Eur. J. Entomol. 102 (4): 669-674, 2005
Effects of Wolbachia-targeted tetracycline on a host-parasitoid-symbiont interaction
- Laboratory of Seribiotechnology, Department of Sericulture, Jnanabharathi Campus, Bangalore University, Bangalore 560056,
The uzifly, Exorista sorbillans (Diptera: Tachinidae), a parasite of the silkworm, Bombyx mori L. (Lepidoptera: Bombycidae), causes heavy losses to the silk industry. This parasitoid harbours a Wolbachia endosymbiont, which controls the fly's reproduction. In the present study a method for curtailing this notorious pest by administering Wolbachia-targeted tetracycline via its silkworm host's diet is investigated. Tetracycline not only influenced the larval growth of the silkworms' by decreasing larval duration, increased silk production and fecundity, without affecting hatchability, it also decreased the reproductive fitness of the uzifly endoparasite by killing the Wolbachia. The antibiotic exerts a beneficial influence by affecting the intestinal flora of silkworm larvae. On the other hand the reproductive fitness of uzifly was greatly reduced in terms of different reproductive abnormalities. When male and female flies that emerged from treated host silkworms were crossed and males from untreated hosts and females from treated hosts were crossed, approximately 72% and 97% of the eggs failed to hatch, respectively. However, of the eggs from crosses between male and female flies that emerged from untreated hosts and between males from treated hosts with females from untreated hosts, an average of 30% failed to hatch and the Wolbachia infection enhanced the fecundity of uziflies. These results demonstrate that the Wolbachia may be essential for uzifly reproduction and that Wolbachia-targeted antibiotics have a beneficial influence on silkworm growth while decreasing the reproductive fitness of the uzifly, E. sorbillans.
Keywords: Wolbachia, Exorista sorbillans, Tachinidae, Bombyx mori, tetracycline, fecundity, cytoplasmic incompatibility, commercial characters
Received: June 7, 2004; Revised: April 25, 2005; Accepted: April 25, 2005; Published: November 3, 2005 Show citation
References
- BARR A.R. 1980: Cytoplasmic incompatibility in natural populations of a mosquito, Culex pipiens L. Nature 283: 71-72
Go to original source...
- BREEUWER J.A.J. 1997: Wolbachia and cytoplasmic incompatibility in the spider mite Tetranychus urticae and T. turkestani. Heredity 79: 41-47
Go to original source...
- BREEUWER J.A.J., STOUTHAMER R., BURNS D.A., PELLETIER D.A., WEISBURG W.G. & WERREN J.H. 1992: Phylogeny of cytoplasmic incompatibility microorganisms in the parasitoid wasp genus Nasonia (Hymenoptera: Pteromalidae) based on 16s ribosomal DNA sequences. Insect Mol. Biol. 1: 25-36
Go to original source...
- CHANNABASAVANNA G.P., SIDDAPPAJI C. & DANDIN S.B. 1993: Integrated management of the Indian uzi fly, Exorista bombycis infesting the mulberry silkworm. In Channabasavanna G.P., Veeranna G. & Dandin S.B. (eds): Recent Advances in Uzi Fly Research. Proceedings of the National Seminar on Uzi Fly and its Control, 16-17 January, 1992. Bangalore, India, pp. 227-237
- CHATTERJEE S.N., MOHANDAS T.P. & TARAPHDAR T. 2003: Molecular characterization of the gene pool of Exorista sorbillans (Diptera: Tachinidae) a parasitoid of silkworm Bombyx mori, in India. Eur. J. Entomol. 100: 195-200
Go to original source...
- DEDEINE F., VAVRE F., FLEURY F., LOPPIN B., HOCHBERG M. & BOULETREAU M. 2001: Removing symbiotic Wolbachia bacteria specifically inhibits oogenesis in a parasitic wasp. Proc Natl Acad Sci. USA 98: 6247-6252
Go to original source...
