Abstract
The discovery of CRISPR-based gene editing and its application to homing-based gene drive has been greeted with excitement, for its potential to control mosquito-borne diseases on a wide scale, and concern, for the invasiveness and potential irreversibility of a release. At the same time, CRISPR-based gene editing has enabled a range of self-limiting gene drive systems to be engineered with much greater ease, including (1) threshold-dependent systems, which tend to spread only when introduced above a certain threshold population frequency, and (2) temporally self-limiting systems, which display transient drive activity before being eliminated by virtue of a fitness cost. As these CRISPR-based gene drive systems are yet to be field-tested, plenty of open questions remain to be addressed, and insights can be gained from precedents set by field trials of other novel genetics-based and biological control systems, such as trials of Wolbachia-transfected mosquitoes, intended for either population replacement or suppression, and trials of genetically sterile male mosquitoes, either using the RIDL system (release of insects carrying a dominant lethal gene) or irradiation. We discuss lessons learned from these field trials and implications for a phased exploration of gene drive technology, including homing-based gene drive, chromosomal translocations, and split gene drive as a system potentially suitable for an intermediate release.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Similar content being viewed by others
References
Akbari OS, Matzen KD, Marshall JM, Huang H, Ward CM et al (2013) A synthetic gene drive system for local, reversible modification and suppression of insect populations. Curr Biol 23:671–677
Alphey L (2002) Re-engineering the sterile insect technique. Insect Biochem Mol Biol 32:1243–1247
Benedict MQ, Robinson AS (2003) The first releases of transgenic mosquitoes: an argument for the sterile insect technique. Trends Parasitol 19:349–355
Benelli G, Jeffries CL, Walker T (2016) Biological control of mosquito vectors: past, present and future. Insects 7:52
Black WC, Alphey L, James AA (2011) Why RIDL is not SIT. Trends Parasitol 27:362–370
Buchman A, Ivy T, Marshall JM, Akbari OS, Hay BA (2018) Engineered reciprocal chromosome translocations drive high threshold, reversible population replacement in Drosophila. ACS Synth Biol 7:1359–1370
Carvalho DO, McKemey AR, Garziera L, Lacroix R, Donnelly CA et al (2015) Suppression of a field population of Aedes aegypti in Brazil by sustained release of transgenic male mosquitoes. PLoS Negl Trop Dis 9:e0003864
Champer J, Buchman A, Akbari OS (2016) Cheating evolution: engineering gene drives to manipulate the fate of wild populations. Nat Rev Genet 17:146–159
Crawford JE, Clarke DW, Criswell V, Desnoyer M, Cornel D et al (2020) Efficient production of male Wolbachia-infected Aedes aegypti mosquitoes enables large-scale suppression of wild mosquitoes. Nat Biotechnol 38:482–492
Curtis CF (1968) Possible use of translocations to fix desirable genes in insect pest populations. Nature 218:368–369
de Campos A, Hartley S, de Koning C, Lezaun J, Velho L (2017) Responsible innovation and political accountability: genetically modified mosquitoes in Brazil. J Respons Innov 4:5–23
Doudna JA, Charpentier E (2014) Genome editing. The new frontier of genome engineering with CRISPR-Cas9. Science 346:1258096
Enserink M (2010) GM mosquito trial alarms opponents, strains ties in Gates-funded project. Science 330:1030–1031
Enserink M (2011) GM mosquito release in Malaysia surprises opponents and scientists—again. Science Insider. Available online at: https://www.sciencemag.org/news/2011/01/gm-mosquito-release-malaysia-surprises-opponents-and-scientists-again
Fu G, Lees RS, Nimmo D, Aw D, Jin L et al (2010) Female-specific flightless phenotype for mosquito control. Proc Natl Acad Sci U S A 107:4550–4554
Galizi R, Doyle LA, Menichelli M, Bernardini F, Deredec A et al (2014) A synthetic sex ratio distortion system for the control of the human malaria mosquito. Nat Commun 5:3977
