Multiple Wolbachia determinants control the evolution of cytoplasmic incompatibilities in Culex pipiens mosquito populations

Molecular Ecology

Volumn 20, Issue 2, 2011, Pages 286-298

  Atyame, Celestine M ^a   Duron, Olivier ^a   Tortosa, Pablo ^b   Pasteur, Nicole ^a   Fort, Philippe ^a   Weill, Mylene ^a  

^a UNIV MONTPELLIER   (France)

^b UNIVERSITÉ DE LA RÉUNION   (France)

Author keywords

Culex pipiens; cytoplasmic incompatibility; evolution; mod resc determinants; Wolbachia

Indexed keywords

MITOCHONDRIAL DNA;

ANIMAL; ARTICLE; CROSS BREEDING; CULEX; CYTOPLASM; DNA SEQUENCE; EVOLUTION; FEMALE; GENETIC MARKER; GENETIC POLYMORPHISM; GENETICS; INDIAN OCEAN; MALE; MICROBIOLOGY; MITOSIS; PHYSIOLOGY; POLYMERASE CHAIN REACTION; SYMBIOSIS; WOLBACHIA;

ANIMALS; BIOLOGICAL EVOLUTION; CROSSES, GENETIC; CULEX; CYTOPLASM; DNA, MITOCHONDRIAL; FEMALE; GENETIC MARKERS; INDIAN OCEAN; MALE; MITOSIS; POLYMERASE CHAIN REACTION; POLYMORPHISM, GENETIC; SEQUENCE ANALYSIS, DNA; SYMBIOSIS; WOLBACHIA;

ARTHROPODA; CULEX PIPIENS; WOLBACHIA;

EID: 78651278823     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/j.1365-294X.2010.04937.x     Document Type: Article

References (67)

