Medusa: A novel gene drive system for confined suppression of insect populations

PLoS ONE

Volumn 9, Issue 7, 2014, Pages

  Marshall, John M ^a   Hay, Bruce A ^b  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b California Institute of Technology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANOPHELES GAMBIAE; ARTICLE; GENE; GENETIC MODEL; MEDUSA GENE; NONHUMAN; POPULATION DYNAMICS; POPULATION GENETICS; POPULATION SIZE; POPULATION STRUCTURE; SPECIES INVASION; TRANSGENE; X CHROMOSOME; Y CHROMOSOME; ALGORITHM; ANIMAL; BIOLOGICAL MODEL; FEMALE; GENETIC ENGINEERING; GENETICS; INHERITANCE; INSECT CHROMOSOME; INSECT CONTROL; MALE; METABOLISM; PROCEDURES; TIME; TRANSGENIC ANIMAL;

ANTIDOTE; TOXIN;

ALGORITHMS; ANIMALS; ANIMALS, GENETICALLY MODIFIED; ANTIDOTES; CHROMOSOMES, INSECT; FEMALE; GENETIC ENGINEERING; GENETICS, POPULATION; INHERITANCE PATTERNS; INSECT CONTROL; MALE; MODELS, GENETIC; TIME FACTORS; TOXINS, BIOLOGICAL; TRANSGENES; X CHROMOSOME; Y CHROMOSOME;

EID: 84904622855     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0102694     Document Type: Article

References (71)

