Skip directly to site content Skip directly to page options Skip directly to A-Z link Skip directly to A-Z link Skip directly to A-Z link
Volume 6, Number 4—August 2000
Perspective

Male-Killing Bacteria in Insects: Mechanisms, Incidence, and Implications

Gregory D.D. Hurst and Francis M. Jiggins

Author affiliations: University College London, United Kingdom

Article in Chinese

Main Article

Table 1

Prevalence of male-killers in natural populations of their insect hosts (proportion of females infected)

Bacterium Host Prevalence (%) Ref.
Spiroplasma sp. (S. ixodetis relative) Adalia bipunctata 0-22 6
Harmonia axyridis 0-49 35
Danaus chrysippus 40 14
Spiroplasma poulsonii Drosophila willistoni group flies 0-3 20
Wolbachia Acraea encedon 61-95 36
Acraea encedana 95 21
Adalia bipunctata 0-5 9
Unnamed Flavobacteria Coleomegilla maculata 23 37
Adonia variegata 13 38
Arsenophonus nasoniae Nasonia vitripennis 4 15
Rickettsia Adalia bipunctata 5-7 6,39
Unknown D. bifasciata 0-7 26
D. prosaltans 13 33
Gastrolina depressa 0-81 22
Epiphyas postvittana 4-7 40
Hypolimnas bolina 0-61 41
Spodoptera littoralis 24 42
Lymantria dispar 9 43

