is an endosymbiotic that can suppress insect-borne diseases through decreasing host virus transmission (population replacement) or through decreasing host population density (population suppression). We contrast natural infections in insect populations with transinfections in mosquitoes to gain insights into factors potentially affecting the long-term success of releases. Natural infections can spread rapidly, whereas the slow spread of transinfections is governed by deleterious effects on host fitness and demographic factors. Cytoplasmic incompatibility (CI) generated by is central to both population replacement and suppression programs, but CI in nature can be variable and evolve, as can fitness effects and virus blocking. spread is also influenced by environmental factors that decrease titer and reduce maternal transmission frequency. More information is needed on the interactions between and host nuclear/mitochondrial genomes, the interaction between invasion success and local ecological factors, and the long-term stability of -mediated virus blocking.


Article metrics loading...

Loading full text...

Full text loading...


Literature Cited

  1. 1. 
    Ahantarig A, Trinachartvanit W, Kittayapong P 2008. Relative Wolbachia density of field-collected Aedes albopictus mosquitoes in Thailand. J. Vector Ecol. 33:173–77
    [Google Scholar]
  2. 2. 
    Ahmed MZ, Araujo-Jnr EV, Welch JJ, Kawahara AY 2015. Wolbachia in butterflies and moths: geographic structure in infection frequency. Front. Zool. 12:16
    [Google Scholar]
  3. 3. 
    Alphey L, Benedict M, Bellini R, Clark GG, Dame DA et al. 2010. Sterile-insect methods for control of mosquito-borne diseases: an analysis. Vector Borne Zoonotic Dis 10:295–311
    [Google Scholar]
  4. 4. 
    Ant TH, Herd CS, Geoghegan V, Hoffmann AA, Sinkins SP 2018. The Wolbachia strain wAu provides highly efficient virus transmission blocking in Aedes aegypti. PLOS Pathog 14:e1006815
    [Google Scholar]
  5. 5. 
    Ant TH, Sinkins SP. 2018. A Wolbachia triple-strain infection generates self-incompatibility in Aedes albopictus and transmission instability in Aedes aegypti. Parasites Vectors 11:295
    [Google Scholar]
  6. 6. 
    Armbruster P, Damsky WE Jr., Giordano R, Birungi J, Munstermann LE, Conn JE 2003. Infection of New- and Old-World Aedes albopictus (Diptera: Culicidae) by the intracellular parasite Wolbachia: implications for host mitochondrial DNA evolution. J. Med. Entomol 40:356–60
    [Google Scholar]
  7. 7. 
    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. 18:3816–30
    [Google Scholar]
  8. 8. 
    Asselin AK, Villegas-Ospina S, Hoffmann AA, Brownlie JC, Johnson KN 2019. Contrasting patterns of virus protection and functional incompatibility genes in two conspecific Wolbachia strains from Drosophila pandora. Appl. Environ. Microbiol 85:e02290–18
    [Google Scholar]
  9. 9. 
    Atyame CM, Delsuc F, Pasteur N, Weill M, Duron O 2011. Diversification of Wolbachia endosymbiont in the Culex pipiens mosquito. Mol. Biol. Evol. 28:2761–72
    [Google Scholar]
  10. 10. 
    Atyame CM, Labbe P, Rousset F, Beji M, Makoundou P et al. 2015. Stable coexistence of incompatible Wolbachia along a narrow contact zone in mosquito field populations. Mol. Ecol. 24:508–21
    [Google Scholar]
  11. 11. 
    Audsley MD, Seleznev A, Joubert DA, Woolfit M, O'Neill SL, McGraw EA 2018. Wolbachia infection alters the relative abundance of resident bacteria in adult Aedes aegypti mosquitoes, but not larvae. Mol. Ecol. 27:297–309
    [Google Scholar]
  12. 12. 
    Bakovic V, Schebeck M, Telschow A, Stauffer C, Schuler H 2018. Spatial spread of Wolbachia in Rhagoletis cerasi populations. Biol. Lett. 14:20180161
    [Google Scholar]
  13. 13. 
    Barrera R, Amador M, Diaz A, Smith J, Munoz-Jordan J, Rosario Y 2008. Unusual productivity of Aedes aegypti in septic tanks and its implications for dengue control. Med. Vet. Entomol. 22:62–69
    [Google Scholar]
  14. 14. 
    Barton NH. 1979. The dynamics of hybrid zones. Heredity 43:341–59
    [Google Scholar]
  15. 15. 
    Barton NH, Turelli M. 2011. Spatial waves of advance with bistable dynamics: cytoplasmic and genetic analogues of Allee effects. Am. Nat. 178:E48–75
    [Google Scholar]
  16. 16. 
    Bian GW, Zhou GL, Lu P, Xi ZY 2013. Replacing a native Wolbachia with a novel strain results in an increase in endosymbiont load and resistance to dengue virus in a mosquito vector. PLOS Neglect. Trop. Dis. 7:e2250
    [Google Scholar]
  17. 17. 