1. Baldo L, Dunning Hotopp JC, Jolley KA, et al. (2006) Multilocus sequence typing system for the endosymbiont Wolbachia pipientis. Applied and Environmental Microbiology, 72, 7098-7110.
2. Barr AR, (1980) Cytoplasmic incompatibility in natural populations of a mosquito, Culex pipiens L. Nature, 283, 71-72.
3. Bordenstein SR, Werren JH, (2007) Bidirectional incompatibility among divergent Wolbachia and incompatibility level differences among closely related Wolbachia in Nasoni. Heredity, 99, 278-287.
4. Brygoo ER, Brunhes J, (1971) Historique de la filariose lymphatique à l'Ãle de La Réunion. Archives de l'Institut Pasteur de Madagascar, 40, 47-56.
5. Callaini G, Dallai R, Riparbelli MG, (1997) Wolbachia-induced delay of paternal chromatin condensation does not prevent maternal chromosomes from entering anaphase in incompatible crosses of Drosophila simulans. Journal of Cell Science, 110 (Pt 2), 271-280.
6. Calvitti M, Moretti R, Lampazzi E, et al. (2010) Characterization of a new Aedes albopictus (Diptera: Culicidae)-Wolbachia pipientis (Rickettsiales: Rickettsiaceae) symbiotic association generated by artificial transfer of the wPip strain from Culex pipiens (Diptera: Culicidae). Journal of Medical Entomology, 47, 179-187.
7. Castresana J, (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Molecular Biology and Evolution, 17, 540-552.
8. Charlat S, Calmet C, Mercot H, (2001) On the mod resc model and the evolution of Wolbachia compatibility types. Genetics, 159, 1415-1422.
9. Charlat S, Calmet C, Andrieu O, Mercot H, (2005) Exploring the evolution of Wolbachia compatibility types: a simulation approach. Genetics, 170, 495-507.
10. Dereeper A, Guignon V, Blanc G, et al. (2008) Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Research, 36, W465-W469.
11. Dobson SL, (2004) Evolution of Wolbachia cytoplasmic incompatibility types. Evolution, 58, 2156-2166.
12. Dobson SL, Marsland EJ, Rattanadechakul W, (2002) Mutualistic Wolbachia infection in Aedes albopictus: accelerating cytoplasmic drive. Genetics, 160, 1087-1094.
13. Duron O, Weill M, (2006) Wolbachia infection influences the development of Culex pipiens embryo in incompatible crosses. Heredity, 96, 493-500.
14. Duron O, Lagnel J, Raymond M, et al. (2005) Transposable element polymorphism of Wolbachia in the mosquito Culex pipiens: evidence of genetic diversity, superinfection and recombination. Molecular Ecology, 14, 1561-1573.
15. Duron O, Bernard C, Unal S, et al. (2006a) Tracking factors modulating cytoplasmic incompatibilities in the mosquito Culex pipiens. Molecular Ecology, 15, 3061-3071.
16. Duron O, Fort P, Weill M, (2006b) Hypervariable prophage WO sequences describe an unexpected high number of Wolbachia variants in the mosquito Culex pipiens. Proceedings of the Royal Society B-Biological Sciences, 273, 495-502.
17. Duron O, Boureux A, Echaubard P, et al. (2007a) Variability and expression of ankyrin domain genes in Wolbachia variants infecting the mosquito Culex pipiens. Journal of Bacteriology, 189, 4442-4448.
18. Duron O, Fort P, Weill M, (2007b) Influence of aging on cytoplasmic incompatibility, sperm modification and Wolbachia density in Culex pipiens mosquitoes. Heredity, 98, 368-374.
19. Duron O, Bouchon D, Boutin S, et al. (2008) The diversity of reproductive parasites among arthropods: Wolbachia do not walk alone. BMC Biology, 6, 27.
20. Engelstadter J, Telschow A, (2009) Cytoplasmic incompatibility and host population structure. Heredity, 103, 196-207.
21. Ferree PM, Sullivan W, (2006) A genetic test of the role of the maternal pronucleus in Wolbachia-induced cytoplasmic incompatibility in Drosophila melanogaster. Genetics, 173, 839-847.
22. Georghiou GP, Metcalf RL, Gidden FE, (1966) Carbamate resistance in mosquitoes: selection of Culex fatigans Wied (Culex quinquefasciatus) for resistance to Baygon. Bulletin of the World Health Organization, 35, 691-708.
23. Guillemaud T, Pasteur N, Rousset F, (1997) Contrasting levels of variability between cytoplasmic genomes and incompatibility types in the mosquito Culex pipiens. Proceedings of the Royal Society of London Series B-Biological Sciences, 264, 245-251.
24. Hedges LM, Brownlie JC, O'Neill SL, Johnson KN, (2008) Wolbachia and virus protection in insects. Science, 322, 702.
25. Hilgenboecker K, Hammerstein P, Schlattmann P, Telschow A, Werren JH, (2008) How many species are infected with Wolbachia?-A statistical analysis of current data. FEMS Microbiology Letters, 281, 215-220.
26. Hochberg Y, (1988) A sharper Bonferroni procedure for multiple tests of significance. Biometrika, 75, 800-802.
27. Hoshizaki S, Shimada T, (1995) PCR-based detection of Wolbachia, cytoplasmic incompatibility microorganisms, infected in natural populations of Laodelphax striatellus (Homoptera: Delphacidae) in central Japan: has the distribution of Wolbachia spread recently? Insect Molecular Biology, 4, 237-243.
28. Huson DH, Bryant D, (2006) Application of phylogenetic networks in evolutionary studies. Molecular Biology and Evolution, 23, 254-267.
29. Kittayapong P, Baimai V, O'Neill SL, (2002) Field prevalence of Wolbachia in the mosquito vector Aedes albopictus. American Journal of Tropical Medicine and Hygiene, 66, 108-111.
30. Klasson L, Walker T, Sebaihia M, et al. (2008) Genome evolution of Wolbachia strain wPip from the Culex pipiens group. Molecular Biology and Evolution, 25, 1877-1887.
31. Klasson L, Westberg J, Sapountzis P, et al. (2009) The mosaic genome structure of the Wolbachia wRi strain infecting Drosophila simulans. Proceedings of the National Academy of Sciences of the United States of America, 106, 5725-5730.
32. Lassy CW, Karr TL, (1996) Cytological analysis of fertilization and early embryonic development in incompatible crosses of Drosophila simulans. Mechanisms of Development, 57, 47-58.
33. Laven H, (1967) Speciation and Evolution in Culex pipiens. In: Genetics of Insect Vectors of Disease (eds, Wright J, Pal R,), 251-275. Elsevier, Amsterdam.