Main Article

References
  1. Moran  N, Baumann  P. Phylogenetics of cytoplasmically inherited microorganisms of arthropods. Trends Ecol Evol. 1994;9:15–20. DOIGoogle Scholar
  2. Baumann  P, Lai  C-Y, Baumann  L, Rouhbakhsh  D, Moran  NA, Clark  MA. Mutualistic associations of aphids and prokaryotes: biology of the genus Buchnera. Appl Environ Microbiol. 1995;61:1–7.PubMedGoogle Scholar
  3. O'Neill  S, Giordano  R, Colbert  AME, Karr  TL, Robertson  HM. 16S rRNA phylogenetic analysis of the bacterial endosymbionts associated with cytoplasmic incompatability in insects. Proc Natl Acad Sci U S A. 1992;89:2699–702. DOIPubMedGoogle Scholar
  4. Hackett  KJ, Lynn  DE, Williamson  DL, Ginsberg  AS, Whitcomb  RF. Cultivation of the Drosophila spiroplasma. Science. 1986;232:1253–5. DOIPubMedGoogle Scholar
  5. Werren  JH, Skinner  SW, Huger  AM. Male-killing bacteria in a parasitic wasp. Science. 1986;231:990–2. DOIPubMedGoogle Scholar
  6. Hurst  GDD, vd Schulenburg  HG, Majerus  TMO, Bertrand  D, Zakharov  IA, Baungaard  J, . Invasion of one insect species, Adalia bipunctata, by two different male-killing bacteria. Insect Mol Biol. 1999;8:133–9. DOIPubMedGoogle Scholar
  7. Hurst  GDD, Hammarton  TC, Majerus  TMO, Bertrand  D, Bandi  C, Majerus  MEN. Close relationship of the inherited parasite of the ladybird, Coleomegilla maculata, to Blattabacterium, the beneficial symbiont of the cockroach. Genet Res. 1997;70:1–6. DOIGoogle Scholar
  8. Werren  JH, Hurst  GDD, Zhang  W, Breeuwer  JAJ, Stouthamer  R, Majerus  MEN. Rickettsial relative associated with male killing in the ladybird beetle (Adalia bipunctata). J Bacteriol. 1994;176:388–94.PubMedGoogle Scholar
  9. Hurst  GDD, Jiggins  FM, vd Schulenburg  JHG, Bertrand  D, West  SA, Goriacheva  II, . Male-killing Wolbachia in two species of insect. Proc R Soc Lond B Biol Sci. 1999;266:735–40. DOIGoogle Scholar
  10. Whitcomb  RF. The genus Spiroplasma. Annu Rev Microbiol. 1980;34:677–709. DOIPubMedGoogle Scholar
  11. Davis  MJ, Ying  Z, Brunner  BR, Pantoja  A, Ferwerda  FH. Rickettsial relative associated with papaya bunchy top disease. Curr Microbiol. 1998;36:80–4. DOIPubMedGoogle Scholar
  12. Stouthamer  R, Breeuwer  JAJ, Hurst  GDD. Wolbachia pipientis: microbial manipulator of arthropod reproduction. Annu Rev Microbiol. 1999;53:71–102. DOIPubMedGoogle Scholar
  13. Bandi  C, Damiani  G, Magrassi  L, Grigolo  A, Fani  R, Sacchi  L. Flavobacteria as intracellular symbionts in cockroaches. Proc R Soc Lond B Biol Sci. 1994;257:43–8. DOIGoogle Scholar
  14. Jiggins  FM, Hurst  GDD, Jiggins  CD. vd Schulenburg JHG, Majerus MEN. The butterfly Danaus chrysippus is infected by a male-killing Spiroplasma bacterium. Parasitology. 2000;120:439–46. DOIPubMedGoogle Scholar
  15. Skinner  SW. Son-killer: a third extrachromosomal factor affecting sex ratios in the parasitoid wasp Nasonia vitripennis. Genetics. 1985;109:745–54.PubMedGoogle Scholar
  16. Werren  JH. The coevolution of autosomal and cytoplasmic sex ratio factors. J Theor Biol. 1987;124:317–34. DOIGoogle Scholar
  17. Hurst  GDD, Majerus  MEN. Why do maternally inherited microorganisms kill males? Heredity. 1993;71:81–95. DOIGoogle Scholar
  18. Roberts  LW, Rapmund  G, Cadigan  FCJ. Sex ratio in Rickettsia tsutsugamushi infected and non-infected colonies of Leptotrombidium (Acari: Trombiculidae). J Med Entomol. 1977;14:89–92.PubMedGoogle Scholar
  19. Takahashi  M, Urakami  H, Yoshida  Y, Furuya  Y, Misumi  H, Hori  E, Occurrence of high ratio of males after introduction of minocycline in a colony of Leptotrombidium fletcheri infected with Orientia tsutsugamushi. Eur J Epidemiol. 1997;13:79–86. DOIPubMedGoogle Scholar
  20. Williamson  DL, Poulson  DF. Sex ratio organisms (Spiroplasmas) of Drosophila. In Sex ratio organisms (Spiroplasmas) of Drosophila, ed. RF Whitcomb, JG Tully. Vol. III. 1979; New York: Academic Press. pp. 175-208.
  21. Jiggins  FM, Hurst  GDD, Dolman  CE, Majerus  MEN. High prevalence of male-killing Wolbachia in the butterfly Acraea encedana. J Evol Biol. 2000;13:495–501. DOIGoogle Scholar
  22. Chang  KS, Shiraishi  T, Nakasuji  F, Morimoto  N. Abnormal sex ratio condition in the walnut leaf beetle, Gastrolina depressa (Coleoptera: Chrysomelidae). Appl Entomol Zool (Jpn). 1991;26:299–306.
  23. Counce  SJ, Poulson  DF. Developmental effects of the sex-ratio agent in embryos of Drosophila willistoni. J Exp Zool. 1962;151:17–31. DOIPubMedGoogle Scholar
