Mutualism Breakdown by Amplification of Wolbachia Genes

PLoS Biology

Volumn 13, Issue 2, 2015, Pages

  Chrostek, Ewa ^a   Teixeira, Luis ^a  

^a INSTITUTO GULBENKIAN DE CIÊNCIA   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; BACTERIAL GENE; BACTERIAL GENOME; BACTERIAL VIRULENCE; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; ENDOSYMBIONT; EVOLUTION; FEMALE; GENE AMPLIFICATION; GENE DOSAGE; GENE STRUCTURE; NONHUMAN; OCTOMOM REGION; REVERTANT; WOLBACHIA; ANIMAL; BACTERIAL COUNT; GENETIC SELECTION; GENETICS; GENOTYPE; GROWTH, DEVELOPMENT AND AGING; IMMUNOLOGY; LONGEVITY; MICROBIOLOGY; MULTIGENE FAMILY; PATHOGENICITY; PHENOTYPE; SYMBIOSIS; VIRULENCE;

DROSOPHILA MELANOGASTER; HEXAPODA; WOLBACHIA;

ANIMALS; BIOLOGICAL EVOLUTION; COLONY COUNT, MICROBIAL; DROSOPHILA MELANOGASTER; GENE DOSAGE; GENOME, BACTERIAL; GENOTYPE; LONGEVITY; MULTIGENE FAMILY; PHENOTYPE; SELECTION, GENETIC; SYMBIOSIS; VIRULENCE; WOLBACHIA;

EID: 84924087160     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.1002065     Document Type: Article

References (107)

1. Moran NA, McCutcheon JP, Nakabachi A, (2008) Genomics and evolution of heritable bacterial symbionts. Annu Rev Genet 42: 165–190. doi: 10.1146/annurev.genet.41.110306.130119 18983256
2. Jaenike J, (2012) Population genetics of beneficial heritable symbionts. Trends Ecol Evol 27: 226–232. doi: 10.1016/j.tree.2011.10.005 22104387
3. Engelstädter J, Hurst GDD, (2009) The ecology and evolution of microbes that manipulate host reproduction. Annu Rev Ecol Evol Syst 40: 127–149.
4. Jaenike J, (2009) Coupled population dynamics of endosymbionts within and between hosts. Oikos 118: 353–362.
5. Unckless RL, Boelio LM, Herren JK, Jaenike J, (2009) Wolbachia as populations within individual insects: causes and consequences of density variation in natural populations. Proc Biol Sci 276: 2805–2811. doi: 10.1098/rspb.2009.0287 19419989
6. Mouton L, Henri H, Charif D, Boulétreau M, Vavre F, (2007) Interaction between host genotype and environmental conditions affects bacterial density in Wolbachia symbiosis. Biol Lett 3: 210–213. 17251124
7. Kondo N, Shimada M, Fukatsu T, (2005) Infection density of Wolbachia endosymbiont affected by co-infection and host genotype. Biol Lett 1: 488–491. 17148240
8. Chrostek E, Marialva MSP, Esteves SS, Weinert LA, Martinez J, et al. (2013) Wolbachia variants induce differential protection to viruses in Drosophila melanogaster: a phenotypic and phylogenomic analysis. PLoS Genet 9: e1003896. doi: 10.1371/journal.pgen.1003896 24348259
9. Weldon SR, Strand MR, Oliver KM, (2013) Phage loss and the breakdown of a defensive symbiosis in aphids. Proc Natl Acad Sci U S A 280: 201221003.
