1932

Abstract

The spread of synthetic gene drives is often discussed in the context of panmictic populations connected by gene flow and described with simple deterministic models. Under such assumptions, an entire species could be altered by releasing a single individual carrying an invasive gene drive, such as a standard homing drive. While this remains a theoretical possibility, gene drive spread in natural populations is more complex and merits a more realistic assessment. The fate of any gene drive released in a population would be inextricably linked to the population's ecology. Given the uncertainty often involved in ecological assessment of natural populations, understanding the sensitivity of gene drive spread to important ecological factors is critical. Here we review how different forms of density dependence, spatial heterogeneity, and mating behaviors can impact the spread of self-sustaining gene drives. We highlight specific aspects of gene drive dynamics and the target populations that need further research.

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2020-11-02
2024-04-26
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Literature Cited

  1. 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]
  2. Akbari OS, Marshall JM, Raban R, Kandul NP, Edula JR, Leon T 2019. Winning the tug-of-war between effector gene design and pathogen evolution in vector population replacement strategies. Front. Genet. 10:1072
    [Google Scholar]
  3. 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]
  4. Alphey L. 2014. Genetic control of mosquitoes. Annu. Rev. Entomol. 59:205–24
    [Google Scholar]
  5. 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]
  6. Altrock PM, Traulsen A, Reeves RG, Reed FA 2010. Using underdominance to bi-stably transform local populations. J. Theor. Biol. 267:162–75
    [Google Scholar]
  7. Backus GA, Delborne JA. 2019. Threshold-dependent gene drives in the wild: spread, controllability, and ecological uncertainty. Bioscience 69:11900–7
    [Google Scholar]
  8. Backus GA, Gross K. 2016. Genetic engineering to eradicate invasive mice on islands: modeling the efficiency and ecological impacts. Ecosphere 7:12e01589
    [Google Scholar]
  9. Barton NH. 1979a. The dynamics of hybrid zones. Heredity 43:3341–59
    [Google Scholar]
  10. Barton NH. 1979b. Gene flow past a cline. Heredity 43:3333–39
    [Google Scholar]
  11. Barton NH, Hewitt GM. 1985. Analysis of hybrid zones. Annu. Rev. Ecol. Syst. 16:113–48
    [Google Scholar]
  12. Barton NH, Hewitt GM. 1989. Adaptation, speciation and hybrid zones. Nature 341:6242497–503
    [Google Scholar]
  13. Barton NH, Rouhani S. 1991. The probability of fixation of a new karyotype in a continuous population. Evolution 45:3499–517
    [Google Scholar]
  14. Barton NH, Turelli M. 2011. Spatial waves of advance with bistable dynamics: cytoplasmic and genetic analogues of Allee effects. Am. Nat. 178:3E48–75
    [Google Scholar]
  15. Beaghton A, Beaghton PJ, Burt A 2016. Gene drive through a landscape: reaction-diffusion models of population suppression and elimination by a sex ratio distorter. Theor. Popul. Biol. 108:51–69
    [Google Scholar]
  16. Beaghton A, Beaghton PJ, Burt A 2017a. Vector control with driving Y chromosomes: modelling the evolution of resistance. Malar. J. 16:1286
    [Google Scholar]
  17. Beaghton A, Hammond A, Nolan T, Crisanti A, Godfray HC, Burt A 2017b. Requirements for driving antipathogen effector genes into populations of disease vectors by homing. Genetics 205:41587–96
    [Google Scholar]
  18. Beeman RW, Friesen KS, Denell RE 1992. Maternal-effect selfish genes in flour beetles. Science 256:505389–92
    [Google Scholar]
  19. Bellows TS. 1981. The descriptive properties of some models for density dependence. J. Anim. Ecol. 50:139–56
    [Google Scholar]
