Hostname: page-component-586b7cd67f-gb8f7 Total loading time: 0 Render date: 2024-11-25T18:17:23.520Z Has data issue: false hasContentIssue false

Insect immunity: early events in the encapsulation process of parasitoid (Leptopilina boulardi) eggs in resistant and susceptible strains of Drosophila

Published online by Cambridge University Press:  06 April 2009

J. Russo
Affiliation:
Université de Rennes1, 34042 Rennes, France
S. Dupas
Affiliation:
Laboratoire de Biologie et Génétique Evolutives, CNRS, 91190 Gif sur Yvette, France INRA-CNRS URA1184, PL. E. Bataillon, 34095 Montpellier, France
F. Frey
Affiliation:
Laboratoire de Biologie et Génétique Evolutives, CNRS, 91190 Gif sur Yvette, France
Y. Carton
Affiliation:
Laboratoire de Biologie et Génétique Evolutives, CNRS, 91190 Gif sur Yvette, France
M. Brehelin
Affiliation:
INRA-CNRS URA1184, PL. E. Bataillon, 34095 Montpellier, France

Summary

Eggs of an immune suppressive strain ( = virulent) of the parasitoid Leptopilina boulardi are encapsulated neither in resistant nor in susceptible strains of Drosophila melanogaster but are encapsulated in Drosophila yakuba. Eggs of a non-immune suppressive strain ( = avirulent) of the same parasitoid are encapsulated in a resistant strain of D. melanogaster and in D. yakuba but are not encapsulated in a susceptible strain of D. melanogaster. Egg chorion in the 2 parasitoid strains showed the same morphology and the same modifications after egg laying whatever the host strain. When a capsule is built, a small dotted dense layer was first spread on the chorion, followed by accumulation layers of cells (plasmatocytes and lamellocytes) and lastly necrosis of the inner haemocytes. The encapsulated eggs darken only at the time of necrosis of haemocytes. In susceptible hosts, neither the tiny dense layer nor haemocyte accumulation occured. We concluded that (1) this tiny dense layer was present before the deposition of the first haemocytes, (2) inhibition of deposition of this dense layer was the initial event of the induced immunosupression, (3) haemocytes other than lamellocytes were engaged in caspsule formation, (4) the immunosupressive factors did not target only the lamellocytes but also the plasmatocytes, (5) darkening of the encapsulated eggs was due to cell necrosis rather than to extracellular melanin deposition.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1996

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

Brehélin, M. (1982). Comparative study of structure and function of blood cells from two Drosophila species. Cell and Tissue Research 221, 607–15.CrossRefGoogle ScholarPubMed
Brehélin, M., Hoffmann, J. A., Matz, G. & Porte, A. (1975). Encapsulation of implanted foreign bodies by haemocytes of Locusta migratoria and Melolontha melolontha. Cell and Tissue Research 160, 283–9.Google Scholar
Carton, Y., Bouletreau, M., Van Alphen, J. J. M. & Van Lenteren, J. C. (1986). The Drosophila parasitic wasps. In The Genetics and Biology of Drosophila, Vol 3C (ed.Ashburger, M. & Thompson, J.), pp. 347394. New York/London: Academic Press.Google Scholar
Carton, Y., Frey, F. & Nappi, A. (1992). Inheritance of cellular immune resistance in Drosophila melanogaster. Heredity 69, 393–9.Google Scholar
Carton, Y. & Kitano, H. (1981). Evolutionary relationships to parasitism by seven species of the Drosophila melanogaster subgroup. Biological Journal of the Linnean Society 16, 227–41.CrossRefGoogle Scholar
Carton, Y. & Nappi, A. J. (1991). The Drosophila immune reaction and the parasitoid capacity to evade it: genetic and coevolutionary aspects. Acta Oecologia 12, 89104.Google Scholar
Nappi, A. J. (1984). Hemocyte reactions and early cellular changes during melanotic tumor formation in Drosophila melanogaster. Journal of Invertebrate Pathology 43, 395406.CrossRefGoogle Scholar
Nappi, A. J. & Vass, E. (1993). Melanogenesis and the generation of cytotoxic molecules during insect cellular immune reactions. Pigment Cell Research 6, 117–26.Google Scholar
Nappi, A. J., Vass, E., Frey, F. & Carton, Y. (1995). Superoxide anion generation in Drosophila during melanotic encapsulation of parasites. European Journal of Cell Biology (in the Press).Google Scholar
Poinar, G. O., Leutenegger, R. & Götz, P. (1968). Ultrastructure of the formation of a melanotic capsule in Diabrotica (Coleoptera) in response to a parasitic nematode (Mermithidae). Journal of Ultrastructure Research 25, 293306.Google Scholar
Ratcliffe, N. A., Leonard, C. M. & Rowley, A. F. (1984). Prophenoloxidase activation: nonself recognition and cell cooperation in insect immunity. Science 226, 557–9.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, 208–12.Google Scholar
Rizki, T. M.(1962). Experimental analysis of hemocyte morphology in insects. American Zoologist 2, 247–56.Google Scholar
Rizki, R. M. & Rizki, T. M. (1979). Cell interactions in the differentiation of a melanotic tumor in Drosophila. Differentiation 12, 167–78.CrossRefGoogle ScholarPubMed
Rizki, R. M. & Rizki, T. M. (1980). Hemocyte responses to implanted tissues in Drosophila melanogaster larvae. Roux's Archives of Developmental Biology 189, 209–13.Google Scholar
Rizki, R. M. & Rizki, T. M. (1990). Parasitoid virus-like particles destroy Drosophila cellular immunity. Proceedings of the National Academy of Sciences, USA 87, 8388–92.Google Scholar
Schmit, A. R. & Ratcliffe, N. A. (1977). The encapsulation of foreign tissue implants in Galleria mellonella larvae. Journal of Insect Physiology 23, 175–84.CrossRefGoogle ScholarPubMed
Söderhäll, K. & Smith, V. J. (1986). The prophenoloxidase activating system: the biochemistry of its activation and role in arthropod cellular immunity, with special reference to crustaceans. In Immunity in Invertebrates (ed. Brehélin, M.), pp. 208–23. Berlin: Springer Verlag.Google Scholar
Vass, E., Nappi, A. J. & Carton, Y. (1993). Comparative study of immune competence and host susceptibility in Drosophila melanogaster parasitized by Leptopilina boulardi and Asobara tabida. Journal of Parasitology 79, 106–12.Google Scholar