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

Genetica

Volumn 120, Issue 1-3, 2004, Pages 51-59

  Merçot, Hervé ^a   Charlat, Sylvain ^a  

^a INSTITUT JACQUES MONOD   (France)

Author keywords

Cytoplasmic incompatibility; Dmsophila melanogaster subgroup; Endosymbiosis; Wolbachia

Indexed keywords

ANIMAL; CONFERENCE PAPER; CYTOPLASM; DROSOPHILA; DROSOPHILA MELANOGASTER; FEMALE; GENETIC POLYMORPHISM; MALE; METABOLISM; MICROBIOLOGY; PATHOLOGY; RICKETTSIOSIS; SEX DIFFERENCE; SPECIES DIFFERENCE; WOLBACHIA;

ANIMALS; CYTOPLASM; DROSOPHILA; DROSOPHILA MELANOGASTER; FEMALE; MALE; POLYMORPHISM, GENETIC; RICKETTSIACEAE INFECTIONS; SEX FACTORS; SPECIES SPECIFICITY; WOLBACHIA;

ANIMALIA; ARTHROPODA; DROSOPHILA MELANOGASTER; DROSOPHILA SIMULANS; MELANOGASTER; WOLBACHIA;

EID: 1842575597     PISSN: 00166707     EISSN: None     Source Type: Journal    
DOI: 10.1023/B:GENE.0000017629.31383.8f     Document Type: Conference Paper

References (90)

