The effect of gene drive on containment of transgenic mosquitoes

Journal of Theoretical Biology

Volumn 258, Issue 2, 2009, Pages 250-265

  Marshall, John M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Branching process; Dengue fever; Extinction probability; Field cage; Malaria

Indexed keywords

ENDONUCLEASE;

DENGUE FEVER; DISEASE CONTROL; GENETICALLY MODIFIED ORGANISM; GENETICS; INVASIBILITY; MALARIA; MOSQUITO; STOCHASTICITY;

ARTICLE; GENETIC ANALYSIS; MEIOSIS; MOSQUITO; PRIORITY JOURNAL; STOCHASTIC MODEL; TRANSGENIC ORGANISM; TRANSPOSON; WOLBACHIA;

ANIMALS; CULICIDAE; GENETIC ENGINEERING; INSECT CONTROL; INSECT VECTORS; MEIOSIS; MODELS, GENETIC; ORGANISMS, GENETICALLY MODIFIED; POPULATION DYNAMICS; REPETITIVE SEQUENCES, NUCLEIC ACID; RISK MANAGEMENT; STOCHASTIC PROCESSES; WOLBACHIA;

BACTERIA (MICROORGANISMS); WOLBACHIA;

EID: 61449199821     PISSN: 00225193     EISSN: 10958541     Source Type: Journal    
DOI: 10.1016/j.jtbi.2009.01.031     Document Type: Article

References (75)