  20. Brownstein JS, Hett E, O'Neill SL 2003. The potential of virulent Wolbachia to modulate disease transmission by insects. J. Invertebr. Pathol. 84:124–29
    [Google Scholar]
  21. Buchman AB, Ivy T, Marshall JM, Akbari OS, Hay BA 2018a. Engineered reciprocal chromosome translocations drive high threshold, reversible population replacement in Drosophila. ACS Synth. Biol. 7:51359–70
    [Google Scholar]
  22. Buchman AB, Marshall JM, Ostrovski D, Yang T, Akbari OS 2018b. Synthetically engineered Medea gene drive system in the worldwide crop pest Drosophila suzukii. . PNAS 115:184725–30
    [Google Scholar]
  23. Bull JC, Bonsall MB. 2008. Overcompensatory population dynamic responses to environmental stochasticity. J. Anim. Ecol. 77:1296–305
    [Google Scholar]
  24. Bull JJ. 2017. Lethal gene drive selects inbreeding. Evol. Med. Public Health 2017:11–16
    [Google Scholar]
  25. Bull JJ, Remien CH, Gomulkiewicz R, Krone SM 2019a. Spatial structure undermines parasite suppression by gene drive cargo. PeerJ 7:e7921
    [Google Scholar]
  26. Bull JJ, Remien CH, Krone SM 2019b. Gene-drive-mediated extinction is thwarted by population structure and evolution of sib mating. Evol. Med. Public Health 2019. 1:66–81
    [Google Scholar]
  27. Burt A. 2003. Site-specific selfish genes as tools for the control and genetic engineering of natural populations. Proc. R. Soc. B Biol. Sci. 270:1518921–28
    [Google Scholar]
  28. Burt A. 2014. Heritable strategies for controlling insect vectors of disease. Philos. Trans. R. Soc. B Biol. Sci. 369:164520130432
    [Google Scholar]
  29. Burt A, Trivers R. 2006. Genes in Conflict: The Biology of Selfish Genetic Elements Cambridge, MA: Harvard Univ. Press
  30. Cash SA, Lorenzen MD, Gould F 2019. The distribution and spread of naturally occurring Medea selfish genetic elements in the United States. Ecol. Evol. 9:2414407–16
    [Google Scholar]
  31. Chambers LK, Singleton GR, Hinds LA 1999. Fertility control of wild mouse populations: the effects of hormonal competence and an imposed level of sterility. Wildl. Res. 26:5579–91
    [Google Scholar]
  32. Champer J, Buchman A, Akbari OS 2016. Cheating evolution: engineering gene drives to manipulate the fate of wild populations. Nat. Rev. Genet. 17:3146
    [Google Scholar]
  33. Champer J, Champer SE, Kim IK, Clark AG, Messer PW 2019a. Design and analysis of CRISPR-based underdominance toxin-antidote gene drives. bioRxiv 861435. https://doi.org/10.1101/861435
    [Crossref]
  34. Champer J, Kim IK, Champer SE, Clark AG, Messer PW 2019b. Suppression gene drive in continuous space can result in unstable persistence of both drive and wild-type alleles. bioRxiv 769810. https://doi.org/10.1101/769810
    [Crossref]
  35. Champer J, Kim IK, Champer SE, Clark AG, Messer PW 2020a. Performance analysis of novel toxin-antidote CRISPR gene drive systems. BMC Biol 18:27
    [Google Scholar]
  36. Champer J, Lee E, Yang E, Liu C, Clark AG, Messer PW 2020b. A toxin-antidote CRISPR gene drive system for regional population modification. Nat. Commun. 11:1082
    [Google Scholar]
  37. 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]
  38. Champer J, Yang E, Lee YL, Liu J, Clark AG, Messer PW 2019c. Resistance is futile: a CRISPR homing gene drive targeting a haplolethal gene. bioRxiv 651737. https://doi.org/10.1101/651737
    [Crossref]
  39. Champer J, Zhao J, Champer SE, Liu J, Messer PW 2020c. Population dynamics of underdominance gene drive systems in continuous space. ACS Synth. Biol. 9:779–92
    [Google Scholar]
  40. 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]
  41. Clutton-Brock TH, Illius AW, Wilson K, Grenfell BT, MacColl ADC, Albon SD 1997. Stability and instability in ungulate populations: an empirical analysis. Am. Nat. 149:2195–219
    [Google Scholar]