1. van Emden HF, Service MW (2004) Pest and Vector Control, New York: Cambridge University Press. 362 p.
2. O'Meara WP, Mangeni JN, Steketee RS, Greenwood B (2010) Changes in the burden of malaria in sub-Saharan Africa. Lancet Inf. Dis. 10: 545-555.
3. 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: e1000324.
4. Dondorp AM, Yeung S, White L, Nguon C, Day NPJ, et al. (2010) Artemisinin resistance: Current status and scenarios for containment. Nature Rev. Microbiol. 8: 272-280.
5. Ranson H, N'Guessan R, Lines J, Moiroux N, Nkuni Z, et al. (2011) Pyrethroid resistance in African anopheline mosquitoes: What are the implications for malaria control? Trends Parasitol. 27: 91-98.
6. Guzman MG, Halstead SB, Artsob H, Bunchy P, Farrar J, et al. (2010) Dengue: A continuing global threat. Nat. Rev. Microbiol. 8: 7-16.
7. Braig HR, Yan G (2001) The spread of genetic constructs in natural insect populations. In: Letourneau DK, Burrows BE, editors. Genetically Engineered Organisms: Assessing Environmental and Human Health Effects. Boca Raton: CRC Press. pp. 251-314.
8. Gould F, Schliekelman P (2004) Population genetics of autocidal control and strain replacement. Annu. Rev. Entomol. 49: 193-217. (Pubitemid 38192422)
9. Sinkins SP, Gould F (2006) Gene drive systems for insect disease vectors. Nat. Rev. Genet. 7: 427-435. (Pubitemid 43780486)
10. Marshall JM, Taylor CE (2009) Malaria control with transgenic mosquitoes. PLoS Med. 6: e20.
11. Burt A (2003) Site-specific selfish genes as tools for the control and genetic engineering of natural populations. Proc. Biol. Sci. 270: 921-928.
12. Dyck VA, Hendrichs J, Robinson AS (2005) Sterile Insect Technique: Principles and Practice in Area-Wide Integrated Pest Management. Dordrecht: Springer. 801 p.
13. Alphey L, Benedict M, Bellini R, Clark GG, Dame DA, et al. (2010) Sterileinsect methods for control of mosquito-borne diseases: an analysis. Vector Borne Zoonotic Dis. 10: 295-311.
14. Harris AF, Nimmo D, McKemey AR, Kelly N, Scaife S, et al. (2011) Field performance of engineered male mosquitoes. Nat. Biotech. 29: 1034-1037.
15. 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. Biotech. 30: 828-830.
16. Hickey WA, Craig GB (1966) Distortion of sex ratio in populations of Aedes aegypti. Canadian J. Genet. Cyt. 8: 260-278.
17. Hamilton WD (1967) Extraordinary sex ratios: A sex-ratio theory for sex linkage and inbreeding has new implications in cytogenetics and entomology. Science 156: 477-488.
18. Lyttle TW (1977) Experimental population genetics of meiotic drive systems. I. Pseudo-Y chromosomal drive as a means of eliminating cage populations of Drosophila melanogaster. Genetics 86: 413-445.
19. Windbichler N, Papathanos PA, Crisanti A (2008) Targeting the X chromosome during spermatogenesis induces Y chromosome transmission ratio distortion and early dominant embryo lethality in Anopheles gambiae. PLoS Genetics 4: e1000291.
20. Deredec A, Burt A, Godfray HCJ (2008) The population genetics of using homing endonuclease genes (HEGs) in vector and pest management. Genetics 179: 2013-2026.
21. Deredec A, Godfray HCJ, Burt A (2011) Requirements for effective malaria control with homing endonuclease genes. Proc. Natl. Acad. Sci. USA 108: 874-880.
22. 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: 212-215.
23. Knols BG, Bossin HC, Mukabana WR, Robinson AS (2007) Transgenic mosquitoes and the fight against malaria: managing technology push in a turbulent GMO world. Am. J. Trop. Med. Hyg. 77: 232-242.
24. Marshall JM (2010) The Cartagena Protocol and genetically modified mosquitoes. Nat. Biotechnol. 28: 896-897.
25. Mumford JD (2012) Science, regulation, and precedent for genetically modified insects. PLoS Negl. Trop. Dis. 6: e1504.
26. Marshall JM (2009) The effect of gene drive on containment of transgenic mosquitoes. J. Theor. Biol. 258: 250-265.
27. Benedict MQ, D'Abbs P, Dobson S, Gottlieb M, Harrington L, et al. (2008) Guidance for contained field trials of vector mosquitoes engineered to contain a gene drive system: Recommendations of a scientific working group. Vector-Borne and Zoonotic Dis. 8: 127-166.
28. Chen CH, 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: 597-600. (Pubitemid 46683145)
29. Davis S, Bax N, Grewe P (2001) Engineered underdominance allows efficient and economical introgression of traits into pest populations. J. Theor. Biol. 212: 83-98. (Pubitemid 32844240)
30. Marshall JM, Hay BA (2012) Confinement of gene drive systems to local populations: A comparative analysis. J. Theor. Biol. 294: 153-171.
31. Fu G, Lees RS, Nimmo D, Aw D, Jin L, et al. (2010) Female-specific flightless phenotype for mosquito control. Proc. Natl. Acad. Sci. USA 107: 4550-4554.
32. Taylor CE, Toure YT, Carnahan J, Norris DE, Dolo G, et al. (2001) Gene flow among populations of the malaria vector, Anopheles gambiae, in Mali, West Africa. Genetics 157: 743-750. (Pubitemid 32165030)
33. 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: e1724.
34. Dietz K (1976) The effect of immigration on genetic control. Theor. Popul. Biol. 9: 58-67.
35. Prout T (1978) The joint effects of the release of sterile males and immigration of fertilized females on a density regulated population. Theor. Popul. Biol. 13: 40-71.
36. Barclay HJ (2001) Modelling incomplete sterility in a sterile release program: Interactions with other factors. Popul. Ecol. 43: 197-206.
37. Silver JB (2008) Mosquito Ecology: Field Sampling Methods. The Netherlands: Springer. 1494 p.
38. Craig GBH, Hickey WA (1967) Genetics of Aedes aegypti. In: Wright JW, Pal R, editors. Genetics of Insect Vectors of Disease. Amsterdam: Elsevier. pp. 67-131.
39. Reiter P (2007) Oviposition, dispersal, and survival in Aedes aegypti: Implications for the efficacy of control strategies. Vector Borne Zoonotic Dis. 7: 261-273.
