Biodiversity & Conservation

, Volume 5, Issue 8, pp 999–1013 | Cite as

What generates the diversity of Wolbachia—arthropod interactions?

  • Thierry Rigaud
  • François Rousset

Wolbachia are strictly endocellular, vertically transmitted bacteria associated with insects and crustaceans. This group of parasites modify their hosts' reproduction so as to increase their own fitness. This paper reviews the variability of these parasitic alterations and their consequences for host biology and populations. Wolbachia induce cytoplasmic incompatibility (a characteristic apparently specific to Wolbachia) in several insects and one isopod crustacean; parthenogenesis (thelytoky) in haplo-diploid insects; feminization in various isopods. The consequences of these phenomena on speciation, population dynamics and genetic polymorphism are discussed. The variability of the mechanisms of host sex determination is one important factor responsible for the diversity of Wolbachia-host interactions. However, parasite characteristics, such as the capacity to disturb host mitosis, and the ability to be horizontally transferred between hosts, also appear to play a role in this diversity.


cytoplasmic incompatibility parthenogenesis feminization parasitic interactions genetic variability 


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  1. Artault, J.C. (1977) Contribution à l'étude des garnitures chromosomiques chez quelques Crustacés Isopodes. Thèse de Troisieme Cycle, Université de Poitiers.Google Scholar
  2. Barr A.R. (1982) Symbiont control of reproduction in Culex pipiens. In Recent Developments in the Genetics of Insect Disease Vectors (W.W.M. Steiner, W.J. Tabachnick, K.S. Rai and S. Narang, eds) pp. 153–8. Champaign, IL: Stipes Publishing Company.Google Scholar
  3. Binnington K. and Hoffmann A.A. (1989) Wolbachia-like organisms and cytoplasmic incompatibility in Drosophila simulans. J. Invertebr. Pathol. 54, 344–52.Google Scholar
  4. Boyle L., O'Neill S.L., Robertson H. and Karr T.L. (1993) Interspecific and intraspecific horizontal transfer of Wolbachia in Drosophila. Science 260, 1796–9.Google Scholar
  5. Breeuwer J.A.J. and Werren J.H. (1990) Microorganisms associated with chromosome destruction and reproductive isolation between two insect species. Nature, 346, 558–60.Google Scholar
  6. Breeuwer J.A.J. and Werren J.H. (1993a) Effect of genotype on cytoplasmic incompatibility between two species of Nasonia. Heredity 70, 428–36.Google Scholar
  7. Breeuwer J.A.J. and Werren J.H. (1993b) Cytoplasmic incompatibility and bacterial density in Nasonia vitripennis. Genetics 135, 565–74.Google Scholar
  8. Breeuwer J.A.J., Stouthamer R., Barns S.M., Pelletier D.A., Weisburg W.G. and Werren J.H. (1992) Phylogeny of cytoplasmic incompatibility microoganisms in the parasitoid wasp genus Nasonia (Hymenoptera, Pteromalidae) based on 16S ribosomal DNA sequences. Insect Mol. Biol. 1, 25–36.Google Scholar
  9. Bull J.J. (1983) Evolution of Sex Determining Mechanisms. Menlo Park, Benjamin/Cummings Publ. Co.Google Scholar
  10. Bulnheim H.P. and Vavra J. (1968) Infection by the microsporidian Octosporea effeminans and its sex determining influence in the amphipod Gammarus duebeni. J. Parasitol. 545, 241–8.Google Scholar
  11. Charniaux-Cotton H. and Payen G. (1985) Sexual Differentiation. In The Biology of Crustacea, Vol 9 (D.E. Bliss, ed.) pp. 217–99. Orlando: Academic press.Google Scholar
  12. Cioran E.M. (1973) De l'inconvénient d'être né. Paris: Gallimard.Google Scholar
  13. Cook J.M. (1993) Sex determination in the Hymenoptera: a review of models and evidence. Heredity 71, 421–35.Google Scholar
