Hostname: page-component-78c5997874-v9fdk Total loading time: 0 Render date: 2024-11-03T05:04:05.543Z Has data issue: false hasContentIssue false
  • English
  • Français

Migration and motility of spermatozoa in the female reproductive tract of the soft tick Ornithodoros moubata (Acari, Argasidae)

Published online by Cambridge University Press:  05 March 2009

J. H. RESLER ,
J. L. FRAZIER ,
J. G. SHEPHERD  and
J. D. MODAFFERI
J. H. RESLER
Affiliation:
Department of Biological Sciences, Binghamton University, P.O. Box 6000, Binghamton, NY 13902-6000, USA
J. L. FRAZIER
Affiliation:
Department of Biological Sciences, Binghamton University, P.O. Box 6000, Binghamton, NY 13902-6000, USA
J. G. SHEPHERD*
Affiliation:
Department of Biological Sciences, Binghamton University, P.O. Box 6000, Binghamton, NY 13902-6000, USA
J. D. MODAFFERI
Affiliation:
Department of Biological Sciences, Binghamton University, P.O. Box 6000, Binghamton, NY 13902-6000, USA
*
*Corresponding author: Tel: +607 777 6538. Fax: +607 777 6521. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

The spermatozoa of ticks are anomalous in many respects: they are very large, cytoplasm-rich cells which lack a flagellum but move with a peculiar gliding motility. Their metamorphosis after deposition in the female has been well documented, but many of the subsequent events in the career of the spermatozoa are controversial or poorly documented. Our observations of motility imply that the many types of motility that have been reported (up to 5 different types in several reports) can be reduced to 2 apparently independent types of active motility: (1) gliding motility generated along the whole spermatozoon and (2) contortions of the anterior tip of the head. These types of motility appear as a consequence of sperm maturation after transfer to the female, but only become pronounced if the female has taken a recent bloodmeal. A consequence of this enhanced gliding motility after feeding is the movement of the spermatozoa out of the naturally ruptured neck of the spermatophore and up the female genital tract. This occurs without any apparent assistance from the female's musculature and likely is the prime mechanism of movement of the spermatozoa to the site of fertilization.

Keywords

motilityspermreproductiontickgliding
Type
Research Article
Information
Parasitology , Volume 136 , Issue 5 , April 2009 , pp. 511 - 521
Copyright
Copyright © 2009 Cambridge University Press