    Brownlie JC, Cass BN, Riegler M, Witsenburg JJ, Iturbe-Ormaetxe I et al. 2009. Evidence for metabolic provisioning by a common invertebrate endosymbiont, Wolbachia pipientis, during periods of nutritional stress. PLOS Pathog 5:e1000368
    [Google Scholar]
  18. 18. 
    Bull JJ, Turelli M. 2013. Wolbachia versus dengue: evolutionary forecasts. Evol. Med. Public Health 1:197–207
    [Google Scholar]
  19. 19. 
    Callahan AG, Ross PA, Hoffmann AA 2018. Small females prefer small males: size assortative mating in Aedes aegypti mosquitoes. Parasites Vectors 11:445
    [Google Scholar]
  20. 20. 
    Calvitti M, Moretti R, Lampazzi E, Bellini R, Dobson SL 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). J. Med. Entomol. 47:179–87
    [Google Scholar]
  21. 21. 
    Caragata EP, Rancès E, Hedges LM, Gofton AW, Johnson KN et al. 2013. Dietary cholesterol modulates pathogen blocking by Wolbachia. PLOS Pathog 9:e1003459
    [Google Scholar]
  22. 22. 
    Carrington LB, Hoffmann AA, Weeks AR 2010. Monitoring long-term evolutionary changes following Wolbachia introduction into a novel host: the Wolbachia popcorn infection in Drosophila simulans. Proc. R. Soc. B 277:2059–68
    [Google Scholar]
  23. 23. 
    Carrington LB, Leslie J, Weeks AR, Hoffmann AA 2009. The popcorn Wolbachia infection of Drosophila melanogaster: Can selection alter Wolbachia longevity effects?. Evolution 63:2648–57
    [Google Scholar]
  24. 24. 
    Carrington LB, Lipkowitz JR, Hoffmann AA, Turelli M 2011. A re-examination of Wolbachia-induced cytoplasmic incompatibility in California Drosophila simulans. PLOS ONE 6:e22565
    [Google Scholar]
  25. 25. 
    Carrington LB, Tran BCN, Le NTH, Luong TTH, Nguyen TT et al. 2018. Field and clinically derived estimates of Wolbachia-mediated blocking of dengue virus transmission potential in Aedes aegypti mosquitoes. PNAS 115:361–66
    [Google Scholar]
  26. 26. 
    Caspari E, Watson GS. 1959. On the evolutionary importance of cytoplasmic sterility in mosquitos. Evolution 13:568–70
    [Google Scholar]
  27. 27. 
    Charlat S, Hornett EA, Dyson EA, Ho PP, Loc NT et al. 2005. Prevalence and penetrance variation of male-killing Wolbachia across Indo-Pacific populations of the butterfly Hypolimnas bolina. Mol. Ecol 14:3525–30
    [Google Scholar]
  28. 28. 
    Charlesworth J, Weinert LA, Araujo EV Jr., Welch JJ 2019. Wolbachia, Cardinium and climate: an analysis of global data. Biol. Lett. 15:20190273
    [Google Scholar]
  29. 29. 
    Chrostek E, Teixeira L. 2015. Mutualism breakdown by amplification of Wolbachia genes. PLOS Biol 13:e1002065
    [Google Scholar]
  30. 30. 
    Cooper BS, Ginsberg PS, Turelli M, Matute DR 2017. Wolbachia in the Drosophila yakuba complex: pervasive frequency variation and weak cytoplasmic incompatibility, but no apparent effect on reproductive isolation. Genetics 205:333–51
    [Google Scholar]
  31. 31. 
    Cooper BS, Vanderpool D, Conner WR, Matute DR, Turelli M 2019. Wolbachia acquisition by Drosophila yakuba-clade hosts and transfer of incompatibility loci between distantly related Wolbachia. Genetics 2121399–419
  32. 32. 
    Corbin C, Heyworth ER, Ferrari J, Hurst GD 2017. Heritable symbionts in a world of varying temperature. Heredity 118:10–20
    [Google Scholar]
  33. 33. 
    Curtis C, Brooks G, Ansari M, Grover K, Krishnamurthy B et al. 1982. A field trial on control of Culex quinquefasciatus by release of males of a strain integrating cytoplasmic incompatibility and a translocation. Entomol. Exp. Appl. 31:181–90
    [Google Scholar]
  34. 34. 
    Dias NP, Zotti MJ, Montoya P, Carvalho IR, Nava DE 2018. Fruit fly management research: a systematic review of monitoring and control tactics in the world. Crop Prot 112:187–200
    [Google Scholar]
  35. 35. 
    Dodson B, Hughes G, Paul O, Matacchiero A, Kramer L, Rasgon JL 2014. Wolbachia enhances West Nile virus (WNV) infection in the mosquito Culex tarsalis. PLOS Neglect. Trop. Dis 8:e2965
    [Google Scholar]
  36. 36. 
