Diversification of Wolbachia endosymbiont in the culex pipiens mosquito

Molecular Biology and Evolution

Volumn 28, Issue 10, 2011, Pages 2761-2772

  Atyame, Célestine M ^a   Delsuc, Frédéric ^a   Pasteur, Nicole ^a   Weill, Mylne ^a   Duron, Olivier ^a  

^a INSTITUT DES SCIENCES DE L EVOLUTION   (France)

Author keywords

endosymbiosis; mitochondrial hitchhiking; Wolbachia

Indexed keywords

MITOCHONDRIAL DNA;

ARTICLE; BACTERIAL STRAIN; BACTERIAL TRANSMISSION; CONTROLLED STUDY; CULEX PIPIENS; CYTOPLASM; ENDOSYMBIONT; GENETIC VARIABILITY; HAPLOTYPE; HOST; MITOCHONDRION; MONOPHYLY; MULTILOCUS SEQUENCE TYPING; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; RICKETTSIACEAE INFECTION; SELECTIVE SWEEP; WOLBACHIA;

ANIMALS; CLUSTER ANALYSIS; CULEX; DNA, MITOCHONDRIAL; GENE REARRANGEMENT; GENETIC MARKERS; PHYLOGENY; PHYLOGEOGRAPHY; SYMBIOSIS; WOLBACHIA;

ALPHAPROTEOBACTERIA; ARTHROPODA; CULEX PIPIENS; HEXAPODA; WOLBACHIA;

EID: 80053216686     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msr083     Document Type: Article

References (91)

