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Virus particles in male accessory reproductive glands of tsetse, Glossina morsitans morsitans (Diptera: Glossinidae) and associated tissue changes

Published online by Cambridge University Press:  01 December 2006

Elizabeth D. Kokwaro*
Affiliation:
Department of Zoological Sciences, Kenyatta University, Nairobi, PO Box 43844-00100, Kenya
*
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Abstract

The present study was undertaken to determine the occurrence of virus particles in male accessory reproductive glands and to describe the changes in the affected tissues. Using electron microscopy techniques, it was possible to identify rod-shaped virus-like particles in accessory reproductive glands of male tsetse, Glossina morsitans morsitans Westwood. The viruses occurred intracellularly within the epithelial cells and in the lumen of the glands. Cell degeneration characterized by abundant clear vacuoles, membrane-bound vesicles, disorganization and elimination of cell organelles typified the infection. The inference, therefore, is that virus infection may be primarily responsible for the necrotic changes identified in the gland cells. It is suggested that the lesions caused in the gland epithelium by the infection would disturb the glandular cells and disrupt synthesis of the secretion. This may eventually destroy the male accessory reproductive glands leading to inability of the male flies to form spermatophores for transferring spermatozoa to the female tsetse. Lack of sperm transfer would consequently result in no egg fertilization.

Cette étude a été entreprise afin de déterminer la fréquence des particules virales dans les glandes accessoires mâles et décrire les modifications dans les tissus infestés. A l'aide de la microscopie électronique, nous avons pu identifier des particules virales en forme de baguette dans les glandes accessoires de mâles de la mouche tsetse, Glossina morsitans morsitans Westwood. Les virus sont présents à l'intérieur des cellules, dans les cellules épithéliales et dans le lumen des glandes. La dégénérescence des cellules, caractérisée par la présence de nombreuses vacuoles claires, des vésicules bordées par une membrane, la désorganisation et la disparition des organites cellulaires, caractérise l'infection. On en conclut que l'infection virale des cellules se traduit en premier par les changements nécrotiques observés dans les cellules de la glande. Il est vraisemblable que les lésions observées dans l'épithélium de la glande, suite à l'infection, perturberont les cellules glandulaires et affecteront la synthèse de la sécrétion. Cela devrait aboutir à la destruction des glandes accessoires mâles et se traduire par l'impossibilité pour les mouches mâles de former des spermatophores et de transmettre des spermatozoïdes aux mouches tsetse femelles et ainsi, empêcher la fertilisation des œufs.