34. Magnin M, Pasteur N, Raymond M, (1987) Multiple incompatibilities within populations of Culex pipiens L. in southern France. Genetica, 74, 125-130.
35. Martin D, Rybicki E, (2000) RDP: detection of recombination amongst aligned sequences. Bioinformatics, 16, 562-563.
36. Martin DP, Williamson C, Posada D, (2005) RDP2: recombination detection and analysis from sequence alignments. Bioinformatics, 21, 260-262.
37. Mercot H, Llorente B, Jacques M, Atlan A, Montchamp-Moreau C, (1995) Variability within the Seychelles cytoplasmic incompatibility system in Drosophila simulans. Genetics, 141, 1015-1023.
38. O'Neill SL, Paterson HE, (1992) Crossing type variability associated with cytoplasmic incompatibility in Australian populations of the mosquito Culex quinquefasciatus Say. Medical and Veterinary Entomology, 6, 209-216.
39. Osborne SE, Leong YS, O'Neill SL, Johnson KN, (2009) Variation in antiviral protection mediated by different Wolbachia strains in Drosophila simulans. PLoS Pathogens, 5, e1000656.
40. Padidam M, Sawyer S, Fauquet CM, (1999) Possible emergence of new geminiviruses by frequent recombination. Virology, 265, 218-225.
41. Poinsot D, Charlat S, Mercot H, (2003) On the mechanism of Wolbachia-induced cytoplasmic incompatibility: confronting the models with the facts. Bioessays, 25, 259-265.
42. Presgraves DC, (2000) A genetic test of the mechanism of Wolbachia-induced cytoplasmic incompatibility in Drosophila. Genetics, 154, 771-776.
43. Rasgon JL, Scott TW, (2003) Wolbachia and cytoplasmic incompatibility in the California Culex pipiens mosquito species complex: parameter estimates and infection dynamics in natural populations. Genetics, 165, 2029-2038.
44. Raymond M, Rousset F, (1995) Genepop (version 1.2), a population genetics software for exact tests and ecumenicism. Journal of Heredity, 86, 248-249.
45. Riegler M, Stauffer C, (2002) Wolbachia infections and superinfections in cytoplasmically incompatible populations of the European cherry fruit fly Rhagoletis cerasi (Diptera, Tephritidae). Molecular Ecology, 11, 2425-2434.
46. Rogers SO, Bendich AJ, (1988) Extraction of DNA from plant tissues. In: Plant Molecular Biology Manuel (eds, Gelvin SB, Schilperoort RA,). pp. 1-10, Kluwer Academic Publishers, Boston.
47. Rousset F, Solignac M, (1995) Evolution of single and double Wolbachia symbioses during speciation in the Drosophila-simulans complex. Proceedings of the National Academy of Sciences of the United States of America, 92, 6389-6393.
48. Rousset F, Raymond M, Kjellberg F, (1991) Cytoplasmic incompatibilities in the mosquito Culex pipiens: How to explain a cytotype polymorphism? Journal of Evolutionary Biology, 4, 69-81.
49. Sanogo YO, Dobson SL, (2004) Molecular discrimination of Wolbachia in the Culex pipiens complex: evidence for variable bacteriophage hyperparasitism. Insect Molecular Biology, 13, 365-369.
50. Sanogo YO, Dobson SL, Bordenstein SR, Novak RJ, (2007) Disruption of the Wolbachia surface protein gene wspB by a transposable element in mosquitoes of the Culex pipiens complex (Diptera, Culicidae). Insect Molecular Biology, 16, 143-154.
51. Serbus LR, Casper-Lindley C, Landmann F, Sullivan W, (2008) The genetics and cell biology of Wolbachia-host interactions. Annual Review of Genetics, 42, 683-707.
52. Sinkins SP, Walker T, Lynd AR, et al. (2005) Wolbachia variability and host effects on crossing type in Culex mosquitoes. Nature, 436, 257-260.
53. Tamura K, Dudley J, Nei M, Kumar S, (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Molecular Biology and Evolution, 24, 1596-1599.
54. Tantely ML, Tortosa P, Alout H, et al. (2010) Insecticide resistance in Culex pipiens quinquefasciatus and Aedes albopictus mosquitoes from La Reunion Island. Insect Biochemistry and Molecular Biology, 40, 317-324.
55. Teixeira L, Ferreira A, Ashburner M, (2008) The bacterial symbiont Wolbachia induces resistance to RNA viral infections in Drosophila melanogaster. PLoS Biology, 6, e2.
56. Thompson JD, Higgins DG, Gibson TJ, (1994) Clustal-WâImproving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research, 22, 4673-4680.
57. Tram U, Sullivan W, (2002) Role of delayed nuclear envelope breakdown and mitosis in Wolbachia-induced cytoplasmic incompatibility. Science, 296, 1124-1126.
58. Turelli M, Hoffmann AA, (1991) Rapid spread of an inherited incompatibility factor in California Drosophila. Nature, 353, 440-442.
59. Walker T, Klasson L, Sebaihia M, et al. (2007) Ankyrin repeat domain-encoding genes in the wPip strain of Wolbachia from the Culex pipiens group. BMC Biology, 5, 39.
60. Werren JH, (1997) Biology of Wolbachia. Annual Review of Entomology, 42, 587-609.
61. Werren JH, Windsor DM, (2000) Wolbachia infection frequencies in insects: evidence of a global equilibrium? Proceedings of the Royal Society of London Series B-Biological Sciences, 267, 1277-1285.
62. Werren JH, Windsor D, Guo L, (1995) Distribution of Wolbachia among neotropical arthropods. Proceedings of the Royal Society of London Series B-Biological Sciences, 262, 197-204.
63. Werren JH, Baldo L, Clark ME, (2008) Wolbachia: master manipulators of invertebrate biology. Nature Reviews Microbiology, 6, 741-751.
64. West SA, Cook JM, Werren JH, Godfray HC, (1998) Wolbachia in two insect host-parasitoid communities. Molecular Ecology, 7, 1457-1465.
65. Wolford JK, Blunt D, Ballecer C, Prochazka M, (2000) High-throughput SNP detection by using DNA pooling and denaturing high performance liquid chromatography (DHPLC). Human Genetics, 107, 483-487.
66. Wu M, Sun LV, Vamathevan J, et al. (2004) Phylogenomics of the reproductive parasite Wolbachia pipientis wMel: a streamlined genome overrun by mobile genetic elements. PLoS Biology, 2, E69.
67. Zabalou S, Apostolaki A, Pattas S, et al. (2008) Multiple rescue factors within a Wolbachia strain. Genetics, 178, 2145-2160.