1. Ahmed A.M., Baggott S.L., Maingon R., and Hurd H. The costs of mounting an immune response are reflected in the reproductive fitness of the mosquito Anopheles gambiae. Oikos 97 (2002) 371-377
2. Alphey L., Beard C.B., Billingsley P., Coetze M., Crisanti A., et al. Malaria control with genetically manipulated insect vectors. Science 298 (2002) 119-121
3. Beier J.C., Killeen G.F., and Githure J.I. Short report: entomologic inoculation rates and Plasmodium falciparum malaria prevalence in Africa. Am. J. Trop. Med. Hyg. 61 (1999) 109-113
4. Benedict M., D'Abbs P., Dobson S., Gottlieb M., Harrington L., et al. Guidance for contained field trials of vector mosquitoes engineered to contain a gene drive system: recommendations of a scientific working group. Vector-Borne Zoonotic Dis. 8 (2008) 127-166
5. Cha S.J., Mori A., Chadee D.D., and Severson D.W. Cage trials using an endogenous meiotic drive gene in the mosquito Aedes aegypti to promote population replacement. Am. J. Trop. Med. Hyg. 74 (2006) 62-68
6. Cha S.J., Chadee D.D., and Severson D.W. Population dynamics of an endogenous meiotic drive system in Aedes aegypti in Trinidad. Am. J. Trop. Med. Hyg. 75 (2006) 70-77
7. Charlat S., Ballard J.W.O., and Mercot H. What maintains noncytoplasmic incompatibility inducing Wolbachia in their hosts: a case study from a natural Drosophila yakuba population. J. Evol. Biol. 17 (2004) 322-330
8. Charlesworth B. Transposable elements in natural populations with a mixture of selected and neutral sites. Genet. Res. 57 (1991) 127-134
9. Charlesworth B., Sniegowski P., and Stephan W. The evolutionary dynamics of repetitive DNA in eukaryotes. Nature 371 (1994) 215-220
10. Chen C.H., Huang H., Ward C.M., Su J.T., Schaeffer L.V., et al. A synthetic maternal-effect selfish genetic element drives population replacement in Drosophila. Science 316 (2007) 597-600
11. Craig G.B. Prospects for vector control through manipulation of populations. Bull. World Health Organ. 29 (1963) 89-97
12. Crow J.F., and Kimura M. An Introduction to Population Genetics Theory (1970), Harper and Row, New York
13. Crow J.F., and Simmons M.J. The mutation load in Drosophila. In: Ashburner M., Carson H.L., and Thompson J.N. (Eds). The Genetics and Biology of Drosophila vol. 3c (1983), Academic Press, London 1-35
14. Curtis C.F. Possible use of translocations to fix desirable genes in insect pest populations. Nature 218 (1968) 368-369
15. Davis S.A., Bax N., and Grewe P. Engineered underdominance allows efficient and economical introgression of traits into pest populations. J. Theor. Biol. 212 (2001) 83-98
16. Dean M.D. A Wolbachia-associated fitness benefit depends on genetic background in Drosophila simulans. Proc. R. Soc. B 273 (2006) 1415-1420
17. Deredec, A., Burt, A., Godfray, C., 2007. Homing endonuclease genes: new tools for population engineering and control. Selfish DNA Meeting, Durham, North Carolina.
18. Dobson S.L., Marsland E.J., and Rattanadechakul W. Mutualistic Wolbachia infection in Aedes albopictus: accelerating cytoplasmic drive. Genetics 160 (2002) 1087-1094
19. Dorman K.S., Sinsheimer J.S., and Lange K. In the garden of branching processes. SIAM Rev. 46 (2004) 202-229
20. Engels W.R. P elements in Drosophila melanogaster. In: Berg D.E., and How M.M. (Eds). Mobile DNA (1989), ASM Press, Washington, DC 439-484
21. Fisher R.A. On the dominance ratio. Proc. R. Soc. Edinburgh 42 (1922) 321-341
22. Haldane J.B.S. A mathematical theory of natural and artificial selection. Part V: selection and mutation. Proc. Cambridge Philos. Soc. 23 (1927) 838-844
23. Harris T. The theory of branching processes (1963), Springer, Berlin
24. Hartl D.L., and Clark A.G. Principles of Population Genetics (1989), Sinauer Associates, Sunderland, Massachusettes
25. Hickey W.A., and Craig G.B. Genetic distortion of sex ratio in a mosquito, Aedes aegypti. Genetics 53 (1966) 1177-1196
26. Hoffmann A.A., Turelli M., and Harshman L.G. Factors affecting the distribution of cytoplasmic incompatibility in Drosophila simulans. Genetics 126 (1990) 933-948
27. Hoffmann A.A., Clancy D.J., and Merton E. Cytoplasmic incompatibility in Australian populations of Drosophila melanogaster. Genetics 136 (1994) 993-999
28. Hoffmann A.A., Hercus M., and Dagher H. Population dynamics of the Wolbachia infection causing cytoplasmic incompatibility in Drosophila melanogaster. Genetics 136 (1998) 993-999
29. Huang Y., Magori K., Lloyd A.L., and Gould F. Introducing desirable transgenes into insect populations using Y-linked meiotic drive-a theoretical assessment. Evolution 61 (2007) 717-726
30. James A.A. Gene drive systems in mosquitoes: rules of the road. Trends Parasitol. 21 (2005) 64-67
31. Koella J.C., and Boëte C. A genetic correlation between age at pupation and melanization immune response of the yellow fever mosquito Aedes aegypti. Evolution 56 (2002) 1074-1079
32. Kraaijeveld A.R., and Godfray H.C. Trade-off between parasitoid resistance and larval competitive ability in Drosophila melanogaster. Nature 389 (1997) 278-280
33. Lange K. Applied Probability (2002), Springer, New York
34. Lanzaro G., Touré Y., Carnahan J., Zheng L., Dolo G., et al. Complexities in the genetic structure of Anopheles gambiae populations in West Africa as revealed by microsatellite DNA analysis. Proc. Natl. Acad. Sci. USA 95 (1998) 14260-14265
35. Le Rouzic A., and Capy P. Reversible introduction of transgenes in natural populations of insects. Insect Mol. Biol. 15 (2006) 227-234
36. Little T.W. Segregation distorters. Annu. Rev. Genet. 25 (1991) 511-557
37. Lyttle T.W. Experimental population genetics of meiotic drive systems: I. Pseudo-Y chromosomal drive as a means of eliminating cage populations of Drosophila melanogaster. Genetics 86 (1977) 413-445
38. Mackay T.F., Lyman R.F., and Jackson M.S. Effects of P element insertions on quantitative traits in Drosophila melanogaster. Genetics 130 (1992) 315-332
39. Magori K., and Gould F. Genetically engineered underdominance for manipulation of pest populations: a deterministic model. Genetics 172 (2006) 2613-2620
