Large fluctuations in the effective population size of the malaria mosquito Anopheles gambiae s.s. during vector control cycle

Evolutionary Applications

Volumn 6, Issue 8, 2013, Pages 1171-1183

  Hodges, Theresa K ^a   Athrey, Giridhar ^a   Deitz, Kevin C ^a   Overgaard, Hans J ^b   Matias, Abrahan ^c   Caccone, Adalgisa ^d   Slotman, Michel A ^a  

^a TEXAS A AND M UNIVERSITY   (United States)

^b NORWEGIAN UNIVERSITY OF LIFE SCIENCES   (Norway)

^c Equatorial Guinea   (United States)

^d YALE UNIVERSITY   (United States)

Author keywords

Anopheles gambiae; Approximate Bayesian computation; Effective population size; Indoor residual spraying; Malaria; Vector control

Indexed keywords

EID: 84889644374     PISSN: 17524563     EISSN: 17524571     Source Type: Journal    
DOI: 10.1111/eva.12094     Document Type: Article

References (70)

1. Athrey, G., K. R. Barr, R. F. Lance, and P. L. Leberg 2012a. Birds in space and time: genetic changes accompanying anthropogenic habitat fragmentation in the endangered black-capped vireo (Vireo atricapilla). Evolutionary Applications 5:540-552.
2. Athrey, G., T. K. Hodges, M. R. Reddy, H. J. Overgaard, A. Matias, F. C. Ridl, I. Kleinschmidt et al. 2012b. The effective population size of malaria mosquitoes: large impact of vector control. PLos Genetics 8:e1003097.
3. Bayoh, M. N., D. K. Mathias, M. R. Odiere, F. M. Mutuku, L. Kamau, J. E. Gimnig, J. M. Vulule et al. 2010. Anopheles gambiae: historical population decline associated with regional distribution of insecticide-treated bed nets in western Nyanza Province, Kenya. Malaria Journal 9:62.
4. Beaumont, M. A. 2010. Approximate Bayesian computation in evolution and ecology. Annual Review of Ecology, Evolution, and Systematics 41:379-406.
5. Beaumont, M. A., W. Y. Zhang, and D. J. Balding 2002. Approximate Bayesian computation in population genetics. Genetics 162:2025-2035.
6. Bradley, J., A. Matias, C. Schwabe, D. Vargas, F. Monti, G. Nseng, and I. Kleinschmidt. 2012. Increased risks of malaria due to limited residual life of insecticide and outdoor biting versus protection by combined use of nets and indoor residual spraying on Bioko Island, Equatorial Guinea. Malaria Journal 11:242.
7. Cartaxo, M. F. S., C. F. J. Ayres, and D. Weetman 2011. Loss of genetic diversity in Culex quinquefasciatus targeted by a lymphatic filariasis vector control program in Recife, Brazil. Transactions of the Royal Society of Tropical Medicine and Hygiene 105:491-499.
8. Ceita, J. G. V. 1986. Malaria in Sao Tome and Principe. Paper read at Proceedings of the Conference on Malaria in Africa, at Washington, DC.
9. Coetzee, M., R. H. Hunt, R. Wilkerson, A. Della Torre, M. B. Coulibaly, and N. J. Besansky 2013. Anopheles coluzzii and Anopheles amharicus, new members of the Anopheles gambiae complex. Zootaxa 3619:246-274.
10. Corbel, V., M. Akogbeto, G. B. Damien, A. Djenontin, F. Chandre, C. Rogier, N. Moiroux et al. 2012. Combination of malaria vector control interventions in pyrethroid resistance area in Benin: a cluster randomised controlled trial. Lancet Infectious Diseases 12:617-626.
11. Cornuet, J. M., and G. Luikart 1996. Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001-2014.
12. Cornuet, J. M., F. Santos, M. A. Beaumont, C. P. Robert, J. M. Marin, D. J. Balding, T. Guillemaud et al. 2008. Inferring population history with DIY ABC: a user-friendly approach to approximate Bayesian computation. Bioinformatics 24:2713-2719.
13. Cornuet, J. M., V. Ravigne, and A. Estoup. 2010. Inference on population history and model checking using DNA sequence and microsatellite data with the software DIYABC (v1.0). BMC Bioinformatics 11:401.