  14. Fine P.E.M. (1978) On the dynamics of symbiote-dependent cytoplasmic incompatibility in culicine mosquitoes. J. Invertebr Pathol. 30, 10–18.Google Scholar
  15. Ghelelovitch S. (1952) Sur le déterminisme génétique de la stérilité dans les croisements entre différentes souches de Culex autogenicus Roubaud. C. R. Acad. Sci. 234, 2386–8.Google Scholar
  16. Gilbert S.F. (1991) Developmental Biology, 3rd edn. Sunderland, MA: Sinauer.Google Scholar
  17. Ginsburger-Vogel T. and Desportes I. (1979) Structure and biology of Marteilia sp in the amphipod Orchestia gammarellus. Mar. Fish. Rev. 41, 3–7.Google Scholar
  18. Grandjean F., Rigaud T., Raimond R., Juchault P. and Souty-Grosset C. (1993) Mitochondrial DNA polymorphism and feminizing sex factors dynamics in a natural population of Armadillidium vulgare (Crustacea, Isopoda). Genetica 92, 55–60.Google Scholar
  19. Hastings I.M. (1994) Selfish DNA as a method of pest control. Philos. Trans. R. Soc. Lond. B 344, 31–24.Google Scholar
  20. Hertig M. (1936) The rickettsia, Wolbachia pipientis. (gen. et sp. n.) and associated inclusions of the mosquito, Culex pipiens. Parasitology 28, 453–86.Google Scholar
  21. Hoffmann A.A. (1988) Partial cytoplasmic incompatibility between two Australian populations of Drosophila melanogaster. Entomol Exp. Appl. 48, 61–7.Google Scholar
  22. Hoffmann A.A., Turelli M. and Simmons G.M. (1986) Unidirectional incompatibility between populations of Drosophila simulans. Evolution 40, 692–701.Google Scholar
  23. Hoffmann A.A., Turelli M. and Harshman L.H. (1988) Factors affecting the distribution of cytoplasmic incompatibility in Drosophila simulans. Genetics 126, 933–48.Google Scholar
  24. Howard R.S. and Lively C.M. (1994) Parasitism, mutation accumulation and the maintenance of sex. Nature 367, 554–7.Google Scholar
  25. Hsiao C. and Hsiao T.H. (1985) Rickettsia as the cause of cytoplasmic incompatibility in the alfalfa weevil, Hypera positica. J. Invertebr. Pathol. 45, 244–6.Google Scholar
  26. Hurst L.D. (1993) The incidences, mechanisms and evolution of cytoplasmic sex ratio distorters in animals. Biol. Rev. 68, 121–93.Google Scholar
  27. Jost E. (1971) Meiosis in the male of Culex pipiens and Aedes albopictus and fertilization in the Culex-pipiens complex. Can. J. Genet. Cytol. 13, 237–50.Google Scholar
  28. Juchault P. and Legrand J.J. (1989) Sex determination and monogeny in terrestrial Isopods Armadillidium vulgare (Latreille, 1804) and Armadillidium nasatum (Budde-Lund, 1885). Monitore Zool. Ital. (N.S.) Monogr. 4, 359–75.Google Scholar
  29. Juchault P. and Mocquard J.P. (1993) Transfer of a parasitic sex factor to the nuclear genome of the host: a hyopothesis on the evolution of sex determining mechanisms in the terrestrial Isopod Armadillidium vulgare Latr. J. Evol. Biol. 6, 511–28.Google Scholar
  30. Juchault P., Legrand J.J. and Martin G. (1974) Action interspécifique du facteur épigénétique féminisant responsable de la thélygénie et de l'intersexualité du Crustacé Armadillidium vulgare (Isopode Oniscoide). Ann. Embryo. Morphogen. 7, 265–76.Google Scholar
  31. Juchault P., Rigaud T. Mocquard J.P. (1992) Evolution of sex determining mechanisms in a wild population of Armadillidium vulgare Latr. (Crustacea, Isopoda). competition between two feminizing parasitic factors. Heredity 69, 382–90.Google Scholar
  32. Juchault P., Rigaud T. and Mocquard J.P. (1993) Evolution of sex determination and sex ratio variability in wild populations of Armadillidium vulgare Latr. (Crustacea, Isopoda): Acta Oecologica 14, 547–62.Google Scholar