1. Ballard, J.W.O., 2000a. When one is not enough: introgression of mitochondrial DNA in Drosophila. Mol. Biol. Evol. 17: 1126-1130.
2. Ballard, J.W.O., 2000b. Comparative genomics of mitochondrial DNA in Drosophila simulans. J. Mol. Evol. 51: 64-75.
3. Ballard, J.W.O., J. Hatzidakis, T.L. Karr & M. Karr, 1996. Reduced variation in Drosophila simulans mitochondrial DNA. Genetics 144: 1519-1528.
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.
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.
6. Binnington, K.C. & A.A. Hoffmann, 1989. Wolbachia-like organisms and cytoplasmic incompatibility in Drosophila simulans. J. Invert. Pathol. 54: 344-352.
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.
8. Bourtzis, K., A. Nirgianaki, G. Markakis & C. Savakis, 1996. Wolbachia infection and cytoplasmic incompatibility in Drosophila species. Genetics 144: 1063-1073.
9. Bourtzis, K., S.L. Dobson, H.R. Braig & S.L. O'Neill, 1998. Rescuing Wolbachia have been overlooked. Nature 391: 852-853.
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.
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.
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.
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.
14. Callaini, G., R. Dallai & M.G. Ripardelli, 1997. Wolbachia-induced delay of paternal chromatin condensation does prevent maternal chromosomes from entering anaphase in incompatible crosses in Drosophila simulans. J. Cell Biol. 110: 271-280.
15. Casiraghi, M., T.J.C. Anderson, C. Bandi, C. Bazzochi & C. Genchi, 2001. A phylogenetic analysis of filarial nematodes: comparison with the phylogeny of Wolbachia endosymbionts. Parasitology 122: 93-103.
16. Charlat, S. & H. Merçot, 2001. Wolbachia, mitochondria and sterility. Trends Ecol. Evol. 16: 431-432.
17. Charlat, S., K. Bourtzis & H. Merçot, 2001. Wolbachia-induced cytoplasmic incompatibility, pp. 621-644 in Symbiosis: mechanisms and model systems, edited by J. Seckbach. Kluwer Academic Publishers, Dordrecht.
18. Charlat, S., A. Nirgianaki, K. Bourtzis & H. Merçot, 2002. Evolution of Wolbachia-induced cytoplasmic incompatibility in Drosophila simulans and D. sechellia. Evolution 56: 1735-1742.
19. Charlat, S., P. Bonnavion & H. Merçot, 2003. Wolbachia segregation dynamics and levels of cytoplasmic incompatibility in Drosophila sechellia. Heredity 90: 157-161.
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.
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.
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.
23. Erickson, J. & A.B. Acton, 1969. Spermatocyte granules in Drosophila melanogaster. Can. J. Genet. Cytol. 11: 153-168.
24. Ghelelovitch, S., 1952. Sur le déterminisme géné tique de la sterilité dans le croisement entre differentes souches de Culex autogenicus Roubaud. C. R. Acad. Sci. Paris 24: 2386-2388.
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.
26. Hertig, M., 1936. The rickettsia Wolbachia pipientis (gen. et sp. n.) and associated inclusions of the mosquitos, Culex pipiens. Parasitology 28: 453-486.
27. Hertig, M. & S.B. Wolbach, 1924. Studies on rickettsia-like microorganisms in insects. J. Med. Res. 44: 329-374.
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.
29. Hoffmann, A.A., 1988. Partial cytoplasmic incompatibility between two australian populations of Drosophila melanogaster. Entomol. Exp. Appl. 48: 61-67.
30. Hoffmann, A.A. & M. Turelli, 1988. Unidirectional incompatibility in Drosophila simulans: Inheritance, geographic variation and fitness effects. Genetics 119: 435-444.
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.
32. Hoffmann, A.A., M. Turelli & G.M. Simmons, 1986. Unidirectional incompatibility between populations of Drosophila simulans. Evolution 40: 692-701.
33. Hoffmann, A.A., M. Turelli & L.G. Harshman, 1990. Factors affecting the distribution of cytoplasmic incompatibility in Drosophila simulans. Genetics 126: 933-948.
34. Hoffmann, A.A., D.J. Clancy & E. Merton, 1994. Cytoplasmic incompatibility in australian populations of Drosophila melanogaster. Genetics 136: 993-999.
35. Hoffmann, A.A., D.J. Clancy & J. Ducan, 1996. Naturally-occurring Wolbachia infection in Drosophila simulans that does not cause cytoplasmic incompatibilty. Heredity 76: 1-8.
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.
37. Holden, P.R., P. Jones & J.F.Y. Brookfield, 1993. Evidence for a Wolbachia symbiont in Drosophila melanogaster. Genet. Res. Camb. 62: 23-29.
38. Hurst, G.D. & F.M. Jiggins, 2000. Male-killing bacteria in insects: mechanisms, incidence and implications. Emerging Infect. Dis. 6: 329-336.
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.
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.
41. King, R.C., 1970. Ovarian Development in Drosophila melanogaster. Academic Press, New York, 227 pp.
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.
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.
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 Tomé. Proc. R. Soc. Lond. B 267: 1487-1495.
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.
46. Lo, N., M. Casiraghi, E. Salati, C. Bazzocchi & C. Bandi, 2002. How many Wolbachia supergroups exist? Mol. Biol. Evol. 19: 341-346.
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.
48. Merçot, H. & D. Poinsot, 1998b. Rescuing Wolbachia have been overlooked and discovered on Mount Kilimanjaro. Nature 391: 853.
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.
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.
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.
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.
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.
54. O'Neill, S.L. & T.L. Karr, 1990. Bi-directional incompatibility between conspecific populations of Drosophila simulans. Nature 348: 178-180.
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.
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.
57. Peacock, W.J. & J. Erickson, 1964. An indicator of polarity in the spermatocyte? Drosophila Inform. Serv. 39: 107-108.
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.
59. Poinsot, D. & H. Merçot, 2001. Wolbachia injection from usual to naïve host in Drosophila simulans (Diptera: Drosophilidae). Eur. J. Entomol. 98: 25-30.
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.
61. Poinsot, D., M. Montchamp-Moreau & H. Merçot, 2000. Wolbachia segregation rate in Drosophila simulans bi-infected cytoplasmic lineages. Heredity 85: 191-198.
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.
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.
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).
65. Roux, V. & D. Raoult, 1995. Phylogenetic analysis of the genus Rickettsia by 16S rDNA sequencing. Res. Microbiol. 146: 385-396.
66. Rousset, F., 1993. Les facteurs déterminant la distribution des Wolbachia, bactéries endosymbiotiques des arthropodes. Thèse de Doctorat de l'Université Paris Sud Orsay, 114 pp.
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.
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.
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.
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.
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.
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.
73. Stouthamer, R., J.A. Breeuwer & G.D. Hurst, 1999. Wolbachia pipientis: microbial manipulator of arthropod reproduction. Ann. Rev. Microbiol. 53: 71-102.
74. Szollosi, D. & A. Debec, 1980. Presence of Rickettsias in haploid Drosophila melanogaster cell lines. Biol. Cell. 38: 129-134.
75. Tram, U. & W. Sullivan, 2002. Role of delayed nuclear envelope breakdown and mitosis in Wolbachia-induced cytoplasmic incompatibility. Science 296: 1124-1126.
76. Turelli, M., 1994. Evolution of incompatibility-inducing microbes and their hosts. Evolution 48: 1500-1513.
77. Turelli, M. & A.A. Hoffmann, 1991. Rapid spread of an inherited incompatibility factor in California Drosophila. Nature 353: 440-442.
78. Turelli, M. & A.A. Hoffmann, 1995. Cytoplasmic incompatibility in Drosophila simulans: Dynamics and parameter estimates from natural populations. Genetics 140: 1319-1338.
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.
80. Ullmann, S.L., 1965. Epsilon granules in Drosophila pole cells and oocytes. J. Embryol. Exptl. Morphol. 13: 73-81.
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.
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.
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.
84. Werren, J.H., 1997. Biology of Wolbachia. Annu. Rev. Entomol. 42: 587-609.
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.
86. Wolstenholme, D.R., 1965. A DNA and RNA-containing cytoplasmic body in Drosophila melanogaster and its relation to flies. Genetics 52: 949-975.
87. Yanders, A.F., J.G. Brewen, W.J. Peackock & D.J. Goodchild, 1968. Meiotic drive and visible polarity in Drosophila spermatocytes. Genetics 59: 245-253.
88. Yen, J.H. & A.R. Barr, 1971. New hypothesis on the cause of cytoplasmic incompatibility in Culex pipiens L. Nature 232: 657-658.
89. Yen, J.H. & A.R. Barr, 1973. The etiological agent of cytoplasmic incompatibility in Culex pipiens. J. Invert. Pathol. 22: 242-250.
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.