The impact of male-killing bacteria on the evolution of aphidophagous coccinellids

European Journal of Entomology

Volumn 103, Issue 1, 2006, Pages 1-7

  Majerus, Michael E N ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Biased sex ratios; Coccinellids; Cytoplasmic bacteria; Male killing; Reproductive manipulation

Indexed keywords

BACTERIUM; HOST-PATHOGEN INTERACTION; MALE-KILLING; SEX RATIO;

BACTERIA (MICROORGANISMS); COCCINELLIDAE;

EID: 32444432053     PISSN: 12105759     EISSN: 18028829     Source Type: Journal    
DOI: 10.14411/eje.2006.001     Document Type: Review

References (51)

1. Banks C.J. 1955: An ecological study of Coccinellidae associated with Aphis fabae Scop. on Vicia faba. Bull. Entomol. Res. 46: 561-587.
2. Dixon A.F.G. 2000: Insect Predator-Prey Dynamics: Ladybird Beetles and Biological Control. Cambridge University Press, Cambridge, ix + 257 pp.
3. Dyson E.M. & Hurst G.D.D. 2004: Persistence of an extreme sex ratio bias in a natural population. Proc. Natl. Acad Sci. USA 101: 6521-6525.
4. Fisher R.A. 1930: The Genetical Theory of Natural Selection. Oxford University Press, Oxford, 272 pp.
5. Hackett K.J., Lynn D.E., Williamson D.L., Ginsberg A.S. & Whitcomb R.F. 1986: Cultivation of the Drosophila spiroplasma. Science 232: 1253-1255.
6. Haddrill P.R. 2001: The Development and Use of Molecular Genetic Markers to Study Sexual Selection and Population Genetics in the 2-spot Ladybird, Adalia bipunctata (L.). Unpubl. Ph.D. thesis, Cambridge University.
7. Hamilton W.D. 1967: Extraordinary sex ratios. Science 156: 477-488.
8. Hurst G.D.D. & Majerus M.E.N. 1993: Why do maternally inherited micro-organisms kill males? Heredity 71: 81-95.
9. Hurst G.D.D., Majerus M.E.N. & Walker L.E. 1992: Cytoplasmic male killing elements in Adalia bipunctata (Linnaeus) (Coleoptera: Coccinellidae). Heredity 69: 84-91.
10. Hurst G.D.D., Purvis E.L., Sloggett J.J. & Majerus M.E.N. 1994: The effect of infection with male-killing Rickettsia on the demography of female Adalia bipunctata L. (two spot ladybird). Heredity 73: 309-316.
11. Hurst G.D.D., Sharpe R.G., Broomfield A.H., Walker L.E., Majerus T.M.O., Zakharov I.A. & Majerus M.E.N. 1995: Sexually transmitted disease in a promiscuous insect, Adalia bipunctata. Ecol. Entomol. 20: 230-236.
12. Hurst G.D.D., Hammarton T.C., Obrycki J.J., Majerus T.M.O., Walker L.E., Bertrand D. & Majerus M.E.N. 1996: Male killing bacterium in a fifth ladybird beetle, Coleomegilla maculata (Coleoptera: Coccinellidae). Heredity 77: 177-185.
13. Hurst G.D.D., Hammarton T.M., Bandi C., Majerus T.M.O., Bertrand D. & Majerus M.E.N. 1997a: The diversity of inherited parasites of insects: the male-killing agent of the ladybird beetle Coleomegilla maculata is a member of the Flavobacteria. Genet. Res. 70: 1-6.
14. Hurst G.D.D., Hurst L.D. & Majerus M.E.N. 1997b: Cytoplasmic sex-ratio distorters. In O'Neill S.L., Hoffmann A.A. & Werren J.H. (eds): Influential Passengers. Oxford University Press, Oxford, pp. 125-154.
15. Hurst G.D.D., Von de Schulenburg H.G., Majerus T.M.O., Bertrand D., Zakharov I.A., Baungaard J., Völkl W., Stouthamer R. & Majerus M.E.N. 1999a: Invasion of one insect species, Adalia bipunctata, by two different male-killing bacteria. Insect Mol. Biol. 8: 133-139.