1. Ahrens ME, Shoemaker D. 2005. Evolutionary history of Wolbachia infections in the fire ant Solenopsis invicta. BMC Evol Biol. 5:35.
2. Arthofer W, Riegler M, Schneider D, Krammer M, Miller WJ, Stauffer C. 2009. Hidden Wolbachia diversity in field populations of the European cherry fruit fly, Rhagoletis cerasi (Diptera, Tephritidae). Mol Ecol. 18:3816-3830.
3. Atyame C, Duron O, Tortosa P, Pasteur N, Fort P, Weill M. 2011. Multiple Wolbachia determinants control the evolution of cytoplasmic incompatibilities in Culex pipiens mosquito populations. Mol Ecol. 20:286-298.
4. Baldo L, Ayoub NA, Hayashi CY, Russell JA, Stahlhut JK, Werren JH. 2008. Insight into the routes of Wolbachia invasion: high levels of horizontal transfer in the spider genus Agelenopsis revealed by Wolbachia strain and mitochondrial DNA diversity. Mol Ecol. 17:557-569.
5. Baldo L, Dunning Hotopp JC, Jolley KA, Bordenstein SR, Biber SA, Choudhury RR, Hayashi C, Maiden MC, Tettelin H, Werren JH. 2006. Multilocus sequence typing system for the endosym-biont Wolbachia pipientis. Appl Environ Microbiol. 72: 7098-7110. (Pubitemid 44748423)
6. Baldo L, Lo N, Werren JH. 2005. Mosaic nature of the Wolbachia surface protein. J Bacteriol. 187:5406-5418. (Pubitemid 41022960)
7. Ballard JW. 2000. When one is not enough: introgression of mitochondrial DNA in Drosophila. Mol Biol Evol. 17:1126-1130. (Pubitemid 30419226)
8. Barr AR. 1975. Culex. In: King RC, editor. Handbook of genetics. New York: Plenum Publishing Corporation. p 347-375.
9. Barr AR. 1982. The Culex pipiens complex. In: Steiner WWM, Tabachnik WJ, Rai KS, Narang S, editors. Recent developments in the genetics of insect disease vectors. Champaign (IL): Stipes Publishing Company. p 551-572.
10. Beard CB, Mills Hamm D, Collins FH. 1993. The mitochondrial genome of the mosquito Anopheles gambiae: DNA sequence, genome organization, and comparisons with mitochondrial sequences of other insects. Insect Mol Biol. 2:103-124.
11. Bordenstein SR, Wernegreen JJ. 2004. Bacteriophage flux in endo-symbionts (Wolbachia): infection frequency, lateral transfer, and recombination rates. Mol Biol Evol. 21:1981-1991. (Pubitemid 39331644)
12. Braig HR, Zhou W, Dobson SL, O'Neill SL. 1998. Cloning and characterization of a gene encoding the major surface protein of the bacterial endosymbiont Wolbachia pipientis. J Bacteriol. 180:2373-2378. (Pubitemid 28217350)
13. Bryant D, Moulton V. 2004. Neighbor-net: an agglomerative method for the construction of phylogenetic networks. Mol Biol Evol. 21:255-265. (Pubitemid 38314614)
14. Castresana J. 2000. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol. 17:540-552. (Pubitemid 30210700)
15. Chafee ME, Funk DJ, Harrison RG, Bordenstein SR. 2010. Lateral phage transfer in obligate intracellular bacteria (Wolbachia): verification from natural populations. Mol Biol Evol. 27:501-505.
16. Charlat S, Duplouy A, Hornett EA, Dyson EA, Davies N, Roderick GK, Wedell N, Hurst GD. 2009. The joint evolutionary histories of Wolbachia and mitochondria in Hypolimnas bolina. BMC Evol Biol. 9:64.
17. Charlat S, Engelstadter J, Dyson EA, Hornett EA, Duplouy A, Tortosa P, Davies N, Roderick GK, Wedell N, Hurst GD. 2006. Competing selfish genetic elements in the butterfly Hypolimnas bolina. Curr Biol. 16:2453-2458. (Pubitemid 44894913)
18. Cordaux R. 2008. ISWpi1 from Wolbachia pipientis defines a novel group of insertion sequences within the IS5 family. Gene 409:20-27.
19. Cornel AJ, McAbee RD, Rasgon J, Stanich MA, Scott TW, Coetzee M. 2003. Differences in extent of genetic introgression between sympatric Culex pipiens and Culex quinquefasciatus (Diptera: Culicidae) in California and South Africa. J Med Entomol. 40:36-51. (Pubitemid 37399457)
20. Dedeine F, Vavre F, Shoemaker DD, Bouletreau M. 2004. Intra-individual coexistence of a Wolbachia strain required for host oogenesis with two strains inducing cytoplasmic incompatibility in the wasp Asobara tabida. Evolution 58:2167-2174. (Pubitemid 39448270)
21. Duplouy A, Hurst GD, O'Neill SL, Charlat S. 2010. Rapid spread of male-killing Wolbachia in the butterfly Hypolimnas bolina. J Evol Biol. 23:231-235.
22. Duron O, Bernard C, Unal S, Berthomieu A, Berticat C, Weill M. 2006. Tracking factors modulating cytoplasmic incompatibilities in the mosquito Culex pipiens. Mol Ecol. 15:3061-3071. (Pubitemid 44215474)