10. Hurst GDD, Johnson AP, Schulenburg JHGVD, Fuyama Y, (2000) Male-killing Wolbachia in Drosophila: a temperature-sensitive trait with a threshold bacterial density. Genetics 156: 699–709. 11014817
11. Sinkins SP, Braig HR, O’Neill SL, (1995). Wolbachia pipientis: bacterial density and unidirectional cytoplasmic incompatibility between infected populations of Aedes albopictus. Exp Parasitol 81: 284–291. 7498425
12. Bourtzis K, Nirgianaki A, Markakis G, Savakis C, (1996) Wolbachia infection and cytoplasmic incompatibility in Drosophila species. Genetics 144: 1063–1073. 8913750
13. Breeuwer JAJ, Werren JH, (1993) Cytoplasmic incompatibility and bacterial density in Nasonia vitripennis. Genetics 135: 565–574. 8244014
14. Bressac C, Rousset F, (1993) The reproductive incompatibility system in Drosophila simulans: DAPI-staining analysis of the Wolbachia symbionts in sperm cysts. J Invertebr Pathol 61: 226–230. 7689622
15. Bordenstein SR, Marshall ML, Fry AJ, Kim U, Wernegreen JJ, (2006) The tripartite associations between bacteriophage, Wolbachia, and arthropods. PLoS Pathog 2: e43. 16710453
16. Boyle L, O’Neill SL, Robertson HM, Karr TL, (1993) Interspecific and intraspecific horizontal transfer of Wolbachia in Drosophila. Science 260: 1796–1799. 8511587
17. Martinez J, Longdon B, Bauer S, Chan Y-S, Miller WJ, et al. (2014) Symbionts commonly provide broad spectrum resistance to viruses in insects: a comparative analysis of Wolbachia strains. PLoS Pathog 10: e1004369. doi: 10.1371/journal.ppat.1004369 25233341
18. Chrostek E, Marialva MSP, Yamada R, O’Neill SL, Teixeira L, (2014) High anti-viral protection without immune upregulation after interspecies Wolbachia transfer. PLoS ONE 9: e99025. doi: 10.1371/journal.pone.0099025 24911519
19. Min KT, Benzer S, (1997) Wolbachia, normally a symbiont of Drosophila, can be virulent, causing degeneration and early death. Proc Natl Acad Sci U S A 94: 10792–10796. 9380712
20. Zug R, Hammerstein P, (2012) Still a host of hosts for Wolbachia: analysis of recent data suggests that 40% of terrestrial arthropod species are infected. PLoS ONE 7: e38544. doi: 10.1371/journal.pone.0038544 22685581
21. 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 Microbiol Lett 281: 215–220. doi: 10.1111/j.1574-6968.2008.01110.x 18312577
22. Werren JH, Baldo L, Clark ME, (2008) Wolbachia: master manipulators of invertebrate biology. Nat Rev Microbiol 6: 741–751. doi: 10.1038/nrmicro1969 18794912
23. Hosokawa T, Koga R, Kikuchi Y, Meng X-Y, Fukatsu T, (2010) Wolbachia as a bacteriocyte-associated nutritional mutualist. Proc Natl Acad Sci U S A 107: 769–774. doi: 10.1073/pnas.0911476107 20080750
24. Teixeira L, Ferreira A, Ashburner M, (2008) The bacterial symbiont Wolbachia induces resistance to RNA viral infections in Drosophila melanogaster. PLoS Biol 6: e2. doi: 10.1371/journal.pbio.1000002 19222304
25. Hedges LM, Brownlie JC, O’Neill SL, Johnson KN, (2008) Wolbachia and virus protection in insects. Science 322: 702. doi: 10.1126/science.1162418 18974344
26. Osborne SE, Leong YS, O’Neill SL, Johnson KN, (2009) Variation in antiviral protection mediated by different Wolbachia strains in Drosophila simulans. PLoS Pathog 5: e1000656. doi: 10.1371/journal.ppat.1000656 19911047
27. Glaser RL, Meola MA, (2010) The native Wolbachia endosymbionts of Drosophila melanogaster and Culex quinquefasciatus increase host resistance to West Nile virus infection. PLoS ONE 5: e11977. doi: 10.1371/journal.pone.0011977 20700535
28. Hoffmann AA, Clancy DJ, Merton E, (1994) Cytoplasmic incompatibility in Australian populations of Drosophila melanogaster. Genetics 136: 993–999. 8005448
29. Hoffmann A, Hercus M, Dagher H, (1998) Population dynamics of the Wolbachia infection causing cytoplasmic incompatibility in Drosophila melanogaster. Genetics 148: 221–231. 9475734
30. Solignac M, Vautrin D, Rousset F, Solignac M, Vautrin DRF, (1994) Widespread occurence of the proteobacteria Wolbachia and partial incompatibility in Drosophila melanogaster. C R Acad Sci III 317: 461–470.
