Attempts to use breeding approaches in Aedes aegypti to create lines with distinct and stable relative Wolbachia densities.
Journal
Heredity
ISSN: 1365-2540
Titre abrégé: Heredity (Edinb)
Pays: England
ID NLM: 0373007
Informations de publication
Date de publication:
10 2022
10 2022
Historique:
received:
22
04
2022
accepted:
17
06
2022
revised:
13
06
2022
pubmed:
23
7
2022
medline:
1
10
2022
entrez:
22
7
2022
Statut:
ppublish
Résumé
Wolbachia is an insect endosymbiont being used for biological control in the mosquito Aedes aegypti because it causes cytoplasmic incompatibility (CI) and limits viral replication of dengue, chikungunya, and Zika viruses. While the genetic mechanism of pathogen blocking (PB) is not fully understood, the strength of both CI and PB are positively correlated with Wolbachia densities in the host. Wolbachia densities are determined by a combination of Wolbachia strain and insect genotype, as well as interactions with the environment. We employed both artificial selection and inbreeding with the goal of creating lines of Ae. aegypti with heritable and distinct Wolbachia densities so that we might better dissect the mechanism underlying PB. We were unable to shift the mean relative Wolbachia density in Ae. aegypti lines by either strategy, with relative densities instead tending to cycle over a narrow range. In lieu of this, we used Wolbachia densities in mosquito legs as predictors of relative densities in the remaining individual's carcass. Because we worked with outbred mosquitoes, our findings indicate either a lack of genetic variation in the mosquito for controlling relative density, natural selection against extreme densities, or a predominance of environmental factors affecting densities. Our study reveals that there are moderating forces acting on relative Wolbachia densities that may help to stabilize density phenotypes post field release. We also show a means to accurately bin vector carcasses into high and low categories for non-DNA omics-based studies of Wolbachia-mediated traits.
Identifiants
pubmed: 35869302
doi: 10.1038/s41437-022-00553-x
pii: 10.1038/s41437-022-00553-x
pmc: PMC9519544
doi:
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
215-224Subventions
Organisme : NIAID NIH HHS
ID : R01 AI151166
Pays : United States
Informations de copyright
© 2022. The Author(s).
Références
Ahantarig A, Trinachartvanit W, Kittayapong P (2008) Relative Wolbachia density of field-collected Aedes albopictus mosquitoes in Thailand. J Vector Ecol 33:173–177
pubmed: 18697321
doi: 10.3376/1081-1710(2008)33[173:RWDOFA]2.0.CO;2
Ahmad NA, Mancini MV, Ant TH, Martinez J, Kamarul GMR, Nazni WA et al. (2021) Wolbachia strain wAlbB maintains high density and dengue inhibition following introduction into a field population of Aedes aegypti. Philos Trans R Soc Lond B Biol Sci 376:20190809
pubmed: 33357050
doi: 10.1098/rstb.2019.0809
Ahmed AM, Baggott SL, Maingon R, Hurd H (2002) The costs of mounting an immune response are reflected in the reproductive fitness of the mosquito Anopheles gambiae. Oikos 97:371–377
doi: 10.1034/j.1600-0706.2002.970307.x
Amuzu HE, McGraw EA (2016) Wolbachia-based dengue virus inhibition is not tissue-specific in Aedes aegypti. PLOS Negl Trop Dis 10:1–18
doi: 10.1371/journal.pntd.0005145
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 14:1–19
doi: 10.1371/journal.ppat.1006815