Gantz VM, Bier E (2015) The mutagenic chain reaction: a method for converting heterozygous to homozygous mutations. Science 348:442–444
Gantz VM, Bier E (2016) The dawn of active genetics. BioEssays 38:50–63
Gantz VM, Jasinskiene N, Tatarenkova O, Fazekas A, Macias VM et al (2015) Highly efficient Cas9-mediated gene drive for population modification of the malaria vector mosquito Anopheles stephensi. Proc Natl Acad Sci U S A 112:E6736–E6743
Garziera L, Pedrosa MC, de Souza FA, Gómez M, Moreira MB et al (2017) Effect of interruption of over-flooding releases of transgenic mosquitoes over wild populations of Aedes aegypti: two case studies in Brazil. Entomol Exp Appl 164:327–339
Gould F, Huang Y, Legros M, Lloyd AL (2008) A killer-rescue system for self-limiting gene drive of anti-pathogen constructs. Proc Biol Sci 275:2823–2829
Hammond A, Galizi R, Kyrou K, Simoni A, Siniscalchi C et al (2016) A CRISPR-Cas9 gene drive system targeting female reproduction in the malaria mosquito vector Anopheles gambiae. Nat Biotechnol 34:78–83
Hancock PA, Ritchie SA, Koenraadt CJM, Scott TW, Hoffmann AA et al (2019) Predicting the spatial dynamics of Wolbachia infections in Aedes aegypti arbovirus vector populations in heterogeneous landscapes. J Appl Ecol 56:1674–1686
Harris AF, Nimmo DD, McKemey AR, Kelly N, Scaife S et al (2011) Field performance of engineered male mosquitoes. Nat Biotechnol 29:1034–1037
Harris AF, McKemey AR, Nimmo DD, Curtis Z, Black I et al (2012) Successful suppression of a field mosquito population by sustained release of engineered male mosquitoes. Nat Biotechnol 30:828–830
Hendrichs J, Robinson A (2009) Sterile insect technique. In: Resh VH, Carde RT (eds) Encyclopedia of insects, 2nd edn. Academic Press, London
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
Hoffmann AA et al (2014) Stability of the wMel Wolbachia infection following invasion into Aedes aegypti populations. PLoS Negl Trop Dis 8:e3115
James S, Collins FH, Welkhoff PA, Emerson C, Godfray HCJ et al (2018) Pathway to deployment of gene drive mosquitoes as a potential biocontrol tool for elimination of malaria in sub-Saharan Africa: recommendations of a scientific working group. Am J Trop Med Hyg 98:1–49
Jiang J, Zhang L, Zhou X, Chen X, Huang G et al (2016) Induction of site-specific chromosomal translocations in embryonic stem cells by CRISPR/Cas9. Sci Rep 6:21918
Klassen W, Curtis CF (2005) History of the sterile insect technique. In: Dyck VA, Hendrichs J (eds) Sterile insect technique: principles and practice in area-wide integrated pest management. IAEA, Geneva, pp 3–36
Knipling EF (1955) Possibilities of insect control or eradication through the use of sexually sterile males. J Econ Entomol 48:459–462
Knipling EF (1968) The potential role of sterility for pest control. In: LeBrecque GC, Smith CN (eds) Principles of insect chemosterilization. Appleton-Century-Crofts, New York, pp 7–40
Kyrou K, Hammond AM, Galizi R, Kranjc N, Burt A et al (2018) A CRISPR-Cas9 gene drive targeting doublesex causes complete population suppression in caged Anopheles gambiae mosquitoes. Nat Biotechnol 36:1062–1066
Laven H (1967) Eradication of Culex pipiens fatigans through cytoplasmic incompatibility. Nature 216:383–384
Laven H, Cousserans J, Guille G (1972) Eradicating mosquitoes using translocations: a first field experiment. Nature 236:456–457
Lekomtsev S, Aligianni S, Lapao A, Bürckstümmer T (2016) Efficient generation and reversion of chromosomal translocations using CRISPR/Cas technology. BMC Genomics 17:739
LePage DP, Metcalf JA, Bordenstein SR, On J, Perlmutter JI et al (2017) Prophage WO genes recapitulate and enhance Wolbachia-induced cytoplasmic incompatibility. Nature 543:243–247
Li M, Yang T, Kandul NP, Bui M, Gamez S, Raban R, Bennett JB, Sánchez HM, Lanzaro GC, Schmidt H, Lee Y, Marshall JM, Akbari OS (2020) Development of a confinable gene-drive system in the human disease vector, Aedes aegypti. eLife 9:e51701
Lorimer N, Hallinan E, Rai KS (1972) Translocation homozygotes in the yellow fever mosquito, Aedes aegypti. J Hered 63:159–166