  33. Juchault P., Frelon M., Bouchon D. and Rigaud T. (1994) New evidence for feminizing bacteria in terrestrial isopods: evolutionary implications. C. R. Acad. Sci. Paris Life Sciences, 317, 225–30.Google Scholar
  34. Kambhampati S., Rai K.S. and Burgun S.J. (1993) Unidirectional cytoplasmic incompatibility in the mosquito, Aedes albopictus. Evolution 47 673–7.Google Scholar
  35. Kellen W., Hoffmann D. and Kwock R. (1981) Wolbachia sp. (Rickettsiales: Rickettsiaceae) a symbiont of the almond moth, Ephestia cautella: ultrastructure and influence on host fertility. J. Invertebr Pathol. 37, 273–83.Google Scholar
  36. Laven, H. (1967) Speciation and evolution in Culex pipiens. In Genetics of Insect Vectors of Disease (J. Wright and R. Pal, eds) pp. 251–75. Elsevier.Google Scholar
  37. Legner E.F. (1985) Effects of scheduled high temperature on male production in thelytokous Muscidifurax uniraptor (Hymenoptera. Pteromalidae). Can. Entomol. 117, 383–9.Google Scholar
  38. Legrand J.J. and Juchault P. (1984) Nouvelles données sur le déterminisme génétique et épigénétique de la monogénie chez le crustacé isopode terrestre Armadillidium vulgare Latr. Génét. Sél. Evol. 16, 57–84.Google Scholar
  39. Legrand J.J. and Juchault P. (1986) Rôle des bactéries symbiotiques dans l'intersexualité, la monogénie et la spéciation chez des Crustacés Oniscoides. Boll. Zool. 53, 161–72.Google Scholar
  40. Legrand J.J., Juchault P. and Martin G. (1985) Inoculation chez la femelle du Crustacé Oniscoide Porcellio dilatatus Brandt d'une bactérie symbiote caractéristique de la sous espèce P.d. petiti, et ses conséquences sur l'issue du croisement des deux sous espèces. C.R. Acad. Sci. Paris 300, 147–50.Google Scholar
  41. Legrand J.J., Legrand-Hamelin E. and Juchault P. (1987) Sex determination in Crustacea. Biol. Rev. 62, 439–70.Google Scholar
  42. Luck R.F., Stouthamer R. Nunney L.P. (1993) Sex determination and sex ratio patterns in parasitic Hymenoptera. In Evolution and Diversity of Sex Ratio in Insects and Mites (D.L. Wrensch and M.A. Ebbert, eds) pp. 442–76. New York: Chapman & Hall.Google Scholar
  43. Martin G., Juchault P. and Legrand J.J. (1973) Mise en évidence d'un micro-organisme intracytoplasmique symbiote de l'Oniscöide Armadillidium vulgare L., dont la présence accompagne l'intersexualité ou la féminisation totale des mâles génétiques de la lignée thélygène. C. R. Acad. Sci. Paris 276, 2213–6.Google Scholar
  44. Martin G., Gruppe S.G., Laulier M., Bouchon D., Rigaud T. and Juchault P. (1994) Evidence for Wolbachia spp. in the estuarine isopod Sphaeroma rugicauda (Crustacea): a likely cytoplasmic sex ratio distorter. Endocytobiosis Cell Res. 10, 215–25.Google Scholar
  45. Maynard-Smith J. (1988) The evolution of recombination. In The Evolution of Sex (R.E. Michod and B.R. Levin, eds) pp. 106–25. Sunderland, MA: Sinauer.Google Scholar
  46. Minchella D.J. and Scott M.E. (1991) Parasitism: a criptic determinant of animal community structure. Trends Ecol. Evol. 6, 250–4.Google Scholar
  47. Montchamp-Moreau C., Ferveur J.F. and Jacques M. (1991) Geographic disibution and inheritance of three cytoplasmic types in Drosophila simulans. Genetics 129, 399–407.Google Scholar
  48. Noda H. (1984) Cytoplasmic incompatibility in a rice planthoper. J Hered. 75, 345–8.Google Scholar
  49. Ochman H. and Wilson A.C. (1987) Evolution in bacteria. evidence for a universal substitution rate in cellular genomes. J. molec Evol. 26, 74–86.Google Scholar
  50. O'Neill S.L. (1989) Cytoplasmic symbionts in Tribolium confusum. J. Invertebr. Pathol. 53, 132–4.Google Scholar
