Antipathogen genes and the replacement of disease-vectoring mosquito populations: A model-based evaluation

Evolutionary Applications

Volumn 7, Issue 10, 2014, Pages 1238-1251

  Robert, Michael A ^a,b   Okamoto, Kenichi W ^a   Gould, Fred ^a,c   Lloyd, Alun L ^a,c  

^a NORTH CAROLINA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF NEW MEXICO   (United States)

^c NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

Aedes aegypti; Antipathogen genes; Dengue fever; Female killing; Ordinary differential equation model; Reduce and replace

Indexed keywords

EID: 84914819037     PISSN: 17524563     EISSN: 17524571     Source Type: Journal    
DOI: 10.1111/eva.12219     Document Type: Article

References (64)

1. Alphey, L., and N. Alphey 2014. Five things to know about genetically modified (GM) insects for vector control. PLoS Pathogens 10:e1003909.
2. Alphey, L., K. Bourtzis, and T. Miller 2009. Genetically modified insects as a tool for biorational control. In: I. Ishaaya, and A. R. Horowitz, eds. Biorational Control of Arthropod Pests, pp. 189-206. Springer, Netherlands, Dordrecht.
3. Alphey, L., M. Benedict, R. Bellini, G.G. Clark, D.A. Dame, M.W. Service, and S.L. Dobson 2010. Sterile-insect methods for control of mosquito-borne diseases: an analysis. Vector Borne and Zoonotic Diseases 10:295-311.
4. Amin, L., and H. Hashim 2014. Factors influencing stakeholders attitudes toward genetically modified Aedes mosquito. Science and Engineering Ethics 2014:1-27.
5. Atkinson, M. P., Z. Su, N. Alphey, L. S. Alphey, P. G. Coleman, and L. M. Wein 2007. Analyzing the control of mosquito-borne diseases by a dominant lethal genetic system. Proceedings of the National Academy of Sciences of the United States of America 104:9540-9545.
6. Barclay, H. J. 2005. "Mathematical models for the use of sterile insects." In V. A. Dyck, J. Hendrichs, and A. S. Robinson, eds. Sterile Insect Technique. Principles and Practice in Area-Wide Integrated Pest Management, pp. 147-174. Springer, Dordrecht.
7. Beech, C. J., S. S. Vasan, M. M. Quinlan, M. L. Capurro, L. Alphey, V. Bayard, M. Bouaré et al. 2009. Deployment of innovative genetic vector control strategies : progress on regulatory and biosafety aspects, capacity building and development of best-practice guidance. Asia-Pacific Journal of Molecular Biology and Biotechnology 17:75-85.
8. Bellows, T. S. 1981. The descriptive properties of some models for density dependence. Journal of Animal Ecology 50:139-156.
9. Benedict, M., P. D'Abbs, S. Dobson, M. Gottlieb, L. Harrington, S. Higgs, A. A. James 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 Diseases 8:127-166.
10. Black, W. C., L. Alphey, and A. A. James 2011. Why RIDL is not SIT. Trends in Parasitology 27:362-370.
11. Burt, A. 2003. Site-specific selfish genes as tools for the control and genetic engineering of natural populations. Proceedings Biological Sciences 270:921-928.
12. Carvalho, D. O., A. L. Costa-da-Silva, R. S. Lees, and M. L. Capurro 2013. Two step male release strategy using transgenic mosquito lines to control transmission of vector-borne diseases. Acta Tropica 132:S170-S177.
13. Catteruccia, F., J. P. Benton, and A. Crisanti 2005. An Anopheles transgenic sexing strain for vector control. Nature Biotechnology 23:1414-1417.
14. Chen, C., H. Huang, C. M. Ward, and J. T. Su 2007. A synthetic maternal-effect selfish genetic element drives population replacement in Drosophila. Science 316:597-600.
15. Davis, S., N. Bax, and P. Grewe 2001. Engineered underdominance allows efficient and economical introgression of traits into pest populations. Journal of Theoretical Biology 212:83-98.
16. Deredec, A., A. Burt, and H. C. J. Godfray 2008. The population genetics of using homing endonuclease genes in vector and pest management. Genetics 179:2013-2026.
17. Dodson, B. L., G. L. Hughes, O. Paul, A. C. Matacchiero, L. D. Kramer, and J. L. Rasgon 2014. Wolbachia enhances West Nile virus (WNV) infection in the mosquito Culex tarsalis. PLoS Neglected Tropical Diseases 8:e2965.
18. Facchinelli, L., L. Valerio, J. M. Ramsey, F. Gould, R. K. Walsh, G. Bond, M. A. Robert et al. 2013. Field cage studies and progressive evaluation of genetically-engineered mosquitoes. PLoS Neglected Tropical Diseases 7:e2001.
19. Foster, G. G., W. G. Vogt, T. L. Woodburn, and P. H. Smith 1988. Computer simulation of genetic control. Comparison of sterile males and field-female Killing Systems. Theoretical and Applied Genetics 76:870-879.