31. Ferreira ÁG, Naylor H, Esteves SS, Pais IS, Martins NE, et al. (2014) The Toll-Dorsal pathway is required for resistance to viral oral infection in Drosophila. PLoS Pathog 10: e1004507. doi: 10.1371/journal.ppat.1004507 25473839
32. Rancès E, Johnson TK, Popovici J, Iturbe-Ormaetxe I, Zakir T, et al. (2013) The toll and Imd pathways are not required for wolbachia-mediated dengue virus interference. J Virol 87: 11945–11949. doi: 10.1128/JVI.01522-13 23986574
33. Obbard DJ, Jiggins FM, Halligan DL, Little TJ, (2006) Natural selection drives extremely rapid evolution in antiviral RNAi genes. Curr Biol 16: 580–585. 16546082
34. Johnson KN, Christian PD, (1999) Molecular characterization of Drosophila C virus isolates. J Invertebr Pathol 73: 248–254. 10222177
35. Kapun M, Nolte V, Flatt T, Schlötterer C, (2010) Host range and specificity of the Drosophila C virus. PLoS ONE 5: e12421. doi: 10.1371/journal.pone.0012421 20865043
36. Brun G, Plus N, Ashburner M, Wright TRF, (1978) The viruses of Drosophila. In: The genetics and biology of Drosophila. New York: Academic Press. pp. 625–702.
37. Zug R, Hammerstein P (2014) Bad guys turned nice? A critical assessment of Wolbachia mutualisms in arthropod hosts. Biol Rev Camb Philos Soc. E-pub ahead of print.
38. Osborne SE, Iturbe-Ormaetxe I, Brownlie JC, O’Neill SL, Johnson KN, (2012) Antiviral protection and the importance of Wolbachia density and tissue tropism in Drosophila. Appl Environ Microbiol 78: 6922–6929. doi: 10.1128/AEM.01727-12 22843518
39. Frentiu FD, Robinson J, Young PR, McGraw EA, O’Neill SL, (2010) Wolbachia-mediated resistance to dengue virus infection and death at the cellular level. PLoS ONE 5: e13398. doi: 10.1371/journal.pone.0013398 20976219
40. Lu P, Bian G, Pan X, Xi Z, (2012) Wolbachia induces density-dependent inhibition to dengue virus in mosquito cells. PLoS Negl Trop Dis 6: e1754. doi: 10.1371/journal.pntd.0001754 22848774
41. Reynolds KT, Thomson LJ, Hoffmann AA, (2003) The effects of host age, host nuclear background and temperature on phenotypic effects of the virulent Wolbachia strain popcorn in Drosophila melanogaster. Genetics 164: 1027–1034. 12871912
42. McGraw EA, Merritt DJ, Droller JN, O’Neill SL, (2002) Wolbachia density and virulence attenuation after transfer into a novel host. Proc Natl Acad Sci U S A 99: 2918–2923. 11880639
43. Werren JH, (1997) Wolbachia run amok. Proc Natl Acad Sci U S A 94: 11154–11155. 9326576
44. Moreira LA, Iturbe-Ormaetxe I, Jeffery JA, Lu G, Pyke AT, et al. (2009) A Wolbachia symbiont in Aedes aegypti limits infection with dengue, Chikungunya, and Plasmodium. Cell 139: 1268–1278. doi: 10.1016/j.cell.2009.11.042 20064373
45. Kambris Z, Cook PE, Phuc HK, Sinkins SP, (2009) Immune activation by life-shortening Wolbachia and reduced filarial competence in mosquitoes. Science 326: 134–136. doi: 10.1126/science.1177531 19797660