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

Alberti, G. (1980). Zur Feinstruktur der Spermien und Spermiocytogenese der Milben (Acari). I. Anactinotrichida. Zoologische Jahrbucher, Abteilung fuer Anatomie. 104, 77–138.Google Scholar
Balashov, Y. S. (1968). Blood-sucking Ticks (Ixodoidea) – Vectors of Disease of Man and Animals. Translated 1972: Miscellaneous Publications of the Entomological Society of America 8, 161–376.Google Scholar
Baum, J., Richard, D., Healer, J., Rug, M., Krnajski, Z., Gilberger, T., Green, J. L., Holder, A. A. and Cowman, A. F. (2006). A conserved molecular motor drives cell invasion and gliding motility across malaria life cycle stages and other apicomplexan parasites. Journal of Biological Chemistry 281, 5197–5208.CrossRefGoogle ScholarPubMed
Bloodgood, R. A. (1995). Flagellar surface motility – gliding and microsphere movements. Methods in Cell Biology 47, 273–279.CrossRefGoogle ScholarPubMed
Borut, S. and Feldman-Muhsam, B. (1976). A new observation on spermateleosis in ticks. Journal of Parasitology 62, 318–329.CrossRefGoogle ScholarPubMed
Breucker, H. and Horstmann, E. (1968). Die Spermatozoen der Zecke Ornithodorus moubata. Zetschrift fuer Zellforschung 88, 1–22.CrossRefGoogle ScholarPubMed
Brinton, L. P., Burgdorfer, W. and Oliver, J. H. Jr. (1974). Histology and fine structure of spermatozoa and egg passage in the female tract of Dermacentor andersoni Stiles (Acari, Ixodoidea). Tissue & Cell 6, 109–125.CrossRefGoogle Scholar
Casteel, D. B. (1917). Cytoplasmic inclusions in male germ cells of the fowl tick, Argas miniatus, and histogenesis of the spermatozoon. Journal of Morphology 28, 643–683.CrossRefGoogle Scholar
Christophers, S. R. (1906). The anatomy and histology of ticks. Scientific Memoirs of the Officers of the Medical and Sanitary Departments of the Government of India 23, 1–55.Google Scholar
Clark, G. (1973). Staining Procedures Used by the Biological Stain Commission, 3rd Edn. Williams & Wilkins, Baltimore, USA.Google Scholar
Douglas, J. R. (1943). The internal anatomy of Dermacentor andersoni Stiles. University of California Publications in Entomology 7, 207–271.Google Scholar
El Said, A. (1976). Contribution to reproduction of Amblyomma hebraeum (Acari: Ixodidae): spermatogenesis and copulation. Ph.D. thesis, University of Geneva, Geneva, Switzerland.Google Scholar
El Said, A., Swiderski, Z., Aeschlimann, A. and Diehl, P. A. (1981). Fine structure of spermiogenesis in the tick Amblyomma hebraeum (Acari: Ixodidae): late stages of differentiation and structure of the mature spermatozoon. Journal of Medical Entomology 18, 464–476.CrossRefGoogle Scholar
Feldman-Muhsam, B. (1964). Some contributions to the understanding of the reproduction of ticks. Acarologia (Hors série) 6, 294–298.Google Scholar
Feldman-Muhsam, B. (1967 a). Spermatophore formation and sperm transfer in Ornithodoros ticks. Science 156, 1252–1253.CrossRefGoogle ScholarPubMed
Feldman-Muhsam, B. (1967 b). Fecudity and viability of sperm cells of Ornithodoros ticks. Wiadomosci Parazitologiczne 13, 539–542.Google ScholarPubMed
Feldman-Muhsam, B. (1986). On 5 types of movement of sperm cells of ticks. Development, Growth, & Differentiation 28 (Suppl.) 58.Google Scholar
Feldman-Muhsam, B. and Filshie, B. K. (1976). Scanning and transmission electron microscopy of the spermiophores of Ornithodoros ticks: an attempt to explain their motility. Tissue & Cell 8, 411–419.CrossRefGoogle ScholarPubMed
Feldman-Muhsam, B. and Filshie, B. K. (1979). The ultrastructure of the prospermium of Ornithodoros ticks and its relation to sperm maturation and capacitation. In The Spermatozoon. (ed. Fawcett, D. W., and Bedford, J. M.), pp. 355–369. Urban & Schwarzenberg, Baltimore, USA.Google Scholar
Feldman-Muhsam, B., Borut, S., Saliternik-Givant, S. and Eden, C. (1973). On the evacuation of sperm from the spermatophore of the tick, Ornithodoros savignyi. Journal of Insect Physiology 19, 951–962.CrossRefGoogle ScholarPubMed
Goroshchenko, YU. L. (1965). Cytological investigations of certain properties of hematogenesis and karyologic systematic subdivision of argasid ticks. Doklady Soisk. Uchen., Step. Kand. Biol. Nauk, Leningrad, (from Balashov 1968, cited above).Google Scholar
Heintzelman, M. B. (2004). Actin and myosin in Gregarina polymorpha. Cell Motility and the Cytoskeleton 58, 83–95.CrossRefGoogle ScholarPubMed
Heintzelman, M. B. (2006). Cellular and molecular mechanics of gliding locomotion in eukaryotes. International Review of Cytology 251, 79–129.CrossRefGoogle ScholarPubMed
Hoiczyk, E. (2000). Gliding motility in cyanobacteria: Observations and possible explanations. Archives of Microbiology 174, 11–17.CrossRefGoogle ScholarPubMed
Kaufman, W. R. (2004). Assuring paternity in a promiscuous world: are there lessons for ticks among the insects? Parasitology 129 (Suppl.) S145–S160.CrossRefGoogle Scholar
Kaufman, W. R. and Lomas, L. O. (1996). “Male factors” in ticks: their role in feeding and egg development. Invertebrate Reproduction and Development 30, 191–198.CrossRefGoogle Scholar
