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. 2000 Jul-Aug;6(4):329–336. doi: 10.3201/eid0604.000402

Male-killing bacteria in insects: mechanisms, incidence, and implications.

G D Hurst 1, F M Jiggins 1
PMCID: PMC2640894  PMID: 10905965

Abstract

Bacteria that are vertically transmitted through female hosts and kill male hosts that inherit them were first recorded in insects during the 1950s. Recent studies have shown these "male-killers" to be diverse and have led to a reappraisal of the biology of many groups of bacteria. Rickettsia, for instance, have been regarded as human pathogens transmitted by arthropods. The finding of a male-killing Rickettsia obligately associated with an insect suggests that the genus' members may be primarily associated with arthropods and are only sometimes pathogens of vertebrates. We examined both how killing of male hosts affects the dynamics of inherited bacteria and how male-killing bacteria affect their host populations. Finally, we assessed the potential use of these microorganisms in the control of insect populations.

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Selected References

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  1. Bandi C., Damiani G., Magrassi L., Grigolo A., Fani R., Sacchi L. Flavobacteria as intracellular symbionts in cockroaches. Proc Biol Sci. 1994 Jul 22;257(1348):43–48. doi: 10.1098/rspb.1994.0092. [DOI] [PubMed] [Google Scholar]
  2. Baumann P., Lai C., Baumann L., Rouhbakhsh D., Moran N. A., Clark M. A. Mutualistic associations of aphids and prokaryotes: biology of the genus buchnera. Appl Environ Microbiol. 1995 Jan;61(1):1–7. doi: 10.1128/aem.61.1.1-7.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. COUNCE S. J., POULSON D. F. Developmental effects of the sexratio agent in embryos of Drosophila willistoni. J Exp Zool. 1962 Oct;151:17–31. doi: 10.1002/jez.1401510103. [DOI] [PubMed] [Google Scholar]
  4. Davis M. J., Ying Z., Brunner B. R., Pantoja A., Ferwerda F. H. Rickettsial relative associated with papaya bunchy top disease. Curr Microbiol. 1998 Feb;36(2):80–84. doi: 10.1007/s002849900283. [DOI] [PubMed] [Google Scholar]
  5. Hackett K. J., Lynn D. E., Williamson D. L., Ginsberg A. S., Whitcomb R. F. Cultivation of the Drosophila sex-ratio spiroplasma. Science. 1986 Jun 6;232(4755):1253–1255. doi: 10.1126/science.232.4755.1253. [DOI] [PubMed] [Google Scholar]
  6. Higashiura Y., Ishihara M., Schaefer P. W. Sex ratio distortion and severe inbreeding depression in the gypsy moth Lymantria dispar L. in Hokkaido, Japan. Heredity (Edinb) 1999 Sep;83(Pt 3):290–297. doi: 10.1038/sj.hdy.6885590. [DOI] [PubMed] [Google Scholar]
  7. Hurst G. D., Bandi C., Sacchi L., Cochrane A. G., Bertrand D., Karaca I., Majerus M. E. Adonia variegata (Coleoptera: Coccinellidae) bears maternally inherited flavobacteria that kill males only. Parasitology. 1999 Feb;118(Pt 2):125–134. doi: 10.1017/s0031182098003655. [DOI] [PubMed] [Google Scholar]
  8. Hurst G. D., Graf von der Schulenburg J. H., Majerus T. M., Bertrand D., Zakharov I. A., Baungaard J., Völkl W., Stouthamer R., Majerus M. E. Invasion of one insect species, Adalia bipunctata, by two different male-killing bacteria. Insect Mol Biol. 1999 Feb;8(1):133–139. doi: 10.1046/j.1365-2583.1999.810133.x. [DOI] [PubMed] [Google Scholar]
  9. Hurst G. D., Hammarton T. C., Obrycki J. J., Majerus T. M., Walker L. E., Bertrand D., Majerus M. E. Male-killing bacterium in a fifth ladybird beetle, Coleomegilla maculata (Coleoptera:Coccinellidae). Heredity (Edinb) 1996 Aug;77(Pt 2):177–185. doi: 10.1038/hdy.1996.122. [DOI] [PubMed] [Google Scholar]