- DEDEINE F., VAVRE F., FLEURY F., SHOEMAKER D.D. & BOULETREAU M. 2004: Intra-individual coexistence of a Wolbachia strain required for host oogenesis with two strains inducing cytoplasmic incompatibnility in the wasp Asobara tabida. Evolution 58: 2167-2174
Go to original source...
- GOVINDAN R. & DEVAIAH M.C. 1995: Bacterial Flacherie of Silkworm. Communication center UAS, Bangalore
- HOERAUF A., NISSEN-PAHLE K., SCHMETZ C., HENKLE-DUHRSEN K., BLAXTER M.L., BUTTNER D.W., GALLIN M.Y., AL-QAOUD K.M., LUCIUS R. & FLEISCHER B. 1999: Tetracycline therapy targets intracellular bacteria in the filarial nematode Litomosoides sigmodontis and results in filarial infertility. J. Clin. Invest. 103: 11-18
Go to original source...
- HURST G.D.D., JIGGINS F.M., SCHULENBURG J.H.G.V.D., BERTRAND D., WEST S.A., GORIACHEVA I.I., ZAKHAROV I.A., WERREN J.H., STOUTHAMER R. & MAJERUS M.E.N. 1999: Malekilling Wolbachia in two species of insect. Proc. R. Soc. Lond. (B) 266: 735-740
Go to original source...
- JEYAPRAKASH A. & HOY M.A. 2000: Long PCR improves Wolbachia DNA amplification: WSP sequence found in 76% of sixty-three arthropod species. Insect Mol. Biol. 9: 393-405
Go to original source...
- KAMBHAMPATI S., RAI K.S. & BURGUN S.J. 1993: Unidirectional Cytoplasmic Incompatibility in the mosquito, Aedes albopictus. Evolution 47: 673-677
Go to original source...
- KHAN I.A. & KHANUM A. 1994: Fundamentals of Biostatistics. Ukaaz Publications, Hyderabad, India, pp. 392-431
- KOZEK W.J. 1997: Transovarially-transmitted intracellular microorganisms in adult and larval stage of Brugia malayi. J. Parasitol. 63: 992-1000
Go to original source...
- LANGWORTHY N.G., RENZ A., MACKENSTED U., HENKLE-DUHRSEN K., BRONSVOORT M.B., TANYA V.N., DONNELLY M.J. & TREES A.J. 2000: Macro filarial activity of tetracycline against the filarial nematode Onchocerca ochengi: elimination of Wolbachia species precedes worm death and suggests a dependent relationship. Proc. R. Soc. Lond. (B) 367: 1063-1069.
Go to original source...
- MADHU M. & PUTTARAJU H.P. 2001: Cytological and molecular incidence for Wolbachia infection in Uzi flies of Exorista species. Cytologia 66: 197-203
Go to original source...
- MAHADEVAPPA D., HALLIYAL V.G., SHANKAR D.G & BHANDIWAD R. 2000: Mulberry Silk Reeling Technology. Oxford and IBH publication Co., India
- MANJUNATHA H.B. & PUTTARAJU H.P. 1993: The egg of the uzifly, Exorista sorbillans (Diptera: Tachinidae). Appl. Entomol. Zool. 28: 574-577
Go to original source...
- MIN K.T. & BENZER S. 1997: Wolbachia, normally a symbiont of Drosophila, can be virulent, causing degeneration and early death. Proc. Natl. Acad. Sci. USA 94: 10792-10796
Go to original source...
- MUKUNDA N. 1999: Effect of Application of Tetracycline and Sulphamethaxazole on the Growth and Development of Silkworm Bombyx mori. M.Sc. Dissertation, Bangalore University, Bangalore
- O'NEILL S.L., GIORDANO R., COLBERT A.M.E., KARR T.L. & ROBERTSON H.M. 1992: 16s rDNA phylogenetic analysis of the bacterial endosymbionts associated with cytoplasmic incompatibility in insets. Proc. Natl. Acad. Sci. USA 89: 2699-2702
Go to original source...