16. Hurst G.D.D., Bandi C., Sacchi L., Cochrane A.G., Bertrand D., Karaca I. & Majerus M.E.N. 1999b: Adonia variegata (Coleoptera: Coccinellidae) bears maternally inherited Flavobacteria that kill males only. Parasitology 118: 125-134.
17. 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. 1999c: Male-killing Wolbachia in two species of insect. Proc. R. Soc. Lond. (B) 266: 735-740.
18. Hurst L.D. 1991: The incidences and evolution of cytoplasmic male-killers. Proc. R. Soc. Lond. (B) 244: 91-99.
19. Jiggins F.M., Hurst G.D.D. & Majerus M.E.N. 1998: Sex-ratio distortion in Acraea encedon (Lepidopera: Nymphalidae) is caused by a male-killing bacterium. Heredity 81: 87-91.
20. Jiggins F.M., Hurst G.D.D. & Majerus M.E.N. 1999: Sex ratio distorting Wolbachia causes sex role reversal in its butterfly host. Proc. R. Soc. Lond. (B) 267: 69-73.
21. Jiggins F.M., Hurst G.D.D., Dolman C.E. & Majerus M.E.N. 2000: High prevalence male-killing Wolbachia in the butterfly Acraea encedana. J. Evol. Biol. 13: 495-501.
22. Jiggins F.M., Hurst G.D.D., Schulenburg J.H.G.v.d. & Majerus M.E.N. 2001: Two male-killing Wolbachia strains coexist within a population of the butterfly Acraea encedon. Heredity 86: 161-166.
23. Jiggins F.M., Randerson J.P., Hurst G.D.D. & Majerus M.E.N. 2002: How can sex ratio distorters reach extreme prevalences? Male-killing Wolbachia are not suppressed and have near-perfect vertical transmission efficiency in Acraea encedon. Evolution 56: 2290-2295.
24. Johnstone R.A. & Hurst G.D.D. 1996: Maternally inherited male-killing microorganisms may confound interpretation of mtDNA variation in insects. Biol. J. Linn. Soc. 58: 453-470.
25. Majerus M.E.N. 1994: Ladybirds. New Naturalist Series 81. Harper Collins, London, 368 pp.
26. Majerus M.E.N. 1999: Simbiontes hereditarios causantes de efectos deletéreos en los artrópodos. Deleterious endosymbionts of Arthropods. In Melic A., De Haro J.J., Méndez M. and Ribera I. (eds): The Evolution and Ecology of Arthropods. Sociedad Entomologica Aragonera, Zaragosa, Spain, pp. 777-806 (In Spanish and English).
27. Majerus M.E.N. 2003a: Sex Wars: Genes, Bacteria, and Sex Ratios. Princeton University Press, Princeton, New Jersey, 280 pp.
28. Majerus M.E.N. 2003b: A new dimension to sex wars: microbes that benefit female hosts. Microbiol. Today 30: 68-70.
29. Majerus M.E.N. & Hurst G.D.D. 1997: Ladybirds as a model system for the study of male-killing symbionts. Entomophaga 42: 13-20.
30. Majerus M.E.N. & Majerus T.M.O. 2000: Female-biased sex ratio due to male-killing in the Japanese ladybird Coccinula sinensis. Ecol. Entomol. 25: 234-238.
31. Majerus M.E.N., Schulenburg J.H.G.v.d. & Zakharov I.A. 2000: Multiple cause of male-killing in a single sample of the 2 spot ladybird, Adalia bipunctata (Coleoptera: Coccinellidae) from Moscow. Heredity 84: 605-609.
32. Majerus T.M.O. 2001: The Evolutionary Genetics of Male-killing in the Coccinellidae. Ph.D. thesis, University of Cambridge.
33. Majerus T.M.O., Majerus M.E.N., Knowles B., Wheeler J., Bertrand D., Kuznetzov V.N., Ueno H. & Hurst G.D.D. 1998: Extreme variation in the prevalence of inherited male-killing microorganisms between three Populations of the ladybird Harmonia axyridis (Coleoptera: Coccinellidae). Heredity 81: 683-691.
