Manipulating the Destiny of Wild Populations Using CRISPR

Literature Cited

1. 1.

   Adelman Z, Akbari O, Bauer J, Bier E, Bloss C et al. 2017. Rules of the road for insect gene drive research and testing. Nat. Biotechnol. 35:8716–18
   [Google Scholar]
2. 2.

   Adolfi A, Gantz VM, Jasinskiene N, Lee H-F, Hwang K et al. 2020. Efficient population modification gene-drive rescue system in the malaria mosquito Anopheles stephensi. Nat. Commun. 11:15553
   [Google Scholar]
3. 3.

   Akbari OS, Antoshechkin I, Hay BA, Ferree PM. 2013. Transcriptome profiling of Nasonia vitripennis testis reveals novel transcripts expressed from the selfish B chromosome, paternal sex ratio. G3 3:91597–605
   [Google Scholar]
4. 4.

   Akbari OS, Bellen HJ, Bier E, Bullock SL, Burt A et al. 2015. Safeguarding gene drive experiments in the laboratory. Science 349:6251927–29
   [Google Scholar]
5. 5.

   Akbari OS, Chen C-H, Marshall JM, Huang H, Antoshechkin I, Hay BA. 2014. Novel synthetic Medea selfish genetic elements drive population replacement in Drosophila; a theoretical exploration of Medea-dependent population suppression. ACS Synth. Biol. 3:12915–28
   [Google Scholar]
6. 6.

   Akbari OS, Matzen KD, Marshall JM, Huang H, Ward CM, Hay BA. 2013. A synthetic gene drive system for local, reversible modification and suppression of insect populations. Curr. Biol. 23:8671–77
   [Google Scholar]
7. 7.

   Alphey LS, Crisanti A, Randazzo F, Akbari OS. 2020. Standardizing the definition of gene drive. PNAS 117:4930864–67
   [Google Scholar]
8. 8.

   Alphey N, Bonsall MB. 2014. Interplay of population genetics and dynamics in the genetic control of mosquitoes. J. R. Soc. Interface 11:9320131071
   [Google Scholar]
9. 9.

   Álvarez MM, Biayna J, Supek F. 2022. TP53-dependent toxicity of CRISPR/Cas9 cuts is differential across genomic loci and can confound genetic screening. Nat. Commun. 13:14520
   [Google Scholar]
10. 10.

    Anderson MAE, Gonzalez E, Ang JXD, Shackleford L, Nevard K et al. 2023. Closing the gap to effective gene drive in Aedes aegypti by exploiting germline regulatory elements. Nat. Commun. 14:1338
    [Google Scholar]
11. 11.

    Anderson MAE, Gonzalez E, Edgington MP, Ang JXD, Purusothaman D-K et al. 2022. A multiplexed, confinable CRISPR/Cas9 gene drive propagates in caged Aedes aegypti populations. bioRxiv 2022.08.12.503466. https://doi.org/10.1101/2022.08.12.503466
12. 12.

    Annas GJ, Beisel CL, Clement K, Crisanti A, Francis S et al. 2021. A code of ethics for gene drive research. CRISPR J. 4:119–24
    [Google Scholar]
13. 13.

    Anzalone AV, Koblan LW, Liu DR. 2020. Genome editing with CRISPR-Cas nucleases, base editors, transposases and prime editors. Nat. Biotechnol. 38:7824–44
    [Google Scholar]
14. 14.

    Backus GA, Delborne JA. 2019. Threshold-dependent gene drives in the wild: spread, controllability, and ecological uncertainty. Bioscience 69:11900–7
    [Google Scholar]
15. 15.

    Baker RH. 1984. Chromosome rearrangements in the control of mosquitoes. Prev. Vet. Med. 2:1529–40
    [Google Scholar]
16. 16.

    Bakerlee CW, Nguyen Ba AN, Shulgina Y, Rojas Echenique JI, Desai MM. 2022. Idiosyncratic epistasis leads to global fitness-correlated trends. Science 376:6593630–35
    [Google Scholar]
17. 17.

    Bakri A, Mehta K, Lance DR. 2005. Sterilizing insects with ionizing radiation. Sterile Insect Technique: Principles and Practice in Area-Wide Integrated Pest Management VA Dyck, J Hendrichs, AS Robinson 355–98. Dordrecht, Neth: Springer
    [Google Scholar]
18. 18.

    Basgall EM, Goetting SC, Goeckel ME, Giersch RM, Roggenkamp E et al. 2018. Gene drive inhibition by the anti-CRISPR proteins AcrIIA2 and AcrIIA4 in Saccharomyces cerevisiae. Microbiology 164:4464–74
    [Google Scholar]
19. 19.

    Basu S, Reitmayer CM, Lumley S, Atkinson B, Schade-Weskott ML. 2023. A Zika virus-responsive sensor-effector system in Aedes aegypti. bioRxiv 2023.02.06.527261. https://doi.org/10.1101/2023.02.06.527261
20. 20.

    Beaghton A, Hammond A, Nolan T, Crisanti A, Godfray HCJ, Burt A. 2017. Requirements for driving antipathogen effector genes into populations of disease vectors by homing. Genetics 205:41587–96
    [Google Scholar]
21. 21.

    Beeman RW, Friesen KS, Denell RE. 1992. Maternal-effect selfish genes in flour beetles. Science 256:505389–92
    [Google Scholar]
22. 22.

    Beerntsen BT, James AA, Christensen BM. 2000. Genetics of mosquito vector competence. Microbiol. Mol. Biol. Rev. 64:1115–37
    [Google Scholar]
23. 23.

    Ben-David E, Burga A, Kruglyak L. 2017. A maternal-effect selfish genetic element in Caenorhabditis elegans. Science 356:63421051–55
    [Google Scholar]
24. 24.

    Bhatt S, Weiss DJ, Cameron E, Bisanzio D, Mappin B et al. 2015. The effect of malaria control on Plasmodium falciparum in Africa between 2000 and 2015. Nature 526:7572207–11
    [Google Scholar]
25. 25.

    Bhaya D, Davison M, Barrangou R. 2011. CRISPR-Cas systems in bacteria and archaea: versatile small RNAs for adaptive defense and regulation. Annu. Rev. Genet. 45:273–97
    [Google Scholar]
26. 26.

    Braig HR, Yan G. 2001. The spread of genetic constructs in natural insect populations. Genetically Engineered Organisms: Assessing Environmental and Human Health Effects DK Letourneau, BE Burrows 251–314. Boca Raton, FL: CRC Press
    [Google Scholar]
27. 27.

    Brouns SJJ, Jore MM, Lundgren M, Westra ER, Slijkhuis RJH et al. 2008. Small CRISPR RNAs guide antiviral defense in prokaryotes. Science 321:5891960–64
    [Google Scholar]
28. 28.