23. Duron O, Bouchon D, Boutin S, Bellamy L, Zhou L, Engelstadter J, Hurst GD. 2008. The diversity of reproductive parasites among arthropods: Wolbachia do not walk alone. BMC Biol. 6:27.
24. Duron O, Boureux A, Echaubard P, Berthomieu A, Berticat C, Fort P, Weill M. 2007. Variability and expression of ankyrin domain genes in Wolbachia variants infecting the mosquito Culex pipiens. J Bacteriol. 189:4442-4448. (Pubitemid 46919631)
25. Duron O, Fort P, Weill M. 2006. Hypervariable prophage WO sequences describe an unexpected high number of Wolbachia variants in the mosquito Culex pipiens. Proc Biol Sci. 273:495-502. (Pubitemid 46780558)
26. Duron O, Lagnel J, Raymond M, Bourtzis K, Fort P, Weill M. 2005. Transposable element polymorphism of Wolbachia in the mosquito Culex pipiens: evidence of genetic diversity, superin-fection and recombination. Mol Ecol. 14:1561-1573. (Pubitemid 40554811)
27. Duron O, Raymond M, Weill M. Forthcoming. Many compatible Wolbachia strains coexist within natural populations of Culex pipiens mosquito. Heredity.
28. Echaubard P, Duron O, Agnew P, Sidobre C, Noel V, Weill M, Michalakis Y. 2010. Rapid evolution of Wolbachia density in insecticide resistant Culex pipiens. Heredity 104:15-19.
29. Engelstadter J, Hurst GDD. 2009. The ecology and evolution of microbes that manipulate host reproduction. Annu Rev Ecol Evol Syst. 40:127-149.
30. Fitch WM. 1997. Networks and viral evolution. J Mol Evol. 44(Suppl 1):S65-S75. (Pubitemid 27098530)
31. Fonseca DM, Keyghobadi N, Malcolm CA, Mehmet C, Schaffner F, Mogi M, Fleischer RC, Wilkerson RC. 2004. Emerging vectors in the Culex pipiens complex. Science 303:1535-1538. (Pubitemid 38314427)
32. Fonseca DM, Smith JL, Wilkerson RC, Fleischer RC. 2006. Pathways of expansion and multiple introductions illustrated by large genetic differentiation among worldwide populations of the southern house mosquito. Am J Trop Med Hyg. 74:284-289. (Pubitemid 46774342)
33. Gavotte L, Henri H, Stouthamer R, Charif D, Charlat S, Bouletreau M, Vavre F. 2007. A survey of the bacteriophage WO in the endosymbiotic bacteria Wolbachia. Mol Biol Evol. 24:427-435. (Pubitemid 46204375)
34. Guillemaud T, Pasteur N, Rousset F. 1997. Contrasting levels of variability between cytoplasmic genomes and incompatibility types in the mosquito Culex pipiens. Proc Biol Sci. 264:245-251. (Pubitemid 27105742)
35. Haine ER. 2008. Symbiont-mediated protection. Proc Biol Sci. 275:353-361.
36. Hedrick PW. 1987. Gametic disequilibrium measures: proceed with caution. Genetics 117:331-341.
37. Hertig M, Wolbach SB. 1924. Studies on Rickettsia-like microorganisms in insects. J Med Res. 44:329-374.7.
38. 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 Micro-biol Lett. 281:215-220. (Pubitemid 351422951)
39. Ho SYW, Phillips MJ, Cooper A, Drummond AJ. 2005. Time dependency of molecular rate estimates and systematic over-estimation of recent divergence times. Mol Biol Evol. 22: 1561-1568. (Pubitemid 40800685)
40. Hochberg Y. 1988. A sharper Bonferroni procedure for multiple tests of significance. Biometrika 75:800-802.
41. Hurst GDD, Jiggins FM. 2005. Problems with mitochondrial DNA as a marker in population, phylogeographic and phylogenetic studies: the effects of inherited symbionts. Proc Biol Sci. 272:1525-1534. (Pubitemid 41414684)
42. Huson DH, Bryant D. 2006. Application of phylogenetic networks in evolutionary studies. Mol Biol Evol. 23:254-267. (Pubitemid 43100040)
43. Irving-Bell RJ. 1983. Cytoplasmic incompatibility within and between Culex molestus and Cx. quinquefasciatus (Diptera: Culicidae). J Med Entomol. 20:44-48. (Pubitemid 13125755)
44. Jiggins FM. 2003. Male-killing Wolbachia and mitochondrial DNA: selective sweeps, hybrid introgression and parasite population dynamics. Genetics 164:5-12. (Pubitemid 36617689)
45. Jiggins FM, von Der Schulenburg JH, Hurst GD, Majerus ME. 2001. Recombination confounds interpretations of Wolbachia evolution. Proc Biol Sci. 268:1423-1427. (Pubitemid 32625609)
46. Keller GP, Windsor DM, Saucedo JM, Werren JH. 2004. Reproductive effects and geographical distributions of two Wolbachia strains infecting the Neotropical beetle, Chelymorpha alternans Boh. (Chrysomelidae, Cassidinae). Mol Ecol. 13:2405-2420. (Pubitemid 38946429)