  42. Craig GB, Hickey WA, VandeHey RC 1960. An inherited male-producing factor in Aedes aegypti. Science 132:34431887–89
    [Google Scholar]
  43. Curtis CF. 1968. Possible use of translocations to fix desirable genes in insect pest populations. Nature 218:5139368–69
    [Google Scholar]
  44. Curtis CF, Robinson AS. 1971. Computer simulation of the use of double translocations for pest control. Genetics 69:197113
    [Google Scholar]
  45. Dao A, Yaro AS, Diallo M, Timbine S, Huestis DL et al. 2014. Signatures of aestivation and migration in Sahelian malaria mosquito populations. Nature 516:7531387–90
    [Google Scholar]
  46. David AS, Kaser JM, Morey AC, Roth AM, Andow DA 2013. Release of genetically engineered insects: a framework to identify potential ecological effects. Ecol. Evol. 3:114000–15
    [Google Scholar]
  47. Davis S, Bax N, Grewe P 2001. Engineered underdominance allows efficient and economical introgression of traits into pest populations. J. Theor. Biol. 212:183–98
    [Google Scholar]
  48. 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]
  49. Deredec A, Burt A, Godfray HC 2008. The population genetics of using homing endonuclease genes in vector and pest management. Genetics 179:42013–26
    [Google Scholar]
  50. Deredec A, Godfray HC, Burt A 2011. Requirements for effective malaria control with homing endonuclease genes. PNAS 108:43E874–80
    [Google Scholar]
  51. Dhole S, Lloyd AL, Gould F 2019. Tethered homing gene drives: a new design for spatially restricted population replacement and suppression. Evol. Appl. 12:81688–1702
    [Google Scholar]
  52. Dhole S, Vella MR, Lloyd AL, Gould F 2018. Invasion and migration of spatially self‐limiting gene drives: a comparative analysis. Evol. Appl. 11:5794–808
    [Google Scholar]
  53. Díaz M, Torre I, Arrizabalaga A 2010. Relative roles of density and rainfall on the short-term regulation of Mediterraneanwood mouse Apodemus sylvaticus populations. Acta Theriol 55:3251–60
    [Google Scholar]
  54. 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]
  55. Doncaster CP. 2006. Comment on “On the regulation of populations of mammals, birds, fish, and insects” III. Science 311:57641100
    [Google Scholar]
  56. Eckhoff PA, Wenger EA, Godfray HC, 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]
  57. Edgington MP, Alphey LS. 2018. Population dynamics of engineered underdominance and killer-rescue gene drives in the control of disease vectors. PLOS Comput. Biol. 14:3e1006059
    [Google Scholar]
  58. Epopa PS, Millogo AA, Collins CM, North A, Tripet F et al. 2017. The use of sequential mark-release-recapture experiments to estimate population size, survival and dispersal of male mosquitoes of the Anopheles gambiae complex in Bana, a west African humid savannah village. Parasites Vectors 10:1376
    [Google Scholar]
  59. Esvelt KM, Smidler AL, Catteruccia F, Church GM 2014. Concerning RNA-guided gene drives for the alteration of wild populations. eLife 3:e03401
    [Google Scholar]
  60. Fisher RA. 1930. The Genetical Theory of Natural Selection Oxford, UK: Clarendon
  61. Fisher RA. 1937. The wave of advance of advantageous genes. Ann. Eugen. 7:4355–69
    [Google Scholar]
  62. Flores HA, O'Neill LS. 2018. Controlling vector-borne diseases by releasing modified mosquitoes. Nat. Rev. Microbiol. 16:8508–18
    [Google Scholar]
  63. Foster WA, Lea AO. 1975. Renewable fecundity of male Aedes aegypti following replenishment of seminal vesicles and accessory glands. J. Insect Physiol. 21:51085–90
    [Google Scholar]
  64. 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]
  65. Galizi R, Hammond A, Kyrou K, Taxiarchi C, Bernardini F et al. 2016. A CRISPR-Cas9 sex-ratio distortion system for genetic control. Sci. Rep. 6:31139
    [Google Scholar]
  66. 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]