  51. O'Neill S.L. and Karr T.M. (1990) Bidirectional incompatibility between conspecific populations of Drosophila simulans. Nature 348, 178–80.Google Scholar
  52. O'Neill S.L., Giordano R., Colbert A.M.E., Karr T.L. and Robertson H.M. (1992) Phylogenetic analysis of the bacterial endosymbionts associated with cytoplasmic incompatibility in insects. Proc. Natl Acad. Sci. USA 89, 2699–702.Google Scholar
  53. Raymond M., Callaghan A., Fort P. and Pasteur N. (1991) Worldwide migration of amplified insecticide resistance genes in mosquitoes. Nature 350, 151–3.Google Scholar
  54. Rigaud T. and Juchault P. (1992) Genetic control of the vertical transmission of a cytoplasmic sex factor in Armadillidium vulgare Latr. (Crustacea, Oniscidea). Heredity 68, 47–52.Google Scholar
  55. Rigaud T. and Juchault P. (1993) Conflict between feminizing sex ratio distorters and an autosomal masculinizing gene in the terrestrial isopod Armadillidium vulgare Latr. Genetics 133, 247–52.Google Scholar
  56. Rigaud T. and Juchault P. (1995) Success and failure of horizontal transfers of feminizing Wolbachia endosymbionts in woodlice. J. Evol. Biol. 8, 249–55.Google Scholar
  57. Rigaud T., Souty-Grosset C., Raimond R., Mocquard J.P. and Juchault P. (1991a) Feminizing endocytobiosis in the terrestrial crustacean Armadillidium vulgare Latr. (Isopoda). recent acquisitions. Endocytobiosis Cell Res. 7, 259–73.Google Scholar
  58. Rigaud T., Juchault P. and Mocquard J.P. (1991b) Experimental study of temperature effects on the sex ratio of broods in terrestrial Crustacea Armadillidium vulgare Latr. Possible implications in natural populations. J. Evol. Biol. 4, 603–17.Google Scholar
  59. Rigaud T. Mocquard P. and Juchault P. (1992) The spread of parasitic sex factors in populations of Armadillidium vulgare Latr (crustacea, Oniscidea): effects on sex ratio. Gen. Sel. Evol. 24, 3–18.Google Scholar
  60. Rousset F. and de Stordeur E. (1994) Properties of Drosophila simulans strains experimentally infected by different clones of the bacterium Wolbachia. Heredity 72, 325–31.Google Scholar
  61. Rousset F. and Raymond M. (1991) Cytoplasmic incompatibility in Insects: why sterilize females? Trends Ecol. Evol. 6, 54–7.Google Scholar
  62. Rousset F. and Solignac M. (1995) Evolution of single and double Wolbachia symbioses during speciation in the Drosophila simulans complex. Proc. Natl. Acad. Sci. USA 92, 6389–93.Google Scholar
  63. Rousset F., Raymond M. and Kjellberg F (1991) Cytoplasmic incompatibility in the mosquito Culex pipiens: how to explain a cytotype polymorphism? J. Evol. Biol. 4, 69–82.Google Scholar
  64. Rousset F., Vautrin D. and Solignac M. (1992a) Molecular identification of Wolbachia, the agent of cytoplasmic incompatibility in Drosophila simulans, and variation in relation to host mitochondrial types. Proc. Roy. Soc. Lond. B 247, 163–8.Google Scholar
  65. Rousset F., Bouchon D., Pintureau B., Juchault P. and Solignac M. (1992b) Wolbachia endosymbionts responsible for various alterations of sexuality in Arthropods. Proc. Roy. Soc. Lond. B 250, 91–8.Google Scholar
  66. Solignac M., Vautrin D. and Rousset F. (1994) Widespread occurrence of Wolbachia and partial cytoplasmic incompatibility in Drosophila melanogaster. C.R. Acad. Sci. Paris Life Sciences 317, 461–70.Google Scholar
  67. Souty-Grosset C., Raimond R. and Tourte M. (1992) Déterminisme épigénétique du sexe et divergence génétique de l'ADN mitochondrial chez Armadillidium vulgare Latr. (Crustacé. Oniscoide): variabilité inter et intrapopulation. C.R. Acad. Sci. Paris 314, 119–25.Google Scholar