Axford JK, Ross PA, Yeap HL, Callahan AG, Hoffmann AA (2016) Fitness of wAlbB Wolbachia infection in Aedes aegypti: Parameter estimates in an outcrossed background and potential for population invasion. Am J Trop Med Hyg 94:507–516
pubmed: 26711515
pmcid: 4775882
doi: 10.4269/ajtmh.15-0608
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 6:1–10
doi: 10.1371/journal.ppat.1000833
Bian G, Zhou G, Lu P, Xi Z (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 Negl Trop Dis 7:e2250
pubmed: 23755311
pmcid: 3675004
doi: 10.1371/journal.pntd.0002250
Bonizzoni M, Dunn WA, Campbell CL, Olson KE, Marinotti O, James AA (2012) Complex modulation of the Aedes aegypti transcriptome in response to dengue virus infection. PLOS One 7:e50512
pubmed: 23209765
pmcid: 3507784
doi: 10.1371/journal.pone.0050512
Chouin-Carneiro T, Ant TH, Herd C, Louis F, Failloux AB, Sinkins SP (2020) Wolbachia strain wAlbA blocks Zika virus transmission in Aedes aegypti. Med Vet Entomol 34:116–119
pubmed: 31120156
doi: 10.1111/mve.12384
Chrostek E, Marialva MSP, Esteves SS, Weinert LA, Martinez J, Jiggins FM et al. (2013) Wolbachia variants induce differential protection to viruses in Drosophila melanogaster: a phenotypic and phylogenomic analysis. PLOS Genet 9:e1003896
pubmed: 24348259
pmcid: 3861217
doi: 10.1371/journal.pgen.1003896
Chrostek E, Teixeira L (2015) Mutualism breakdown by amplification of Wolbachia genes. PLOS Biol 13:1002065
doi: 10.1371/journal.pbio.1002065
Correa CC, Ballard JWO (2012) Wolbachia gonadal density in female and male Drosophila vary with laboratory adaptation and respond differently to physiological and environmental challenges. J Invertebr Pathol 111:197–204
pubmed: 22903036
doi: 10.1016/j.jip.2012.08.003
Dutra HLC, Rocha MN, Dias FBS, Mansur SB, Caragata EP, Moreira LA (2016) Wolbachia blocks currently circulating Zika virus isolates in Brazilian Aedes aegypti mosquitoes. Cell Host Microbe 19:771–774
pubmed: 27156023
pmcid: 4906366
doi: 10.1016/j.chom.2016.04.021
Dutton TJ, Sinkins SP (2004) Strain-specific quantification of Wolbachia density in Aedes albopictus and effects of larval rearing conditions. Insect Mol Biol 13:317–322
pubmed: 15157232
doi: 10.1111/j.0962-1075.2004.00490.x
Emerson KJ, Glaser RL (2017) Cytonuclear epistasis controls the density of symbiont Wolbachia pipientis in nongonadal tissues of mosquito Culex quinquefasciatus. G3 Genes Genomes Genet 7:2627–2635
Flores HA, O’Neill SL (2018) Controlling vector-borne diseases by releasing modified mosquitoes. Nat Rev Microbiol 16:508–518
pubmed: 29777177
pmcid: 7612058
doi: 10.1038/s41579-018-0025-0
Ford SA, Albert I, Allen SL, Chenoweth SF, Jones M, Koh C et al. (2020) Artificial selection finds new hypotheses for the mechanism of Wolbachia-mediated dengue blocking in mosquitoes. Front Microbiol 11:1456
pubmed: 32733407
pmcid: 7358395
doi: 10.3389/fmicb.2020.01456
Ford SA, Allen SL, Ohm JR, Sigle LT, Sebastian A, Albert I et al. (2019) Selection on Aedes aegypti alters Wolbachia-mediated dengue virus blocking and fitness. Nat Microbiol 4:1832–1839
pubmed: 31451771
pmcid: 6990461
doi: 10.1038/s41564-019-0533-3
Fraser JE, O'Donnell TB, Duyvestyn JM, O'Neill SL, Simmons CP, Flores HA (2020) Novel phenotype of Wolbachia strain wPip in Aedes aegypti challenges assumptions on mechanisms of Wolbachia-mediated dengue virus inhibition. PLOS Pathog 16:e1008410
pubmed: 32726353
pmcid: 7416964