    Buchman AB, Gamez S, Li M, Antoshechkin I, Li H-H et al. 2019. Engineered resistance to Zika virus in transgenic Aedes aegypti expressing a polycistronic cluster of synthetic small RNAs. PNAS 116:93656–61
    [Google Scholar]
29. 29.

    Buchman AB, Gamez S, Li M, Antoshechkin I, Li H-H et al. 2020. Broad dengue neutralization in mosquitoes expressing an engineered antibody. PLOS Pathog. 16:1e1008103
    [Google Scholar]
30. 30.

    Buchman AB, Ivy T, Marshall JM, Akbari OS, Hay BA. 2018. Engineered reciprocal chromosome translocations drive high threshold, reversible population replacement in Drosophila. ACS Synth. Biol. 7:51359–70
    [Google Scholar]
31. 31.

    Buchman AB, Marshall JM, Ostrovski D, Yang T, Akbari OS. 2018. Synthetically engineered Medea gene drive system in the worldwide crop pest Drosophila suzukii. PNAS 115:184725–30
    [Google Scholar]
32. 32.

    Buchman AB, Shriner I, Yang T, Liu J, Antoshechkin I et al. 2021. Engineered reproductively isolated species drive reversible population replacement. Nat. Commun. 12:13281
    [Google Scholar]
33. 33.

    Bui M, Dalla Benetta E, Dong Y, Zhao Y, Yang T et al. 2023. CRISPR mediated transactivation in the human disease vector Aedes aegypti. PLOS Pathog. 19:1e1010842
    [Google Scholar]
34. 34.

    Bull JJ. 2015. Evolutionary decay and the prospects for long-term disease intervention using engineered insect vectors. Evol. Med. Public Health 2015:1152–66
    [Google Scholar]
35. 35.

    Bull JJ. 2016. Lethal gene drive selects inbreeding. Evol. Med. Public Health 2017:11–16
    [Google Scholar]
36. 36.

    Burga A, Ben-David E, Kruglyak L. 2020. Toxin-antidote elements across the tree of life. Annu. Rev. Genet. 54:387–415
    [Google Scholar]
37. 37.

    Burt A. 2003. Site-specific selfish genes as tools for the control and genetic engineering of natural populations. Proc. Biol. Sci. 270:1518921–28
    [Google Scholar]
38. 38.

    Burt A, Koufopanou V. 2004. Homing endonuclease genes: the rise and fall and rise again of a selfish element. Curr. Opin. Genet. Dev. 14:6609–15
    [Google Scholar]
39. 39.

    Burt A, Trivers R. 2009. Genes in Conflict: The Biology of Selfish Genetic Elements Cambridge, MA: Harvard Univ. Press
40. 40.

    Carballar-Lejarazú R, Dong Y, Pham TB, Tushar T, Corder RM et al. 2023. Dual effector population modification gene-drive strains of the African malaria mosquitoes, Anopheles gambiae and Anopheles coluzzii. PNAS 120:29e2221118120
    [Google Scholar]
41. 41.

    Carballar-Lejarazú R, Ogaugwu C, Tushar T, Kelsey A, Pham TB et al. 2020. Next-generation gene drive for population modification of the malaria vector mosquito, Anopheles gambiae. PNAS 117:3722805–14
    [Google Scholar]
42. 42.

    Carrami EM, Eckermann KN, Ahmed HMM, Sánchez C HM, Dippel S et al. 2018. Consequences of resistance evolution in a Cas9-based sex conversion-suppression gene drive for insect pest management. PNAS 115:246189–94
    [Google Scholar]
43. 43.

    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. 9:7e0003864
    [Google Scholar]
44. 44.

    Champer J, Buchman A, Akbari OS. 2016. Cheating evolution: engineering gene drives to manipulate the fate of wild populations. Nat. Rev. Genet. 17:3146–59
    [Google Scholar]
45. 45.

    Champer J, Champer SE, Kim IK, Clark AG, Messer PW. 2021. Design and analysis of CRISPR-based underdominance toxin-antidote gene drives. Evol. Appl. 14:41052–69
    [Google Scholar]
46. 46.

    Champer J, Chung J, Lee YL, Liu C, Yang E et al. 2019. Molecular safeguarding of CRISPR gene drive experiments. eLife 8:e41439
    [Google Scholar]
47. 47.

    Champer J, Kim IK, Champer SE, Clark AG, Messer PW. 2020. Performance analysis of novel toxin-antidote CRISPR gene drive systems. BMC Biol. 18:127
    [Google Scholar]
48. 48.

    Champer J, Kim IK, Champer SE, Clark AG, Messer PW. 2021. Suppression gene drive in continuous space can result in unstable persistence of both drive and wild-type alleles. Mol. Ecol. 30:41086–1101
    [Google Scholar]
49. 49.

    Champer J, Lee E, Yang E, Liu C, Clark AG, Messer PW. 2020. A toxin-antidote CRISPR gene drive system for regional population modification. Nat. Commun. 11:1082
    [Google Scholar]
50. 50.

    Champer J, Liu J, Oh SY, Reeves R, Luthra A et al. 2018. Reducing resistance allele formation in CRISPR gene drive. PNAS 115:215522–27
    [Google Scholar]
51. 51.

    Champer J, Reeves R, Oh SY, Liu C, Liu J et al. 2017. Novel CRISPR/Cas9 gene drive constructs reveal insights into mechanisms of resistance allele formation and drive efficiency in genetically diverse populations. PLOS Genet. 13:7e1006796
    [Google Scholar]
52. 52.

    Champer J, Yang E, Lee E, Liu J, Clark AG, Messer PW. 2020. A CRISPR homing gene drive targeting a haplolethal gene removes resistance alleles and successfully spreads through a cage population. PNAS 117:3924377–83
    [Google Scholar]
53. 53.

    Champer J, Zhao J, Champer SE, Liu J, Messer PW. 2020. Population dynamics of underdominance gene drive systems in continuous space. ACS Synth. Biol. 9:4779–92
    [Google Scholar]
54. 54.

    Chan Y-S, Huen DS, Glauert R, Whiteway E, Russell S. 2013. Optimising homing endonuclease gene drive performance in a semi-refractory species: the Drosophila melanogaster experience. PLOS ONE 8:1e54130
    [Google Scholar]
55. 55.

    Chan Y-S, Naujoks DA, Huen DS, Russell S. 2011. Insect population control by homing endonuclease-based gene drive: an evaluation in Drosophila melanogaster. Genetics 188:133–44
    [Google Scholar]
56. 56.

    Chen C-H, Huang H, Ward CM, Su JT, Schaeffer LV et al. 2007. A synthetic maternal-effect selfish genetic element drives population replacement in Drosophila. Science 316:5824597–600
    [Google Scholar]
57. 57.

    Chen J, Xu X, Champer J. 2023. Assessment of distant-site rescue elements for CRISPR toxin-antidote gene drives. Front. Bioeng. Biotechnol. 11:1138702
    [Google Scholar]
58. 58.