46. Bian G, Xu Y, Lu P, Xie Y, Xi Z, (2010) The endosymbiotic bacterium Wolbachia induces resistance to dengue virus in Aedes aegypti. PLoS Pathog 6: e1000833. doi: 10.1371/journal.ppat.1000833 20368968
47. Kambris Z, Blagborough AM, Pinto SB, Blagrove MSC, Godfray HCJ, et al. (2010) Wolbachia stimulates immune gene expression and inhibits plasmodium development in Anopheles gambiae. PLoS Pathog 6: e1001143. doi: 10.1371/journal.ppat.1001143 20949079
48. Hughes GL, Koga R, Xue P, Fukatsu T, Rasgon JL, (2011) Wolbachia infections are virulent and inhibit the human malaria parasite Plasmodium falciparum in Anopheles gambiae. PLoS Pathog 7: e1002043. doi: 10.1371/journal.ppat.1002043 21625582
49. Bian G, Joshi D, Dong Y, Lu P, Zhou G, et al. (2013) Wolbachia invades Anopheles stephensi populations and induces refractoriness to Plasmodium infection. Science 340: 748–751. doi: 10.1126/science.1236192 23661760
50. Walker T, Johnson PH, Moreira LA, Iturbe-Ormaetxe I, Frentiu FD, et al. (2011) The wMel Wolbachia strain blocks dengue and invades caged Aedes aegypti populations. Nature 476: 450–453. doi: 10.1038/nature10355 21866159
51. Van den Hurk AF, Hall-Mendelin S, Pyke AT, Frentiu FD, McElroy K, et al. (2012) Impact of Wolbachia on infection with chikungunya and yellow fever viruses in the mosquito vector Aedes aegypti. PLoS Negl Trop Dis 6: e1892. doi: 10.1371/journal.pntd.0001892 23133693
52. Blagrove MSC, Arias-Goeta C, Failloux A-B, Sinkins SP, (2012) Wolbachia strain wMel induces cytoplasmic incompatibility and blocks dengue transmission in Aedes albopictus. Proc Natl Acad Sci U S A 109: 255–260. doi: 10.1073/pnas.1112021108 22123944
53. Hoffmann AA, Montgomery BL, Popovici J, Iturbe-Ormaetxe I, Johnson PH, et al. (2011) Successful establishment of Wolbachia in Aedes populations to suppress dengue transmission. Nature 476: 454–457. doi: 10.1038/nature10356 21866160
54. Frentiu FD, Zakir T, Walker T, Popovici J, Pyke AT, et al. (2014) Limited dengue virus replication in field-collected Aedes aegypti mosquitoes infected with Wolbachia. PLoS Negl Trop Dis 8: e2688. doi: 10.1371/journal.pntd.0002688 24587459
55. Hoffmann AA, Iturbe-Ormaetxe I, Callahan AG, Phillips BL, Billington K, et al. (2014) Stability of the wMel Wolbachia infection following invasion into Aedes aegypti populations. PLoS Negl Trop Dis 8: e3115. doi: 10.1371/journal.pntd.0003115 25211492
56. McMeniman CJ, Lane RV, Cass BN, Fong AWC, Sidhu M, et al. (2009) Stable introduction of a life-shortening Wolbachia infection into the mosquito Aedes aegypti. Science 323: 141–144. doi: 10.1126/science.1165326 19119237
57. McMeniman CJ, O’Neill SL, (2010) A virulent Wolbachia infection decreases the viability of the dengue vector Aedes aegypti during periods of embryonic quiescence. PLoS Negl Trop Dis 4: e748. doi: 10.1371/journal.pntd.0000748 20644622