14. Costantini, C., S. G. Li, A. DellaTorre, N. Sagnon, M. Coluzzi, and C. E. Taylor 1996. Density, survival and dispersal of Anopheles gambiae complex mosquitoes in a West African Sudan savanna village. Medical and Veterinary Entomology 10:203-219.
15. Cristescu, R., W. B. Sherwin, K. Handasyde, V. Cahill, and D. W. Cooper 2010. Detecting bottlenecks using BOTTLENECK 1.2.02 in wild populations: the importance of the microsatellite structure. Conservation Genetics 11:1043-1049.
16. Davidson, G. 1962. Anopheles gambiae Complex. Nature 196:907.
17. Dinov, I. D. 2006. SOCR: statistics online computational resource. Journal of Statistical Software 16:1-16.
18. Earl, D. A., and B. M. vonHoldt 2012. STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genetics Resources 4:359-361.
19. Fanello, C., F. Santolamazza, and A. Della Torre 2002. Simultaneous identification of species and molecular forms of the Anopheles gambiae complex by PCR-RFLP. Medical and Veterinary Entomology 16:461-464.
20. Goudet, J. 2002. FSTAT 2.9.3.2, a program to estimate and test gene diversities and fixation indices. Available from http://www2.unil.ch/popgen/softwares/fstat.htm (accessed on 9 September 2012).
21. Hill, W. G. 1981. Estimation of effective population-size from data on linkage disequilibrium. Genetical Research 38:209-216.
22. Hunt, R. H., M. Coetzee, and M. Fettene 1998. The Anopheles gambiae complex: a new species from Ethiopia. Transactions of the Royal Society of Tropical Medicine and Hygiene 92:231-235.
23. Jensen, A. L. 1997. Matrix population model with density-dependent recruitment for assessment of age-structured wildlife populations. Bulletin of Mathematical Biology 59:255-262.
24. Jones, O. R., and J. L. Wang 2010. COLONY: a program for parentage and sibship inference from multilocus genotype data. Molecular Ecology Resources 10:551-555.
25. Kleinschmidt, I., B. Sharp, M. Torrez, L. Benavente, and C. Schwabe 2005. Effect of indoor residual spraying on malarial parasitemia prevalence in children on Bioko Island, Equatorial Guinea [MIM-IK-219912]. Acta Tropica 95:S214-S215.
26. Kleinschmidt, I., C. Schwabe, M. Shiva, J. L. Segura, V. Sima, S. J. A. Mabunda, and M. Coleman 2009. Combining indoor residual spraying and insecticide-treated net interventions. American Journal of Tropical Medicine and Hygiene 81:519-524.
27. Lombaert, E., T. Guillemaud, C. E. Thomas, L. J. L. Handley, J. Li, S. Wang, H. Pang et al. 2011. Inferring the origin of populations introduced from a genetically structured native range by approximate Bayesian computation: case study of the invasive ladybird Harmonia axyridis. Molecular Ecology 20:4654-4670.
28. Luikart, G., N. Ryman, D. A. Tallmon, M. K. Schwartz, and F. W. Allendorf 2010. Estimation of census and effective population sizes: the increasing usefulness of DNA-based approaches. Conservation Genetics 11:355-373.
29. Midega, J. T., E. J. Muturi, F. N. Baliraine, C. M. Mbogo, J. Githure, J. C. Beier, and G. Y. Yan 2010. Population structure of Anopheles gambiae along the Kenyan coast. Acta Tropica 114:103-108.
30. N'Guessan, R., V. Corbel, M. Akogbeto, and M. Rowland 2007. Reduced efficacy of insecticide-treated nets and indoor residual spraying for malaria control in pyrethroid resistance area, Benin. Emerging Infectious Diseases 13:199-206.
31. Okumu, F. O., and S. J. Moore. 2011. Combining indoor residual spraying and insecticide-treated nets for malaria control in Africa: a review of possible outcomes and an outline of suggestions for the future. Malaria Journal 10:208.