doi: 10.1371/journal.ppat.1008410
Frentiu FD, Zakir T, Walker T, Popovici J, Pyke AT, van den Hurk A et al. (2014) Limited dengue virus replication in field-collected Aedes aegypti mosquitoes infected with Wolbachia. PLOS Negl Trop Dis 8:e2688
pubmed: 24587459
pmcid: 3930499
doi: 10.1371/journal.pntd.0002688
Geoghegan V, Stainton K, Rainey SM, Ant TH, Dowle AA, Larson T et al. (2017) Perturbed cholesterol and vesicular trafficking associated with dengue blocking in Wolbachia-infected Aedes aegypti cells. Nat Commun 8:1–10
doi: 10.1038/s41467-017-00610-8
Gu X, Ross PA, Rodriguez-Andres J, Robinson KL, Yang Q, Lau M-J et al. (2022) A wMel Wolbachia variant in Aedes aegypti from field‐collected Drosophila melanogaster with increased phenotypic stability under heat stress. Environ Microbiol 24:2119–2135
pubmed: 35319146
doi: 10.1111/1462-2920.15966
Heaton NS, Perera R, Berger KL, Khadka S, LaCount DJ, Kuhn RJ et al. (2010) Dengue virus nonstructural protein 3 redistributes fatty acid synthase to sites of viral replication and increases cellular fatty acid synthesis. Proc Natl Acad Sci USA 107:17345–17350
pubmed: 20855599
pmcid: 2951450
doi: 10.1073/pnas.1010811107
Hedges LM, Brownlie JC, O’Neill SL, Johnson KN (2008) Wolbachia and virus protection in insects. Science 322:702
pubmed: 18974344
doi: 10.1126/science.1162418
Hien NT, Anh DD, Le NH, Yen NT, Phong TV, Nam VS et al. (2022) Environmental factors influence the local establishment of Wolbachia in Aedes aegypti mosquitoes in two small communities in central Vietnam. Gates Open Res 5:147
pubmed: 35602266
pmcid: 9098883
doi: 10.12688/gatesopenres.13347.2
Hoffmann AA, Iturbe-Ormaetxe I, Callahan AG, Phillips BL, Billington K, Axford JK et al. (2014) Stability of the wMel Wolbachia infection following invasion into Aedes aegypti populations. PLOS Negl Trop Dis 8:e3115
pubmed: 25211492
pmcid: 4161343
doi: 10.1371/journal.pntd.0003115
Hoffmann AA, Montgomery BL, Popovici J, Iturbe-Ormaetxe I, Johnson PH, Muzzi F et al. (2011) Successful establishment of Wolbachia in Aedes populations to suppress dengue transmission. Nature 476:454–459
pubmed: 21866160
doi: 10.1038/nature10356
Ikeda T, Ishikawa H, Sasaki T (2003) Infection density of Wolbachia and level of cytoplasmic incompatibility in the Mediterranean flour moth, Ephestia kuehniella. J Invertebr Pathol 84:1–5
pubmed: 13678706
doi: 10.1016/S0022-2011(03)00106-X
Iturbe-Ormaetxe I, Walker T, O’Neill SL (2011) Wolbachia and the biological control of mosquito-borne disease. EMBO Rep 12:508–518
pubmed: 21546911
pmcid: 3128286
doi: 10.1038/embor.2011.84
Joubert DA, Walker T, Carrington LB, De Bruyne JT, Kien DHT, Hoang NLT et al. (2016) Establishment of a Wolbachia superinfection in Aedes aegypti mosquitoes as a potential approach for future resistance management. PLOS Pathog 12:1–19
doi: 10.1371/journal.ppat.1005434
Kabouridis PS, Janzen J, Magee AL, Ley SC (2000) Cholesterol depletion disrupts lipid rafts and modulates the activity of multiple signaling pathways in T lymphocytes. Eur J Immunol 30:954–963
pubmed: 10741414
doi: 10.1002/1521-4141(200003)30:3<954::AID-IMMU954>3.0.CO;2-Y
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
pubmed: 19797660
pmcid: 2867033
doi: 10.1126/science.1177531
Kondo N, Shimada M, Fukatsu T (2005) Infection density of Wolbachia endosymbiont affected by co-infection and host genotype. Biol Lett 1:488–491