20. Fouque, F., R. Carinci, P. Gaborit, J. Issaly, D. J. Bicout, and P. Sabatier 2006. Aedes aegypti survival and dengue transmission patterns in French Guiana. Journal of Vector Ecology 31:390-399.
21. Fu, G., R. S. Lees, D. Nimmo, D. Aw, L. Jin, P. Gray, T. U. Berendonk et al. 2010. Female-specific flightless phenotype for mosquito control. Proceedings of the National Academy of Sciences of the United States of America 107:4550-4554.
22. Gong, P., M. J. Epton, G. Fu, S. Scaife, A. Hiscox, K. C. Condon, G. C. Condon et al. 2005. A dominant lethal genetic system for autocidal control of the Mediterranean fruitfly". Nature Biotechnology 23:453-456.
23. Gould, F., and P. Schliekelman 2004. Population genetics of autocidal control and strain replacement". Annual Review of Entomology 49:193-217.
24. Gould, F., Y. Huang, M. Legros, and A. L. Lloyd 2008. A killer-rescue system for self-limiting gene drive of anti-pathogen constructs. Proceedings. Biological Sciences/The Royal Society 275:2823-2829.
25. Hanh, T. T. T., P. S. Hill, B. H. Kay, and T. M. Quy 2009. Development of a framework for evaluating the sustainability of community-based dengue control projects. The American Journal of Tropical Medicine and Hygiene 80:312-318.
26. Harrington, L. C., J. D. Edman, and T. W. Scott 2001. Why do Aedes aegypti (Diptera: Culicidae) feed preferentially and frequently on human blood? Journal of Medical Entomology 38:411-422.
27. Hay, B. A., C. Chen, C. M. Ward, H. Huang, J. T. Su, and M. Guo 2010. Engineering the genomes of wild insect populations: challenges, and opportunities provided by synthetic Medea selfish genetic elements. Journal of Insect Physiology 56:1402-1413.
28. Heinrich, J. C., and M. J. Scott 2000. A repressible female-specific lethal genetic system for making transgenic insect strains suitable for a sterile-release program. Proceedings of the National Academy of Sciences of the United States of America 97:8229-8232.
29. Hemingway, J., B. J. Beaty, M. Rowland, T. W. Scott, and B. L. Sharp 2006. The innovative vector control consortium: improved control of mosquito-borne diseases. Trends in Parasitology 22:308-312.
30. Hill, C. A., F. C. Kafatos, S. K. Stansfield, and F. H. Collins 2005. Arthropod-borne diseases: vector control in the genomics era. Nature Reviews. Microbiology 3:262-268.
31. Hoffmann, A. A., B. L. Montgomery, J. Popovici, I. Iturbe-Ormaetxe, P. H. Johnson, F. Muzzi, M. Greenfield et al. 2011. Successful establishment of Wolbachia in Aedes populations to suppress dengue transmission. Nature 476:454-457.
32. Huang, Y., K. Magori, A. L. Lloyd, and F. Gould 2007. Introducing transgenes into insect populations using combined gene-drive strategies: modeling and analysis. Insect Biochemistry and Molecular Biology 37:1054-1063.
33. Huang, Y., A. L. Lloyd, M. Legros, and F. Gould 2009. Gene drive in age-structured insect populations. Evolutionary Applications 2:143-159.
34. Labbé, G. M. C., S. Scaife, S. A. Morgan, Z. H. Curtis, and L. Alphey 2012. Female-specific flightless (fsRIDL) phenotype for control of Aedes albopictus. PLoS Neglected Tropical Diseases 6:e1724.
35. Legros, M., A. L. Lloyd, Y. Huang, and F. Gould 2009. Density-dependent intraspecific competition in the larval stage of Aedes Aegypti (Diptera: Culicidae): revisiting the current paradigm. Journal of Medical Entomology 46:409-419.
36. Legros, M., C. Xu, K. Okamoto, T. W. Scott, A. C. Morrison, A. L. Lloyd, and F. Gould 2012. Assessing the feasibility of controlling Aedes aegypti with transgenic methods: a model-based evaluation. PLoS ONE 7:e52235.
37. Magori, K., and F. Gould 2006. Genetically engineered underdominance for manipulation of pest populations: a deterministic model. Genetics 172:2613-2620.
38. Marshall, J. M., and B. A. Hay 2011. Inverse Medea as a novel gene drive system for local population replacement: a theoretical analysis. The Journal of Heredity 102:336-341.
39. Marshall, J. M., G. W. Pittman, A. B. Buchman, and B. A. Hay 2011. Semele: a killer-male, rescue-female system for suppression and replacement of insect disease vector populations. Genetics 187:535-551.
40. Mathur, G., I. Sanchez-Vargas, D. Alvarez, K. E. Olson, O. Marinotti, and A. A. James 2010. Transgene-mediated suppression of dengue viruses in the salivary glands of the yellow fever mosquito, Aedes aegypti. Insect Molecular Biology 19:753-763.
41. McNaughton, D. 2012. The importance of long-term social research in enabling participation and developing engagement strategies for new dengue control technologies. PLoS Neglected Tropical Diseases 6:e1785.