34. Majerus T.M.O., Schulenburg J.H.G.v.d., Majerus M.E.N. & Hurst G.D.D. 1999: Molecular identification of a male-killing agent in the ladybird Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae). Insect Mol. Biol. 8: 551-555.
35. Matsuka M., Hashi H. & Okada I. 1975: Abnormal sex ratio found in the lady beetle Harmonia axyridis Pallas (Coleoptera: Coccinellidae). Appl. Entomol. Zool. 10: 84-89.
36. Osawa N. & Nishida T. 1992: Seasonal variation in elytral colour polymorphism in Harmonia axyridis (the ladybird beetle): the role of non-random mating. Heredity 69: 297-307.
37. Owen D.F. & Chanter D.O. 1969: Population biology of tropical African butterflies. Sex ratio and genetic variation in Acraea encedon. J. Zool. Lond. 157: 345-374.
38. Randerson J.P., Smith N.G.C. & Hurst L.D. 2000: The evolutionary dynamics of male-killers and their hosts. Heredity 84: 152-160.
39. Ransford M.O. 1997: Sperm Competition in the 2-spot Ladybird, Adalia bipunctata. Unpubl. Ph.D. thesis, University of Cambridge.
40. Schulenburg J.H.G.v.d. 2000: The Evolution and Dynamics of Male-killing in the Two-spot Ladybird Adalia bipunctata L. (Coleoptera: Coccinellidae). Unpubl. Ph.D. thesis, University of Cambridge.
41. Schulenburg J.H.G.v.d., Habig M., Sloggett J.J., Webberley M., Bertrand D., Hurst G.D.D. & Majerus M.E.N. 2001: The incidence of male-killing Rickettsia (alpha proteobacteria) in the 10-spot ladybird, Adalia decempunctata. L. (Coleoptera: Coccinellidae), Appl. Environ. Microbiol. 67: 270-277.
42. Shull H.F. 1948: An all-female strain of lady beetles with reversions to normal sex ratio. Am. Nat. 82: 241-251.
43. Tinsley M.C. 2003: The Ecology and Evolution of Male-killing Bacteria in Ladybirds. Unpubl. Ph.D. thesis, University of Cambridge.
44. Welch V.L., Sloggett J.J., Webberley K.M. & Hurst G.D.D. 2001: Short range clinal variation in the prevalence of a sexually transmitted fungus associated with urbanisation. Ecol. Entomol. 26: 547-550.
45. Webberley M.K., Hurst G.D.D., Busko J. & Majerus M.E.N. 2002: Lack of parasite mediated sexual selection in a ladybird/sexually transmitted disease system. Anim. Behav. 63: 131-141.
46. Werren J.H., Skinner S.W. & Huger A.M. 1986: Male-killing bacteria in a parasitic wasp. Science 231: 990-992.
47. Werren J.H., Hurst G.D.D., Zhang W., Breeuwer J.A.J., Stouthamer R. & Majerus M.E.N. 1994: Rickettsial relative associated with male killing in the ladybird beetle (Adalia bipunctata). J. Bacteriol. 176: 388-394.
48. Wratten S.D. 1973: The effectiveness of the coccinellid beetle, A. bipunctata (L.) as a predator of the lime aphid, Eucallipterus tiliae (L.). J. Anim. Ecol. 42: 785-802.
49. Wratten S.D. 1976: Searching by Adalia bipunctata (L.) (Coleoptera: Coccinellidae) and escape behaviour of its aphid and cicadellid prey on lime (Tilia x vulgaris Hayne). Ecol. Entomol. 1: 139-142.
50. Zakharov I.A. & Shaikevich E.V. 2001: The Stockholm populations of Adalia bipunctata (L.) (Coleoptera: Coccinellidae) - a case of extreme female-biased population sex ratio. Hereditas 134: 263-266.
51. Zakharov I.A., Hurst G.D.D., Chernysheva N.E. & Majerus M.E.N. 1996: The maternally inherited bacterium causing female bias in the Petersburg population of Adalia bipunctata does not belong to the genus Rickettsia. Russ. J. Genet. 32: 1303-1306.