  67. Getz WM, Lloyd-Smith JO. 2006. Comment on “On the regulation of populations of mammals, birds, fish, and insects” I. Science 311:57641100
    [Google Scholar]
  68. Giese B, Frieß J, Barton N, Messer P, Débarre F et al. 2019. Gene drives: dynamics and regulatory matters—a report from the workshop “Evaluation of Spatial and Temporal Control of Gene Drives,” April 4–5, 2019, Vienna. BioEssays 10:91900151
    [Google Scholar]
  69. Gimnig JE, Ombok M, Otieno S, Kaufman MG, Vulule JM, Walker ED 2002. Density-dependent development of Anopheles gambiae (Diptera: Culicidae) larvae in artificial habitats. J. Med. Entomol. 39:1162–72
    [Google Scholar]
  70. Girardin L, Calvez V, Débarre F 2019. Catch me if you can: a spatial model for a brake-driven gene drive reversal. Bull. Math. Biol. 81:125054–88
    [Google Scholar]
  71. Godfray HC, North A, Burt A 2017. How driving endonuclease genes can be used to combat pests and disease vectors. BMC Biol 15:181
    [Google Scholar]
  72. Godwin J, Serr M, Barnhill-Dilling SK, Blondel DV, Brown PR et al. 2019. Rodent gene drives for conservation: opportunities and data needs. Proc. R. Soc. B 286:191420191606
    [Google Scholar]
  73. Goubert C, Minard G, Vieira C, Boulesteix M 2016. Population genetics of the Asian tiger mosquito Aedes albopictus, an invasive vector of human diseases. Heredity 117:3125–34
    [Google Scholar]
  74. Gould F. 2008. Broadening the application of evolutionarily based genetic pest management. Evol. Int. J. Org. Evol. 62:2500–10
    [Google Scholar]
  75. Gould F, Huang Y, Legros M, Lloyd AL 2008. A Killer–Rescue system for self-limiting gene drive of anti-pathogen constructs. Proc. R. Soc. B Biol. Sci. 275:16532823–29
    [Google Scholar]
  76. Gould F, Schliekelman P. 2004. Population genetics of autocidal control and strain replacement. Annu. Rev. Entomol. 49:193–217
    [Google Scholar]
  77. Grunwald HA, Gantz VM, Poplawski G, Xu XS, Bier E, Cooper KL 2019. Super-Mendelian inheritance mediated by CRISPR-Cas9 in the female mouse germline. Nature 566:7742105–9
    [Google Scholar]
  78. Guagliardo SAJ, Lee Y, Pierce AA, Wong J, Chu YY et al. 2019. The genetic structure of Aedes aegypti populations is driven by boat traffic in the Peruvian Amazon. PLOS Negl. Trop. Dis. 13:9e0007552
    [Google Scholar]
  79. 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 34:178–83
    [Google Scholar]
  80. Hammond A, Kyrou K, Gribble M, Karlsson X, Morianou I et al. 2018. Improved CRISPR-based suppression gene drives mitigate resistance and impose a large reproductive load on laboratory-contained mosquito populations. bioRxiv 360339. https://doi.org/10.1101/360339
    [Crossref]
  81. Hancock PA, Godfray HC. 2012. Modelling the spread of Wolbachia in spatially heterogeneous environments. J. R. Soc. Interface 9:763045–54
    [Google Scholar]
  82. Hancock PA, Ritchie SA, Koenraadt CJM, Scott TW, Hoffmann AA, Godfray HC 2019. Predicting the spatial dynamics of Wolbachia infections in Aedes aegypti arbovirus vector populations in heterogeneous landscapes. J. Appl. Ecol. 56:71674–86
    [Google Scholar]
  83. Hancock PA, White VL, Callahan AG, Godfray CHJ, Hoffmann AA, Ritchie SA 2016a. Density‐dependent population dynamics in Aedes aegypti slow the spread of wMel Wolbachia. . J. Appl. Ecol 53:3785–93
    [Google Scholar]
  84. Hancock PA, White VL, Ritchie SA, Hoffmann AA, Godfray HC 2016b. Predicting Wolbachia invasion dynamics in Aedes aegypti populations using models of density-dependent demographic traits. BMC Biol 14:196
    [Google Scholar]
  85. Hay BA, Oberhofer G, Guo M 2021. Engineering the composition and fate of wild populations with gene drive. Annu. Rev. Entomol. 66: In press. https://doi.org/10.1146/annurev-ento-020117-043154
    [Crossref] [Google Scholar]
  86. Herrando-Pérez S, Delean S, Brook BW, Bradshaw CJA 2012. Density dependence: an ecological Tower of Babel. Oecologia 170:3585–603