    Dutra HLC, dos Santos LMB, Caragata EP, Silva JBL, Villela DAM et al. 2015. From lab to field: the influence of urban landscapes on the invasive potential of Wolbachia in Brazilian Aedes aegypti mosquitoes. PLOS Neglect. Trop. Dis. 9:e0003689
    [Google Scholar]
  37. 37. 
    Endersby-Harshman NM, Axford JK, Hoffmann AA 2019. Environmental concentrations of antibiotics may diminish Wolbachia infections in Aedes aegypti (Diptera: Culicidae). J. Med. Entomol. 56:1078–86
    [Google Scholar]
  38. 38. 
    Endler JA. 1977. Geographic Variation, Speciation, and Clines Princeton, NJ: Princeton Univ. Press
  39. 39. 
    Ferguson NM, Kien DTH, Clapham H, Aguas R, Trung VT et al. 2015. Modeling the impact on virus transmission of Wolbachia-mediated blocking of dengue virus infection of Aedes aegypti. Sci. Transl. Med 7:279ra37
    [Google Scholar]
  40. 40. 
    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 Neglect. Trop. Dis 8:e2688
    [Google Scholar]
  41. 41. 
    Fu YQ, Gavotte L, Mercer DR, Dobson SL 2010. Artificial triple Wolbachia infection in Aedes albopictus yields a new pattern of unidirectional cytoplasmic incompatibility. Appl. Environ. Microbiol. 76:5887–91
    [Google Scholar]
  42. 42. 
    Garcia GdA, Sylvestre G, Aguiar R, da Costa GB, Martins AJ et al. 2019. Matching the genetics of released and local Aedes aegypti populations is critical to assure Wolbachia invasion. PLOS Neglect. Trop. Dis. 13:e0007023
    [Google Scholar]
  43. 43. 
    Gavotte L, Mercer DR, Stoeckle JJ, Dobson SL 2010. Costs and benefits of Wolbachia infection in immature Aedes albopictus depend upon sex and competition level. J. Invertebr. Pathol. 105:341–46
    [Google Scholar]
  44. 44. 
    Gloria-Soria A, Chiodo TG, Powell JR 2018. Lack of evidence for natural Wolbachia infections in Aedes aegypti (Diptera: Culicidae). J. Med. Entomol. 55:1354–56
    [Google Scholar]
  45. 45. 
    Graham RI, Grzywacz D, Mushobozi WL, Wilson K 2012. Wolbachia in a major African crop pest increases susceptibility to viral disease rather than protects. Ecol. Lett. 15:993–1000
    [Google Scholar]
  46. 46. 
    Gruntenko NE, Ilinsky YY, Adonyeva NV, Burdina EV, Bykov RA et al. 2017. Various Wolbachia genotypes differently influence host Drosophila dopamine metabolism and survival under heat stress conditions. BMC Evol. Biol. 17:252
    [Google Scholar]
  47. 47. 
    Hale LR, Hoffmann AA. 1990. Mitochondrial DNA polymorphism and cytoplasmic incompatibility in natural populations of Drosophila simulans. Evolution 44:1383–86
    [Google Scholar]
  48. 48. 
    Hancock PA, Godfray HCJ. 2012. Modelling the spread of Wolbachia in spatially heterogeneous environments. J. R. Soc. Interface 9:3045–54
    [Google Scholar]
  49. 49. 
    Hancock PA, White VL, Callahan AG, Godfray CHJ, Hoffmann AA, Ritchie SA 2016. Density-dependent population dynamics in Aedes aegypti slow the spread of wMel Wolbachia. J. Appl. Ecol 53:785–93
    [Google Scholar]
  50. 50. 
    Hartberg W. 1971. Observations on the mating behaviour of Aedes aegypti in nature. Bull. World Health Organ. 45:847–50
    [Google Scholar]
  51. 51. 
    Haygood R, Turelli M. 2009. Evolution of incompatibility-inducing microbes in subdivided host populations. Evolution 63:432–47
    [Google Scholar]
  52. 52. 
    Hedges LM, Brownlie JC, O'Neill SL, Johnson KN 2008. Wolbachia and virus protection in insects. Science 322:702
    [Google Scholar]
  53. 53. 
    Hegde S, Khanipov K, Albayrak L, Golovko G, Pimenova M et al. 2018. Microbiome interaction networks and community structure from laboratory-reared and field-collected Aedes aegypti, Aedes albopictus, and Culex quinquefasciatus mosquito vectors. Front. Microbiol. 9:2160
    [Google Scholar]
  54. 54. 
    Hoffmann AA, Iturbe-Ormaetxe I, Callahan AG, Phillips B, Billington K et al. 2014. Stability of the wMel Wolbachia infection following invasion into Aedes aegypti populations. PLOS Neglect. Trop. Dis. 8:e3115
    [Google Scholar]
  55. 55. 
