Wolbachia infections in Drosophila melanogaster and D. simulans: polymorphism and levels of cytoplasmic incompatibility

  • Hervé Merçot
  • Sylvain Charlat
Part of the Contemporary Issues in Genetics and Evolution book series (CIGE, volume 11)


Wolbachia are endosymbiotic bacteria, widespread in terrestrial Arthropods. They are mainly transmitted vertically, from mothers to offspring and induce various alterations of their hosts′ sexuality and reproduction, the most commonly reported phenomenon being Cytoplasmic Incompatibility (CI), observed in Drosophila melanogaster and D. simulans. Basically, CI results in a more or less intense embryonic mortality, occurring in crosses between males infected by Wolbachia and uninfected females. In D. simulans, Wolbachia and CI were observed in 1986. Since then, this host species has become a model system for investigating the polymorphism of Wolbachia infections and CI. In this review we describe the different Wolbachia infections currently known to occur in D. melanogaster and D. simulans. The two species are highly contrasting with regard to symbiotic diversity: while five Wolbachia variants have been described in D. simulans natural populations, D. melanogaster seems to harbor one Wolbachia variant only. Another marked difference between these two Drosophila species is their permissiveness with regard to CI, which seems to be fully expressed in D. simulans but partially or totally repressed in D. melanogaster, demonstrating the involvement of host factors in the control of CI levels. The potential of the two host species regarding the understanding of CI and its evolution is also discussed.

Key words

cytoplasmic incompatibility Drosophila melanogaster subgroup endosymbiosis Wolbachia 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Ballard, J.W.O., 2000a. When one is not enough: introgression of mitochondrial DNA in Drosophila. Mol. Biol. Evol. 17: 1126–1130.CrossRefGoogle Scholar
  2. Ballard, J.W.O., 2000b. Comparative genomics of mitochondrial DNA in Drosophila simulans. J. Mol. Evol. 51: 64–75.Google Scholar
  3. Ballard, J.W.O., J. Hatzidakis, T.L. Karr & M. Karr, 1996. Reduced variation in Drosophila simulans mitochondrial DNA. Genetics 144: 1519–1528.PubMedGoogle Scholar
  4. Bandi, C., T.J.C. Anderson, C. Genchi, M.L. Blaxter, 1998. Phylogeny of Wolbachia bacteria in filarial nematodes. Proc. R. Soc. Lond. B 265: 2407–2413.CrossRefGoogle Scholar
  5. Bandi, C., A.J. Trees & N.W. Brattig, 2001. Wolbachia in filerial nematodes: Evolutionnary aspects and implication for the pathogenesis and treatment of filarial diseases. Vet. Parasitol. 98: 215–238.PubMedCrossRefGoogle Scholar
  6. Binnington, K.C. & A.A. Hoffmann, 1989 Wolbachia-like organisms and cytoplasmic incompatibility in Drosophila simulans. J. Invert. Pathol. 54: 344–352.CrossRefGoogle Scholar
  7. Bourtzis, K., A. Nirgianaki, P. Onyango & C. Savakis, 1994. A prokaryotic dnaA sequence in Drosophila melanogaster. Wolbachia infection and cytoplasmic incompatibility among laboratory strains. Inset. Mol. Biol. 3: 131–142.CrossRefGoogle Scholar
