Incompatible and sterile insect techniques combined eliminate mosquitoes.
Journal
Nature
ISSN: 1476-4687
Titre abrégé: Nature
Pays: England
ID NLM: 0410462
Informations de publication
Date de publication:
08 2019
08 2019
Historique:
received:
05
11
2018
accepted:
19
06
2019
pubmed:
19
7
2019
medline:
20
11
2019
entrez:
19
7
2019
Statut:
ppublish
Résumé
The radiation-based sterile insect technique (SIT) has successfully suppressed field populations of several insect pest species, but its effect on mosquito vector control has been limited. The related incompatible insect technique (IIT)-which uses sterilization caused by the maternally inherited endosymbiotic bacteria Wolbachia-is a promising alternative, but can be undermined by accidental release of females infected with the same Wolbachia strain as the released males. Here we show that combining incompatible and sterile insect techniques (IIT-SIT) enables near elimination of field populations of the world's most invasive mosquito species, Aedes albopictus. Millions of factory-reared adult males with an artificial triple-Wolbachia infection were released, with prior pupal irradiation of the released mosquitoes to prevent unintentionally released triply infected females from successfully reproducing in the field. This successful field trial demonstrates the feasibility of area-wide application of combined IIT-SIT for mosquito vector control.
Identifiants
pubmed: 31316207
doi: 10.1038/s41586-019-1407-9
pii: 10.1038/s41586-019-1407-9
doi:
Types de publication
Evaluation Study
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
56-61Commentaires et corrections
Type : CommentIn
Type : CommentIn
Type : CommentIn
Références
Dyck, V. A., Hendrichs, J. & Robinson, A. S. Sterile Insect Technique: Principles and Practice in Area-Wide Integrated Pest Management (Springer Netherlands, 2005).
Dame, D. A., Curtis, C. F., Benedict, M. Q., Robinson, A. S. & Knols, B. G. Historical applications of induced sterilisation in field populations of mosquitoes. Malar. J. 8 (Suppl 2), S2 (2009).
doi: 10.1186/1475-2875-8-S2-S2
Helinski, M. E., Parker, A. G. & Knols, B. G. Radiation biology of mosquitoes. Malar. J. 8 (Suppl 2), S6 (2009).
doi: 10.1186/1475-2875-8-S2-S6
Lees, R. S., Gilles, J. R., Hendrichs, J., Vreysen, M. J. & Bourtzis, K. Back to the future: the sterile insect technique against mosquito disease vectors. Curr. Opin. Insect Sci. 10, 156–162 (2015).
doi: 10.1016/j.cois.2015.05.011
Laven, H. Eradication of Culex pipiens fatigans through cytoplasmic incompatibility. Nature 216, 383–384 (1967).
doi: 10.1038/216383a0
LePage, D. P. et al. Prophage WO genes recapitulate and enhance Wolbachia-induced cytoplasmic incompatibility. Nature 543, 243–247 (2017).
doi: 10.1038/nature21391
Yen, J. H. & Barr, A. R. New hypothesis of the cause of cytoplasmic incompatibility in Culex pipiens L. Nature 232, 657–658 (1971).
doi: 10.1038/232657a0
Chambers, E. W., Hapairai, L., Peel, B. A., Bossin, H. & Dobson, S. L. Male mating competitiveness of a Wolbachia-introgressed Aedes polynesiensis strain under semi-field conditions. PLoS Negl. Trop. Dis. 5, e1271 (2011).
doi: 10.1371/journal.pntd.0001271
Zhang, D., Zheng, X., Xi, Z., Bourtzis, K. & Gilles, J. R. Combining the sterile insect technique with the incompatible insect technique: I impact of Wolbachia infection on the fitness of triple- and double-infected strains of Aedes albopictus. PLoS ONE 10, e0121126 (2015).
doi: 10.1371/journal.pone.0121126
Atyame, C. M. et al. Comparison of irradiation and Wolbachia based approaches for sterile-male strategies targeting Aedes albopictus. PLoS ONE 11, e0146834 (2016).