    Chitnis N, Schapira A, Smith T, Steketee R. 2010. Comparing the effectiveness of malaria vector-control interventions through a mathematical model. Am. J. Trop. Med. Hyg. 83:2230–40
    [Google Scholar]
59. 59.

    Colleaux L, d'Auriol L, Betermier M, Cottarel G, Jacquier A et al. 1986. Universal code equivalent of a yeast mitochondrial intron reading frame is expressed into E. coli as a specific double strand endonuclease. Cell 44:4521–33
    [Google Scholar]
60. 60.

    Connolly JB, Mumford JD, Glandorf DCM, Hartley S, Lewis OT et al. 2022. Recommendations for environmental risk assessment of gene drive applications for malaria vector control. Malar. J. 21:1152
    [Google Scholar]
61. 61.

    Cook F, Bull JJ, Gomulkiewicz R. 2022. Gene drive escape from resistance depends on mechanism and ecology. Evol. Appl. 15:5721–34
    [Google Scholar]
62. 62.

    Cosmides LM, Tooby J. 1981. Cytoplasmic inheritance and intragenomic conflict. J. Theor. Biol. 89:183–129
    [Google Scholar]
63. 63.

    Craig GB Jr., Hickey WA, Vandehey RC. 1960. An inherited male-producing factor in Aedes aegypti. Science 132:34431887–89
    [Google Scholar]
64. 64.

    Curtis CF. 1968. Possible use of translocations to fix desirable genes in insect pest populations. Nature 218:5139368–69
    [Google Scholar]
65. 65.

    Curtis CF. 1975. Male-linked translocations and the control of insect pest populations. Experientia 31:101139–41
    [Google Scholar]
66. 66.

    Dalla Benetta E, Akbari OS, Ferree PM. 2021. Mechanistically comparing reproductive manipulations caused by selfish chromosomes and bacterial symbionts. Heredity 126:5707–16
    [Google Scholar]
67. 67.

    Dalla Benetta E, Antoshechkin I, Yang T, Nguyen HQM, Ferree PM, Akbari OS. 2020. Genome elimination mediated by gene expression from a selfish chromosome. Sci. Adv. 6:14eaaz9808
    [Google Scholar]
68. 68.

    Dalla Benetta E, López-Denman A, Li H-H, Masri RA, Brogan DJ et al. 2023. Engineered antiviral sensor targets infected mosquitoes. bioRxiv 2023.01.27.525922. https://doi.org/10.1101/2023.01.27.525922
69. 69.

    de Lara Capurro M, Coleman J, Beerntsen BT, Myles KM, Olson KE et al. 2000. Virus-expressed, recombinant single-chain antibody blocks sporozoite infection of salivary glands in Plasmodium gallinaceum-infected Aedes aegypti. Am. J. Trop. Med. Hyg. 62:4427–33
    [Google Scholar]
70. 70.

    Del Amo VL, Bishop AL, Sánchez C HM, Bennett JB et al. 2020. A transcomplementing gene drive provides a flexible platform for laboratory investigation and potential field deployment. Nat. Commun. 11:352
    [Google Scholar]
71. 71.

    Delborne J, Kuzma J, Gould F, Frow E, Leitschuh C, Sudweeks J. 2018. Mapping research and governance needs for gene drives. J. Responsible Innov. 5:Suppl. 1S4–12
    [Google Scholar]
72. 72.

    Deredec A, Burt A, Godfray HCJ. 2008. The population genetics of using homing endonuclease genes in vector and pest management. Genetics 179:42013–26
    [Google Scholar]
73. 73.

    Deredec A, Godfray HCJ, Burt A. 2011. Requirements for effective malaria control with homing endonuclease genes. PNAS 108:43E874–80
    [Google Scholar]
74. 74.

    Dhole S, Lloyd AL, Gould F. 2019. Tethered homing gene drives: a new design for spatially restricted population replacement and suppression. Evol. Appl. 12:181688–702
    [Google Scholar]
75. 75.

    Dhole S, Lloyd AL, Gould F. 2020. Gene drive dynamics in natural populations: the importance of density dependence, space, and sex. Annu. Rev. Ecol. Evol. Syst. 51:505–31
    [Google Scholar]
76. 76.

    DiCarlo JE, Chavez A, Dietz SL, Esvelt KM, Church GM. 2015. Safeguarding CRISPR-Cas9 gene drives in yeast. Nat. Biotechnol. 33:121250–55
    [Google Scholar]
77. 77.

    Dong Y, Simões ML, Dimopoulos G. 2020. Versatile transgenic multistage effector-gene combinations for Plasmodium falciparum suppression in Anopheles. Sci. Adv. 6:20eaay5898
    [Google Scholar]
78. 78.

    Doolittle WF, Sapienza C. 1980. Selfish genes, the phenotype paradigm and genome evolution. Nature 284:5757601–3
    [Google Scholar]
79. 79.

    Drury DW, Dapper AL, Siniard DJ, Zentner GE, Wade MJ. 2017. CRISPR/Cas9 gene drives in genetically variable and nonrandomly mating wild populations. Sci. Adv. 3:5e1601910
    [Google Scholar]
80. 80.

    Eberhard WG. 1980. Evolutionary consequences of intracellular organelle competition. Q. Rev. Biol. 55:3231–49
    [Google Scholar]
81. 81.

    Eckhoff PA, Wenger EA, Godfray HCJ, Burt A. 2017. Impact of mosquito gene drive on malaria elimination in a computational model with explicit spatial and temporal dynamics. PNAS 114:2E255–64
    [Google Scholar]
82. 82.

    Emerson C, James S, Littler K, Randazzo FF. 2017. Principles for gene drive research. Science 358:63671135–36
    [Google Scholar]
83. 83.

    Enkerlin WR, Gutiérrez Ruelas JM, Pantaleon R, Soto Litera C, Villaseñor Cortés A et al. 2017. The Moscamed Regional Programme: review of a success story of area-wide sterile insect technique application. Entomol. Exp. Appl. 164:3188–203
    [Google Scholar]
84. 84.

    Esvelt KM, Smidler AL, Catteruccia F, Church GM. 2014. Emerging technology: concerning RNA-guided gene drives for the alteration of wild populations. eLife 3:e03401
    [Google Scholar]
85. 85.

    Franz AWE, Sanchez-Vargas I, Adelman ZN, Blair CD, Beaty BJ et al. 2006. Engineering RNA interference-based resistance to dengue virus type 2 in genetically modified Aedes aegypti. PNAS 103:114198–203
    [Google Scholar]
86. 86.

    Franz AWE, Sanchez-Vargas I, Raban RR, Black WC IV, James AA, Olson KE. 2014. Fitness impact and stability of a transgene conferring resistance to dengue-2 virus following introgression into a genetically diverse Aedes aegypti strain. PLOS Negl. Trop. Dis. 8:5e2833
    [Google Scholar]
87. 87.