    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 476:454–57
    [Google Scholar]
  56. 56. 
    Hoffmann AA, Ross PA. 2018. Rates and patterns of laboratory adaptation in (mostly) insects. J. Econ. Entomol. 111:501–9
    [Google Scholar]
  57. 57. 
    Hoffmann AA, Ross PA, Rašić G 2015. Wolbachia strains for disease control: ecological and evolutionary considerations. Evol. Appl. 8:751–68
    [Google Scholar]
  58. 58. 
    Hoffmann AA, Turelli M. 1997. Cytoplasmic incompatibility in insects. Influential Passengers: Microorganisms and Invertebrate Reproduction S O'Neill, AA Hoffmann, JH Werren 42–80 Oxford, UK: Oxford Univ. Press
    [Google Scholar]
  59. 59. 
    Hoffmann AA, Turelli M. 2013. Facilitating Wolbachia introductions into mosquito populations through insecticide-resistance selection. Proc. R. Soc. B 280:20130371
    [Google Scholar]
  60. 60. 
    Hoffmann AA, Turelli M, Harshman LG 1990. Factors affecting the distribution of cytoplasmic incompatibility in Drosophila simulans. Genetics 126:933–48
    [Google Scholar]
  61. 61. 
    Hornett EA, Charlat S, Wedell N, Jiggins CD, Hurst GDD 2009. Rapidly shifting sex ratio across a species range. Curr. Biol. 19:1628–31
    [Google Scholar]
  62. 62. 
    Hughes GL, Rasgon JL. 2014. Transinfection: a method to investigate Wolbachia–host interactions and control arthropod-borne disease. Insect Mol. Biol. 23:141–51
    [Google Scholar]
  63. 63. 
    Huigens M, De Almeida R, Boons P, Luck R, Stouthamer R 2004. Natural interspecific and intraspecific horizontal transfer of parthenogenesis–inducing Wolbachia in Trichogramma wasps. Proc. R. Soc. B 271:509–15
    [Google Scholar]
  64. 64. 
    Hurst GDD, Jiggins FM. 2005. Problems with mitochondrial DNA as a marker in population, phylogeographic and phylogenetic studies: the effects of inherited symbionts. Proc. R. Soc. B 272:1525–34
    [Google Scholar]
  65. 65. 
    Jansen VAA, Turelli M, Godfray HCJ 2008. Stochastic spread of Wolbachia. . Proc. R. Soc. B 275:2769–76
    [Google Scholar]
  66. 66. 
    Jasper M, Schmidt TL, Ahmad NW, Sinkins SP, Hoffmann AA 2019. A genomic approach to inferring kinship reveals limited intergenerational dispersal in the yellow fever mosquito. Mol. Ecol. Resour. 19:51254–64
    [Google Scholar]
  67. 67. 
    Joubert DA, Walker T, Carrington LB, De Bruyne JT, Kien DHT et al. 2016. Establishment of a Wolbachia superinfection in Aedes aegypti mosquitoes as a potential approach for future resistance management. PLOS Pathog 12:e1005434
    [Google Scholar]
  68. 68. 
    King JG, Souto-Maior C, Sartori LM, Maciel-de-Freitas R, Gomes MGM 2018. Variation in Wolbachia effects on Aedes mosquitoes as a determinant of invasiveness and vectorial capacity. Nat. Commun. 9:1483
    [Google Scholar]
  69. 69. 
    Koukou K, Pavlikaki H, Kilias G, Werren JH, Bourtzis K, Alahiotisi SN 2006. Influence of antibiotic treatment and Wolbachia curing on sexual isolation among Drosophila melanogaster cage populations. Evolution 60:87–96
    [Google Scholar]
  70. 70. 
    Krafsur E. 1998. Sterile insect technique for suppressing and eradicating insect population: 55 years and counting. J. Agric. Entomol. 15:303–17
    [Google Scholar]
  71. 71. 
    Kriesner P, Conner WR, Weeks AR, Turelli M, Hoffmann AA 2016. Persistence of a Wolbachia infection frequency cline in Drosophila melanogaster and the possible role of reproductive dormancy. Evolution 70:979–97
    [Google Scholar]
  72. 72. 
    Kriesner P, Hoffmann AA, Lee SF, Turelli M, Weeks AR 2013. Rapid sequential spread of two Wolbachia variants in Drosophila simulans. PLOS Pathog 9:e1003607
    [Google Scholar]
  73. 73. 
    Kulkarni A, Yu W, Jiang J, Sanchez C, Karna AK et al. 2019. Wolbachia pipientis occurs in Aedes aegypti populations in New Mexico and Florida, USA. Ecol. Evol. 9:6148–56
    [Google Scholar]
  74. 74. 
    Laven H. 1959. Speciation by cytoplasmic isolation in the Culex pipiens complex. Proc. Cold Spring Harb. Symp. Quant. Biol. 24:166–72
    [Google Scholar]
  75. 75. 