  8. Bourtzis, K., A. Nirgianaki, G. Markakis & C. Savakis, 1996. Wolbachia infection and cytoplasmic incompatibility in Drosophila species.Genetics 144: 1063–1073.PubMedGoogle Scholar
  9. Bourtzis, K., S.L. Dobson, H.R. Braig & S.L. O’Neill, 1998. Rescuing Wolbachia have been overlooked. Nature 391: 852–853.Google Scholar
  10. Boyle, L., S.L. O’Neill, H.M. Robertson & T.L. Karr, 1993. Interspecific and intraspecific horizontal transfer of Wolbachia in Drosophila. Science 260: 1796–1799.PubMedCrossRefGoogle Scholar
  11. Braig, H.R., H. Guzman, R.B. Tesh & S.L. O’Neill, 1994. Replacement of the natural Wolbachia symbiont of Drosophila simulans with a mosquito counterpart. Nature 367: 453–455.Google Scholar
  12. Bressac, C. & F. Rousset, 1993. The reproductive incompatibility system in Drosophila simulans: DAPI-staining analysis of the Wolbachia symbionts in sperm cysts. J. Invert. Pathol. 63: 226–230.CrossRefGoogle Scholar
  13. Callaini, G., M.G. Riparbelli, R. Giordano & R. Dallai, 1996. Mitotic defects associated with cytoplasmic incompatibility in Drosophila simulans. J. Invert. Pathol. 67: 55–64.Google Scholar
  14. Callaini, G., R. Dallai & M.G. Ripardelli, 1997. Wolbachia-mduced delay of paternal chromatin condensation does prevent maternal chromosomes from entering anaphase in incompatible crosses in Drosophila simulans. J. Cell Biol. 110: 271–280.Google Scholar
  15. Casiraghi, M., T.J.C. Anderson, C. Bandi, C. Bazzochi & C. Genchi, 2001. A phylogenetic analysis of filarial nematodes: comparison with the phytogeny of Wolbachia endosymbionts. Parasitology 122:93–103.Google Scholar
  16. Charlat, S. & H. Merçot, 2001. Wolbachia, mitochondria and sterility. Trends Ecol. Evol. 16: 431–132.Google Scholar
  17. Charlat, S., K. Bourtzis & H. Merçot, 2001. Wolbachia-mduced cytoplasmic incompatibility, pp. 621-644 in Symbiosis: mechanisms and model systems, edited by J. Seckbach. Springer Science+Business Media Dordrecht, Dordrecht.Google Scholar
  18. Charlat, S., A. Nirgianaki, K. Bourtzis & H. Merçot, 2002. Evolution of Wolbachia-mductd cytoplasmic incompatibility in Drosophila simulans and D. sechellia. Evolution 56: 1735–1742.PubMedGoogle Scholar
  19. Charlat, S., P. Bonnavion & H. Merçot, 2003. Wolbachia segregation dynamics and levels of cytoplasmic incompatibility in Drosophila sechellia. Heredity 90: 157–161.Google Scholar
  20. Charlat, S., L. Le Chat & H. Merçot, 2003. Characterization of non-cytoplasmic incompatibility inducing Wolbachia in two continental African populations of Drosophila simulans. Heredity 90: 49–55.Google Scholar
  21. Clancy, D. & A.A Hoffmann, 1997. Behavior of Wolbachia endosymbionts from Drosophila simulans in Drosophila serrata, a novel host. Am. Nat. 149: 975–988.Google Scholar
  22. Dobson, S.L., K. Bourtzis, H.R. Braig, B.F. Jones, W. Zhou, F. Rousset & S.L. O’Neill, 1999. Wolbachia infections are distributed throughout insect somatic and germ line tissues. Insect Biochem. Mol. Biol. 29: 153–160.PubMedCrossRefGoogle Scholar
  23. Erickson, J. & A.B. Acton, 1969. Spermatocyte granules in Drosophila melanogaster. Can. J. Genet. Cytol. 11: 153–168.Google Scholar
  24. Ghelelovitch, S., 1952. Sur 1e déterminisme génétique de la sterilité dans 1e croisement entre differentes souches de Culex autogenicus Roubaud. C. R. Acad. Sci. Paris 24: 2386–2388.Google Scholar