doi: 10.1371/journal.pone.0146834
Curtis, C. F. et al. 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, 181–190 (1982).
doi: 10.1111/j.1570-7458.1982.tb03133.x
Dobson, S. L., Fox, C. W. & Jiggins, F. M. The effect of Wolbachia-induced cytoplasmic incompatibility on host population size in natural and manipulated systems. Proc. R. Soc. Lond. B 269, 437–445 (2002).
doi: 10.1098/rspb.2001.1876
Pal, R. in The Use of Genetics in Insect Control (eds Pal, R. & Whitten, M. J.) 73–95 (Elsevier, 1974).
Curtis, C. F. Testing systems for the genetic control of mosquitoes. In Proceedings of XV International Congress of Entomology (eds White, D. & Packer, J. S.) 106–116 (1976)
Arunachalam, N. & Curtis, C. F. Integration of radiation with cytoplasmic incompatibility for genetic control in the Culex pipiens complex (Diptera: Culicidae). J. Med. Entomol. 22, 648–653 (1985).
doi: 10.1093/jmedent/22.6.648
Sharma, V. P., Subbarao, S. K., Adak, T. & Razdan, R. K. Integration of gamma irradiation and cytoplasmic incompatibility in Culex pipiens fatigans (Diptera: Culicidae). J. Med. Entomol. 15, 155–156 (1979).
doi: 10.1093/jmedent/15.2.155
Curtis, C. F. & Shahid, M. A. Radiation sterilization and cytoplasmic incompatibility in a “tropicalized” strain of the Culex pipiens complex (Diptera: Culicidae). J. Med. Entomol. 24, 273–274 (1987).
doi: 10.1093/jmedent/24.2.273
Mains, J. W., Brelsfoard, C. L., Rose, R. I. & Dobson, S. L. Female adult Aedes albopictus suppression by Wolbachia-infected male mosquitoes. Sci. Rep. 6, 33846 (2016).
doi: 10.1038/srep33846
Atyame, C. M. et al. Cytoplasmic incompatibility as a means of controlling Culex pipiens quinquefasciatus mosquito in the islands of the south-western Indian Ocean. PLoS Negl. Trop. Dis. 5, e1440 (2011).
doi: 10.1371/journal.pntd.0001440
Brelsfoard, C. L., Séchan, Y. & Dobson, S. L. Interspecific hybridization yields strategy for South Pacific filariasis vector elimination. PLoS Negl. Trop. Dis. 2, e129 (2008).
doi: 10.1371/journal.pntd.0000129
Xi, Z., Dean, J. L., Khoo, C. & Dobson, S. L. Generation of a novel Wolbachia infection in Aedes albopictus (Asian tiger mosquito) via embryonic microinjection. Insect Biochem. Mol. Biol. 35, 903–910 (2005).
doi: 10.1016/j.ibmb.2005.03.015
Xi, Z., Khoo, C. C. & Dobson, S. L. Wolbachia establishment and invasion in an Aedes aegypti laboratory population. Science 310, 326–328 (2005).
doi: 10.1126/science.1117607
Brelsfoard, C. L., St Clair, W. & Dobson, S. L. Integration of irradiation with cytoplasmic incompatibility to facilitate a lymphatic filariasis vector elimination approach. Parasit. Vectors 2, 38 (2009).
doi: 10.1186/1756-3305-2-38
Zhang, D., Lees, R. S., Xi, Z., Gilles, J. R. & Bourtzis, K. Combining the sterile insect technique with Wolbachia-based approaches: II a safer approach to Aedes albopictus population suppression programmes, designed to minimize the consequences of inadvertent female release. PLoS ONE 10, e0135194 (2015).
doi: 10.1371/journal.pone.0135194
Zhang, D., Lees, R. S., Xi, Z., Bourtzis, K. & Gilles, J. R. 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 11, e0151864 (2016).