47. Kittayapong P, Baisley KJ, Baimai V, O'Neill SL. 2000. Distribution and diversity of Wolbachia infections in Southeast Asian mosquitoes (Diptera: Culicidae). J Med Entomol. 37:340-345.
48. Klasson L, Walker T, Sebaihia M, et al. (12 co-authors). 2008. Genome evolution of Wolbachia strain wPip from the Culex pipiens group. Mol Biol Evol. 25:1877-1887.
49. Klasson L, Westberg J, Sapountzis P, et al. (12 co-authors). 2009. The mosaic genome structure of the Wolbachia wRi strain infecting Drosophila simulans. Proc Natl Acad Sci USA. 106:5725-5730.
50. Krzywinski J, Grushko OG, Besansky NJ. 1997. Analysis of the complete mitochondrial DNA from Anopheles funestus: an improved dipteran mitochondrial genome annotation and a temporal dimension of mosquito evolution. Mol Phyl Evol. 39:417-423.
51. Laven H. 1958. Speciation by cytoplasmic isolation in the Culex pipiens complex. Cold Spring Harb Symp Quant Biol. 24:166-173.
52. Laven H. 1967. Speciation and evolution in Culex pipiens. In: Wright J, Pal R, editors. Genetics of insect vectors of disease. Amsterdam (The Netherlands): Elsevier.
53. Lewontin RC. 1964. The interaction of selection and linkage. I. General considerations, heterotic models. Genetics 49:49-67.
54. Librado P, Rozas J. 2009. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25: 1451-1452.
55. Lo N, Paraskevopoulos C, Bourtzis K, O'Neill SL, Werren JH, Bordenstein SR, Bandi C. 2007. Taxonomic status of the intracellular bacterium Wolbachia pipientis. Int J Syst Evol Microbiol. 57:654-657. (Pubitemid 46442146)
56. Marshall JF, Staley J. 1937. Some notes regarding the morphological and biological differentiation of Culex pipiens Linnaeus and Culex molestus Forskal (Diptera, Culicidae). Proc R Entomol Soc Lond Ser A Gen Entomol. 12:17-27.
57. Mercot H, Charlat S. 2004. Wolbachia infections in Drosophila melanogaster and D. simulans: polymorphism and levels of cytoplasmic incompatibility. Genetica 120:51-59. (Pubitemid 38448257)
58. Mitchell SE, Cockburn AF, Seawright JA. 1993. The mitochondrial genome of Anopheles quadrimaculatus species A: complete nucleotide sequence and gene organization. Genome 36:1058-1073. (Pubitemid 2035266)
59. Moran NA, McCutcheon JP, Nakabachi A. 2008. Genomics and evolution of heritable bacterial symbionts. Ann Rev Genet. 42:165-190.
60. Narang S, Seawright JA. 1982. Linkage relationships and genetic mapping in Culex and Anopheles. In: Steiner WWM, Tabachnick WJ, Rai KS, Narang S, editors. Recent developments in the genetics of insect disease vectors. Champaign (IL): Stipes Publishing Company. p 231-272.
61. Narita S, Nomura M, Kato Y, Fukatsu T. 2006. Genetic structure of sibling butterfly species affected by Wolbachia infection sweep: evolutionary and biogeographical implications. Mol Ecol. 15:1095-1108.
62. O'Neill SL, Giordano R, Colbert AM, Karr TL, Robertson HM. 1992. 16S rRNA phylogenetic analysis of the bacterial endosymbionts associated with cytoplasmic incompatibility in insects. Proc Natl Acad Sci USA. 89:2699-2702.
63. O'Neill SL, Paterson HE. 1992. Crossing type variability associated with cytoplasmic incompatibility in Australian populations of the mosquito Culex quinquefasciatus Say. Med Vet Entomol. 6:209-216.
64. Posada D, Crandall KA. 1998. MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817-818. (Pubitemid 28552116)
65. Rasgon JL, Cornel AJ, Scott TW. 2006. Evolutionary history of a mosquito endosymbiont revealed through mitochondrial hitchhiking. Proc Biol Sci. 273:1603-1611. (Pubitemid 46931045)
66. Rasgon JL, Scott TW. 2004. An initial survey for Wolbachia (Rickettsiales: Rickettsiaceae) infections in selected California mosquitoes (Diptera: Culicidae). J Med Entomol. 41:255-257. (Pubitemid 38403268)
67. Raychoudhury R, Baldo L, Oliveira DC, Werren JH. 2009. Modes of acquisition of Wolbachia: horizontal transfer, hybrid introgres-sion, and codivergence in the Nasonia species complex. Evolution 63:165-183.
68. Raymond M, Callaghan A, Fort P, Pasteur N. 1991. Worldwide migration of amplified insecticide resistance genes in mosquitoes. Nature 350:151-153. (Pubitemid 21912184)