    Frieß JL, Lalyer CR, Giese B, Simon S, Otto M. 2023. Review of gene drive modelling and implications for risk assessment of gene drive organisms. Ecol. Model. 478:110285
    [Google Scholar]
88. 88.

    Fu G, Lees RS, Nimmo D, Aw D, Jin L et al. 2010. Female-specific flightless phenotype for mosquito control. PNAS 107:104550–54
    [Google Scholar]
89. 89.

    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
    [Google Scholar]
90. 90.

    Gallagher DN, Haber JE. 2018. Repair of a site-specific DNA cleavage: old-school lessons for Cas9-mediated gene editing. ACS Chem. Biol. 13:2397–405
    [Google Scholar]
91. 91.

    Gamez S, Chaverra-Rodriguez D, Buchman A, Kandul NP, Mendez-Sanchez SC et al. 2021. Exploiting a Y chromosome-linked Cas9 for sex selection and gene drive. Nat. Commun. 12:7202
    [Google Scholar]
92. 92.

    Gantz VM, Bier E. 2015. The mutagenic chain reaction: a method for converting heterozygous to homozygous mutations. Science 348:6233442–44
    [Google Scholar]
93. 93.

    Gantz VM, Bier E. 2016. The dawn of active genetics. Bioessays 38:150–63
    [Google Scholar]
94. 94.

    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. PNAS 112:49E6736–43
    [Google Scholar]
95. 95.

    Gershenson S. 1929. A new sex-ratio abnormality in Drosophila obscura. Genetics. 136488–507
96. 96.

    Gierus L, Birand A, Bunting MD, Godahewa GI, Piltz SG et al. 2022. Leveraging a natural murine meiotic drive to suppress invasive populations. PNAS 119:46e2213308119
    [Google Scholar]
97. 97.

    Godfray HCJ, North A, Burt A. 2017. How driving endonuclease genes can be used to combat pests and disease vectors. BMC Biol. 15:181
    [Google Scholar]
98. 98.

    Goeckel ME, Basgall EM, Lewis IC, Goetting SC, Yan Y et al. 2019. Modulating CRISPR gene drive activity through nucleocytoplasmic localization of Cas9 in S. cerevisiae. Fungal Biol. Biotechnol. 6:2
    [Google Scholar]
99. 99.

    Gould F. 2008. Broadening the application of evolutionarily based genetic pest management. Evolution 62:2500–10
    [Google Scholar]
100. 100.

     Gould F, Schliekelman P. 2004. Population genetics of autocidal control and strain replacement. Annu. Rev. Entomol. 49:193–217
     [Google Scholar]
101. 101.

     Griffin JT, Hollingsworth TD, Okell LC, Churcher TS, White M et al. 2010. Reducing Plasmodium falciparum malaria transmission in Africa: a model-based evaluation of intervention strategies. PLOS Med. 7:8e1000324
     [Google Scholar]
102. 102.

     Grunwald HA, Gantz VM, Poplawski G, Xu X-RS, Bier E, Cooper KL. 2019. Super-Mendelian inheritance mediated by CRISPR-Cas9 in the female mouse germline. Nature 566:7742105–9
     [Google Scholar]
103. 103.

     Guichard A, Haque T, Bobik M, Xu X-RS, Klanseck C et al. 2019. Efficient allelic-drive in Drosophila. Nat. Commun. 10:11640
     [Google Scholar]
104. 104.

     Hamilton WD. 1967. Extraordinary sex ratios: A sex-ratio theory for sex linkage and inbreeding has new implications in cytogenetics and entomology. Science 156:3774477–88
     [Google Scholar]
105. 105.

     Hammond AM, 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. 34:178–83
     [Google Scholar]
106. 106.

     Hammond AM, Karlsson X, Morianou I, Kyrou K, Beaghton A et al. 2021. Regulating the expression of gene drives is key to increasing their invasive potential and the mitigation of resistance. PLOS Genet. 17:1e1009321
     [Google Scholar]
107. 107.

     Hammond AM, Kyrou K, Bruttini M, North A, Galizi R et al. 2017. The creation and selection of mutations resistant to a gene drive over multiple generations in the malaria mosquito. PLOS Genet. 13:10e1007039
     [Google Scholar]
108. 108.

     Hammond AM, Pollegioni P, Persampieri T, North A, Minuz R et al. 2021. Gene-drive suppression of mosquito populations in large cages as a bridge between lab and field. Nat. Commun. 12:14589
     [Google Scholar]
109. 109.

     Harris AF, McKemey AR, Nimmo D, Curtis Z, Black I et al. 2012. Successful suppression of a field mosquito population by sustained release of engineered male mosquitoes. Nat. Biotechnol. 30:9828–30
     [Google Scholar]
110. 110.

     Hartl DL. 1975. Modifier theory and meiotic drive. Theor. . Popul. Biol. 7:2168–74
     [Google Scholar]
111. 111.

     Hartley S, Taitingfong R, Fidelman P. 2022. The principles driving gene drives for conservation. Environ. Sci. Policy 135:36–45
     [Google Scholar]
112. 112.

     Hickey WA, Craig GB Jr. 1966. Distortion of sex ratio in populations of Aedes aegypti. Can. J. Genet. Cytol. 8:2260–78
     [Google Scholar]
113. 113.

     Hickey WA, Craig GB Jr. 1966. Genetic distortion of sex ratio in a mosquito, Aedes aegypti. Genetics 53:61177–96
     [Google Scholar]
114. 114.

     Hosack GR, Ickowicz A, Hayes KR. 2021. Quantifying the risk of vector-borne disease transmission attributable to genetically modified vectors. R. Soc. Open Sci. 8:3201525
     [Google Scholar]
115. 115.

     Hurst LD. 1993. scat⁺ is a selfish gene analogous to Medea of Tribolium castaneum. Cell 75:3407–8
     [Google Scholar]
116. 116.

     Ito J, Ghosh A, Moreira LA, Wimmer EA, Jacobs-Lorena M. 2002. Transgenic anopheline mosquitoes impaired in transmission of a malaria parasite. Nature 417:6887452–55
     [Google Scholar]
117. 117.

     Jaenike J. 2001. Sex chromosome meiotic drive. Annu. Rev. Ecol. Syst. 32:25–49
     [Google Scholar]
118. 118.

     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. 98:61–49
     [Google Scholar]
119. 119.

     James SL, Marshall JM, Christophides GK, Okumu FO, Nolan T. 2020. Toward the definition of efficacy and safety criteria for advancing gene drive-modified mosquitoes to field testing. Vector Borne Zoonotic Dis. 20:4237–51
     [Google Scholar]
120. 120.