  25. Giordano, R., S.L. O’Neill & H.M. Robertson, 1995. Wolbachia infections and the expression of cytoplasmic incompatibility in Drosophila sechellia and D. mauritiana. Genetics 140: 1307–1317.PubMedGoogle Scholar
  26. Hertig, M., 1936. The rickettsia Wolbachia pipientis (gen. et sp. n.) and associated inclusions of the mosquitos, Culex pipiens. Parasitology 28: 453–486.CrossRefGoogle Scholar
  27. Hertig, M. & S.B. Wolbach, 1924. Studies on rickettsia-like microorganisms in insects. J. Med. Res. 44: 329–374.Google Scholar
  28. Hey, J. & R.M. Kliman, 1993. Population genetics and phylogenetics of DNA sequence variation at multiple loci within the Drosophila melanogaster species complex. Mol. Biol. Evol. 10: 804–822.PubMedGoogle Scholar
  29. Hoffmann, A.A., 1988. Partial cytoplasmic incompatibility between two australian populations of Drosophila melanogaster. Entomol. Exp. Appl. 48: 61–67.Google Scholar
  30. Hoffmann, A.A.& M. Turelli, 1988. Unidirectional incompatibility in Drosophila simulans: Inheritance, geographic variation and fitness effects. Genetics 119: 435–444.Google Scholar
  31. Hoffmann, A.A. & M. Turelli, 1997. Cytoplasmic incompatibility in insects, pp. 42-80 in Influential Passengers: Inherited Microorganisms and Arthropod Reproduction, edited by S.L. O’Neill, A.A. Hoffmann and J.H. Werren. Oxford University Press, Oxford.Google Scholar
  32. Hoffmann, A.A., M. Turelli & G.M. Simmons, 1986. Unidirectional incompatibility between populations of Drosophila simulans. Evolution 40: 692–701.Google Scholar
  33. Hoffmann, A.A., M. Turelli & L.G. Harshman, 1990. Factors affecting the distribution of cytoplasmic incompatibility in Drosophila simulans. Genetics 126: 933–948.Google Scholar
  34. Hoffmann, A.A., D.J. Clancy & E. Merton, 1994. Cytoplasmic incompatibility in australian populations of Drosophila melanogaster. Genetics 136: 993–999.Google Scholar
  35. Hoffmann, A.A., DJ. Clancy & J. Ducan, 1996. Naturally-occurring Wolbachia infection in Drosophila simulans that does not cause cytoplasmic incompatibilty. Heredity 76: 1–8.PubMedCrossRefGoogle Scholar
  36. Hoffmann, A.A., M. Hercus& H. Dagher, 1998. Population dynamics of the Wolbachia infection causing cytoplasmic incompatibility in populations of Drosophila melanogaster. Genetics 148: 221–231.Google Scholar
  37. Holden, PR., P. Jones & J.F.Y. Brookfield, 1993. Evidence for a Wolbachia symbiont in Drosophila melanogaster. Genet. Res. Camb. 62: 23–29.Google Scholar
  38. Hurst, G.D. & F.M. Jiggins, 2000. Male-killing bacteria in insects: mechanisms, incidence and implications. Emerging Infect. Dis. 6: 329-336.Google Scholar
  39. James, A.C. & J.W.O. Ballard, 2000. The expression of cytoplasmic incompatibility and its impact on population frequencies and the distribution of Wolbachia strains in Drosophila simulans. Evolution 54: 1661–1672.Google Scholar
  40. James, A.C., M.D. Dean, M.E. McMahon & J.W.O. Ballard, 2002. Dynamics of double and single Wolbachia infections in Drosophila simulans from New Caledonia. Heredity 88: 182–189.Google Scholar