pubmed: 17148240
pmcid: 1626364
doi: 10.1098/rsbl.2005.0340
Kraemer MUG, Reiner RC, Brady OJ, Messina JP, Gilbert M, Pigott DM et al. (2019) Past and future spread of the arbovirus vectors Aedes aegypti and Aedes albopictus. Nat Microbiol 4:854–863
pubmed: 30833735
pmcid: 6522366
doi: 10.1038/s41564-019-0376-y
Lindsey ARI, Bhattacharya T, Newton ILG, Hardy RW (2018) Conflict in the intracellular lives of endosymbionts and viruses: A mechanistic look at Wolbachia-mediated pathogen-blocking. Viruses 10:141
pmcid: 5923435
doi: 10.3390/v10040141
Liu XC, Li ZX (2021) Transmission of the wMel Wolbachia strain is modulated by its titre and by immune genes in Drosophila melanogaster (Wolbachia density and transmission). J Invertebr Pathol 181:107591
pubmed: 33882275
doi: 10.1016/j.jip.2021.107591
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25:402–408
pubmed: 11846609
doi: 10.1006/meth.2001.1262
Madhav M, Brown G, Morgan JAT, Asgari S, McGraw EA, James P (2020) Transinfection of buffalo flies (Haematobia irritans exigua) with Wolbachia and effect on host biology. Parasit Vectors 13:296
pubmed: 32522243
pmcid: 7285521
doi: 10.1186/s13071-020-04161-8
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 USA 99:2918–2923
pubmed: 11880639
pmcid: 122448
doi: 10.1073/pnas.052466499
McMeniman CJ, Lane RV, Cass BN, Fong AWC, Sidhu M, Wang YF et al. (2009) Stable introduction of a life-shortening Wolbachia infection into the mosquito Aedes aegypti. Science 323:141–144
pubmed: 19119237
doi: 10.1126/science.1165326
Mejia AJ, Dutra HLC, Jones MJ, Perera R, McGraw EA (2022) Cross-tissue and generation predictability of relative Wolbachia densities in the mosquito Aedes aegypti. Parasites Vectors 15:1–10
doi: 10.1186/s13071-022-05231-9
Merle H, Donnio A, Jean-Charles A, Guyomarch J, Hage R, Najioullah F et al. (2018) Ocular manifestations of emerging arboviruses: dengue fever, chikungunya, Zika virus, West Nile virus, and Yellow Fever. J Fr Ophtalmol 41:e235–e243
pubmed: 29929827
doi: 10.1016/j.jfo.2018.05.002
Miller WJ, Ehrman L, Schneider D (2010) Infectious speciation revisited: impact of symbiont-depletion on female fitness and mating behavior of Drosophila paulistorum. PLOS Pathog 6:e1001214
pubmed: 21151959
pmcid: 2996333
doi: 10.1371/journal.ppat.1001214
Min KT, Benzer S (1997) Wolbachia, normally a symbiont of Drosophila, can be virulent, causing degeneration and early death. Proc Natl Acad Sci USA 94:10792–10796
pubmed: 9380712
pmcid: 23488
doi: 10.1073/pnas.94.20.10792
Moreira LA, Iturbe-Ormaetxe I, Jeffery JA, Lu G, Pyke AT, Hedges LM et al. (2009) A Wolbachia symbiont in Aedes aegypti limits infection with dengue, chikungunya, and Plasmodium. Cell 139:1268–1278
pubmed: 20064373
doi: 10.1016/j.cell.2009.11.042
Mouton L, Henri H, Bouletreau M, Vavre F (2003) Strain-specific regulation of intracellular Wolbachia density in multiply infected insects. Mol Ecol 12:3459–3465
pubmed: 14629360
doi: 10.1046/j.1365-294X.2003.02015.x
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
pubmed: 17251124
pmcid: 2375926
doi: 10.1098/rsbl.2006.0590
Nazni WA, Hoffmann AA, NoorAfizah A, Cheong YL, Mancini MV, Golding N et al. (2019) Establishment of Wolbachia strain wAlbB in Malaysian populations of Aedes aegypti for dengue control. Curr Biol 29:4241–4248.e5
pubmed: 31761702
pmcid: 6926472
doi: 10.1016/j.cub.2019.11.007