    [Google Scholar]
  87. Herrmann BG, Bauer H. 2012. The mouse t-haplotype: a selfish chromosome—genetics, molecular mechanism, and evolution. Evolution of the House Mouse M Macholán, SJE Baird, P Munclinger, J Piálek pp. 297314 Cambridge, UK: Cambridge Univ. Press
    [Google Scholar]
  88. Huang Y, Lloyd AL, Legros M, Gould F 2009. Gene‐drive in age‐structured insect populations. Evol. Appl. 2:2143–59
    [Google Scholar]
  89. Huang Y, Lloyd AL, Legros M, Gould F 2011. Gene‐drive into insect populations with age and spatial structure: a theoretical assessment. Evol. Appl. 4:3415–28
    [Google Scholar]
  90. Huestis DL, Dao A, Diallo M, Sanogo ZL, Samake D et al. 2019. Windborne long-distance migration of malaria mosquitoes in the Sahel. Nature 574:7778404–8
    [Google Scholar]
  91. 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. 98:6_Suppl.1–49
    [Google Scholar]
  92. Khamis D, El Mouden C, Kura K, Bonsall MB 2018. Ecological effects on underdominance threshold drives for vector control. J. Theor. Biol. 456:1–15
    [Google Scholar]
  93. Kotsakiozi P, Evans BR, Gloria‐Soria A, Kamgang B, Mayanja M et al. 2018. Population structure of a vector of human diseases: Aedes aegypti in its ancestral range, Africa. Ecol. Evol. 8:167835–48
    [Google Scholar]
  94. 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]
  95. Lambert B, North A, Burt A, Godfray HC 2018. The use of driving endonuclease genes to suppress mosquito vectors of malaria in temporally variable environments. Malar. J. 17:1154
    [Google Scholar]
  96. Lande R. 1985. The fixation of chromosomal rearrangements in a subdivided population with local extinction and colonization. Heredity 54:3323–32
    [Google Scholar]
  97. Lande R, Sæther B-E, Engen S 1997. Threshold harvesting for sustainability of fluctuating resources. Ecology 78:51341–50
    [Google Scholar]
  98. Láruson , Reed FA 2016. Stability of underdominant genetic polymorphisms in population networks. J. Theor. Biol. 390:156–63
    [Google Scholar]
  99. Leftwich PT, Bolton M, Chapman T 2016. Evolutionary biology and genetic techniques for insect control. Evol. Appl. 9:1212–30
    [Google Scholar]
  100. Leftwich PT, Edgington MP, Harvey-Samuel T, Carabajal Paladino ZL, Norman VC, Alphey L 2018. Recent advances in threshold-dependent gene drives for mosquitoes. Biochem. Soc. Trans. 46:51203–12
    [Google Scholar]
  101. Legros M, Lloyd AL, Huang Y, Gould F 2009. Density-dependent intraspecific competition in the larval stage of Aedes aegypti (Diptera: Culicidae): revisiting the current paradigm. J. Med. Entomol. 46:3409–19
    [Google Scholar]
  102. Legros M, Xu C, Morrison A, Scott TW, Lloyd AL, Gould F 2013. Modeling the dynamics of a non-limited and a self-limited gene drive system in structured Aedes aegypti populations. PLOS ONE 8:12e83354
    [Google Scholar]
  103. Lehmann T, Weetman D, Huestis DL, Yaro AS, Kassogue Y et al. 2017. Tracing the origin of the early wet‐season Anopheles coluzzii in the Sahel. Evol. Appl. 10:7704–17
    [Google Scholar]
  104. Leitschuh CM, Kanavy D, Backus GA, Valdez RX, Serr M et al. 2018. Developing gene drive technologies to eradicate invasive rodents from islands. J. Responsible Innov. 5:Suppl. 1S121–38
    [Google Scholar]
  105. Lindholm AK, Dyer KA, Firman RC, Fishman L, Forstmeier W et al. 2016. The ecology and evolutionary dynamics of meiotic drive. Trends Ecol. Evol. 31:4315–26
    [Google Scholar]
  106. Lindström J, Kokko H. 2002. Cohort effects and population dynamics. Ecol. Lett. 5:3338–44
    [Google Scholar]
  107. Lord CC. 1998. Density dependence in larval Aedes albopictus (Diptera: Culicidae). J. Med. Entomol. 35:5825–29
    [Google Scholar]
  108. Macias VM, Ohm JR, Rasgon JL 2017. Gene drive for mosquito control: Where did it come from and where are we headed. ? Int. J. Environ. Res. Public Health 14:91006
