prior to entry into the seminal vesicle, where meiosis I is completed and meiosis II takes place. In the primary oocyte, completion of meiosis only occurs after fertilization within the seminal receptacle by an entire male gamete. Following the 2 meiotic divisions in the oocyte and subsequent extrusion of the 2 polar bodies, the haploid chromosome complement of the female unites with that of the male, re-establishing the diploid number of the zygote (2n = 10). Male chromosomes within the oocyte remain visible throughout late oogenesis and fusion occurs without the formation of pronuclei.

Type
Research Article
Information
Parasitology , Volume 92 , Issue 1 , February 1986 , pp. 181 - 197
Copyright
Copyright © Cambridge University Press 1986

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Awadzi, K., Schulz-Key, H., Howells, R. E., Haddock, D. R. W. & Gilles, H. M. (1982). The chemotherapy of onchocerciasis, VIII. Levamisole and its combination with the benzimidazoles. Annals of Tropical Medicine and Parasitology 76, 459–73.CrossRefGoogle ScholarPubMed
Beams, H. W. & Sekhon, S. S. (1972). Cytodifferentiation during spermiogenesis in Rhabditis pellio. Journal of Ultrastructure Research 38, 511–27.CrossRefGoogle ScholarPubMed
Brenner, S. (1974). The genetics of Caenorhabditis elegans. Genetics 77, 71–94.CrossRefGoogle ScholarPubMed
Butschli, O. (1873). Beiträge zur Kenntnis der freilebenden Nematoden. Nova Acta der Kais Leopold Carol Deutsche Akademie der Naturforschung 36, 1–144.Google Scholar
Chen, S. N. & Howells, R. E. (1979). The in vitro cultivation of the infective larvae and the early mammalian stages of the filarial worm Brugia pahangi. Annals of Tropical Medicine and Parasitology 73, 473–86.CrossRefGoogle ScholarPubMed
Cleator, M., Delves, C. J., Howells, R. E. & Rees, H. H. (1984). Developmental hormones in parasitic nematodes. Parasitology 89, xvi.Google Scholar
Favard, P. (1961). Evolution des ultrastructures cellulaires au course de la spermatogenese de l' Ascaris. Annales des sciences naturelles Zoologie 12, 53–152.Google Scholar
Foor, W. E. (1968). Zygote formation in Ascaris lumbricoides. Journal of Cell Biology 39, 119–34.CrossRefGoogle ScholarPubMed
Harada, R., Maeda, T., Nakashima, A., Sadakata, Y., Ando, M., Yonamine, K., Otsuji, Y. & Sato, H. (1970). Electron microscopical studies on the mechanisms of oogenesis and fertilisation in Dirofilaria immitis. In Recent Advances in Researches on Filariasis and Schistosomiasis in Japan (ed. Sasa, M.), pp. 99–121. Tokyo: University of Tokyo Press.Google Scholar
Highnam, K. & Hill, L. (1977). The Comparative Endocrinology of the Invertebrates. London: Edward Arnold.Google Scholar
Hirai, H., Sakaguchi, Y. & Tada, I. (1985). Chromosomes of Onchocerca volvulus and O. gutturosa. Zeitschrift für Parasitenkunde 71, 135–9.CrossRefGoogle ScholarPubMed
Hirsch, D., Oppenheim, D. & Klass, M. (1975). Development of the reproductive system of Caenorhabditis elegans. Developmental Biology 49, 200–19.CrossRefGoogle Scholar
Kaulenas, M. S. & Fairbairn, D. (1968). RNA metabolism of fertilised Ascaris lumbricoides eggs during uterine development. Experimental Cell Research, 52, 233–51.CrossRefGoogle ScholarPubMed
Kimble, J. E. & White, J. G. (1981). On the control of germ cell development in Caenorhabditis elegans. Developmental Biology 81, 208–19.CrossRefGoogle ScholarPubMed