     James SL, O'Brochta DA, Randazzo F, Akbari OS. 2023. A gene drive is a gene drive: the debate over lumping or splitting definitions. Nat. Commun. 14:11749
     [Google Scholar]
121. 121.

     Jinek M, Chylinski K, Fonfara I, Hauer M, Doudna JA, Charpentier E. 2012. A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 337:6096816–21
     [Google Scholar]
122. 122.

     Juste SS, Okamoto EM, Feng X, Del Amo VL. 2023. Next-generation CRISPR gene-drive systems using Cas12a nuclease. bioRxiv 2023.02.20.529271. https://doi.org/10.1101/2023.02.20.529271
123. 123.

     Kandul NP, Liu J, Akbari OS. 2021. Temperature-inducible precision-guided sterile insect technique. CRISPR J. 4:6822–35
     [Google Scholar]
124. 124.

     Kandul NP, Liu J, Bennett JB, Marshall JM, Akbari OS. 2021. A confinable home-and-rescue gene drive for population modification. eLife 10:e65939
     [Google Scholar]
125. 125.

     Kandul NP, Liu J, Buchman A, Gantz VM, Bier E, Akbari OS. 2020. Assessment of a split homing based gene drive for efficient knockout of multiple genes. G3 10:2827–37
     [Google Scholar]
126. 126.

     Kandul NP, Liu J, Buchman A, Shriner IC, Corder RM et al. 2022. Precision guided sterile males suppress populations of an invasive crop pest. GEN Biotechnol. 1:4372–85
     [Google Scholar]
127. 127.

     Kandul NP, Liu J, Sanchez C HM, Wu SL, Marshall JM, Akbari OS. 2019. Reply to “Concerns about the feasibility of using ‘precision guided sterile males’ to control insects. .” Nat. Commun. 10:13955
     [Google Scholar]
128. 128.

     Kandul NP, Liu J, Sanchez C HM, Wu SL, Marshall JM, Akbari OS. 2019. Transforming insect population control with precision guided sterile males with demonstration in flies. Nat. Commun. 10:184
     [Google Scholar]
129. 129.

     Kidwell MG, Ribeiro JM. 1992. Can transposable elements be used to drive disease refractoriness genes into vector populations?. Parasitol. Today 8:10325–29
     [Google Scholar]
130. 130.

     Knipling EF. 1955. Possibilities of insect control or eradication through the use of sexually sterile males. J. Econ. Entomol. 48:4459–62
     [Google Scholar]
131. 131.

     Knipling EF. 1959. Sterile-male method of population control. Science 130:3380902–4
     [Google Scholar]
132. 132.

     Kolopack PA, Lavery JV. 2017. Informed consent in field trials of gene-drive mosquitoes. Gates Open Res. 1:14
     [Google Scholar]
133. 133.

     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. 36:111062–66
     [Google Scholar]
134. 134.

     Labbé GMC, Scaife S, Morgan SA, Curtis ZH, Alphey L. 2012. Female-specific flightless (fsRIDL) phenotype for control of Aedes albopictus. PLOS Negl. Trop. Dis. 6:7e1724
     [Google Scholar]
135. 135.

     Lai C, Alvarez O, Read K, van Fossan D, Conner CM et al. 2022. Robust and efficient active genetics gene conversion in the rat and mouse. bioRxiv 2022.08.30.505951. https://doi.org/10.1101/2022.08.30.505951
136. 136.

     Langmüller AM, Champer J, Lapinska S, Xie L, Metzloff M et al. 2022. Fitness effects of CRISPR endonucleases in Drosophila melanogaster populations. eLife 11:e71809
     [Google Scholar]
137. 137.

     Laven H. 1969. Eradicating mosquitoes using translocations. Nature 221:5184958–59
     [Google Scholar]
138. 138.

     Laven H, Cousserans J, Guille G. 1972. Eradicating mosquitoes using translocations: a first field experiment. Nature 236:456–57
     [Google Scholar]
139. 139.

     Leftwich PT, Edgington MP, Harvey-Samuel T, Carabajal Paladino LZ, Norman VC, Alphey L. 2018. Recent advances in threshold-dependent gene drives for mosquitoes. Biochem. Soc. Trans. 46:51203–12
     [Google Scholar]
140. 140.

     Leung S, Windbichler N, Wenger EA, Bever CA, Selvaraj P. 2022. Population replacement gene drive characteristics for malaria elimination in a range of seasonal transmission settings: a modelling study. Malar. J. 21:1226
     [Google Scholar]
141. 141.

     Lewis IC, Yan Y, Finnigan GC. 2021. Analysis of a Cas12a-based gene-drive system in budding yeast. Access Microbiol. 3:12000301
     [Google Scholar]
142. 142.

     Li M, Kandul NP, Sun R, Yang T, Benetta ED et al. 2023. Targeting sex determination to suppress mosquito populations. bioRxiv 2023.04.18.537404. https://doi.org/10.1101/2023.04.18.537404
143. 143.

     Li M, Yang T, Bui M, Gamez S, Wise T et al. 2021. Suppressing mosquito populations with precision guided sterile males. Nat. Commun. 12:5374
     [Google Scholar]
144. 144.

     Li M, Yang T, Kandul NP, Bui M, Gamez S et al. 2020. Development of a confinable gene drive system in the human disease vector Aedes aegypti. eLife 9:e51701
     [Google Scholar]
145. 145.

     Liu W-L, Hsu C-W, Chan S-P, Yen P-S, Su MP et al. 2022. Author correction: Transgenic refractory Aedes aegypti lines are resistant to multiple serotypes of dengue virus. Sci. Rep. 12:1754
     [Google Scholar]
146. 146.

     Long KC, Alphey L, Annas GJ, Bloss CS, Campbell KJ et al. 2020. Core commitments for field trials of gene drive organisms. Science 370:65231417–19
     [Google Scholar]
147. 147.

     Lutrat C, Burckbuchler M, Olmo RP, Beugnon R, Fontaine A et al. 2022. Combining two Genetic Sexing Strains allows sorting of non-transgenic males for Aedes genetic control. bioRxiv 2022.03.11.483912. https://doi.org/10.1101/2022.03.11.483912
148. 148.

     Lyttle TW. 1993. Cheaters sometimes prosper: distortion of mendelian segregation by meiotic drive. Trends Genet. 9:6205–10
     [Google Scholar]
149. 149.

     Macdonald G. 1957. The Epidemiology and Control of Malaria. London: Oxford Univ. Press
150. 150.

     Magori K, Gould F. 2006. Genetically engineered underdominance for manipulation of pest populations: a deterministic model. Genetics 172:42613–20
     [Google Scholar]
151. 151.

     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. 13:2424–30
     [Google Scholar]
152. 152.

     Marshall JM, Buchman A, Sánchez C HM, Akbari OS. 2017. Overcoming evolved resistance to population-suppressing homing-based gene drives. Sci. Rep. 7:13776
     [Google Scholar]
153. 153.