58. Sun LV, Riegler M, Neill SLO, (2003) Development of a physical and genetic map of the virulent Wolbachia strain wMelPop. J Bacteriol 185: 7077–7084. 14645266
59. Wu M, Sun LV, Vamathevan J, Riegler M, Deboy R, et al. (2004) Phylogenomics of the reproductive parasite Wolbachia pipientis wMel: a streamlined genome overrun by mobile genetic elements. PLoS Biol 2: e69. 15024419
60. Riegler M, Sidhu M, Miller WJ, O’Neill SL, (2005) Evidence for a global Wolbachia replacement in Drosophila melanogaster. Curr Biol 15: 1428–1433. 16085497
61. Riegler M, Iturbe-Ormaetxe I, Woolfit M, Miller WJ, O’Neill SL, (2012) Tandem repeat markers as novel diagnostic tools for high resolution fingerprinting of Wolbachia. BMC Microbiol 12 (Suppl 1): S12. doi: 10.1186/1471-2180-12-S1-S12 22375862
62. Woolfit M, Iturbe-Ormaetxe I, Brownlie JC, Walker T, Riegler M, et al. (2013) Genomic evolution of the pathogenic Wolbachia strain, wMelPop. Genome Biol Evol 5: 2189–2204. doi: 10.1093/gbe/evt169 24190075
63. Elde NC, Child SJ, Eickbush MT, Kitzman JO, Rogers KS, et al. (2012) Poxviruses deploy genomic accordions to adapt rapidly against host antiviral defenses. Cell 150: 831–841. doi: 10.1016/j.cell.2012.05.049 22901812
64. Andersson DI, Hughes D, (2009) Gene amplification and adaptive evolution in bacteria. Annu Rev Genet 43: 167–195. doi: 10.1146/annurev-genet-102108-134805 19686082
65. Kroll JS, Loynds BM, Moxon ER, (1991) The Haemophilus influenzae capsulation gene cluster: a compound transposon. Mol Microbiol 5: 1549–1560. 1664907
66. Mekalanos JJ, (1983) Duplication and amplification of toxin genes in Vibrio cholerae. Cell 35: 253–263. 6627396
67. Mavingui P, Laeremans T, Flores M, Romero D, Martínez-Romero E, et al. (1998) Genes essential for nod factor production and nodulation are located on a symbiotic amplicon (AMPRtrCFN299pc60) in Rhizobium tropici. J Bacteriol 180: 2866–2874. 9603874
68. Richardson MF, Weinert LA, Welch JJ, Linheiro RS, Magwire MM, et al. (2012) Population genomics of the Wolbachia endosymbiont in Drosophila melanogaster. PLoS Genet 8: e1003129. doi: 10.1371/journal.pgen.1003129 23284297
69. Early AM, Clark AG, (2013) Monophyly of Wolbachia pipientis genomes within Drosophila melanogaster: geographic structuring, titre variation and host effects across five populations. Mol Ecol 22: 5765–5778. doi: 10.1111/mec.12530 24118111
70. Ilinsky Y, (2013) Coevolution of Drosophila melanogaster mtDNA and Wolbachia genotypes. PLoS ONE 8: e54373. doi: 10.1371/journal.pone.0054373 23349865
71. Bouchon D, Rigaud T, Juchault P, (1998) Evidence for widespread Wolbachia infection in isopod crustaceans: molecular identification and host feminization. Proc Biol Sci 265: 1081–1090. 9684374
72. Le Clec’h W, Raimond M, Guillot S, Bouchon D, Sicard M, (2013) Horizontal transfers of feminizing versus non-feminizing Wolbachia strains: from harmless passengers to pathogens. Environ Microbiol 15: 2922–2936.