Type
Research Paper
Copyright
Copyright © ICIPE 2006

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References

Bertram, M. J., Neubaum, D. M. and Wolfner, M. F. (1996) Localization of the Drosophila male accessory gland protein Acp 36 DE in the mated female suggests a role in sperm storage. Insect Biochemistry and Molecular Biology 26, 971980.CrossRefGoogle Scholar
Blum, M. S. and Hilker, M. (2002) Chemical protection of insect eggs, pp. 61–90. In Chemoecology of Insect Eggs and Egg Deposition (Edited by Hilker M. and Meiners J.). Blackwell, Berlin..CrossRefGoogle Scholar
Chen, P. S. (1971) Biochemical Aspects of Insect Development. Karger, Basel. 230 pp.Google ScholarPubMed
De Wilde, J. and De Loof, A. (1973) Reproduction – The Physiology of Insecta. 2nd edn. Academic Press Inc., London. pp. 1195.CrossRefGoogle Scholar
Eisner, T., Rossini, C., González, A., Lyengar, V. K., Siegler, M. V. S. and Smedley, S. R. (2002) Paternal Investment in Egg Defence. Blackwell, Berlin. pp. 91116.Google Scholar
Fuchs, M. S. and Hiss, E. A. (1970) The partial purification and separation of the protein components of matrone from Aedes aegypti. Journal of Insect Physiology 16, 931939.CrossRefGoogle ScholarPubMed
Fuchs, M. S., Craig, G. B. Jr and Hiss, E. A. (1968) The biochemical basis of monogamy in mosquitoes. I. Extraction of the active principle from Aedes aegypti. Life Science 7, 835839.CrossRefGoogle ScholarPubMed
Fuchs, M. S., Craig, G. B. Jr and Despommier, D. D. (1969) The protein nature of the substance inducing female monogamy in Aedes aegypti. Journal of Insect Physiology 15, 701709.CrossRefGoogle Scholar
Gillott, C. (2003) Male accessory gland secretions: modulators of female reproductive physiology and behaviour. Annual Review of Entomology 48, 163184.CrossRefGoogle Scholar
Hartmann, R. and Loher, W. (1996) Control mechanisms of the behaviour ‘secondary defense’ in the grasshopper Gomphocerus rufus L. (Gomophocerinae: Orthoptera). Journal of Comparative Physiology A 178, 329336.CrossRefGoogle ScholarPubMed
Hartmann, R. and Loher, W. (1999) Post-mating effects in the grasshopper, Gomphocerus rufus L. mediated by the spermatheca. Journal of Comparative Physiology A 184, 325332.CrossRefGoogle Scholar
Hilker, M. and Meiners, J. (Eds) (2002) Chemoecology of Insect Eggs and Egg Deposition. Blackwell, Berlin, 416 pp.Google Scholar
Jaenson, T. G. T. (1978) Virus-like rods associated with salivary gland hyperplasia in tsetse, Glossina pallidipes. Transactions of the Royal Society of Tropical Medicine and Hygiene 72, 234–238.CrossRefGoogle ScholarPubMed
Jenni, L. (1973) Virus-like particles in a strain of G. morsitans centralis. Transactions of the Royal Society of Tropical Medicine and Hygiene 67, 295.CrossRefGoogle Scholar
Jenni, L. and Steiger, R. (1974) Virus-like particles of Glossina fuscipes fuscipes Newst. Acta Tropica 31, 177–180.Google Scholar
Jura, W. G. Z. O., Odhiambo, T. R., Otieno, L. H. and Tabu, N. O. (1988) Gonadal lesions in virus-infected male and female tsetse, Glossina pallidipes (Diptera: Glossinidae). Journal of Invertebrate Pathology 52, 1–8.CrossRefGoogle ScholarPubMed
Kokwaro, E. D. and Odhiambo, T. R. (1981) Spermatophore of tsetse Glossina morsitans morsitans Westwood: an ultrastructural study. Insect Science and its Application 1, 185190.Google Scholar
Kokwaro, E. D., Odhiambo, T. R. and Murithi, J. K. (1981) Ultrastructural and histochemical study of the spermatheca of the tsetse Glossina morsitans morsitans Westwood. Insect Science and Its Application 2, 135143.Google Scholar
Kokwaro, E. D., Okot-Kotber, M., Odhiambo, T. R. and Murithi, J. K. (1987) Biochemical evidence for the origin of spermatophore material in Glossina morsitans morsitans Westwood. Experientia 43, 448451.CrossRefGoogle Scholar
Kokwaro, E. D., Nyindo, M. and Chimtawi, M. (1990) Ultrastructural changes in salivary glands of tsetse, Glossina morsitans morsitans infected with virus and rickettsia-like organisms. Journal of Invertebrate Pathology 56, 337346.CrossRefGoogle ScholarPubMed
Lung, O., Kuo, L. and Wolfner, M. F. (2001) Drosophila males transfer antibacterial proteins from their accessory gland and ejaculatory duct to their mates. Journal of Insect Physiology 47, 617622.CrossRefGoogle ScholarPubMed
Neubaum, D. M. and Wolfner, M. F. (1999) Mated Drosophila melanogaster females require a seminal fluid protein, Acp 36 DE, to store sperm efficiently. Genetics 153, 845857.CrossRefGoogle Scholar
Odhiambo, T. R., Kokwaro, E. D. and Sequeira, L. M. (1983) Histochemical and ultrastructural studies of the male accessory reproductive glands and the spermatophore of the tsetse, G. morsitans morsitans. Insect Science and Its Application 4, 227–236.Google Scholar
Otieno, L. H., Kokwaro, E. D., Chimtawi, M. and Onyango, P. (1980) Prevalence of enlarged salivary glands in wild population of Glossina pallidipes in Kenya, with a note on the ultrastructure of the affected organ. Journal of Invertebrate Pathology 36, 113–118.CrossRefGoogle Scholar
Price, C. S. C., Dyer, K. A. and Coyne, J. A. (1999) Sperm competition between Drosophila males involves both displacement and incapacitation. Nature 400, 449452.CrossRefGoogle ScholarPubMed
Sang, C. S., Jura, W. G. Z. O., Otieno, L. H., Mwangi, R. W. and Ogaja, P. (1999) The effects of a tsetse DNA virus infection on the functions of the male accessory reproductive gland in the host fly Glossina morsitans centralis (Diptera: Glossinidae). Current Microbiology 38, 349354.CrossRefGoogle ScholarPubMed
Viscuso, R., Narcisi, L., Sottile, L. and Violetta, B. M. (2001) Role of the male accessory glands in spermatodesm reorganization in Orthoptera: Tettigonioidea. Tissue and Cell 33, 33–39.CrossRefGoogle ScholarPubMed
Yi, S. X. and Gillott, C. (2000) Effects of tissue extracts on oviduct contraction in the migratory grasshopper, Melanoplus sanguinipes. Journal of Insect Physiology 46, 519525.CrossRefGoogle ScholarPubMed