     Marshall JM, Raban RR, Kandul NP, Edula JR, León TM, Akbari OS. 2019. Winning the tug-of-war between effector gene design and pathogen evolution in vector population replacement strategies. Front. Genet. 10:1072
     [Google Scholar]
154. 154.

     Maselko M, Feltman N, Upadhyay A, Hayward A, Das S et al. 2020. Engineering multiple species-like genetic incompatibilities in insects. Nat. Commun. 11:14468
     [Google Scholar]
155. 155.

     Maselko M, Heinsch SC, Chacón JM, Harcombe WR, Smanski MJ. 2017. Engineering species-like barriers to sexual reproduction. Nat. Commun. 8:1883
     [Google Scholar]
156. 156.

     Mathur G, Sanchez-Vargas I, Alvarez D, Olson KE, Marinotti O, James AA. 2010. Transgene-mediated suppression of dengue viruses in the salivary glands of the yellow fever mosquito, Aedes aegypti. Insect Mol. Biol. 19:6753–63
     [Google Scholar]
157. 157.

     McClintock B. 1950. The origin and behavior of mutable loci in maize. 366344–55
158. 158.

     McDonald IC, Overland DE. 1973. House fly genetics: II. Isolation of a heat-sensitive translocation homozygote. J. Hered. 64:5253–56
     [Google Scholar]
159. 159.

     Metzloff M, Yang E, Dhole S, Clark AG, Messer PW, Champer J. 2022. Experimental demonstration of tethered gene drive systems for confined population modification or suppression. BMC Biol. 20:1119
     [Google Scholar]
160. 160.

     Millett P, Alexanian T, Palmer MJ, Evans SW, Kuiken T, Oye K. 2022. iGEM and gene drives: a case study for governance. Health Secur. 20:126–34
     [Google Scholar]
161. 161.

     Mingzuyu Pan AJC, Champer J. 2022. Making waves: comparative analysis of gene drive spread characteristics in a continuous space model. bioRxiv 2022.11.01.514650. https://doi.org/10.1101/2022.11.01.514650
162. 162.

     Mondal A, Vásquez VN, Marshall JM. 2022. Target product profiles for mosquito gene drives: incorporating insights from mathematical models. Front. Trop. Dis. 3:828876
     [Google Scholar]
163. 163.

     Moreira LA, Ito J, Ghosh A, Devenport M, Zieler H et al. 2002. Bee venom phospholipase inhibits malaria parasite development in transgenic mosquitoes. J. Biol. Chem. 277:4340839–43
     [Google Scholar]
164. 164.

     Nash A, Urdaneta GM, Beaghton AK, Hoermann A, Papathanos PA et al. 2019. Integral gene drives for population replacement. Biol. Open 8:1bio037762
     [Google Scholar]
165. 165.

     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 7:e33423
     [Google Scholar]
166. 166.

     Noble C, Min J, Olejarz J, Buchthal J, Chavez A et al. 2019. Daisy-chain gene drives for the alteration of local populations. PNAS 116:178275–82
     [Google Scholar]
167. 167.

     Noble C, Olejarz J, Esvelt KM, Church GM, Nowak MA. 2017. Evolutionary dynamics of CRISPR gene drives. Sci. Adv. 3:4e1601964
     [Google Scholar]
168. 168.

     Normandin AM, Fitzgerald LM, Yip J. 2022. Hurdles in responsive community engagement for the development of environmental biotechnologies. Synth. Biol. 7:1ysac022
     [Google Scholar]
169. 169.

     North AR, Burt A, Godfray HCJ. 2019. Modelling the potential of genetic control of malaria mosquitoes at national scale. BMC Biol. 17:126
     [Google Scholar]
170. 170.

     North AR, Godfray HCJ. 2018. Modelling the persistence of mosquito vectors of malaria in Burkina Faso. Malar. J. 17:1140
     [Google Scholar]
171. 171.

     Nuckolls NL, Bravo Núñez MA, Eickbush MT, Young JM, Lange JJ et al. 2017. wtf genes are prolific dual poison-antidote meiotic drivers. eLife 6:e26033
     [Google Scholar]
172. 172.

     Oberhofer G, Ivy T, Hay BA. 2018. Behavior of homing endonuclease gene drives targeting genes required for viability or female fertility with multiplexed guide RNAs. PNAS 115:40E9343–52
     [Google Scholar]
173. 173.

     Oberhofer G, Ivy T, Hay BA. 2019. Cleave and Rescue, a novel selfish genetic element and general strategy for gene drive. PNAS 116:136250–59
     [Google Scholar]
174. 174.

     Oberhofer G, Ivy T, Hay BA. 2020. Gene drive and resilience through renewal with next generation Cleave and Rescue selfish genetic elements. PNAS 117:169013–21
     [Google Scholar]
175. 175.

     Oberhofer G, Ivy T, Hay BA. 2020. 2-Locus Cleave and Rescue selfish elements harness a recombination rate-dependent generational clock for self limiting gene drive. bioRxiv 2020.07.09.196253. https://doi.org/10.1101/2020.07.09.196253
176. 176.

     Oberhofer G, Ivy T, Hay BA. 2021. Gene drive that results in addiction to a temperature-sensitive version of an essential gene triggers population collapse in Drosophila. PNAS 118:49e2107413118
     [Google Scholar]
177. 177.

     Oberhofer G, Ivy T, Hay BA. 2021. Split versions of Cleave and Rescue selfish genetic elements for measured self limiting gene drive. PLOS Genet. 17:2e1009385
     [Google Scholar]
178. 178.

     Orgel LE, Crick FH. 1980. Selfish DNA: the ultimate parasite. Nature 284:5757604–7
     [Google Scholar]
179. 179.

     Orozco-Dávila D, Quintero L, Hernández E, Solís E, Artiaga T et al. 2017. Mass rearing and sterile insect releases for the control of Anastrepha spp. pests in Mexico—a review. Entomol. Exp. Appl. 164:3176–87
     [Google Scholar]
180. 180.

     Papathanos PA, Bourtzis K, Tripet F, Bossin H, Virginio JF et al. 2018. A perspective on the need and current status of efficient sex separation methods for mosquito genetic control. Parasit. Vectors 11:Suppl. 2654
     [Google Scholar]
181. 181.

     Pescod P, Bevivino G, Anthousi A, Shelton R, Margiotta M et al. 2023. Measuring the impact of genetic heterogeneity and chromosomal inversions on the efficacy of CRISPR-Cas9 gene drives in different strains of Anopheles gambiae. bioRxiv 2023.03.31.535088. https://doi.org/10.1101/2023.03.31.535088
182. 182.

     Peters LL, Barker JE. 1993. Novel inheritance of the murine severe combined anemia and thrombocytopenia (Scat) phenotype. Cell 74:1135–42
     [Google Scholar]
183. 183.