  41. King, R.C., 1970. Ovarian Development in Drosophila melanogaster. Academic Press, New York, 227 pp.Google Scholar
  42. King, R.C. & R.P. Mills, 1962. Oogenesis in adult Drosophila melanogaster. XI Studies of some organelles of the nutrient stream in egg chambers of D. melanogaster and D. willistoni. Growth 21: 235–253.Google Scholar
  43. Kose, H. & T.L. Karr, 1995. Organization of Wolbachia pipientis in the Drosophila fertilized egg and embryo revealed by an anti-Wolbachia monoclonal antibody. Mech. Dev. 51: 275–288.Google Scholar
  44. Lachaise, D., M. Harry, M. Solignac, F. Lemeunier, V. Bénassi & M-L. Carriou. 2000. Evolutionary novelties in islands: Drosophila santomea, a new melanogaster sister species from Sao 1. Tomé. Proc. R. Soc. Lond. B 267: 1487–1495.Google Scholar
  45. Lassy, C.W. T.L. Karr, 1996. Cytological analysis of fertilization and early embryonic development in incompatible crosses of Drosophila simulans. Mech. Dev. 57: 47–58.Google Scholar
  46. Lo, N., M. Casiraghi, E. Salati, C. Bazzocchi & C. Bandi, 2002. How many Wolbachia supergroups exist? Mol. Biol. Evol. 19: 341-346.Google Scholar
  47. Merçot, H. & D. Poinsot, 1998a. Wolbachia transmission in a naturally bi-infected Drosophila simulans strain from New Caledonia. Entomol. Exp. Appl. 86: 97–103.CrossRefGoogle Scholar
  48. Merçot, H.& D. Poinsot, 1998b. Rescuing Wolbachia have been overlooked and discovered on Mount Kilimanjaro. Nature 391: 853.Google Scholar
  49. Merçot, H., B. Llorente, M. Jacques, A. Atlan & C. Montchamp-Moreau, 1995. Variability within the Seychelles cytoplasmic incompatibility system in Drosophila simulans. Genetics 141: 1015–1023.Google Scholar
  50. Min, K.T.& S. Benzer, 1997. Wolbachia, normally a symbiont of Drosophila, can be virulent, causing degeneration and early death. Proc. Natl. Acad. Sci. USA 94: 10792–10796.Google Scholar
  51. Montchamp-Moreau, C., J-F. Ferveur & M. Jacques, 1991. Geographic distribution and inheritance of three cytoplasmic incompatibility types in Drosophila simulans. Genetics 129: 399–407.Google Scholar
  52. Nigro, L., 1991. The effect of heteroplasmy on cytoplasmic incompatibility in transplasmic lines of Drosophila simulans showing a complete replacement of the mitochondrial DNA. Heredity 66: 41–45.Google Scholar
  53. Olsen, K., K.T. Reynolds & A.A. Hoffmann, 2001. A field cage test of the effects of the endosymbiont Wolbachia on Drosophila melanogaster. Heredity 86: 731–737.Google Scholar
  54. O’Neill.
    S.L.& T.L. Karr, 1990. Bi-directional incompatibility between conspecific populations of Drosophila simulans. Nature 348: 178–180.CrossRefGoogle Scholar
  55. O’Neill, S.L., R. Giordano, A.M.E. Colbert, T.L. Karr & H.M. Robertson, 1992. 16S rRNA phylogenetic analysis of the bacterial endosymbionts associated with cytoplasmic incompatibility in insects. Proc. Natl. Acad. Sci. USA 89: 2699–2702.Google Scholar
  56. O’Neill, S.L., A.A. Hoffmann & J.H. Werren (eds), 1997. Influential Passengers: Inherited Microorganisms and Arthropod Reproduction. Oxford University Press, Oxford, 226 pp.Google Scholar
  57. Peacock, W.J. & J. Erickson, 1964. An indicator of polarity in the spermatocyte? Drosophila Inform. Serv. 39: 107–108.Google Scholar