Newton ILG, Savytskyy O, Sheehan KB (2015) Wolbachia utilize host actin for efficient maternal transmission in Drosophila melanogaster. PLOS Pathog 11:e1004798
pubmed: 25906062
pmcid: 4408098
doi: 10.1371/journal.ppat.1004798
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 78:6922–6929
pubmed: 22843518
pmcid: 3457512
doi: 10.1128/AEM.01727-12
Pan X, Zhou G, Wu J, Bian G, Lu P, Raikhel AS et al. (2012) Wolbachia induces reactive oxygen species (ROS)-dependent activation of the Toll pathway to control dengue virus in the mosquito Aedes aegypti. Proc Natl Acad Sci USA 109:E23
pubmed: 22123956
doi: 10.1073/pnas.1116932108
Pinto SB, Riback TIS, Sylvestre G, Costa G, Peixoto J, Dias FBS et al. (2021) Effectiveness of Wolbachia-infected mosquito deployments in reducing the incidence of dengue and other Aedes-borne diseases in Niterói, Brazil: a quasi-experimental study. PLOS Negl Trop Dis 15:e0009556
pubmed: 34252106
pmcid: 8297942
doi: 10.1371/journal.pntd.0009556
Rainey SM, Martinez J, McFarlane M, Juneja P, Sarkies P, Lulla A et al. (2016) Wolbachia blocks viral genome replication early in infection without a transcriptional response by the endosymbiont or host small RNA pathways. PLOS Pathog 12:1–22
doi: 10.1371/journal.ppat.1005536
Rancès E, Ye YH, Woolfit M, McGraw EA, O’Neill SL (2012) The relative importance of innate immune priming in Wolbachia-mediated dengue interference. PLOS Pathog 8:e1002548
pubmed: 22383881
pmcid: 3285598
doi: 10.1371/journal.ppat.1002548
Ross PA, Robinson KL, Yang Q, Callahan AG, Schmidt TL, Axford JK et al. (2022) A decade of stability for wMel Wolbachia in natural Aedes aegypti populations. PLOS Pathog 18:e1010256
pubmed: 35196357
pmcid: 8901071
doi: 10.1371/journal.ppat.1010256
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 13:e1006006
pubmed: 28056065
pmcid: 5215852
doi: 10.1371/journal.ppat.1006006
Ryan PA, Turley AP, Wilson G, Hurst TP, Retzki K, Brown-Kenyon J et al. (2020) Establishment of wMel Wolbachia in Aedes aegypti mosquitoes and reduction of local dengue transmission in Cairns and surrounding locations in northern Queensland, Australia. Gates Open Res 3:1547
pubmed: 31667465
pmcid: 6801363
doi: 10.12688/gatesopenres.13061.2
Schwartz A, Koella JC (2004) The cost of immunity in the Yellow Fever mosquito, Aedes aegypti depends on immune activation. J Evol Biol 17:834–840
pubmed: 15271083
doi: 10.1111/j.1420-9101.2004.00720.x
Serbus LR, White PM, Silva JP, Rabe A, Teixeira L, Albertson R et al. (2015) The impact of host diet on Wolbachia titer in Drosophila. PLOS Pathog 11:1–25
Sim S, Ramirez JL, Dimopoulos G (2012) Dengue virus infection of the Aedes aegypti salivary gland and chemosensory apparatus induces genes that modulate infection and blood-feeding behavior. PLOS Pathog 8:e0004873
doi: 10.1371/journal.ppat.1002631
Souza-Neto JA, Powell JR, Bonizzoni M (2019) Aedes aegypti vector competence studies: a review. Infect Genet Evol 67:191–209
pubmed: 30465912
doi: 10.1016/j.meegid.2018.11.009
Teixeira L, Ferreira Á, Ashburner M (2008) The bacterial symbiont Wolbachia induces resistance to RNA viral infections in Drosophila melanogaster. PLOS Biol 6:2753–2763
doi: 10.1371/journal.pbio.1000002
Terradas G, Allen SL, Chenoweth SF, McGraw EA (2017) Family level variation in Wolbachia-mediated dengue virus blocking in Aedes aegypti. Parasites Vectors 10:1–12
doi: 10.1186/s13071-017-2589-3