73. Sasaki T, Kubo T, Ishikawa H, (2002) Interspecific transfer of Wolbachia between two lepidopteran insects expressing cytoplasmic incompatibility: a Wolbachia variant naturally infecting Cadra cautella causes male killing in Ephestia kuehniella. Genetics 162: 1313–1319. 12454075
74. Toft C, Andersson SGE, (2010) Evolutionary microbial genomics: insights into bacterial host adaptation. Nat Rev Genet 11: 465–475. doi: 10.1038/nrg2798 20517341
75. Degnan PH, Yu Y, Sisneros N, Wing RA, Moran NA, (2009) Hamiltonella defensa, genome evolution of protective bacterial endosymbiont from pathogenic ancestors. Proc Natl Acad Sci U S A 106: 9063–9068. doi: 10.1073/pnas.0900194106 19451630
76. Burke GR, Moran NA, (2011) Massive genomic decay in Serratia symbiotica, a recently evolved symbiont of aphids. Genome Biol Evol 3: 195–208. doi: 10.1093/gbe/evr002 21266540
77. Gil R, Belda E, Gosalbes MJ, Delaye L, Vallier A, et al. (2008) Massive presence of insertion sequences in the genome of SOPE, the primary endosymbiont of the rice weevil Sitophilus oryzae. Int Microbiol 11: 41–48. 18683631
78. Sloan DB, Moran NA, (2013) The evolution of genomic instability in the obligate endosymbionts of whiteflies. Genome Biol Evol 5: 783–793. doi: 10.1093/gbe/evt044 23542079
79. Plague GR, Dunbar HE, Tran PL, Moran NA, (2008) Extensive proliferation of transposable elements in heritable bacterial symbionts. J Bacteriol 190: 777–779. 17981967
80. Klasson L, Walker T, Sebaihia M, Sanders MJ, Quail MA, et al. (2008) Genome evolution of Wolbachia strain wPip from the Culex pipiens group. Mol Biol Evol 25: 1877–1887. doi: 10.1093/molbev/msn133 18550617
81. Klasson L, Westberg J, Sapountzis P, Näslund K, Lutnaes Y, et al. (2009) The mosaic genome structure of the Wolbachia wRi strain infecting Drosophila simulans. Proc Natl Acad Sci U S A 106: 5725–5730. doi: 10.1073/pnas.0810753106 19307581
82. Ellegaard KM, Klasson L, Näslund K, Bourtzis K, Andersson SGE, (2013) Comparative genomics of Wolbachia and the bacterial species concept. PLoS Genet 9: e1003381. doi: 10.1371/journal.pgen.1003381 23593012
83. Foster J, Ganatra M, Kamal I, Ware J, Makarova K, et al. (2005) The Wolbachia genome of Brugia malayi: endosymbiont evolution within a human pathogenic nematode. PLoS Biol 3: e121. 15780005
84. Oakeson KF, Gil R, Clayton AL, Dunn DM, von Niederhausern AC, et al. (2014) Genome degeneration and adaptation in a nascent stage of symbiosis. Genome Biol Evol 6: 76–93. doi: 10.1093/gbe/evt210 24407854
85. Baldo L, Bordenstein S, Wernegreen JJ, Werren JH, (2006) Widespread recombination throughout Wolbachia genomes. Mol Biol Evol 23: 437–449. 16267140
86. Dunbar HE, Wilson ACC, Ferguson NR, Moran NA, (2007) Aphid thermal tolerance is governed by a point mutation in bacterial symbionts. PLoS Biol 5: e96. 17425405
87. Oliver KM, Degnan PH, Hunter MS, Moran NA, (2009) Bacteriophages encode factors required for protection in a symbiotic mutualism. Science 325: 992–994. doi: 10.1126/science.1174463 19696350
88. Klasson L, Kambris Z, Cook PE, Walker T, Sinkins SP, (2009) Horizontal gene transfer between Wolbachia and the mosquito Aedes aegypti. BMC Genomics 10: 33. doi: 10.1186/1471-2164-10-33 19154594
89. Woolfit M, Iturbe-Ormaetxe I, McGraw EA, O’Neill SL, (2009) An ancient horizontal gene transfer between mosquito and the endosymbiotic bacterium Wolbachia pipientis. Mol Biol Evol 26: 367–374. doi: 10.1093/molbev/msn253 18988686