Keeley, A. and Soldati, D. (2004). The glideosome: a molecular machine powering motility and host-cell invasion by Apicomplexa. Trends in Cell Biology 14, 528–532.CrossRefGoogle ScholarPubMed
Lees, A. D. and Beament, J. W. L. (1948). An egg-waxing organ in ticks. Quarterly Journal of Microscopical Science 89, 291–332.Google ScholarPubMed
Merz, A. J. and Forest, K. T. (2002). Bacterial surface motility: Slime trails, grappling hooks and nozzles. Current Biology 12, R297–R303.CrossRefGoogle ScholarPubMed
Nuttall, G. H. F. and Merriman, G. (1911). The process of copulation in Ornithodoros moubata. Parasitology 4, 39–45.CrossRefGoogle Scholar
Oliver, J. H. Jr. (1974). Symposium on reproduction of arthropods of medical and veterinary importance. IV. Reproduction in ticks (Ixodoidea). Journal of Medical Entomology 11, 26–34.CrossRefGoogle ScholarPubMed
Oliver, J. H. Jr. (l982). Tick reproduction: sperm development and cytogenetics. In Physiology of Ticks (ed. Obenchain, F. D and Galun, R.), pp. 245–275. Pergamon Press, Oxford, UK.CrossRefGoogle Scholar
Oliver, J. H. Jr. and Brinton, L. P. (1973). Sperm maturation in ticks: an example of capacitation in invertebrates? In Proceedings of the Third International Congress of Acarology, Prague, 1971, pp. 733–737. W. Junk, The Hague.CrossRefGoogle Scholar
Pearse, A. G. E. (1961). Histochemistry: Theoretical and Applied. Little, Brown, & Co., Boston, USA.Google Scholar
Pinkerton, A. M., Hall, J. D., and Shepherd, J. (1982). Scanning electron microscopy of post-ejaculatory spermiogenesis in the tick Ornithodoros moubata. Tissue & Cell 14, 785–797.CrossRefGoogle ScholarPubMed
Poulsen, N. C. (1999). Diatom gliding is the result of an actin-myosin motility system. Cell Motility and the Cytoskeleton 44, 23–33.3.0.CO;2-D>CrossRefGoogle ScholarPubMed
Reger, J. F. (1974). The origin and fine structure of cellular processes in spermatozoa of the tick Dermacentor andersoni. Journal of Ultrastructure Research 48, 420–434.CrossRefGoogle Scholar
Resler, J. H. (1981). A light and electron microscopic examination of the onset of sperm motility and endospermatophore evacuation in the African soft tick Ornithodoros moubata. M.A. thesis, State University of NewYork, Binghamton, NY, USA.Google Scholar
Reynolds, E. S. (1963). The use of lead citrate at high pH as an electron opaque stain in electron microscopy. Journal of Cell Biology 17, 208–213.CrossRefGoogle ScholarPubMed
Robinson, G. G. (1942). The mechanism of insemination in the argasid tick, Ornithodoros moubata Murray. Parasitology 34, 195–198.CrossRefGoogle Scholar
Robinson, L. E. and Davidson, J. (1914). The anatomy of Argas persicus (Oken 1818). Part III. Parasitology 6, 382–424.CrossRefGoogle Scholar
Rothschild, LORD. (1961). Structure and movements of tick spermatozoa (Arachnida, Acari). Quarterly Journal of Microscopical Science 102, 239–247.Google Scholar
Sahli, R., Germond, J. E. and Diehl, P. A. (1985). Ornithodoros moubata: spermateleosis and secretory activity of the sperm. Experimental Parasitology 60, 383–395.CrossRefGoogle ScholarPubMed
Samson, K. (1909). Zur Spermohistiogenese der Zecken. Sitzungsberichte der Gesellschaft Naturforschung und Freunde, Berlin 8, 486–499.Google Scholar
Shepherd, J., Levine, S. and Hall, J. D. (1982 a). Maturation of tick spermatozoa in vitro. International Journal of Invertebrate Reproduction 4, 311–321.CrossRefGoogle Scholar
Shepherd, J., Oliver, J. H. Jr. and Hall, J. D. (1982 b). A polypeptide from male accessory glands which triggers maturation of tick spermatozoa. International Journal of Invertebrate Reproduction 5, 129–137.CrossRefGoogle Scholar
Sokolov, I. I. (1956). On the question of fertilization in ixodoid ticks (in Russian). Zoologicheskii Zhurnal 35, 511–528.Google Scholar
Sonenshine, D. E. (1970). A contribution to the internal anatomy and histology of the bat tick Ornithodoros kelleyi. Part II. The reproductive, muscular, respiratory, excretory, and nervous systems. Journal of Medical Entomology 7, 289–312.CrossRefGoogle Scholar
Spurr, A. R. (1969). A low-viscosity epoxy resin embedding medium for electron microscopy. Journal of Ultrastructure Research 26, 31–43.CrossRefGoogle ScholarPubMed
Tatchell, R. J. (1962). Studies on the male accessory reproductive glands and the spermatophore of the tick, Argas persicus Oken. Parasitology 52, 133–142.CrossRefGoogle Scholar
Till, W. M. (1961). A contribution to the anatomy and histology of the brown ear tick Rhipicephalus appendicalatus Neumann. Memoirs of the Entomological Society of South Africa 6, 1–24.Google Scholar
Wagner-Jevseenko, O. (1958). Fortpflanzung bei Ornithodoros moubata und genitale Ubertragung von Borrelia duttoni. Acta Tropica 15, 118–168.Google Scholar
Walsby, A. E. (1968). Mucilage secretion and the movements of blue-green algae. Protoplasma 65, 223–238.CrossRefGoogle Scholar
Wüest, J., El Said, A., Swiderski, Z. and Aeschlimann, A. (1978). Morphology of the spermatid and spermatozoon of Amblyomma hebraeum Koch Acarina, Ixodidae). Zeitschrift fuer Parasitenkunde 55, 91–99.CrossRefGoogle ScholarPubMed