Lowe RE, Bailey DL, Dame DA, Savage KE, Kaiser PE (1980) Efficiency of techniques for the mass release of sterile male Anopheles albimanus. Am J Trop Med Hyg 29:695–703
Mains JW, Brelsfoard CL, Rose RI, Dobson SL (2016) Female adult Aedes albopictus suppression by Wolbachia-infected male mosquitoes. Sci Rep 6:33846
Marshall JM (2010) The Cartagena protocol and genetically modified mosquitoes. Nat Biotechnol 28:896–897
Marshall JM (2011) The Cartagena protocol in the context of recent releases of transgenic and Wolbachia-infected mosquitoes. Asia-Pacific J Mol Biol Biotechnol 19:93–100
Marshall JM, Akbari OS (2018) Can CRISPR-based gene drive be confined in the wild? A question for molecular and population biology. ACS Chem Biol 13:424–430
McNaughton D (2012) The importance of long-term social research in enabling participation and developing engagement strategies for new dengue control technologies. PLoS Negl Trop Dis 8:e1785
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
Murphy B, Jansen C, Murray J, De Barro P (2010) Risk analysis on the Australian release of Aedes aegypti (L.) (Diptera: Culicidae) containing Wolbachia. CSIRO, Canberra
Nature (1975) Oh New Delhi, Oh Geneva (editorial). Nature 256:355–357
Nightingale K (2010) GM mosquito wild release takes campaigners by surprise. SciDev.Net. Available online at: https://www.scidev.net/global/policy/news/gm-mosquito-wild-release-takes-campaigners-by-surprise.html
Noble C, Adlam B, Church GM, Esvelt KM, Nowak MA (2018) Current CRISPR gene drive systems are likely to be highly invasive in wild populations. eLife. https://doi.org/10.7554/eLife.33423
O’Connor L, Pilchart 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 Negl Trop Dis 6:e1797
Robinson AS (2002) Mutations and their use in insect control. Rev Mutat Res 511:113–132
Sánchez HM, Bennett JB, Wu SL, Rašić G, Akbari OS et al (2020) Confinement and reversibility of threshold-dependent gene drive systems in spatially-explicit Aedes aegypti populations. BMC Biol 18:50
Secretariat of the Convention on Biological Diversity (2000) Cartagena protocol on biosafety to the convention on biological diversity. World Trade Center, Montreal
Serebrovskii AS (1940) On the possibility of a new method for the control of insect pests. Zool Zhurnal 19:618–630
Singh KRP, Patterson RS, LaBrecque GC, Razdan RK (1975) Mass rearing of Culex fatigans. J Commun Dis 7:31–53
Thomas DD, Donnelly CA, Wood RJ, Alphey LS (2000) Insect population control using a dominant, repressible, lethal genetic system. Science 287:2474–2476
Turelli M, Hoffmann AA (1991) Rapid spread of an inherited incompatibility factor in California Drosophila. Nature 353:440–442
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
Weidhaas DE, Schmidt CH, Seabrook EL (1962) Field studies on the release of sterile males for the control of Anopheles quadrimaculatus. Mosq News 22:283–291
Wyss JH (2000) Screw-worm eradication in the Americas. In: Tan KH (ed) Area-wide control of fruit flies and other insect pests. Penerbit Universiti Sains Malaysia, Penang, pp 79–86
Xu XS, Bulger EA, Gantz VM, Klanseck C, Heimler SR et al (2020) Active genetic neutralizing elements for halting or deleting gene drives. Mol Cell 80:246–262
Zheng X, Zhang D, Li Y, Yang C, Wu Y et al (2019) Incompatible and sterile insect techniques combined eliminate mosquitoes. Nature 572:56–61
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2021 The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd.
About this chapter
Cite this chapter
Marshall, J.M., Vásquez, V.N. (2021). Field Trials of Gene Drive Mosquitoes: Lessons from Releases of Genetically Sterile Males and Wolbachia-infected Mosquitoes. In: Tyagi, B.K. (eds) Genetically Modified and other Innovative Vector Control Technologies. Springer, Singapore. https://doi.org/10.1007/978-981-16-2964-8_2
Download citation
DOI: https://doi.org/10.1007/978-981-16-2964-8_2
Published:
Publisher Name: Springer, Singapore
Print ISBN: 978-981-16-2963-1
Online ISBN: 978-981-16-2964-8
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)