32. Olayemi, I. K., and A. T. Ande 2009. Life table analysis of Anopheles gambiae (Diptera: Culicidae) in relation to malaria transmission. Journal of Vector Borne Diseases 46:295-298.
33. Overgaard, H. J., V. P. Reddy, S. Abaga, A. Matias, M. R. Reddy, V. Kulkarni, C. Schwabe et al. 2012. Malaria transmission after five years of vector control on Bioko Island, Equatorial Guinea. Parasit Vectors 5:253.
34. Paaijmans, K. P., M. O. Wandago, A. K. Githeko, and W. Takken 2007. Unexpected high losses of Anopheles gambiae larvae due to rainfall. PLoS ONE 2:e1146.
35. Peakall, R., and P. E. Smouse 2006. GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Molecular Ecology Notes 6:288-295.
36. Peter, B. M., D. Wegmann, and L. Excoffier 2010. Distinguishing between population bottleneck and population subdivision by a Bayesian model choice procedure. Molecular Ecology 19:4648-4660.
37. Pinto, J., M. J. Donnelly, C. A. Sousa, V. Gil, C. Ferreira, N. Elissa, V. E. Do Rosario et al. 2002. Genetic structure of Anopheles gambiae (Diptera: Culicidae) in Sao Tome and Principe (West Africa): implications for malaria control. Molecular Ecology 11:2183-2187.
38. Pinto, J., M. J. Donnelly, C. A. Sousa, J. Malta-Vacas, V. Gil, C. Ferreira, V. Petrarca et al. 2003. An island within an island: genetic differentiation of Anopheles gambiae in Sao Tome, West Africa, and its relevance to malaria vector control. Heredity 91:407-414.
39. Pringle, G. 1967. Malaria in pare area of Tanzania III. The course of malaria transmission since suspension of an experimental programme of residual insecticide spraying. Transactions of the Royal Society of Tropical Medicine and Hygiene 61:69-79.
40. Pritchard, J. K., M. Stephens, and P. Donnelly 2000. Inference of population structure using multilocus genotype data. Genetics 155:945-959.
41. R Core Team (2012). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, http://www.R-project.org/ (accessed on 15 October 2012).
42. Raymond, M., and F. Rousset 1995. Genepop (version-1.2) - population-genetics software for exact tests and ecumenicism. Journal of Heredity 86:248-249.
43. Reddy, M. R., H. J. Overgaard, S. Abaga, V. P. Reddy, A. Caccone, A. E. Kiszewski, and M. A. Slotman. 2011. Outdoor host seeking behaviour of Anopheles gambiae mosquitoes following initiation of malaria vector control on Bioko Island, Equatorial Guinea. Malaria Journal 10:184.
44. Rousset, F. 2008. GENEPOP ' 007: a complete re-implementation of the GENEPOP software for Windows and Linux. Molecular Ecology Resources 8:103-106.
45. Rowland, M., P. Mahmood, J. Iqbal, I. Carneiro, and D. Chavasse 2000. Indoor residual spraying with alphacypermethrin controls malaria in Pakistan: a community randomized trial. Tropical Medicine & International Health 5:472-481.
46. Russell, T. L., N. J. Govella, S. Azizi, C. J. Drakeley, S. P. Kachur, and G. F. Killeen. 2011. Increased proportions of outdoor feeding among residual malaria vector populations following increased use of insecticide-treated nets in rural Tanzania. Malaria Journal 10:80.
47. Sharp, B., I. Kleinschmidt, F. Ridl, and J. Kuklinski 2005. Effect of Indoor Residual Spraying on numbers and sporozoite rates of A. funestus and A. gambiae s.s on Bioko Island, Equatorial Guinea [MIM-JK-38665]. Acta Tropica 95:S498-S499.
48. Sharp, B. L., F. C. Ridl, D. Govender, J. Kuklinski, and I. Kleinschmidt. 2007. Malaria vector control by indoor residual insecticide spraying on the tropical island of Bioko, Equatorial Guinea. Malaria Journal 6:52.
49. Silver, J. B. 2008. Mosquito Ecology: Field Sampling Methods, 3rd edn. Springer, New York, NY.