    Laven H. 1967. Eradication of Culex pipiens fatigans through cytoplasmic incompatibility. Nature 216:383–84
    [Google Scholar]
  76. 76. 
    Li SJ, Ahmed MZ, Lv N, Shi PQ, Wang XM et al. 2017. Plant-mediated horizontal transmission of Wolbachia between whiteflies. ISME J 11:1019–28
    [Google Scholar]
  77. 77. 
    Li Y-Y, Floate K, Fields P, Pang B-P 2014. Review of treatment methods to remove Wolbachia bacteria from arthropods. Symbiosis 62:1–15
    [Google Scholar]
  78. 78. 
    Lindsey A, Bhattacharya T, Newton I, Hardy R 2018. Conflict in the intracellular lives of endosymbionts and viruses: a mechanistic look at Wolbachia-mediated pathogen-blocking. Viruses 10:E141
    [Google Scholar]
  79. 79. 
    Lopez V, Cortesero AM, Poinsot D 2018. Influence of the symbiont Wolbachia on life history traits of the cabbage root fly (Delia radicum). J. Invertebr. Pathol. 158:24–31
    [Google Scholar]
  80. 80. 
    Lu P, Bian GW, Pan XL, Xi ZY 2012. Wolbachia induces density-dependent inhibition to dengue virus in mosquito cells. PLOS Neglect. Trop. Dis. 6:e1754
    [Google Scholar]
  81. 81. 
    Mains JW, Brelsfoard CL, Crain PR, Huang YX, Dobson SL 2013. Population impacts of Wolbachia on Aedes albopictus. Ecol. Appl 23:493–501
    [Google Scholar]
  82. 82. 
    Mains JW, Brelsfoard CL, Rose RI, Dobson SL 2016. Female adult Aedes albopictus suppression by Wolbachia-infected male mosquitoes. Sci. Rep. 6:33846
    [Google Scholar]
  83. 83. 
    Mains JW, Kelly PH, Dobson KL, Petrie WD, Dobson SL 2019. Localized control of Aedes aegypti (Diptera: Culicidae) in Miami, FL, via inundative releases of Wolbachia-infected male mosquitoes. J. Med. Entomol. 56:1296–303
    [Google Scholar]
  84. 84. 
    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
    [Google Scholar]
  85. 85. 
    Martinez J, Ok S, Smith S, Snoeck K, Day JP, Jiggins FM 2015. Should symbionts be nice or selfish? Antiviral effects of Wolbachia are costly but reproductive parasitism is not. PLOS Pathog 11:e1005021
    [Google Scholar]
  86. 86. 
    Martinez J, Tolosana I, Ok S, Smith S, Snoeck K et al. 2017. Symbiont strain is the main determinant of variation in Wolbachia-mediated protection against viruses across Drosophila species. Mol. Ecol. 26:4072–84
    [Google Scholar]
  87. 87. 
    McGraw EA, Merritt DJ, Droller JN, O'Neill SL 2002. Wolbachia density and virulence attenuation after transfer into a novel host. PNAS 99:2918–23
    [Google Scholar]
  88. 88. 
    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 Neglect. Trop. Dis. 4:e748
    [Google Scholar]
  89. 89. 
    McNaughton D, Duong TTH. 2014. Designing a community engagement framework for a new dengue control method: a case study from central Vietnam. PLOS Neglect. Trop. Dis. 8:e2794
    [Google Scholar]
  90. 90. 
    Meany MK, Conner WR, Richter SV, Bailey JA, Turelli M, Cooper BS 2019. Loss of cytoplasmic incompatibility and minimal fecundity effects explain relatively low Wolbachia frequencies in Drosophila mauritiana. Evolution 73:1278–95
    [Google Scholar]
  91. 91. 
    Moreira LA, Iturbe-Ormaetxe I, Jeffery JA, Lu GJ, Pyke AT et al. 2009. A Wolbachia symbiont in Aedes aegypti limits infection with dengue, chikungunya, and Plasmodium. Cell 139:1268–78
    [Google Scholar]
  92. 92. 
    Moretti R, Yen PS, Houé V, Lampazzi E, Desiderio A et al. 2018. Combining Wolbachia-induced sterility and virus protection to fight Aedes albopictus-borne viruses. PLOS Neglect. Trop. Dis. 12:e0006626
    [Google Scholar]
  93. 93. 
    Mousson L, Zouache K, Arias-Goeta C, Raquin V, Mavingui P, Failloux AB 2012. The native Wolbachia symbionts limit transmission of dengue virus in Aedes albopictus. PLOS Neglect. Trop. Dis 6:e1989
    [Google Scholar]
  94. 94. 
    Murdock CC, Blanford S, Hughes GL, Rasgon JL, Thomas MB 2014. Temperature alters Plasmodium blocking by Wolbachia. Sci. Rep 4:3932
    [Google Scholar]
  95. 95. 