  68. Stevens L. and Wade M.J. (1990) Cytoplasmically inherited reproductive incompatibility in Tribolium flour beetles: the rate of spread and effect on population size. Genetics 124, 367–72.Google Scholar
  69. Stevens L. and Wicklow D.T. (1992) Multispecies interactions affect cytoplasmic incompatibilities, in Tribolium flour beetles. Am. Nat. 140, 642–53.Google Scholar
  70. Stouthamer R. and Kazmer D.J. (1994) Cytogenetics of microbe-associated parthenogenesis and its consequences for gene flow in Trichogramma wasps. Heredity 73, 317–27.Google Scholar
  71. Stouthamer R. and Luck R.F. (1993) Influence of microbe-associated parthenogenesis on the fecundity of Trichogramma deion and Trichogramma pretiosum. Ent. Exp. Appl. 67, 183–92.Google Scholar
  72. Stouthamer R., Luck R.F. and Hamilton W.D. (1990) Antibiotics cause parthenogenetic Trichogramma (Hymenoptera/Trichogrammatidae) to revert to sex. Proc. Natl Acad. Sci. USA 87, 2424–7.Google Scholar
  73. Stouthamer R., Breeuwer J.A.J., Luck R.F. and Werren J.H. (1993) Molecular identification of microorganisms associated with parthenogenesis. Nature. 361, 66–8.Google Scholar
  74. Taylor D.R. (1990) Evolutionary consequences of cytoplasmic sex ratio distorters. Evol. Ecol. 4, 235–48.Google Scholar
  75. Trpis M., Perrone J.B., Reissig M. and Parker K.L. (1981) Control of cytoplasmic incompatibility in the Aedes scutellaris complex. J. Hered. 72, 313–7.Google Scholar
  76. Turelli M., Hoffmann A.A. (1992) Rapid spread of an inherited incompatibility factor in California Drosophila. Nature 353, 440–2.Google Scholar
  77. Turelli M., Hoffmann A.A. and McKechnie S.W. (1992) Dynamics of cytoplasmic incompatibility and mtDNA variation in natural Drosophila simulans populations. Genetics 132, 713–23.Google Scholar
  78. Vandel A. (1941) Recherches sur la génétique et la sexualité des Isopodes terrestres. VI. Les phénomènes de monogénie chez les Oniscoïdes. Bull. Biol. Fr. Bel. 75, 316–63.Google Scholar
  79. Wade M.J. and Stevens L. (1985) Microorganism mediated reproductive isolation in flour beetle (genus Tribolium). Science 227, 527–8.Google Scholar
  80. Weiss E. (1974) Wolbachia. In Bergey's Manual of Determinative Bacteriology (R.E. Buchaman and N.E. Gobbons, eds), pp. 898–900. Baltimore: Williams and Wilkins.Google Scholar
  81. Wilkins A.S. (1993) Genetic Analysis of Animal Development, 2nd edn. New York: Wiley-Liss.Google Scholar
  82. Wright J. and Barr A.R. (1981) Wolbachia and the normal and incompatible eggs of Aedes polynesiensis (Diptera: Culicidae). J. Invertebr. Pathol. 38, 409–18.Google Scholar
  83. Yen J.H. and Barr A.R. (1971) New hypothesis on the cause of cytoplasmic incompatibility in Culex pipiens L. Nature 232, 657–8.Google Scholar
  84. Zchori-Dein E., Roush R.T. and Hunter M.S. (1992) Male production induced by antibiotic treatment in Encarsia formosa (Hymenoptera: Aphelinidae), an asexual species. Experientia 48, 102–5.Google Scholar
  85. Zchori-Fein E., Rosen D. and Roush R.T. (1994) Microorganisms associated with thelytoky in Aphytis lignanensis Compere (Hymenoptera: Aphelinidae). Int. J. Insect Morphol. Embryol. 23, 169–72.Google Scholar

Copyright information

© Chapman & Hall 1996

Authors and Affiliations

  • Thierry Rigaud
    • 1
  • François Rousset
    • 2
  1. 1.Laboratoire de Biologie Animale, URA CNRS 1975Université de PoitiersPoitiers CedexFrance
  2. 2.I.S.E.M., URA CNRS 327 ‘Génétique et Environnement’, CC 065Université de Montpellier 2Montpellier Cedex 05France

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