    [Google Scholar]
  109. Magori K, Gould F. 2006. Genetically engineered underdominance for manipulation of pest populations: a deterministic model. Genetics 172:42613–20
    [Google Scholar]
  110. Manser A, König B, Lindholm AK 2015. Female house mice avoid fertilization by t haplotype incompatible males in a mate choice experiment. J. Evol. Biol. 28:154–64
    [Google Scholar]
  111. Manser A, Lindholm AK, Simmons LW, Firman RC 2017. Sperm competition suppresses gene drive among experimentally evolving populations of house mice. Mol. Ecol. 26:205784–92
    [Google Scholar]
  112. Marlow NJ, Thompson PC, Rose K, Kok NE 2016. Compensatory responses by a fox population to artificial density reduction in a rangeland area in Western Australia. Conserv. Sci. West. Aust. 10:31–10
    [Google Scholar]
  113. Marshall JM. 2010. The Cartagena Protocol and genetically modified mosquitoes. Nat. Biotechnol. 28:9896–97
    [Google Scholar]
  114. 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]
  115. Marshall JM, Hay BA. 2011. Inverse Medea as a novel gene drive system for local population replacement: a theoretical analysis. J. Hered. 102:3336–41
    [Google Scholar]
  116. Marshall JM, Hay BA. 2012a. Confinement of gene drive systems to local populations: a comparative analysis. J. Theor. Biol. 294:153–71
    [Google Scholar]
  117. Marshall JM, Hay BA. 2012b. General principles of single‐construct chromosomal gene drive. Evol. Int. J. Org. Evol. 66:72150–66
    [Google Scholar]
  118. Marshall JM, Pittman GW, Buchman AB, Hay BA 2011. Semele: a killer-male, rescue-female system for suppression and replacement of insect disease vector populations. Genetics 187:2535–51
    [Google Scholar]
  119. May RM. 1973. Stability and Complexity in Model Ecosystems, Vol. 1: Princeton, NJ: Princeton Univ. Press
  120. Michalakis Y, Olivieri I. 1993. The influence of local extinctions on the probability of fixation of chromosomal rearrangements. J. Evol. Biol. 6:2153–70
    [Google Scholar]
  121. Min J, Noble C, Najjar D, Esvelt K 2017. Daisy quorum drives for the genetic restoration of wild populations. bioRxiv 115618. https://doi.org/10.1101/115618
    [Crossref]
  122. Moro D, Byrne M, Kennedy M, Campbell S, Tizard M 2018. Identifying knowledge gaps for gene drive research to control invasive animal species: the next CRISPR step. Glob. Ecol. Conserv. 13:e00363
    [Google Scholar]
  123. Muriu SM, Coulson T, Mbogo CM, Godfray HC 2013. Larval density dependence in Anopheles gambiae ss, the major African vector of malaria. J. Anim. Ecol. 82:116674
    [Google Scholar]
  124. Natl. Acad. Sci. Eng. Med. 2016. Gene Drives on the Horizon: Advancing Science, Navigating Uncertainty, and Aligning Research with Public Values Washington, DC: Natl. Acad. Press
  125. 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]
  126. 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]
  127. North AR, Burt A, Godfray HC 2013. Modelling the spatial spread of a homing endonuclease gene in a mosquito population. J. Appl. Ecol. 50:51216–25
    [Google Scholar]
  128. North AR, Burt A, Godfray HC 2019. Modelling the potential of genetic control of malaria mosquitoes at national scale. BMC Biol 17:126
    [Google Scholar]
  129. North AR, Godfray HC. 2018. Modelling the persistence of mosquito vectors of malaria in Burkina Faso. Malar. J. 17:1140
    [Google Scholar]
  130. 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]
  131. 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]
  132. Okamoto KW, Robert MA, Lloyd AL, Gould F 2013. A reduce and replace strategy for suppressing vector-borne diseases: insights from a stochastic, spatial model. PLOS ONE 8:12e81860
    [Google Scholar]
  133. Peacock E, Garshelis DL. 2006. Comment on “On the regulation of populations of mammals, birds, fish, and insects” IV. Science 313:578345