doi: 10.1371/journal.pone.0151864
Bourtzis, K. et al. Harnessing mosquito-Wolbachia symbiosis for vector and disease control. Acta Trop. 132 (Suppl), S150–S163 (2014).
doi: 10.1016/j.actatropica.2013.11.004
Fonseca, D. M. et al. Area-wide management of Aedes albopictus. Part 2: gauging the efficacy of traditional integrated pest control measures against urban container mosquitoes. Pest Manag. Sci. 69, 1351–1361 (2013).
doi: 10.1002/ps.3511
Unlu, I., Farajollahi, A., Strickman, D. & Fonseca, D. M. Crouching tiger, hidden trouble: urban sources of Aedes albopictus (Diptera: Culicidae) refractory to source-reduction. PLoS ONE 8, e77999 (2013).
doi: 10.1371/journal.pone.0077999
Xi, Z., Khoo, C. C. & Dobson, S. L. Interspecific transfer of Wolbachia into the mosquito disease vector Aedes albopictus. Proc. R. Soc. Lond. B 273, 1317–1322 (2006).
doi: 10.1098/rspb.2005.3405
Fu, Y., Gavotte, L., Mercer, D. R. & Dobson, S. L. Artificial triple Wolbachia infection in Aedes albopictus yields a new pattern of unidirectional cytoplasmic incompatibility. Appl. Environ. Microbiol. 76, 5887–5891 (2010).
doi: 10.1128/AEM.00218-10
Blagrove, M. S., Arias-Goeta, C., Failloux, A. B. & Sinkins, S. P. Wolbachia strain wMel induces cytoplasmic incompatibility and blocks dengue transmission in Aedes albopictus. Proc. Natl Acad. Sci. USA 109, 255–260 (2012).
doi: 10.1073/pnas.1112021108
Suh, E., Mercer, D. R., Fu, Y. & Dobson, S. L. Pathogenicity of life-shortening Wolbachia in Aedes albopictus after transfer from Drosophila melanogaster. Appl. Environ. Microbiol. 75, 7783–7788 (2009).
doi: 10.1128/AEM.01331-09
Calvitti, M., Moretti, R., Lampazzi, E., Bellini, R. & Dobson, S. L. 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, 179–187 (2010).
pubmed: 20380298
Laven, H. & Aslamkhan, M. Control of Culex pipiens pipiens and C. p. fatigans with integrated genetical systems. Pak. J. Sci. 22, 303–312 (1970).
Bian, G., Xu, Y., Lu, P., Xie, Y. & Xi, Z. The endosymbiotic bacterium Wolbachia induces resistance to dengue virus in Aedes aegypti. PLoS Pathog. 6, e1000833 (2010).
doi: 10.1371/journal.ppat.1000833
Moreira, L. A. et al. A Wolbachia symbiont in Aedes aegypti limits infection with dengue, Chikungunya, and Plasmodium. Cell 139, 1268–1278 (2009).
doi: 10.1016/j.cell.2009.11.042
Dutra, H. L. et al. Wolbachia blocks currently circulating Zika virus isolates in Brazilian Aedes aegypti mosquitoes. Cell Host Microbe 19, 771–774 (2016).
doi: 10.1016/j.chom.2016.04.021
Aliota, M. T., Peinado, S. A., Velez, I. D. & Osorio, J. E. The wMel strain of Wolbachia reduces transmission of Zika virus by Aedes aegypti. Sci. Rep. 6, 28792 (2016).
doi: 10.1038/srep28792
Zhang, D. et al. Establishment of a medium-scale mosquito facility: optimization of the larval mass-rearing unit for Aedes albopictus (Diptera: Culicidae). Parasit. Vectors 10, 569 (2017).
doi: 10.1186/s13071-017-2511-z
Zhang, D. et al. Establishment of a medium-scale mosquito facility: tests on mass production cages for Aedes albopictus (Diptera: Culicidae). Parasit. Vectors 11, 189 (2018).