Thannickal VJ, Fanburg BL (2000) Reactive oxygen species in cell signaling. Am J Physiol Lung Cell Mol Physiol 279:1005–1028
doi: 10.1152/ajplung.2000.279.6.L1005
Ulrich JN, Beier JC, Devine GJ, Hugo LE (2016) Heat sensitivity of wMel Wolbachia during Aedes aegypti development. PLOS Negl Trop Dis 10:e0004873
pubmed: 27459519
pmcid: 4961373
doi: 10.1371/journal.pntd.0004873
Utarini A, Indriani C, Ahmad RA, Tantowijoyo W, Arguni E, Ansari MR et al. (2021) Efficacy of Wolbachia-infected mosquito deployments for the control of dengue. N Engl J Med 384:2177–2186
pubmed: 34107180
pmcid: 8103655
doi: 10.1056/NEJMoa2030243
van den Hurk AF, Hall-Mendelin S, Pyke AT, Frentiu FD, McElroy K, Day A 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
pubmed: 23133693
pmcid: 3486898
doi: 10.1371/journal.pntd.0001892
Walker T, Johnson PH, Moreira LA, Iturbe-Ormaetxe I, Frentiu FD, McMeniman CJ et al. (2011) The wMel Wolbachia strain blocks dengue and invades caged Aedes aegypti populations. Nature 476:450–455
pubmed: 21866159
doi: 10.1038/nature10355
Werren JH (1997) Biology of Wolbachia. Annu Rev Entomol Vol 42:587–609
doi: 10.1146/annurev.ento.42.1.587
Werren JH, Baldo L, Clark ME (2008) Wolbachia: Master manipulators of invertebrate biology. Nat Rev Microbiol 6:741–751
pubmed: 18794912
doi: 10.1038/nrmicro1969
White PM, Serbus LR, Debec A, Codina A, Bray W, Guichet A et al. (2017) Reliance of Wolbachia on high rates of host proteolysis revealed by a genome-wide RNAi screen of Drosophila cells. Genetics 205:1473–1488
pubmed: 28159754
pmcid: 5378107
doi: 10.1534/genetics.116.198903
Wiwatanaratanabutr I, Kittayapong P (2009) Effects of crowding and temperature on Wolbachia infection density among life cycle stages of Aedes albopictus. J Invertebr Pathol 102:220–224
pubmed: 19686755
doi: 10.1016/j.jip.2009.08.009
Woolfit M, Iturbe-Ormaetxe I, Brownlie JC, Walker T, Riegler M, Seleznev A et al. (2013) Genomic evolution of the pathogenic Wolbachia strain, wMelPop. Genome Biol Evol 5:2189–2204
pubmed: 24190075
pmcid: 3845649
doi: 10.1093/gbe/evt169
Wu M, Sun LV, Vamathevan J, Riegler M, Deboy R, Brownlie JC et al. (2004) Phylogenomics of the reproductive parasite Wolbachia pipientis wMel: A streamlined genome overrun by mobile genetic elements. PLOS Biol 2:327–341
doi: 10.1371/journal.pbio.0020069
Xi Z, Dean JL, Khoo C, Dobson SL (2005) Generation of a novel Wolbachia infection in Aedes albopictus (Asian tiger mosquito) via embryonic microinjection. Insect Biochem Mol Biol 35:903–910
pubmed: 15944085
pmcid: 1410910
doi: 10.1016/j.ibmb.2005.03.015
Xi Z, Khoo CCH, Dobson SL (2005) Wolbachia establishment and invasion in an Aedes aegypti laboratory population. Science 310:326–8
pubmed: 16224027
doi: 10.1126/science.1117607
Xu J, Hopkins K, Sabin L, Yasunaga A, Subramanian H, Lamborn I et al. (2013) ERK signaling couples nutrient status to antiviral defense in the insect gut. Proc Natl Acad Sci USA 110:15025–15030
pubmed: 23980175
pmcid: 3773808
doi: 10.1073/pnas.1303193110
Ye YH, Woolfit M, Rancès E, O’Neill SL, McGraw EA (2013) Wolbachia-associated bacterial protection in the mosquito Aedes aegypti. PLOS Negl Trop Dis 7:e2362
pubmed: 23951381
pmcid: 3738474
doi: 10.1371/journal.pntd.0002362
Zug R, Hammerstein P (2015) Bad guys turned nice? A critical assessment of Wolbachia mutualisms in arthropod hosts. Biol Rev Camb Philos Soc 90:89–111
pubmed: 24618033
doi: 10.1111/brv.12098