90. Korochkina S, Barreau C, Pradel G, Jeffery E, Li J, et al. (2006) A mosquito-specific protein family includes candidate receptors for malaria sporozoite invasion of salivary glands. Cell Microbiol 8: 163–175. 16367875
91. Iturbe-Ormaetxe I, Burke GR, Riegler M, Neill SLO, (2005) Distribution, expression, and motif variability of ankyrin domain genes in Wolbachia pipientis. J Bacteriol 187: 5136–5145. 16030207
92. Hacker J, Blum-Oehler G, Mühldorfer I, Tschäpe H, (1997) Pathogenicity islands of virulent bacteria: structure, function and impact on microbial evolution. Mol Microbiol 23: 1089–1097. 9106201
93. Schmidt H, Hensel M, (2004) Pathogenicity islands in bacterial pathogenesis. Clin Microbiol Rev 17: 14–56. 14726454
94. Carrington LB, Leslie J, Weeks AR, Hoffmann AA, (2009) The popcorn Wolbachia infection of Drosophila melanogaster: can selection alter Wolbachia longevity effects? Evolution 63: 2648–2657. doi: 10.1111/j.1558-5646.2009.00745.x 19500146
95. McGraw EA, O’Neill SL, (2013) Beyond insecticides: new thinking on an ancient problem. Nat Rev Microbiol 11: 181–193. doi: 10.1038/nrmicro2968 23411863
96. Jin C, Ren X, Rasgon JL, (2009) The virulent Wolbachia strain wMelPop efficiently establishes somatic infections in the malaria vector Anopheles gambiae. Appl Environ Microbiol 75: 3373–3376. doi: 10.1128/AEM.00207-09 19329661
97. Suh E, Mercer DR, Fu Y, Dobson SL, (2009) Pathogenicity of life-shortening Wolbachia in Aedes albopictus after transfer from Drosophila melanogaster. Appl Environ Microbiol 75: 7783–7788. doi: 10.1128/AEM.01331-09 19820149
98. Schneider DI, Riegler M, Arthofer W, Merçot H, Stauffer C, et al. (2013) Uncovering Wolbachia diversity upon artificial host transfer. PLoS ONE 8: e82402. doi: 10.1371/journal.pone.0082402 24376534
99. Ryder E, Blows F, Ashburner M, Bautista-Llacer R, Coulson D, et al. (2004) The DrosDel collection: a set of P-element insertions for generating custom chromosomal aberrations in Drosophila melanogaster. Genetics 167: 797–813. 15238529
100. Pfaffl MW, (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29: e45. 11328886
101. R Project for Statistical Computing (2012) R [computer program]. Available: http://www.R-project.org/. Accessed 9 January 2015.
102. Zabalou S, Charlat S, Nirgianaki A, Lachaise D, Merçot H, et al. (2004) Natural Wolbachia infections in the Drosophila yakuba species complex do not induce cytoplasmic incompatibility but fully rescue the wRi modification. Genetics 167: 827–834. 15238531
103. Veneti Z, Clark ME, Zabalou S, Karr TL, Savakis C, et al. (2003) Cytoplasmic incompatibility and sperm cyst infection in different Drosophila-Wolbachia associations. Genetics 164: 545–552. 12807775
104. Chu DTW, Klymkowsky MW, (1989) The appearance of acetylated α-tubulin during early development and cellular differentiation in Xenopus. Dev Biol 136: 104–117. 2680681
105. Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K, et al. (2011) Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol 7: 539. doi: 10.1038/msb.2011.75 21988835
106. McWilliam H, Li W, Uludag M, Squizzato S, Park YM, et al. (2013) Analysis tool web services from the EMBL-EBI. Nucleic Acids Res 41: W597–W600. doi: 10.1093/nar/gkt376 23671338
107. Goujon M, McWilliam H, Li W, Valentin F, Squizzato S, et al. (2010) A new bioinformatics analysis tools framework at EMBL-EBI. Nucleic Acids Res 38: W695–W699. doi: 10.1093/nar/gkq313 20439314