40. Marshall (2011) The toxin and antidote puzzle: New ways to control insect pest populations through manipulating inheritance. Bioeng. Bugs 2: 235-240.
41. Yakob L, Alphey L, Bonsall MB (2008) Aedes aegypti control: The concomitant tole of competition, space and transgenic technologies. J. Appl. Ecol. 45: 1258-1265. (Pubitemid 351951837)
42. Yakob L, Kiss IZ, Bonsall MB (2008) A network approach to modelling population aggregation and genetic control of pest insects. Theor. Popul. Biol. 74: 324-331.
43. Yakob L, Bonsall MB (2009) Importance of space and competition in optimizing genetic control strategies. J. Econ. Entomol. 102: 50-57.
44. Magori K, Legros M, Puente ME, Focks DA, Scott TW, et al. (2009) Skeeter Buster: A stochastic, spatially explicit modeling tool for Aedes aegypti population replacement and population suppression strategies. PLoS NTDs 3: e508.
45. della Torre A, Fanello C, Akogbeto M, Dossou-yovo J, Favia G, et al. (2001) Molecular evidence of incipient speciation within Anopheles gambiae s.s. in West Africa. Insect Mol. Biol. 10: 9-18. (Pubitemid 32176696)
46. Tripet F, Dolo G, Lanzaro GC (2005) Multilevel analyses of genetic differentiation in Anopheles gambiae s.s. reveal patterns of gene flow important for malaria-fighting mosquito projects. Genetics 169: 313-324. (Pubitemid 40239173)
47. Dye C (1984) Models for the population dynamics of the yellow fever mosquito, Aedes aegypti. J. Anim. Ecol. 53: 247-268.
48. Muriu SM, Coulson T, Mbogo C, Godfray HCJ (2012) Larval density dependence in Anopheles gambiae s.s., the major African vector of malaria. J. Anim. Ecol. 82: 166-174.
49. Akbari OS, Chen CH, Marshall JM, Huang H, Antoshechkin I, et al. (2012) Novel synthetic Medea selfish genetic elements drive population replacement in Drosophila; a theoretical exploration of Medea-dependent population suppression. ACS Synth. Biol. doi: 10.1021/sb300079h.
50. 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.
51. Siegrist SE, Haque NS, Chen CH, Hay BA, Hariharan IK (2010) Inactivation of both Foxo and reaper promotes long-term adult neurogenesis in Drosophila. Curr. Biol. 20: 643-648.
52. Liu J, Li C, Yu Z, Huang P, Wu H, et al. (2012) Efficient and specific modifications of the Drosophila genome by means of an easy TALEN strategy. J. Genet. Genom. 39: 209-215.
53. Corradini N, Rossi F, Giordano E, Caizzi R, Verni F, et al. (2007) Drosophila melanogaster as a model for studying protein-encoding genes that are resident in constitutive heterochromatin. Heredity 98: 3-12. (Pubitemid 44973571)
54. Criscione F, Qi Y, Saunders R, Hall B, Tu Z (2013) A unique Y gene in the Asian malaria mosquito Anopheles stephensi encodes a small lysine-rich protein and is transcribed at the onset of embryonic development. Insect Mol. Biol. 22: 433-441.
55. Vicario S, Moriyama EN, Powell JR (2007) Codon usage in twelve species of Drosophila. BMC Evol. Biol. 7: 226.
56. Diaz-Castillo C, Golic KG (2007) Evolution of gene sequence in response to chromosomal location. Genetics 177: 359-374. (Pubitemid 47555854)
57. Miskei M, Adam C, Kovacs L, Karanyi Z, Dombradi V (2011) Molecular evolution of phosphoprotein phosphatases in Drosophila. PLoS ONE 6: e22218.
58. Yasuhara JC, Wakimoto BT (2008) Molecular landscape of modified histones in Drosophila heterochromatic genes and euchromatin-heterochromatin transition zones. PLoS Genet. 4: e16.
59. Li G, Zhou L (2013) Genome-wide identification of chromatin transitional regions reveals diverse mechanisms defining the boundary of facultative heterochromatin. PLoS ONE 8: e67156.
60. Lycett GJ, Kafatos F, Loukeris TG (2004) Conditional expression in the malaria mosquito Anopheles stephensi with Tet-On and Tet-Off systems. Genetics 167: 1781-1790. (Pubitemid 39265914)
61. Ford D, Hoe N, Landis GN, Tozer K, Luu A, et al. (2007) Alteration of Drosophila life span using conditional, tissue-specific expression of transgenes triggered by doxycyline or RU486/Mifepristone. Exp. Gerontol. 42: 483-497. (Pubitemid 46756091)
62. Mondal K, VijayRaghavan K, Varadarajan R (2007) Design and utility of temperature-sensitive Gal4 mutants for conditional gene expression in Drosophila. Fly (Austin) 1: 282-286.
63. Marios E, Scali C, Soichot J, Kappler C, Levashina EA, et al. (2012) High-throughput sorting of mosquito larvae for laboratory studies and for future vector control interventions. Malaria J. 11: 302.
64. Hay BA, Chen CH, Ward CM, Huang H, Su JT, et al. (2010) Engineering the genomes of wild insect populations: Challenges, and opportunities provided by synthetic Medea selfish genetic elements. J. Insect Physiol. 56: 1402-1413.
65. Morgan LV (1925) Polyploidy in Drosophila melanogaster with two attached X chromosomes. Genetics 10: 148-178.
66. Lyttle TW (1981) Experimental population genetics of meiotic drive systems. III. Neutralization of sex-ratio distortion in Drosophila through sex-chromosome aneuploidy. Genetics 98: 317-334.
67. Hauser M (2011) A historic account of the invasion of Drosophila suzukii (Matsumura) (Diptera: Drosophilidae) in the continental United States, with remarks on their identification. Pest Manag. Sci. 67: 1352-1357.
68. Cini A, Ioriatti C, Anfora G (2012) A review of the invasion of Drosophila suzukii in Europe and a draft research agenda for integrated pest management. Bull. Insectol. 65: 149-160.
69. Huh JR, Guo M, Hay BA (2004) Compensatory proliferation induced by cell death in the Drosophila wind disc requires activity of the apical cell death caspase Dronc in a nonapoptotic role. Curr. Biol. 14: 1262-1266. (Pubitemid 38991813)
70. Hancock PA, Godfray HCJ (2007) Application of the lumped age-class technique to studying dynamics of malaria-mosquito-human interactions. Malar. J. 6: 98.
71. Alphey N, Bonsall MB, Alphey L (2011) Modeling resistance to genetic control of insects. J. Theor. Biol. 270: 42-55.