Lee, C. C. (1975). Dirofilaria immitis: ultrastructural aspects of oocyte development and zygote formation. Experimental Parasitology 37, 449–68.CrossRefGoogle ScholarPubMed
Maeda, T., Harada, R., Nakashima, A., Sadakata, Y., Ando, M., Yonamine, K., Otsuji, Y. & Sato, H. (1970). Electron microscopic studies on spermatogenesis in Dirofilaria immitis. In Recent Advances in Researches on Filariasis and Schistosomiasis in Japan (ed. Sada, M.), pp. 73–97. Tokyo: University of Tokyo Press.Google Scholar
McLaren, D. J. (1973 a). The structure and development of the spermatozoan of Dipetalonema viteae (Nematoda: Filarioidea). Parasitology 66, 447–68.CrossRefGoogle Scholar
McLaren, D. J. (1973 b). Oogenesis and fertilisation in Dipetalonema viteae (Nematoda: Filarioidea). Parasitology 66, 465–72.CrossRefGoogle Scholar
McFadzean, J. A. & Smiles, J. (1956). Studies on Litomosoides carinii by phase contrast microscopy. The development of the larvae. Journal of Helminthology 30, 25–32.CrossRefGoogle ScholarPubMed
Nigon, V. (1965). Developpement et reproduction des nematodes. In Traite de Zoologie, Vol. 4 (ed. Grasse, P. P.), pp. 218–386. Paris: Masson et Cie.Google Scholar
Orihel, T. C. (1961). Morphology of larval stages of Dirofilaria immitis in the dog. Journal of Parasitology 47, 251–62.CrossRefGoogle ScholarPubMed
Prestage, J. J. (1960). The fine structure of the growth region of the ovary in Ascaris lumbricoides var. suum with special reference to the rachis. Journal of Parasitology 46, 69–78.CrossRefGoogle Scholar
Sakaguchi, Y., Kihara, S. & Tada, I. (1980). The chromosomes and gametogenesis of Dirofilaria immitis. Japanese Journal of Parasitology 20, 377–81.Google Scholar
Sakaguchi, Y., Tada, I., Ash, L. R. & Aoki, Y. (1983). Karyotypes of Brugia pahangi and B. malayi (Nematoda: Filariodiea). Journal of Parasitology 69, 1090–3.CrossRefGoogle Scholar
Seurat, L. G. (1920). Histoire Naturelle des Nematodes de la Berberie. Université d' Alger, Alger.Google Scholar
Taylor, A. E. R. (1960). The spermatogenesis and embryology of Litomosoides carinii by phase contrast microscopy. The development of the larvae. Journal of Helminthology 34, 3–12.CrossRefGoogle Scholar
Terry, A., Terry, R. & Worms, M. J. (1961). Dipetalonema witei, filarial parasite of the jird, Meriones libycus. The reproductive system, gametogenesis and development of the microfilaria. Journal of Parasitology, 47, 703–11.CrossRefGoogle ScholarPubMed
Triantaphyllou, A. C. (1971). Cytogenetics, host parasite interactions and physiology. In Plant Parasitic Nematodes, Vol. 2 (ed. Zuckermanm, B. M., Main, W. F. and Rohde, R. A.), pp. 1–34. New York: Academic Press.Google Scholar
Triantaphylloy, A. C. & Hirschmann, H. (1966). Gametogenesis and reproduction in wheat nematode Anguina tritici. Nematologica 12, 437–43.Google Scholar
Van Beneden, E. (1883). Recherches sur la maturation de l'oeuf et la fecondation (Ascaris megalocephala). Archives Biologie, Paris, 4, 265–640.Google Scholar
Walton, A. C. (1924). Studies on nematode gametogenesis. Zeitschrift für Zellen-und Gewebelehre 1, 167–239.CrossRefGoogle Scholar
White, M. J. P. (1973). Animal Cytology and Evolution. 3rd Edn.Cambridge: Cambridge University Press.Google Scholar