     Pfitzner C, White MA, Piltz SG, Scherer M, Adikusuma F et al. 2020. Progress toward zygotic and germline gene drives in mice. CRISPR J. 3:5388–97
     [Google Scholar]
184. 184.

     Pham TB, Phong CH, Bennett JB, Hwang K, Jasinskiene N et al. 2019. Experimental population modification of the malaria vector mosquito, Anopheles stephensi. PLOS Genet. 15:12e1008440
     [Google Scholar]
185. 185.

     Raban RR, Akbari OS. 2022. An introduction to the molecular genetics of gene drives and thoughts on their gradual transition to field use. Transgenic Insects: Techniques and Applications MQ Benedict, MJ Scott 1–21. Wallingford, UK: CABI
     [Google Scholar]
186. 186.

     Raban RR, Marshall JM, Akbari OS. 2020. Progress towards engineering gene drives for population control. J. Exp. Biol. 223:Suppl. 1jeb208181
     [Google Scholar]
187. 187.

     Rašić G, Lobo NF, Jeffrey Gutiérrez EH, Sánchez C HM, Marshall JM. 2021. Monitoring needs for gene drive mosquito projects: lessons from vector control field trials and invasive species. Front. Genet. 12:780327
     [Google Scholar]
188. 188.

     Ravindran S. 2012. Barbara McClintock and the discovery of jumping genes. PNAS 109:5020198–99
     [Google Scholar]
189. 189.

     Reeves RG, Bryk J, Altrock PM, Denton JA, Reed FA. 2014. First steps towards underdominant genetic transformation of insect populations. PLOS ONE 9:5e97557
     [Google Scholar]
190. 190.

     Reid W, Williams AE, Sanchez-Vargas I, Lin J, Juncu R et al. 2022. Assessing single-locus CRISPR/Cas9-based gene drive variants in the mosquito Aedes aegypti via single-generation crosses and modeling. G3 12:12jkac280
     [Google Scholar]
191. 191.

     Ribeiro JM, Kidwell MG. 1994. Transposable elements as population drive mechanisms: specification of critical parameter values. J. Med. Entomol. 31:110–16
     [Google Scholar]
192. 192.

     Robinson AS. 1976. Progress in the use of chromosomal translocations for the control of insect pests. Biol. Rev. Camb. Philos. Soc. 51:11–24
     [Google Scholar]
193. 193.

     Roggenkamp E, Giersch RM, Schrock MN, Turnquist E, Halloran M, Finnigan GC. 2018. Tuning CRISPR-Cas9 gene drives in Saccharomyces cerevisiae. G3 8:3999–1018
     [Google Scholar]
194. 194.

     Roggenkamp E, Giersch RM, Wedeman E, Eaton M, Turnquist E et al. 2017. CRISPR-UnLOCK: multipurpose Cas9-based strategies for conversion of yeast libraries and strains. Front. Microbiol. 8:1773
     [Google Scholar]
195. 195.

     Samuel GH, Pohlenz T, Dong Y, Coskun N, Adelman ZN et al. 2023. RNA interference is essential to modulating the pathogenesis of mosquito-borne viruses in the yellow fever mosquito. PNAS 120:11e2213701120
     [Google Scholar]
196. 196.

     Sánchez C HM, Bennett JB, Wu SL, Rašić G, Akbari OS, Marshall JM. 2020. Modeling confinement and reversibility of threshold-dependent gene drive systems in spatially-explicit Aedes aegypti populations. BMC Biol. 18:150
     [Google Scholar]
197. 197.

     Schairer CE, Taitingfong R, Akbari OS, Bloss CS. 2019. A typology of community and stakeholder engagement based on documented examples in the field of novel vector control. PLOS Negl. Trop. Dis. 13:11e0007863
     [Google Scholar]
198. 198.

     Schairer CE, Triplett C, Akbari OS, Bloss CS. 2022. California residents’ perceptions of gene drive systems to control mosquito-borne disease. Front. Bioeng. Biotechnol. 10:848707
     [Google Scholar]
199. 199.

     Schairer CE, Triplett C, Buchman A, Akbari OS, Bloss CS. 2020. Interdisciplinary development of a standardized introduction to gene drives for lay audiences. BMC Med. Res. Methodol. 20:1273
     [Google Scholar]
200. 200.

     Seidel HS, Ailion M, Li J, van Oudenaarden A, Rockman MV, Kruglyak L. 2011. A novel sperm-delivered toxin causes late-stage embryo lethality and transmission ratio distortion in C. elegans. PLOS Biol. 9:7e1001115
     [Google Scholar]
201. 201.

     Serebrovskii AS. 1940. On the possibility of a new method for the control of insect pests. Zool. Zhurnal 19:618–30
     [Google Scholar]
202. 202.

     Serebrovsky AS. 1969. On the possibility of a new method for the control of insect pests. Sterile-Male Technique for Eradication or Control of Harmful Insects123–237. Vienna: Int. Atom. Energy Ag.
     [Google Scholar]
203. 203.

     Shapiro RS, Chavez A, Porter CBM, Hamblin M, Kaas CS et al. 2018. A CRISPR-Cas9-based gene drive platform for genetic interaction analysis in Candida albicans. Nat. Microbiol. 3:173–82
     [Google Scholar]
204. 204.

     Simoni A, Hammond AM, Beaghton AK, Galizi R, Taxiarchi C et al. 2020. A male-biased sex-distorter gene drive for the human malaria vector Anopheles gambiae. Nat. Biotechnol. 38:91054–60
     [Google Scholar]
205. 205.

     Simoni A, Siniscalchi C, Chan YS, Huen DS, Russell S et al. 2015. Development of synthetic selfish elements based on modular nucleases in Drosophila melanogaster. . Nucleic Acids Res. 42:117461–72
     [Google Scholar]
206. 206.

     Smidler AL, Pai JJ, Apte RA, Sánchez C HM, Corder RM et al. 2023. A confinable female-lethal population suppression system in the malaria vector. Anopheles gambiae. Sci. Adv. 9:27eade8903
     [Google Scholar]
207. 207.

     Snow JW. 1988. Radiation, insects and eradication in North America: an overview from screwworm to bollworm. Modern Insect Control: Nuclear Techniques and Biotechnology3–13. Vienna: Int. At. Energy Agency
     [Google Scholar]
208. 208.

     Spinner SAM, Barnes ZH, Puinean AM, Gray P, Dafa'alla T et al. 2022. New self-sexing Aedes aegypti strain eliminates barriers to scalable and sustainable vector control for governments and communities in dengue-prone environments. Front. Bioeng. Biotechnol. 10:975786
     [Google Scholar]
209. 209.

     Taitingfong RI, Triplett C, Vásquez VN, Rajagopalan RM, Raban R et al. 2023. Exploring the value of a global gene drive project registry. Nat. Biotechnol. 41:9–13
     [Google Scholar]
210. 210.