69. Raymond M, Rousset F. 1995. Genepop (version 1.2), a population genetics software for exact tests and ecumenicism. J Hered. 86:248-249.
70. Reidenbach KR, Cook S, Bertone MA, Harbach RE, Wiegmann BM, Besansky NJ. 2009. Phylogenetic analysis and temporal diversification of mosquitoes (Diptera: Culicidae) based on nuclear genes and morphology. BMC Evol Biol. 9:298.
71. Ricci I, Cancrini G, Gabrielli S, D'Amelio S, Favi G. 2002. Searching for Wolbachia (Rickettsiales: Rickettsiaceae) in mosquitoes (Diptera: Culicidae): large polymerase chain reaction survey and new identifications. J Med Entomol. 39:562-567. (Pubitemid 135695980)
72. Rich SM, Licht MC, Hudson RR, Ayala FJ. 1998. Malaria's eve: evidence of a recent population bottleneck throughout the world populations of Plasmodium falciparum. Proc Natl Acad Sci USA. 95:4425-4430. (Pubitemid 28207928)
73. Riegler M, Sidhu M, Miller WJ, O'Neill SL. 2005. Evidence for a global Wolbachia replacement in Drosophila melanogaster. Curr Biol. 15:1428-1433. (Pubitemid 41097549)
74. Rogers SO, Bendich AJ. 1988. Extraction of DNA from plant tissues. In: Gelvin SB, Schilperoort RA, editors. Plant molecular biology manual. Boston (MA): Kluwer Academic Publishers. p 1-10.
75. Ronquist F, Huelsenbeck JP. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572-1574. (Pubitemid 37038874)
76. Ros VI, Fleming VM, Feil EJ, Breeuwer JA. 2009. How diverse is the genus Wolbachia? Multiple-gene sequencing reveals a putatively new Wolbachia supergroup recovered from spider mites (Acari: Tetranychidae). Appl Environ Microbiol. 75:1036-1043.
77. Roubaud E. 1941. Phénomènes d'amixie dans les intercroisements de Culicides du groupe pipiens. C R Acad Sci. 212:257-259.
78. Rousset F, Solignac M. 1995. Evolution of single and double Wolbachia symbioses during speciation in the Drosophila simulans complex. Proc Natl Acad Sci USA. 92:6389-6393.
79. Rozeboom LE. 1958. Hybridization of Culex pipiens fatigans Wiedemann from the Philippine Islands with American strains of Culex pipiens group (Diptera: Culicidae). Am J Trop Med Hyg. 7:526-530.
80. Salzberg SL, Puiu D, Sommer DD, Nene V, Lee NH. 2009. The genome sequence of Wolbachia endosymbiont of Culex quinquefasciatus JHB. J Bacteriol. 191:1725.
81. Sawyer SA. 1999. GENECONV: a computer package for the statistical detection of gene conversion [Internet]. Distributed by the author. Department of Mathematics, Washington University in St. Louis. Missouri, USA. Available (2011) from http://www.math .wustl.edu/~sawyer/geneconv/.
82. Sinkins SP, Walker T, Lynd AR, Steven AR, Makepeace BL, Godfray HC, Parkhill J. 2005. Wolbachia variability and host effects on crossing type in Culex mosquitoes. Nature 436:257-260. (Pubitemid 41021276)
83. Tamura K, Dudley J, Nei M, Kumar S. 2007. MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol. 24:1596-1599. (Pubitemid 47236692)
84. Thompson JD, Gibson TJ, Higgins DG. 2002. Multiple sequence alignment using ClustalW and ClustalX. Curr Protoc Bioinfor-matics. Chapter 2:Unit 2.3. http://www.ncbi.nlm.nih.gov/pubmed/18792934.
85. Vavre F, Fleury F, Lepetit D, Fouillet P, Bouletreau M. 1999. Phylogenetic evidence for horizontal transmission of Wolbachia in host-parasitoid associations. Mol Biol Evol. 16:1711-1723.
86. Venkatesan M, Westbrook CJ, Hauer MC, Rasgon JL. 2007. Evidence for a population expansion in the West Nile Virus vector Culex tarsalis. Mol Biol Evol. 24:1208-1218. (Pubitemid 47343646)
87. Walker T, Klasson L, Sebaihia M, Sanders MJ, Thomson NR, Parkhill J, Sinkins SP. 2007. Ankyrin repeat domain-encoding genes in the wPip strain of Wolbachia from the Culex pipiens group. BMC Biol. 5:39.
88. Weeks AR, Turelli M, Harcombe WR, Reynolds KT, Hoffmann AA. 2007. From parasite to mutualist: rapid evolution of Wolbachia in natural populations of Drosophila. PLoS Biol. 5:e114.
89. Werren JH, Baldo L, Clark ME. 2008. Wolbachia: master manipulators of invertebrate biology. Nat Rev Microbiol. 6:741-751.
90. Wu M, Sun LV, Vamathevan J, et al. (30 co-authors). 2004. Phylogenomics of the reproductive parasite Wolbachia pipientis wMel: a streamlined genome overrun by mobile genetic elements. PLoS Biol. 2:E69.
91. Yen JH, Barr AR. 1971. New hypothesis of the cause of cytoplasmic incompatibility in Culex pipiens L. Nature 232:657-658.