40. Manoukis, N.C., 2006. Studies on the ecology and adaptation of Anopholes gambiae in Mali and their impacts on malaria transmission and control. Ph.D. Thesis, University of California, Los Angeles.
41. Marelli M.T., Li C., Rasgon J.L., and Jacobs-Lorena M. Transgenic malaria-resistant mosquitoes have a fitness advantage when feeding on Plasmodium-infected blood. Proc. Natl. Acad. Sci. USA 104 (2007) 5580-5583
42. Marshall J.M. The impact of dissociation on transposon-mediated disease control strategies. Genetics 178 (2008) 1673-1682
43. Marshall J.M. A branching process model for the early spread of a transposable element in a diploid population. J. Math. Biol. 57 (2008) 811-840
44. Maside X., Assimacopoulos S., and Charlesworth B. Rates of movement of transposable elements on the second chromosome of Drosophila melanogaster. Genet. Res. 75 (2000) 275-284
45. Moreira L.A., Wang J., Collins F.H., and Jacobs-Lorena M. Fitness of anopheline mosquitoes expressing transgenes that inhibit Plasmodium development. Genetics 166 (2004) 1337-1341
46. Moret Y., and Schmid-Hempel P. Survival for immunity: the price of immune system activation for bumblebee workers. Science 290 (2000) 1166-1168
47. Mukai T., Chigusa S.I., Mettler L.E., and Crow J.F. Mutation rate and dominance of genes affecting viability in Drosophila melanogaster. Genetics 72 (1972) 335-355
48. Nuzhdin S.V., Pasyukova E.G., and Mackay T.F.C. Accumulation of transposable elements in laboratory lines of Drosophila melanogaster. Genetica 100 (1997) 167-175
49. Ohnishi O. Spontaneous and ethyl methane-sulfonate-induced mutations controlling variability in Drosophila melanogaster I: recessive lethal mutations. Genetics 87 (1977) 335-348
50. Rasgon J.L., and Gould F. Transposable element insertion location bias and the dynamics of gene drive in mosquito populations. Insect Mol. Biol. 14 (2005) 493-500
51. Rasgon J.L., and Scott T.W. Wolbachia and cytoplasmic incompatibility in the California Culex pipiens mosquito species complex: parameter estimates and infection dynamics in natural populations. Genetics 165 (2003) 2029-2038
52. Rong Y.S., and Golic K.G. The homologous chromosome is an effective template for the repair of mitotic DNA double-strand breaks in Drosophila. Genetics 165 (2003) 1831-1842
53. Scott T.W., Takken W., Knols B.G., and Boëte C. The ecology of genetically modified mosquitoes. Science 298 (2002) 117-119
54. Seleme M., Busseau I., Malinsky S., Bucheton A., and Teninges D. High-frequency retrotransposition of a marked I factor in Drosophila melanogaster correlates with a dynamic expression pattern of the ORF1 protein in the cytoplasm of oocytes. Genetics 151 (1999) 761-771
55. Sinkins S.P., and Godfray H.C. Use of Wolbachia to drive nuclear transgenes through insect populations. Proc. Biol. Sci. 271 (2004) 1421-1426
56. Sinkins S.P., and Gould F. Gene drive systems for insect disease vectors. Nat. Rev. Genet. 7 (2006) 427-435
57. Spiess E.B. Genes in Populations (1977), Wiley, New York
58. Stevens L., and Wade M.J. Cytoplasmically inherited reproductive incompatibility in Tribolium flour beetles: the rate of spread and effect on population size. Genetics 124 (1990) 367-372
59. Stouthammer R., Breeuwer J.A., and Hurst G.D. Wolbachia pipientis: microbial manipulator of arthropod reproduction. Annu. Rev. Microbiol. 53 (1999) 71-102
60. Subramanian R.A., Arensburger P., Atkinson P.W., and O'Brochta D.A. Transposable element dynamics of the hAT element Herves in the human malaria vector Anopheles gambiae s.s. Genetics 176 (2007) 2477-2487
61. Taylor C.E., and Manoukis N.C. Effective population size in relation to genetic modification of Anopholes gambiae sensu stricto. In: Takken W., and Scott T.W. (Eds). Ecological Aspects for Application of Genetically Modified Mosquitoes (2003), Wageningen, The Netherlands 133-146
62. Taylor C., Touré Y.T., Carnahan J., Norris D.E., Dolo G., et al. Gene flow among populations of the Malaria vector Anopholes gambiae in Mali, West Africa. Genetics 157 (2001) 743-750
63. Touré Y.T., Petrarca V., Traore S.F., Coulibaly A., Maiga H.M., et al. Ecological genetic studies in the chromosomal form Mopti of Anopholes gambiae s. str. in Mali, West Africa. Genetica 94 (1994) 213-223
64. Townsend J.P., and Hartl D.L. The kinetics of transposable element autoregulation. Genetica 108 (2000) 229-237
65. Tripet F., Dolo G., and Lanzaro G.C. Multilevel analyses of genetic differentiation in Anopholes gambiae s.s. reveal patterns of gene flow important for malaria-fighting mosquito projects. Genetics 169 (2005) 313-324
66. Turelli M., Hoffmann A.A., and McKechnie S.W. Dynamics of cytoplasmic incompatibility and mtDNA variation in natural Drosophila simulans populations. Genetics 132 (1992) 713-723
67. Turelli M., and Hoffmann A.A. Cytoplasmic incompatibility in Drosophila simulans: dynamics and parameter estimates from natural populations. Genetics 140 (1995) 1319-1338
68. Turelli M., and Hoffmann A.A. Microbe-induced cytoplasmic incompatibility as a mechanism for introducing transgenes into arthropod populations. Insect Mol. Biol. 8 (1999) 243-255
69. Vasilyeva L.A., Bubenshchikova E.V., and Ratner V.A. Heavy heat shock induced retrotransposon transposition in Drosophila. Genet. Res. 74 (1999) 111-119
70. Wade M.J., and Beeman R.W. The population dynamics of maternal-effect selfish genes. Genetics 138 (1994) 1309-1314
71. Weeks A.R., Turelli M., Harcombe W.R., Reynolds K.T., and Hoffmann A.A. From parasite to mutualist: rapid evolution of Wolbachia in natural populations of Drosophila. PLoS Biol. 5 (2007) e114
72. Weinreich M.D., Gasch A., and Reznikoff W.S. Evidence that the cis preference of the Tn5 transposase is caused by nonproductive multimerization. Genet. Dev. 8 (1994) 2363-2374
73. Windbichler N., Papathanos P.A., Catteruccia F., Ranson H., Burt A., et al. Homing endonuclease mediated gene targeting in Anopheles gambiae cells and embryos. Nucleic Acids Res. 35 (2007) 5922-5933
74. Wright S. Evolution in Mendelian populations. Genetics 16 (1931) 97-159
75. Wu C.T., and Morris J.R. Transvection and other homology effects. Curr. Opin. Genet. Dev. 9 (1999) 237-246