50. Simard, F., T. Lehmann, J. J. Lemasson, M. Diatta, and D. Fontenille 2000. Persistence of Anopheles arabiensis during the severe dry season conditions in Senegal: an indirect approach using microsatellite loci. Insect Molecular Biology 9:467-479.
51. Sousa, C. A., J. Pinto, A. P. G. Almeida, C. Ferreira, V. E. Do Rosari, and J. D. Charlwood 2001. Dogs as a favored host choice of Anopheles gambiae sensu stricto (Diptera: Culicidae) of Sao Tome, west Africa. Journal of Medical Entomology 38:122-125.
52. Takken, W. 2002. Do insecticide-treated bednets have an effect on malaria vectors? Tropical Medicine & International Health 7:1022-1030.
53. Tallmon, D. A., D. Gregovich, R. S. Waples, C. S. Baker, J. Jackson, B. L. Taylor, E. Archer et al. 2010. When are genetic methods useful for estimating contemporary abundance and detecting population trends? Molecular Ecology Resources 10:684-692.
54. Taylor, C. E., Y. T. Toure, M. Coluzzi, and V. Petrarca 1993. Effective population-size and persistence of Anopheles arabiensis during the dry season in West-Africa. Medical and Veterinary Entomology 7:351-357.
55. Touré, Y. T., G. Dolo, V. Petrarca, S. F. Traore, M. Bouare, A. Dao, J. Carnahan et al. 1998. Mark-release-recapture experiments with Anopheles gambiae sl in Banambani Village, Mali, to determine population size and structure. Medical and Veterinary Entomology 12:74-83.
56. Van Oosterhout, C., W. F. Hutchinson, D. P. M. Wills, and P. Shipley 2004. MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes 4:535-538.
57. Wang, J. L. 2001. A pseudo-likelihood method for estimating effective population size from temporally spaced samples. Genetical Research 78:243-257.
58. Wang, J. 2009. A new method for estimating effective population sizes from a single sample of multilocus genotypes. Molecular Ecology 18:2148-2164.
59. Wang, J. L., and M. C. Whitlock 2003. Estimating effective population size and migration rates from genetic samples over space and time. Genetics 163:429-446.
60. Waples, R. S. 2006. A bias correction for estimates of effective population size based on linkage disequilibrium at unlinked gene loci. Conservation Genetics 7:167-184.
61. Waples, R. S., and C. Do 2008. LDNE: a program for estimating effective population size from data on linkage disequilibrium. Molecular Ecology Resources 8:753-756.
62. e using highly variable genetic markers: a largely untapped resource for applied conservation and evolution. Evolutionary Applications 3:244-262.
63. Wegmann, D., and L. Excoffier 2010. Bayesian inference of the demographic history of chimpanzees. Molecular Biology and Evolution 27:1425-1435.
64. White, G. B. 1974. Anopheles-Gambiae complex and disease transmission in Africa. Transactions of the Royal Society of Tropical Medicine and Hygiene 68:278-302.
65. Wondji, C., F. Simard, T. Lehmann, E. Fondjo, S. Same-Ekobo, and D. Fontenille 2005. Impact of insecticide-treated bed nets implementation on the genetic structure of Anopheles arabiensis in an area of irrigated rice fields in the Sahelian region of Cameroon. Molecular Ecology 14:3683-3693.
66. World Malaria Report 2011. World Health Organization. Switzerland, Geneva.
67. Wright, S. 1931. Evolution in Mendelian populations. Genetics 16:0097-0159.
68. Wright, S. 1938. Size of population and breeding structure in relation to evolution. Science 87:430-431.
69. Zheng, L. B., M. O. Benedict, A. J. Cornel, F. H. Collins, and F. C. Kafatos 1996. An integrated genetic map of the African human malaria vector mosquito, Anopheles gambiae. Genetics 143:941-952.
70. Zhou, G. F., A. K. Githeko, N. Minakawa, and G. Y. Yan. 2010. Community-wide benefits of targeted indoor residual spray for malaria control in the Western Kenya Highland. Malaria Journal 9:67.