    Murray JV, Jansen CC, De Barro P 2016. Risk associated with the release of Wolbachia-infected Aedes aegypti mosquitoes into the environment in an effort to control dengue. Front. Public Health 4:43
    [Google Scholar]
  96. 96. 
    Narita S, Nomura M, Kageyama D 2007. Naturally occurring single and double infection with Wolbachia strains in the butterfly Eurema hecabe: transmission efficiencies and population density dynamics of each Wolbachia strain. FEMS Microbiol. Ecol. 61:235–45
    [Google Scholar]
  97. 97. 
    National Environment Agency 2018. Wolbachia–Aedes mosquito suppression strategy. Rep., Natl. Environ. Agency, Singapore. www.nea.gov.sg/corporate-functions/resources/research/wolbachia-aedes-mosquito-suppression-strategy
    [Google Scholar]
  98. 98. 
    Nguyen TH, Le Nguyen H, Nguyen TY, Vu SN, Tran ND et al. 2015. Field evaluation of the establishment potential of wMelPop Wolbachia in Australia and Vietnam for dengue control. Parasites Vectors 8:563
    [Google Scholar]
  99. 99. 
    O'Connor L, Plichart C, Sang AC, Brelsfoard CL, Bossin HC, Dobson SL 2012. Open release of male mosquitoes infected with a Wolbachia biopesticide: field performance and infection containment. PLOS Neglect. Trop. Dis. 6:e1797
    [Google Scholar]
  100. 100. 
    O'Neill SL, Giordano R, Colbert A, Karr TL, Robertson HM 1992. 16S rRNA phylogenetic analysis of the bacterial endosymbionts associated with cytoplasmic incompatibility in insects. PNAS 89:2699–702
    [Google Scholar]
  101. 101. 
    O'Neill SL, Hoffmann AA, Werren JH 1997. Influential Passengers: Inherited Microorganisms and Arthropod Reproduction Oxford, UK: Oxford Univ. Press
  102. 102. 
    O'Neill SL, Ryan PA, Turley AP, Wilson G, Retzki K et al. 2018. Scaled deployment of Wolbachia to protect the community from dengue and other Aedes transmitted arboviruses. Gates Open Res 2:36
    [Google Scholar]
  103. 103. 
    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 simulans. Appl. Environ. Microbiol 78:6922–29
    [Google Scholar]
  104. 104. 
    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
    [Google Scholar]
  105. 105. 
    Paris V, Cottingham E, Ross PA, Axford JK, Hoffmann AA 2018. Effects of alternative blood sources on Wolbachia infected Aedes aegypti females within and across generations. Insects 9:E140
    [Google Scholar]
  106. 106. 
    Ponton F, Wilson K, Holmes A, Raubenheimer D, Robinson KL, Simpson SJ 2015. Macronutrients mediate the functional relationship between Drosophila and Wolbachia. Proc. R. Soc. B 282:20142029
    [Google Scholar]
  107. 107. 
    Rašić G, Endersby EM, Williams C, Hoffmann AA 2014. Using Wolbachia-based releases for suppression of Aedes mosquitoes: insights from genetic data and population simulations. Ecol. Appl. 241226–34
  108. 108. 
    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 1641027–34
  109. 109. 
    Richardson KM, Griffin PC, Lee SF, Ross PA, Endersby-Harshman NM et al. 2018. A Wolbachia infection from Drosophila that causes cytoplasmic incompatibility despite low prevalence and densities in males. Heredity 122428–40
  110. 110. 
    Richardson MF, Weinert LA, Welch JJ, Linheiro RS, Magwire MM et al. 2012. Population genomics of the Wolbachia endosymbiont in Drosophila melanogaster. PLOS Genet 8e1003129
  111. 111. 
    Ritchie SA. 2018. Wolbachia and the near cessation of dengue outbreaks in Northern Australia despite continued dengue importations via travellers. J. Travel Med. 25tay084
  112. 112. 
    Ritchie SA, Montgomery BL, Hoffmann AA 2013. Novel estimates of Aedes aegypti (Diptera: Culicidae) population size and adult survival based on Wolbachia releases. J. Med. Entomol. 50624–31
  113. 113. 
    Ritchie SA, Townsend M, Paton CJ, Callahan AG, Hoffmann AA 2015. Application of wMelPop Wolbachia strain to crash local populations of Aedes aegypti. PLOS Neglect. Trop. Dis 9e0003930
  114. 114. 
    Ritchie SA, van den Hurk AF, Smout MJ, Staunton KM, Hoffmann AA 2018. Mission accomplished? We need a guide to the ‘post release’ world of Wolbachia for Aedes-borne disease control. Trends Parasitol 34217–26
  115. 115. 
    Ross PA, Endersby NM, Hoffmann AA 2016. Costs of three Wolbachia infections on the survival of Aedes aegypti larvae under starvation conditions. PLOS Neglect. Trop. Dis. 10e0004320
  116. 116. 