doi: 10.1186/s13071-018-2750-7
Li, Y. et al. Comparative evaluation of the efficiency of the BG-Sentinel trap, CDC light trap and Mosquito-oviposition trap for the surveillance of vector mosquitoes. Parasit. Vectors 9, 446 (2016).
doi: 10.1186/s13071-016-1724-x
Halasa, Y. A. et al. Quantifying the impact of mosquitoes on quality of life and enjoyment of yard and porch activities in New Jersey. PLoS ONE 9, e89221 (2014).
doi: 10.1371/journal.pone.0089221
Schmidt, T. L. et al. Genome-wide SNPs reveal the drivers of gene flow in an urban population of the Asian tiger mosquito, Aedes albopictus. PLoS Negl. Trop. Dis. 11, e0006009 (2017).
doi: 10.1371/journal.pntd.0006009
Sanogo, Y. O. & Dobson, S. L. Molecular discrimination of Wolbachia in the Culex pipiens complex: evidence for variable bacteriophage hyperparasitism. Insect Mol. Biol. 13, 365–369 (2004).
doi: 10.1111/j.0962-1075.2004.00498.x
Zhou, W., Rousset, F. & O’Neil, S. Phylogeny and PCR-based classification of Wolbachia strains using wsp gene sequences. Proc. R. Soc. Lond. B 265, 509–515 (1998).
doi: 10.1098/rspb.1998.0324
Heddi, A., Grenier, A. M., Khatchadourian, C., Charles, H. & Nardon, P. Four intracellular genomes direct weevil biology: nuclear, mitochondrial, principal endosymbiont, and Wolbachia. Proc. Natl Acad. Sci. USA 96, 6814–6819 (1999).
doi: 10.1073/pnas.96.12.6814
Das, S., Garver, L., Ramirez, J. R., Xi, Z. & Dimopoulos, G. Protocol for dengue infections in mosquitoes (A. aegypti) and infection phenotype determination. J. Vis. Exp. (5), PMC2557096 (2007).
Lu, P., Bian, G., Pan, X. & Xi, Z. Wolbachia induces density-dependent inhibition to dengue virus in mosquito cells. PLoS Negl. Trop. Dis. 6, e1754 (2012).
doi: 10.1371/journal.pntd.0001754
Zhang, M. et al. Quantitative analysis of replication and tropisms of Dengue virus type 2 in Aedes albopictus. Am. J. Trop. Med. Hyg. 83, 700–707 (2010).
doi: 10.4269/ajtmh.2010.10-0193
McGraw, E. A., Merritt, D. J., Droller, J. N. & O’Neill, S. L. Wolbachia-mediated sperm modification is dependent on the host genotype in Drosophila. Proc. R. Soc. Lond. B 268, 2565–2570 (2001).
doi: 10.1098/rspb.2001.1839
Bian, G., Zhou, G., Lu, P. & Xi, Z. 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 (2013).
doi: 10.1371/journal.pntd.0002250
Bian, G. et al. Wolbachia invades Anopheles stephensi populations and induces refractoriness to Plasmodium infection. Science 340, 748–751 (2013).
doi: 10.1126/science.1236192
Carvalho, D. O. et al. Mass production of genetically modified Aedes aegypti for field releases in Brazil. J. Vis. Exp. 3579, e3579 (2014). 10.3791/3579
Focks, D. A. An improved separator for the developmental stages, sexes, and species of mosquitoes (Diptera: Culicidae). J. Med. Entomol. 17, 567–568 (1980).
doi: 10.1093/jmedent/17.6.567
Methods in Anopheles research. Malaria Research and Reference Reagent Resource Center http://www.mr4.org/Publications/MethodsinAnophelesResearch.aspx (2014).
Fried, M. Determination of sterile-insect competitiveness. J. Econ. Entomol. 64, 869–872 (1971).
doi: 10.1093/jee/64.4.869