  58. Poinsot.
    D. & H. Merçot, 1999. Wolbachia can rescue from cytoplasmic incompatibility while being unable to induce it, pp. 221-234 in From Symbiosis to Eukaryotism-ENDOCYTOBIOLOGY VII, edited by E. Wagner et al. Universities of Geneva and Freiburg im Breisgau.Google Scholar
  59. Poinsot, D. & H. Merçot, 2001. Wolbachia injection from usual to naïve host in Drosophila simulans (Diptera: Drosophilidae). Eur. J. Entomol. 98: 25–30.Google Scholar
  60. Poinsot, D., K. Bourtzis, G. Markakis, C. Savakis & H. Merçot, 1998. Injection of a Wolbachia from Drosophila melanogaster into D. simulans: host effect and cytoplasmic incompatibility relationships. Genetics 150: 227–237.Google Scholar
  61. Poinsot, D., M. Montchamp-Moreau & H. Merçot, 2000. Wolbachia segregation rate in Drosophila simulans bi-infected cytoplasmic lineages. Heredity 85: 191–198.Google Scholar
  62. Poinsot, D., S. Charlat & H. Merçot, 2003. On the mechanism of Wolbachia-induced cytoplasmic incompatibility: confrounting the models to the facts. BioEssays 25: 259–265.Google Scholar
  63. Reynolds, K.T. & A.A. Hoffmann, 2002. Male age, host effects and the weak expression or non-expression of cytoplasmic incompatibility in Drosophila strains infected by maternally transmitted Wolbachia. Genet. Res. Camb. 80: 79–87.Google Scholar
  64. Riegler, M., S. Charlat, C. Stauffer & H. Merçot, 2003. Wolbachia transfer from a true fruit fly into the real fruit fly: investigating the outcomes of host/symbiont co-evolution (submitted).Google Scholar
  65. Roux, V. & D. Raoult, 1995. Phylogenetic analysis of the genus Rickettsia by 16S rDNA sequencing. Res. Microbiol. 146: 385–396.Google Scholar
  66. Rousset, F., 1993. Les facteurs déterminant la distribution des Wolbachia, bactéries endosymbiotiques des arthropodes. Thése de Doctorat de l’Université Paris Sud Orsay, 114 pp.Google Scholar
  67. Rousset, F. & E. de Stordeur, 1994. Properties of Drosophila simulans strains experimentally infected by different clones of the bacterium Wolbachia. Heredity 71: 325–331.CrossRefGoogle Scholar
  68. Rousset, F. & M. Solignac, 1995. Evolution of single and double Wolbachia symbioses during speciation in the Drosophila simulans complex. Proc. Natl. Acad. Sci. USA 92: 6389–6393.Google Scholar
  69. Rousset, F., D. Vautrin & M. Solignac, 1992. Molecular identification of Wolbachia, the agent of cytoplasmic incompatibility in Drosophila simulans and variability in relation with host mitochondrial types. Proc. R. Soc. Lond. B 247: 163-168.Google Scholar
  70. Rousset, F., H.R. Braig & S.L. O’Neill, 1999. A stable triple Wolbachia infection in Drosophila with nearly additive incompatibility effects. Heredity 82: 620–627.Google Scholar
  71. Solignac, M. & M. Monnerot, 1986. Race formation, speciation, and introgression within Drosophila simulans, D. mauritiana, and D. sechellia inferred from mitochondrial DNA analysis. Evolution 40: 531–539.Google Scholar
  72. Solignac, M., D. Vautrin & F. Rousset, 1994. Widespread occurrence of the proteobacteria Wolbachia and partial cytoplasmic incompatibility in Drosophila melanogaster. C. R. Acad. Sci. Paris 317: 461–470.Google Scholar
  73. Stouthamer, R., J.A. Breeuwer & G.D. Hurst, 1999. Wolbachia pipientis: microbial manipulator of arthropod reproduction. Ann. Rev. Microbiol. 53: 71–102.Google Scholar