    Ross PA, Endersby-Harshman NM, Hoffmann AA 2019. A comprehensive assessment of inbreeding and laboratory adaptation in Aedes aegypti mosquitoes. Evol. Appl. 12572–86
  117. 117. 
    Ross PA, Ritchie SA, Axford JK, Hoffmann AA 2019. Loss of cytoplasmic incompatibility in Wolbachia-infected Aedes aegypti under field conditions. PLOS Neglect. Trop. Dis. 13e0007357
  118. 118. 
    Ross PA, Wiwatanaratanabutr I, Axford JK, White VL, Endersby-Harshman NM, Hoffmann AA 2017. Wolbachia infections in Aedes aegypti differ markedly in their response to cyclical heat stress. PLOS Pathog 13e1006006
  119. 119. 
    Russell RC, Webb CE, Williams CR, Ritchie SA 2005. Mark–release–recapture study to measure dispersal of the mosquito Aedes aegypti in Cairns, Queensland, Australia. Med. Vet. Entomol. 19451–57
  120. 120. 
    Sazama EJ, Bosch MJ, Shouldis CS, Ouellette SP, Wesner JS 2017. Incidence of Wolbachia in aquatic insects. Ecol. Evol. 71165–69
  121. 121. 
    Sazama EJ, Ouellette SP, Wesner JS 2019. Bacterial endosymbionts are common among, but not necessarily within, insect species. Environ. Entomol. 48127–33
  122. 122. 
    Schmidt TL, Barton NH, Rašić G, Turley AP, Montgomery BL et al. 2017. Local introduction and heterogeneous spatial spread of dengue-suppressing Wolbachia through an urban population of Aedes aegypti. PLOS Biol 15e2001894
  123. 123. 
    Schmidt TL, Filipović I, Hoffmann AA, Rašić G 2018. Fine-scale landscape genomics helps explain the slow spatial spread of Wolbachia through the Aedes aegypti population in Cairns, Australia. Heredity 120386–95
  124. 124. 
    Schneider DI, Ehrman L, Engl T, Kaltenpoth M, Hua-Van A et al. 2019. Symbiont-driven male mating success in the Neotropical Drosophila paulistorum superspecies. Behav. Genet. 4983–98
  125. 125. 
    Segoli M, Hoffmann AA, Lloyd J, Omodei GJ, Ritchie SA 2014. The effect of virus-blocking Wolbachia on male competitiveness of the dengue vector mosquito, Aedes aegypti. PLOS Neglect. Trop. Dis. 8e3294
  126. 126. 
    Shi M, White VL, Schlub T, Eden JS, Hoffmann AA, Holmes EC 2018. No detectable effect of Wolbachia wMel on the prevalence and abundance of the RNA virome of Drosophila melanogaster. Proc. R. Soc. B 28520181165
  127. 127. 
    Simhadri RK, Fast EM, Guo R, Schultz MJ, Vaisman N et al. 2017. The gut commensal microbiome of Drosophila melanogaster is modified by the endosymbiont Wolbachia. mSphere 216
  128. 128. 
    Smith C. 2019. Marlon Brando's private island is now being used as a living laboratory for mosquito eradication. ABC News Feb. 22. https://www.abc.net.au/news/science/2019-02-23/marlon-brando-resort-mosquito-eradication-french-polynesia/10825010
  129. 129. 
    Soma DD, Maïga H, Mamai W, Bimbile-Somda NS, Venter N et al. 2017. Does mosquito mass-rearing produce an inferior mosquito?. Malar. J. 16357
  130. 130. 
    Sumi T, Miura K, Miyatake T 2017. Wolbachia density changes seasonally amongst populations of the pale grass blue butterfly, Zizeeria maha (Lepidoptera: Lycaenidae). PLOS ONE 12e0175373
  131. 131. 
    Teixeira L, Ferreira A, Ashburner M 2008. The bacterial symbiont Wolbachia induces resistance to RNA viral infections in Drosophila melanogaster. PLOS Biol 62753–63
  132. 132. 
    Terradas G, McGraw EA. 2017. Wolbachia-mediated virus blocking in the mosquito vector Aedes aegypti. Curr. Opin. Insect Sci 2237–44
  133. 133. 
    Toews DP, Brelsford A. 2012. The biogeography of mitochondrial and nuclear discordance in animals. Mol. Ecol. 213907–30
  134. 134. 
    Toju H, Fukatsu T. 2011. Diversity and infection prevalence of endosymbionts in natural populations of the chestnut weevil: relevance of local climate and host plants. Mol. Ecol. 20853–68
  135. 135. 
    Toomey ME, Panaram K, Fast EM, Beatty C, Frydman HM 2013. Evolutionarily conserved Wolbachia-encoded factors control pattern of stem-cell niche tropism in Drosophila ovaries and favor infection. PNAS 11010788–93
  136. 136. 