    [Google Scholar]
  134. 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]
  135. Piálek J, Barton NH. 1997. The spread of an advantageous allele across a barrier: the effects of random drift and selection against heterozygotes. Genetics 145:2493–504
    [Google Scholar]
  136. Price TAR, Wedell N. 2008. Selfish genetic elements and sexual selection: their impact on male fertility. Genetica 132:3295307
    [Google Scholar]
  137. Prowse TAA, Adikusuma F, Cassey P, Thomas P, Ross JV 2019. A Y-chromosome shredding gene drive for controlling pest vertebrate populations. eLife 8:e41873
    [Google Scholar]
  138. Prowse TAA, Cassey P, Ross JV, Pfitzner C, Wittmann TA, Thomas P 2017. Dodging silver bullets: Good CRISPR gene-drive design is critical for eradicating exotic vertebrates. Proc. R. Soc. B Biol. Sci. 284:186020170799
    [Google Scholar]
  139. Raban RR, Marshall JM, Akbari OS 2020. Progress towards engineering gene drives for population control. J. Exp. Biol. 223:jeb208181
    [Google Scholar]
  140. Rajagopalan PK, Curtis CF, Brooks GD, Menon PK 1977. The density dependence of larval mortality of Culex pipiens fatigans in an urban situation and prediction of its effects on genetic control operations. Indian J. Med. Res. 65:77–85
    [Google Scholar]
  141. Rasgon JL, Styer LM, Scott TW 2003. Wolbachia-induced mortality as a mechanism to modulate pathogen transmission by vector arthropods. J. Med. Entomol. 40:2125–32
    [Google Scholar]
  142. Rašić G, Endersby-Harshman N, Tantowijoyo W, Goundar A, White V et al. 2015. Aedes aegypti has spatially structured and seasonally stable populations in Yogyakarta, Indonesia. Parasites Vectors 8:1610
    [Google Scholar]
  143. Rašić G, Filipović I, Weeks AR, Hoffmann AA 2014. Genome-wide SNPs lead to strong signals of geographic structure and relatedness patterns in the major arbovirus vector. Aedes aegypti. BMC Genom. 15:1275
    [Google Scholar]
  144. Robert MA, Okamoto K, Lloyd AL, Gould F 2013. A reduce and replace strategy for suppressing vector-borne diseases: insights from a deterministic model. PLOS ONE 8:9e73233
    [Google Scholar]
  145. Rode NO, Estoup A, Bourguet D, Courtier-Orgogozo V, Débarre F 2019. Population management using gene drive: molecular design, models of spread dynamics and assessment of ecological risks. Conserv. Genet. 20:671–90
    [Google Scholar]
  146. Ross JV. 2006. Comment on “On the regulation of populations of mammals, birds, fish, and insects” II. Science 311:57641100
    [Google Scholar]
  147. Rouhani S, Barton N. 1987. Speciation and the “shifting balance” in a continuous population. Theor. Popul. Biol. 31:3465–92
    [Google Scholar]
  148. Sæther B-E. 1997. Environmental stochasticity and population dynamics of large herbivores: a search for mechanisms. Trends Ecol. Evol. 12:4143–49
    [Google Scholar]
  149. Sánchez CMH, Wu SL, Bennett JB, Marshall JM 2019. MGDrivE: a modular simulation framework for the spread of gene drives through spatially explicit mosquito populations. Methods Ecol. Evol. 11:229–39
    [Google Scholar]
  150. Schmidt TL, Barton NH, Rašić G, Turley AP, Montgomery BL et al. 2017. Local introduction and heterogeneous spatial spread of dengue-suppressing Wolbachia through an urban population of Aedes aegypti. . PLOS Biol 15:5e2001894
    [Google Scholar]
  151. Serebrovsky AS. 1940. On the possibility of a new method for the control of insect pests. Zool. Zhurnal. 19:618–90
    [Google Scholar]
  152. Serebrovsky AS. 1969. On the possibility of a new method for the control of insect pests. Proceedings of a Panel on Application of the Sterile-Male Technique for the Eradication or Control of Harmful Species of Insects, Organised by the Joint FAO/IAEA Division of Atomic Energy in Food and Agriculture and Held in Vienna, 27–31 May 1968123–37 Vienna: Int. Atomic Energy Agency