42. McNaughton, D., and T. T. H. Duong 2014. Designing a community engagement framework for a new dengue control method: a case study from central Vietnam. PLoS Neglected Tropical Diseases 8:e2794.
43. Muir, L. E., and B. H. Kay 1998. Aedes aegypti survival and dispersal estimated by mark-release-recapture in Northern Australia. American Journal of Tropical Medicine and Hygiene 58:277-282.
44. Okamoto, K. W., M. A. Robert, A. L. Lloyd, and F. Gould 2013. A reduce and replace strategy for suppressing vector-borne diseases: insights from a stochastic, spatial model. PLoS ONE 8:e81860.
45. Okamoto, K. W., M. A. Robert, F. Gould, and A. L. Lloyd 2014. Feasibly introgression of an anti-pathogen transgene into an urban mosquito population without using gene-drive. PLoS Neglected Tropical Diseases 8:e2827.
46. Phuc, H. K., M. H. Andreasen, R. S. Burton, C. Vass, M. J. Epton, G. Pape, G. Fu et al. 2007. Late-acting dominant lethal genetic systems and mosquito control. BMC Biology 5:11.
47. Popovici, J., L. A. Moreira, A. Poinsignon, I. Iturbe-ormaetxe, D. Mcnaughton, and S. L. O. Neill 2010. Assessing key safety concerns of a Wolbachia-based strategy to control dengue transmission by Aedes mosquitoes. Memórias do Instituto Oswaldo Cruz 105:957-964.
48. Ramsey, J. M., J. G. Bond, M. E. Macotela, L. Facchinelli, L. Valerio, D. M. Brown, T. W. Scott et al. 2014. A regulatory structure for working with genetically modified mosquitoes: lessons from Mexico. PLoS Neglected Tropical Diseases 8:e2623.
49. Rasgon, J. L. 2009. Multi-locus assortment (MLA) for transgene dispersal and elimination in mosquito populations. PLoS ONE 4:e5833.
50. Robert, M. A., K. Okamoto, A. L. Lloyd, and F. Gould 2013. A reduce and replace strategy for suppressing vector-borne diseases: insights from a deterministic model. PLoS ONE 8:e73233.
51. Rueda, L. M., K. J. Patel, R. C. Axtell, and R. E. Stinner 1990. Temperature-dependent development and survival rates of Culex quinquefasciatus and Aedes aegypti (Diptera: Culicidae). Journal of Medical Entomology 27:892-898.
52. Schliekelman, P., and F. Gould 2000. Pest control by the release of insects carrying a female-killing allele on multiple loci. Journal of Economic Entomology 93:1566-1579.
53. Scott, T. W., W. Takken, B. G. J. Knols, and C. Boëte 2002. The ecology of genetically modified mosquitoes. Science 298:117-119.
54. Sinkins, S. P., and F. Gould 2006. Gene drive systems for insect disease vectors. Nature Reviews Genetics 7:427-435.
55. Styer, L. M., S. L. Minnick, A. K. Sun, and T. W. Scott 2007. Mortality and reproductive dynamics of Aedes aegypti (Diptera: Culicidae) fed human blood. Vector-borne and zoonotic diseases 7:86-98.
56. Thomas, D. D., C. A. Donnelly, R. J. Wood, and L. S. Alphey 2000. Insect population control using a dominant, repressible, lethal genetic system. Science 287:2474-2476.
57. Turelli, M., and A. A. Hoffmann 1999. Microbe-induced cytoplasmic incompatibility as a mechanism for introducing transgenes into arthropod populations. Insect Molecular Biology 8:243-255.
58. Walsh, R. K., L. Facchinelli, J. M. Ramsey, J. G. Bond, and F. Gould 2011. Assessing the impact of density dependence in field populations of Aedes aegypti. Journal of Vector Ecology 36:300-307.
59. Ward, C. M., J. T. Su, Y. Huang, A. L. Lloyd, F. Gould, and B. A. Hay 2011. Medea selfish genetic elements as tools for altering traits of wild populations: a theoretical analysis. Evolution 65:1149-1162.
60. White, S. M., P. Rohani, and S. M. Sait 2010. Modelling pulsed releases for sterile insect techniques: fitness costs of sterile and transgenic males and the effects on mosquito dynamics. Journal of Applied Ecology 47:1329-1339.
61. Whitten, M. J. 1969. Automated sexing of pupae and its usefulness in control by sterile insects. Journal of Economic Entomology 62:272-273.
62. Whitten, M. J., and G. G. Foster 1975. Genetical methods of pest control. Annual Review of Entomology 20:461-476.
63. Wise de Valdez, M. R., D. Nimmo, J. Betz, H. Gong, A. A. James, L. Alphey, and W. C. Black 2011. Genetic elimination of dengue vector mosquitoes. Proceedings of the National Academy of Sciences of the United States of America 108:4772-4775.
64. Yakob, L., L. Alphey, and M. B. Bonsall 2008. Aedes aegypti control: the concomitant role of competition, space and transgenic technologies. Journal of Applied Ecology 45:1258-1265.