    Tortosa P, Charlat S, Labbe P, Dehecq J-S, Barre H, Weill M 2010. Wolbachia age-sex-specific density in Aedes albopictus: a host evolutionary response to cytoplasmic incompatibility?. PLOS ONE 5e9700
  137. 137. 
    Turelli M. 1994. Evolution of incompatibility-inducing microbes and their hosts. Evolution 481500–13
  138. 138. 
    Turelli M. 2010. Cytoplasmic incompatibility in populations with overlapping generations. Evolution 64232–41
  139. 139. 
    Turelli M, Barton NH. 2017. Deploying dengue-suppressing Wolbachia: Robust models predict slow but effective spatial spread in Aedes aegypti. Theor. Popul. Biol 11545–60
  140. 140. 
    Turelli M, Cooper BS, Richardson KM, Ginsberg PS, Peckenpaugh B et al. 2018. Rapid global spread of wRi-like Wolbachia across multiple Drosophila. Curr. Biol 28963–71
  141. 141. 
    Turelli M, Hoffmann AA. 1991. Rapid spread of an inherited incompatibility factor in California Drosophila. Nature 353440–42
  142. 142. 
    Turelli M, Hoffmann AA. 1995. Cytoplasmic incompatibility in Drosophila simulans: dynamics and parameter estimates from natural populations. Genetics 1401319–38
  143. 143. 
    Turelli M, Hoffmann AA, McKechnie SW 1992. Dynamics of cytoplasmic incompatibility and mtDNA variation in natural Drosophila simulans populations. Genetics 132713–23
  144. 144. 
    Vala F, Egas M, Breeuwer JAJ, Sabelis MW 2004. Wolbachia affects oviposition and mating behaviour of its spider mite host. J. Evol. Biol. 17692–700
  145. 145. 
    Veneti Z, Zabalou S, Papafotiou G, Paraskevopoulos C, Pattas S et al. 2012. Loss of reproductive parasitism following transfer of male-killing Wolbachia to Drosophila melanogaster and Drosophila simulans. Heredity 109306–12
  146. 146. 
    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 476450–53
  147. 147. 
    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 5997–1005
  148. 148. 
    Weinert LA, Araujo-Jnr EV, Ahmed MZ, Welch JJ 2015. The incidence of bacterial endosymbionts in terrestrial arthropods. Proc. R. Soc. B 28220150249
  149. 149. 
    Wilson AJ, Harrup LE. 2018. Reproducibility and relevance in insect-arbovirus infection studies. Curr. Opin. Insect Sci. 28105–12
  150. 150. 
    Woodford L, Bianco G, Ivanova Y, Dale M, Elmer K et al. 2018. Vector species-specific association between natural Wolbachia infections and avian malaria in black fly populations. Sci. Rep. 84188
  151. 151. 
    Xi ZY, Khoo CCH, Dobson SL 2005. Wolbachia establishment and invasion in an Aedes aegypti laboratory population. Science 310326–28
  152. 152. 
    Xue L, Fang X, Hyman JM 2018. Comparing the effectiveness of different strains of Wolbachia for controlling chikungunya, dengue fever, and zika. PLOS Neglect. Trop. Dis. 12e0006666
  153. 153. 
    Yeap HL, Axford JK, Popovici J, Endersby NM, Iturbe-Ormaetxe I et al. 2014. Assessing quality of life-shortening Wolbachia-infected Aedes aegypti mosquitoes in the field based on capture rates and morphometric assessments. Parasites Vectors 758
  154. 154. 
    Yeap HL, Mee P, Walker T, Weeks AR, O'Neill SL et al. 2011. Dynamics of the “popcorn” Wolbachia infection in outbred Aedes aegypti informs prospects for mosquito vector control. Genetics 187583–95
  155. 155. 
    Zhang DJ, Lees RS, Xi ZY, Bourtzis K, Gilles JRL 2016. Combining the sterile insect technique with the incompatible insect technique: III-robust mating competitiveness of irradiated triple Wolbachia-infected Aedes albopictus males under semi-field conditions. PLOS ONE 11e0151864
  156. 156. 
    Zhang DJ, Li YJ, Sun Q, Zheng XY, Gilles JRL et al. 2018. Establishment of a medium-scale mosquito facility: tests on mass production cages for Aedes albopictus (Diptera: Culicidae). Parasites Vectors 11189
  157. 157. 
    Zheng X, Zhang D, Li Y, Yang C, Wu Y et al. 2019. Incompatible and sterile insect techniques combined eliminate mosquitoes. . Nature 57256–-61
  158. 158. 
    Zug R, Hammerstein P. 2015. Bad guys turned nice? A critical assessment of Wolbachia mutualisms in arthropod hosts. Biol. Rev. 9089–111

Data & Media loading...

Supplemental Material

Supplementary Data

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error