    [Google Scholar]
  153. Sibly RM, Barker D, Denham MC, Hone J, Pagel M 2005. On the regulation of populations of mammals, birds, fish, and insects. Science 309:5734607–10
    [Google Scholar]
  154. Sinclair ARE. 2003. Mammal population regulation, keystone processes and ecosystem dynamics. Philos. Trans. R. Soc. B Biol. Sci. 358:14381729–40
    [Google Scholar]
  155. Sinkins SP, Gould F. 2006. Gene drive systems for insect disease vectors. Nat. Rev. Genet. 7:6427–35
    [Google Scholar]
  156. Stephens PA, Sutherland WJ, Freckleton RP 1999. What is the Allee effect. ? Oikos 87:185–90
    [Google Scholar]
  157. Stokes AN. 1976. On two types of moving front in quasilinear diffusion. Math. Biosci. 31:3–4307–15
    [Google Scholar]
  158. Sudweeks J, Hollingsworth B, Blondel DV, Campbell KJ, Dhole S et al. 2019. Locally fixed alleles: a method to localize gene drive to island populations. Sci. Rep. 9:15821
    [Google Scholar]
  159. Tanaka H, Stone HA, Nelson DR 2017. Spatial gene drives and pushed genetic waves. PNAS 114:328452–57
    [Google Scholar]
  160. Twigg LE, Williams CK. 1999. Fertility control of overabundant species; can it work for feral rabbits. ? Ecol. Lett. 2:5281–85
    [Google Scholar]
  161. Vanderplank FL. 1947. Experiments in the hybridisation of tsetse-flies (Glossina, Diptera) and the possibility of a new method of control. Trans. R. Entomol. Soc. Lond. 98:1–18
    [Google Scholar]
  162. Vella MR, Gunning CE, Lloyd AL, Gould F 2017. Evaluating strategies for reversing CRISPR-Cas9 gene drives. Sci. Rep. 7:11038
    [Google Scholar]
  163. Walsh RK, Aguilar CL, Facchinelli L, Valerio L, Ramsey JM et al. 2013. Regulation of Aedes aegypti population dynamics in field systems: quantifying direct and delayed density dependence. Am. J. Trop. Med. Hyg. 89:168–77
    [Google Scholar]
  164. Walsh RK, Bradley C, Apperson CS, Gould F 2012. An experimental field study of delayed density dependence in natural populations of Aedes albopictus. . PLOS ONE 7:4e35959
    [Google Scholar]
  165. Walsh RK, Facchinelli L, Ramsey JM, Bond JG, Gould F 2011. Assessing the impact of density dependence in field populations of Aedes aegypti.J. . Vector Ecol 36:2300–7
    [Google Scholar]
  166. 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. Evol. : Int. J. Org. Evol. 65:41149–62
    [Google Scholar]
  167. Wedell N. 2013. The dynamic relationship between polyandry and selfish genetic elements. Philos. Trans. R. Soc. B Biol. Sci. 368:161320120049
    [Google Scholar]
  168. Wedell N, Price TAR. 2015. Selfish genetic elements and sexual selection. Current Perspectives on Sexual Selection T Hoquet 165–90 Dordrecht, Neth: Springer
    [Google Scholar]
  169. Wilkins KE, Prowse TAA, Cassey P, Thomas PQ, Ross JV 2018. Pest demography critically determines the viability of synthetic gene drives for population control. Math. Biosci. 305:160–69
    [Google Scholar]
  170. Williams RW, Berger A. 1980. The relation of female polygamy to gonotrophic activity in the ROCK strain of Aedes aegypti.Mosq. . News 40:4597–604
    [Google Scholar]
  171. 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]
  172. Yakob L, Bonsall MB. 2009. Importance of space and competition in optimizing genetic control strategies. J. Econ. Entomol. 102:150–57
    [Google Scholar]
  173. Yoshioka M, Couret J, Kim F, McMillan J, Burkot TR et al. 2012. Diet and density dependent competition affect larval performance and oviposition site selection in the mosquito species Aedes albopictus (Diptera: Culicidae). Parasites Vectors 5:1225
    [Google Scholar]
  174. Young ADM, Downe AER. 1982. Renewal of sexual receptivity in mated female mosquitoes. Aedes aegypti. Physiol. Entomol. 7:4467–71
    [Google Scholar]
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