  24. Sakaguchi  B, Poulson  DF. Interspecific transfer of the "sex-ratio" condition from Drosophila willistoni to D. melanogaster. Genetics. 1963;48:841–61.PubMedGoogle Scholar
  25. Hurst  GDD, Purvis  EL, Sloggett  JJ, Majerus  MEN. The effect of infection with male-killing Rickettsia on the demography of female Adalia bipunctata L. (two spot ladybird). Heredity. 1994;73:309–16. DOIGoogle Scholar
  26. Ikeda  H. The cytoplasmically inherited 'sex-ratio' condition in natural and experimental populations of Drosophila bifasciata. Genetics. 1970;65:311–33.PubMedGoogle Scholar
  27. Malogolowkin-Cohen  C, Rodriguez-Pereira  MAQ. Sexual drive of normal and SR flies of Drosophila nebulosa. Evolution. 1975;29:579–80. DOIGoogle Scholar
  28. Ebbert  M. The interaction phenotype in the Drosophila willistoni - spiroplasma symbiosis. Evolution. 1991;45:971–88. DOIGoogle Scholar
  29. Sakaguchi  B, Poulson  DF. Distribution of "sex-ratio" agent in tissues of Drosophila willistoni. Genetics. 1961;46:1665–76.PubMedGoogle Scholar
  30. 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;68:286–92. DOIPubMedGoogle Scholar
  31. Jiggins  FM, Hurst  GDD, Majerus  MEN. Sex ratio distorting Wolbachia causes sex role reversal in its butterfly host. Proc R Soc Lond B Biol Sci. 2000;267:69–73. DOIGoogle Scholar
  32. Hurst  GDD, McVean  GAT. Parasitic male-killing bacteria and the evolution of clutch size. Ecol Entomol. 1998;23:350–3. DOIGoogle Scholar
  33. Cavalcanti  AGL, Falcao  DN, Castro  LE. "Sex-ratio" in Drosophila prosaltans-a character due to interaction between nuclear genes and cytoplasmic factors. Am Nat. 1957;91:327–9. DOIGoogle Scholar
  34. Robinson  AS. Sex Ratio manipulation in relation to insect pest control. Annu Rev Genet. 1983;17:191–214. DOIPubMedGoogle Scholar
  35. Majerus  TMO, Majerus  MEN, Knowles  B, Wheeler  J, Bertrand  D, Kuznetsov  VN, Extreme variation in the prevalence of inherited male-killing microorganisms between three populations of Harmonia axyridis (Coleoptera: Coccinellidae). Heredity. 1998;81:683–91. DOIGoogle Scholar
  36. Jiggins  FM, Hurst  GDD, Majerus  MEN. Sex ratio distortion in Acraea encedon (Lepidoptera: Nymphalidae) is caused by a male-killing bacterium. Heredity. 1998;81:87–91. DOIGoogle Scholar
  37. Hurst  GDD, Hammarton  TC, Obrycki  JJ, Majerus  TM, Walker  LE, Bertrand  D, Male-killing bacteria in a fifth ladybird beetle, Coleomegilla maculata (Coleoptera: Coccinellidae). Heredity. 1996;77:177–85. DOIPubMedGoogle Scholar
  38. Hurst  GDD, Bandi  C, Sacchi  L, Cochrane  A, Bertrand  D, Karaca  I, Adonia variegata (Coleoptera: Coccinellidae) bears maternally inherited Flavobacteria that kill males only. Parasitology. 1999;118:125–34. DOIPubMedGoogle Scholar
  39. Hurst  GDD, Majerus  MEN, Walker  LE. The importance of cytoplasmic male killing elements in natural populations of the two spot ladybird, Adalia bipunctata (Linnaeus) (Coleoptera: Coccinellidae). Biol J Linn Soc Lond. 1993;49:195–202.
  40. Geier  PW, Briese  DT, Lewis  T. The light brown apple moth Epiphyas postvittana (Walker). 2. Uneven sex ratios and a condition contributing to them in the field. Aust J Ecol. 1978;3:467–88. DOIGoogle Scholar
  41. Clarke  C, Sheppard  PM, Scali  V. All female broods in the butterfly Hypolimnas bolina (L.). Proc R Soc Lond B Biol Sci. 1975;189:29–37. DOIGoogle Scholar
  42. Brimacombe  LC. All-female broods in field and laboratory populations of the Egyptian cotton leafworm, Spodoptera littoralis (Boisduval) (Lepidoptera: Noctuidae). Bull Entomol Res. 1980;70:475–81. DOIGoogle Scholar
  43. Higashiru  Y, Ishihara  M, Schaefer  PW. Sex ratio distortion and severe inbreeding depression in the gypsy moth Lymantria dispar L. in Hokkaido, Japan. Heredity. 1999;83:290–7. DOIPubMedGoogle Scholar

Main Article

Page created: December 16, 2010
Page updated: December 16, 2010
Page reviewed: December 16, 2010
The conclusions, findings, and opinions expressed by authors contributing to this journal do not necessarily reflect the official position of the U.S. Department of Health and Human Services, the Public Health Service, the Centers for Disease Control and Prevention, or the authors' affiliated institutions. Use of trade names is for identification only and does not imply endorsement by any of the groups named above.
file_external