     Tanaka H, Stone HA, Nelson DR. 2017. Spatial gene drives and pushed genetic waves. PNAS 114:328452–57
     [Google Scholar]
211. 211.

     Taxiarchi C, Beaghton A, Don NI, Kyrou K, Gribble M et al. 2021. A genetically encoded anti-CRISPR protein constrains gene drive spread and prevents population suppression. Nat. Commun. 12:13977
     [Google Scholar]
212. 212.

     Terns MP, Terns RM. 2011. CRISPR-based adaptive immune systems. Curr. Opin. Microbiol. 14:3321–27
     [Google Scholar]
213. 213.

     Terradas G, Bennett JB, Li Z, Marshall JM, Bier E. 2023. Genetic conversion of a split-drive into a full-drive element. Nat. Commun. 14:1191
     [Google Scholar]
214. 214.

     Terradas G, Buchman AB, Bennett JB, Shriner I, Marshall JM et al. 2021. Inherently confinable split-drive systems in Drosophila. . Nat. Commun. 12:1480
     [Google Scholar]
215. 215.

     Thomas DD, Donnelly CA, Wood RJ, Alphey LS. 2000. Insect population control using a dominant, repressible, lethal genetic system. Science 287:54622474–76
     [Google Scholar]
216. 216.

     Unckless RL, Clark AG, Messer PW. 2017. Evolution of resistance against CRISPR/Cas9 gene drive. Genetics 205:2827–41
     [Google Scholar]
217. 217.

     Vella MR, Gunning CE, Lloyd AL, Gould F. 2017. Evaluating strategies for reversing CRISPR-Cas9 gene drives. Sci. Rep. 7:111038
     [Google Scholar]
218. 218.

     Verkuijl SAN, Anderson MAE, Alphey L, Bonsall MB. 2022. Daisy-chain gene drives: the role of low cut-rate, resistance mutations, and maternal deposition. PLOS Genet. 18:9e1010370
     [Google Scholar]
219. 219.

     Verkuijl SAN, Ang JXD, Alphey L, Bonsall MB, Anderson MAE. 2022. The challenges in developing efficient and robust synthetic homing endonuclease gene drives. Front. Bioeng. Biotechnol. 10:856981
     [Google Scholar]
220. 220.

     Verkuijl SAN, Gonzalez E, Li M, Ang JXD, Kandul NP et al. 2022. A CRISPR endonuclease gene drive reveals distinct mechanisms of inheritance bias. Nat. Commun. 13:17145
     [Google Scholar]
221. 221.

     Wang G-H, Gamez S, Raban RR, Marshall JM, Alphey L et al. 2021. Combating mosquito-borne diseases using genetic control technologies. Nat. Commun. 12:14388
     [Google Scholar]
222. 222.

     Ward CM, Su JT, Huang Y, Lloyd AL, Gould F, Hay BA. 2011. Medea selfish genetic elements as tools for altering traits of wild populations: a theoretical analysis. Evolution 65:41149–62
     [Google Scholar]
223. 223.

     Warmbrod KL, Kobokovich AL, West R, Gronvall GK, Montague M. 2022. The need for a tiered registry for US gene drive governance. Health Secur. 20:143–49
     [Google Scholar]
224. 224.

     Weitzel AJ, Grunwald HA, Weber C, Levina R, Gantz VM et al. 2021. Meiotic Cas9 expression mediates gene conversion in the male and female mouse germline. PLOS Biol. 19:12e3001478
     [Google Scholar]
225. 225.

     Werren JH, Baldo L, Clark ME. 2008. Wolbachia: master manipulators of invertebrate biology. Nat. Rev. Microbiol. 6:10741–51
     [Google Scholar]
226. 226.

     Werren JH, Nur U, Wu CI. 1988. Selfish genetic elements. Trends Ecol. Evol. 3:11297–302
     [Google Scholar]
227. 227.

     Whitten MJ. 1971. Insect control by genetic manipulation of natural populations. Science 171:3972682–84
     [Google Scholar]
228. 228.

     Wiedenheft B, Sternberg SH, Doudna JA. 2012. RNA-guided genetic silencing systems in bacteria and archaea. Nature 482:7385331–38
     [Google Scholar]
229. 229.

     Windbichler N, Menichelli M, Papathanos PA, Thyme SB, Li H et al. 2011. A synthetic homing endonuclease-based gene drive system in the human malaria mosquito. Nature 473:7346212–15
     [Google Scholar]
230. 230.

     Windbichler N, Papathanos PA, Catteruccia F, Ranson H, Burt A, Crisanti A. 2007. Homing endonuclease mediated gene targeting in Anopheles gambiae cells and embryos. Nucleic Acids Res. 35:175922–33
     [Google Scholar]
231. 231.

     Winegard TC. 2019. The Mosquito: A Human History of Our Deadliest Predator New York: Penguin
232. 232.

     World Health Organ. 2020. World Malaria Report 2020: 20 Years of Global Progress and Challenges Geneva: World Health Organ.
233. 233.

     Xu X-RS, Bulger EA, Gantz VM, Klanseck C, Heimler SR et al. 2020. Active genetic neutralizing elements for halting or deleting gene drives. Mol. Cell 80:2246–62.e4
     [Google Scholar]
234. 234.

     Yan Y, Finnigan GC. 2018. Development of a multi-locus CRISPR gene drive system in budding yeast. Sci. Rep. 8:117277
     [Google Scholar]
235. 235.

     Yan Y, Finnigan GC. 2019. Analysis of CRISPR gene drive design in budding yeast. Access Microbiol. 1:9e000059
     [Google Scholar]
236. 236.

     Yang E, Metzloff M, Langmüller AM, Xu X, Clark AG et al. 2022. A homing suppression gene drive with multiplexed gRNAs maintains high drive conversion efficiency and avoids functional resistance alleles. G3 12:6jkac081
     [Google Scholar]
237. 237.

     Yen P-S, James A, Li J-C, Chen C-H, Failloux A-B. 2018. Synthetic miRNAs induce dual arboviral-resistance phenotypes in the vector mosquito Aedes aegypti. Commun. Biol. 1:11
     [Google Scholar]
238. 238.

     Yoshida S, Matsuoka H, Luo E, Iwai K, Arai M et al. 1999. A single-chain antibody fragment specific for the Plasmodium berghei ookinete protein Pbs21 confers transmission blockade in the mosquito midgut. Mol. Biochem. Parasitol. 104:2195–204
     [Google Scholar]
239. 239.

     Yoshida S, Shimada Y, Kondoh D, Kouzuma Y, Ghosh AK et al. 2007. Hemolytic C-type lectin CEL-III from sea cucumber expressed in transgenic mosquitoes impairs malaria parasite development. PLOS Pathog. 3:12e192
     [Google Scholar]