  10. Hurst GDD, Walker LE, Majerus MEN. Bacterial Infections of Hemocytes Associated with the Maternally Inherited Male-Killing Trait in British Populations of the Two Spot Ladybird, Adalia bipunctata. J Invertebr Pathol. 1996 Nov;68(3):286–292. doi: 10.1006/jipa.1996.0098. [DOI] [PubMed] [Google Scholar]
  11. Ikeda H. The cytoplasmically-inherited "sex-ratio" condition in natural and experimental populations of Drosophila bifasciata. Genetics. 1970 Jun;65(2):311–333. doi: 10.1093/genetics/65.2.311. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Jiggins F. M., Hurst G. D., Jiggins C. D., v d Schulenburg J. H., Majerus M. E. The butterfly Danaus chrysippus is infected by a male-killing Spiroplasma bacterium. Parasitology. 2000 May;120(Pt 5):439–446. doi: 10.1017/s0031182099005867. [DOI] [PubMed] [Google Scholar]
  13. Jiggins F. M., Hurst G. D., Majerus M. E. Sex-ratio-distorting Wolbachia causes sex-role reversal in its butterfly host. Proc Biol Sci. 2000 Jan 7;267(1438):69–73. doi: 10.1098/rspb.2000.0968. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. O'Neill S. L., Giordano R., Colbert A. M., Karr T. L., Robertson H. M. 16S rRNA phylogenetic analysis of the bacterial endosymbionts associated with cytoplasmic incompatibility in insects. Proc Natl Acad Sci U S A. 1992 Apr 1;89(7):2699–2702. doi: 10.1073/pnas.89.7.2699. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. doi: 10.1098/rspb.1999.0698. [DOI] [PMC free article] [Google Scholar]
  16. Roberts L. W., Rapmund G., Cadigan F. C., Jr Sex ratios in rickettsia tsutsugamushi-infected and noninfected colonies of Leptotrombidium (Acari: trombiculidae). J Med Entomol. 1977 Aug 20;14(1):89–92. doi: 10.1093/jmedent/14.1.89. [DOI] [PubMed] [Google Scholar]
  17. Robinson A. S. Sex-ratio manipulation in relation to insect pest control. Annu Rev Genet. 1983;17:191–214. doi: 10.1146/annurev.ge.17.120183.001203. [DOI] [PubMed] [Google Scholar]
  18. SAKAGUCHI B., POULSON D. F. Distribution of "sex-ratio" agent in tissues of Drosophila willistoni. Genetics. 1961 Dec;46:1665–1676. doi: 10.1093/genetics/46.12.1665. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Sakaguchi B, Poulson D F. Interspecific Transfer of the "Sex-Ratio" Condition from Drosophila Willistoni to D. Melanogaster. Genetics. 1963 Jun;48(6):841–861. doi: 10.1093/genetics/48.6.841. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Skinner S. W. Son-killer: a third extrachromosomal factor affecting the sex ratio in the parasitoid wasp, Nasonia (=Mormoniella) vitripennis. Genetics. 1985 Apr;109(4):745–759. doi: 10.1093/genetics/109.4.745. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Stouthamer R., Breeuwer J. A., Hurst G. D. Wolbachia pipientis: microbial manipulator of arthropod reproduction. Annu Rev Microbiol. 1999;53:71–102. doi: 10.1146/annurev.micro.53.1.71. [DOI] [PubMed] [Google Scholar]
  22. Takahashi M., Urakami H., Yoshida Y., Furuya Y., Misumi H., Hori E., Kawamura A., Jr, Tanaka H. Occurrence of high ratio of males after introduction of minocycline in a colony of Leptotrombidium fletcheri infected with Orientia tsutsugamushi. Eur J Epidemiol. 1997 Jan;13(1):79–86. doi: 10.1023/a:1007341721795. [DOI] [PubMed] [Google Scholar]
  23. Werren J. H., Hurst G. D., Zhang W., Breeuwer J. A., Stouthamer R., Majerus M. E. Rickettsial relative associated with male killing in the ladybird beetle (Adalia bipunctata). J Bacteriol. 1994 Jan;176(2):388–394. doi: 10.1128/jb.176.2.388-394.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Werren J. H., Skinner S. W., Huger A. M. Male-killing bacteria in a parasitic wasp. Science. 1986 Feb 28;231(4741):990–992. doi: 10.1126/science.3945814. [DOI] [PubMed] [Google Scholar]
  25. Whitcomb R. F. The genus Spiroplasma. Annu Rev Microbiol. 1980;34:677–709. doi: 10.1146/annurev.mi.34.100180.003333. [DOI] [PubMed] [Google Scholar]

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