  74. Szollosi, D. & A. Debec, 1980. Presence of Rickettsias in haploid Drosophila melanogaster cell lines. Biol. Cell. 38: 129–134.Google Scholar
  75. Tram, U. & W. Sullivan, 2002. Role of delayed nuclear envelope breakdown and mitosis in Wolbachia-induced cytoplasmic incompatibility. Science 296: 1124–1126.PubMedCrossRefGoogle Scholar
  76. Turelli, M., 1994. Evolution of incompatibility-inducing microbes and their hosts. Evolution 48: 1500–1513.CrossRefGoogle Scholar
  77. Turelli, M. & A.A. Hoffmann, 1991. Rapid spread of an inherited incompatibility factor in California Drosophila. Nature 353: 440-442.Google Scholar
  78. Turelli, M. & A.A. Hoffmann, 1995. Cytoplasmic incompatibility in Drosophila simulans: Dynamics and parameter estimates from natural populations. Genetics 140: 1319–1338.Google Scholar
  79. Turelli, M., A.A. Hoffmann & S.W. McKechnie, 1992. Dynamics of cytoplasmic incompatibility and mtDNA variation in Drosophila simulans populations. Genetics 132: 713–723.PubMedGoogle Scholar
  80. Ullmann, S.L., 1965. Epsilon granules in Drosophila pole cells and oocytes. J. Embryol. Exptl. Morphol. 13: 73–81.Google Scholar
  81. Van Meer, M.M.M. & R. Stouthamer, 1999. Cross-order transfer of Wolbachia from Muscidiforax uniraptor (Hymenoptera: Pteromaldae) to Drosophila simulans (Diptera: Drosophilidae). Heredity 82: 163–169.CrossRefGoogle Scholar
  82. Vandekerckhove, T.T.M., S. Watteyne, A. Willems, J.G. Swing, J. Mertens & M. Gillis, 1999. Phylogenetic analysis of the 16S rRNA of the cytoplasmic bacterium Wolbachia from the novel host Folsomia Candida (Hexapoda: Collembola) and its implications for wolbachial taxonomy. FEMS Microbiol. Lett. 180: 279–286.Google Scholar
  83. Weeks, A.R., K.T. Reynolds & A.A. Hoffmann, 2002. Wolbachia dynamics and host effects: What has (and has not) been demonstrated? Trends Ecol. Evol. 17: 257–262.CrossRefGoogle Scholar
  84. Werren, J.H., 1997. Biology of Wolbachia. Annu. Rev. Entomol. 42: 587–609.PubMedCrossRefGoogle Scholar
  85. Werren, J.H., W. Zhang & L.R. Guo., 1995. Evolution and phylogeny of Wolbachia: reproductive parasites of arthropods. Proc. R. Soc. Lond. B 261: 55–63.Google Scholar
  86. Wolstenholme, D.R., 1965. A DNA and RNA-containing cytoplasmic body in Dwsophila melanogaster and its relation to flies. Genetics 52: 949–975.Google Scholar
  87. Yanders, A.F., J.G. Brewen, W.J. Peackock & D.J. Goodchild, 1968. Meiotic drive and visible polarity in Dwsophila spermatocytes. Genetics 59: 245–253.Google Scholar
  88. Yen, J.H. & A.R. Barr, 1971. New hypothesis on the cause of cytoplasmic incompatibility in Culex pipiens L. Nature 232: 657–658.PubMedCrossRefGoogle Scholar
  89. Yen, J.H. & A.R. Barr, 1973. The etiological agent of cytoplasmic incompatibility in Culex pipiens. J. Invert. Pathol. 22: 242–250.CrossRefGoogle Scholar
  90. Zhou, W.G., F. Rousset & S.L. O’Neill, 1998. Phylogeny and PCR-based classification of Wolbachia strains using wsp gene sequences. Proc. R. Soc. Lond. B 265: 509–515.Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2004

Authors and Affiliations

  • Hervé Merçot
    • 1
  • Sylvain Charlat
    • 1
  1. 1.Laboratoire Dynamique du Génome et EvolutionInstitut Jacques Monod, CNRS - UniversitésParis Cedex 05France

Personalised recommendations