- PUTTARAJU H.P. & MADHU M. 2002: Presence of Wolbachia endosymbionts in different silkworm species and races and in their Uzi fly parasites. J. Invertebr. Pathol. 79: 120-122
Go to original source...
- QU X.M., QI G.R. & HUANG Z.R. 1984: Comparative studies on antibacterial substances of silkworm after Escherichia coli infection and ultrasonic treatment. Acta Entomol. Sin. 27: 275-279
- ROUSSET F., BOUCHON D., PINTUREAU B., JUCHAULT P. & SOLIGNAC M. 1992: Wolbachia endosymbionts responsible for various alterations of sexuality in arthropods. Proc. R. Soc. Lond. (B) 250: 91-98
Go to original source...
- SAMBROOK J., FRITSCH E.F. & MINIATIS T. 1989: Molecular Cloning: A Laboratory Manual. 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York, 999 pp
- SHIVASHANKARAPPA L.H. & PUTTARAJU H.P. 1995: Effect of diflubenzuron on the reproduction of uzifly, Exorista bombycis (E. sorbillans) (Diptera: Tachinidae). Sericologia 15: 763-766
- SHYAMALA M.B., SHARADA K., BHAT M.G. & BHAT J.V. 1960: Chloromycetin in the nutrition of the silkworm Bombyx mori L. II Influence on digestion and utilization of protein, fat and minerals. J. Insect Physiol. 4: 229-234
Go to original source...
- STOUTHAMER R., BREEUWER J.A.J., LUCK R.F. & WERREN H. 1993: Molecular identification of microorganisms associated with parthenogenesis. Nature 361: 66-68
Go to original source...
- TAYLOR M.J. & HOERAUF A. 2001: A new approach to the treatment of filariasis. Car. Opin. Infect. Dis. 14: 727-731
Go to original source...
- TRPIS M., PERRONE J.B., REISSIG M. & PARKER K.L. 1981: Control of cytoplasmic incompatibility in the Aedes scuttellaris complex. J. Heredity 72: 313-317
Go to original source...
- ULLAL S.R. & NARASIMHANNA M.N. 1994: Handbook of Practical Sericulture. Arun Ramanath, Omkar offset, Bangalore
- VALA F., VAN OPIJNEN T., BREEUWER J.A. & SABELIS M.W. 2003: Genetic conflict over sex-ratio: mite-endosymbiont interactions. Am. Nat. 161: 254-266
Go to original source...
- VENKATACHALAMURTHY M. R. & SREENIVASAYA M. 1953: Effect of antibiotics on the growth of the silkworm, Bombyx mori L. Nature 173: 684-685
Go to original source...
- WADE M.J. & CHANG N.W. 1995: Increased male fertility in Tribolium confusum beetle after infection with the intracellular parasite Wolbachia. Nature 51: 72-74
Go to original source...
- WERREN J.H. 1997: Biology of Wolbachia. Annu. Rev. Entomol. 42: 587-609
Go to original source...
- WERREN J.H. & BEUKEBOOM L. 1998: Sex determination, sex ratios and genetic conflict. Annu. Rev. Ecol. Syst. 29: 233-261
Go to original source...
- WERREN J.H., WINDSOR D. & GUO L. 1995: Distribution of Wolbachia among neotropical arthropods. Proc. R. Soc. Lond. (B) 262: 197-204
Go to original source...
- ZABALOU S., RIEGLER M., THEODORAKOPOULOU M., STAUFFER C., SAVAKIS C. & BOURTZIS K. 2004: Wolbachia-induced cytoplasmic incompatibility as a means for insect pest population control. Proc. Natl. Acad. Sci. USA 101: 15042-15045
Go to original source...
This is an open access article distributed under the terms of the Creative Commons Attribution 4.0 International License (CC BY 4.0), which permits use, distribution, and reproduction in any medium, provided the original publication is properly cited. No use, distribution or reproduction is permitted which does not comply with these terms.