Geographic population structure of the African malaria vector Anopheles gambiae suggests a role for the forest-savannah biome transition as a barrier to gene flow

Evolutionary Applications

Volumn 6, Issue 6, 2013, Pages 910-924

  Pinto, J ^a   Egyir Yawson, A ^a,b   Vicente, J L ^a   Gomes, B ^a   Santolamazza, F ^c   Moreno, M ^d   Charlwood, J D ^a,e   Simard, F ^f   Elissa, N ^g   Weetman, D ^e   Donnelly, M J ^e   Caccone, A ^h   della Torre, A ^c  

^a INSTITUTO DE HIGIENE E MEDICINA TROPICAL   (Portugal)

^b Ghana Atomic Energy Commission   (Ghana)

^c SAPIENZA UNIVERSITY OF ROME   (Italy)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e LIVERPOOL SCHOOL OF TROPICAL MEDICINE   (United Kingdom)

^f INSTITUT DE RECHERCHE POUR LE DÉVELOPPEMENT   (France)

^g INSTITUT PASTEUR DE MADAGASCAR   (Madagascar)

^h YALE UNIVERSITY   (United States)

Author keywords

Anopheles gambiae; Geographic regions; Microsatellites; Molecular forms; Population structure

Indexed keywords

EID: 84882985458     PISSN: 17524563     EISSN: 17524571     Source Type: Journal    
DOI: 10.1111/eva.12075     Document Type: Article

References (77)

1. Antao, T., A. Lopes, R. J. Lopes, A. Beja-Pereira, and G. Luikart 2008. LOSITAN: a workbench to detect molecular adaptation based on a Fst-outlier method. BMC Bioinformatics 9:323.
2. Beaumont, M. A., and R. A. Nichols 1996. Evaluating loci for use in the genetic analysis of population structure. Proceedings of the Royal Society B: Biological Sciences 263:1619-1626.
3. Calzetta, M., F. Santolamazza, G. C. Carrara, P. J. Cani, F. Fortes, M. A. Di Deco, A. della Torre et al. 2008. Distribution and chromosomal characterization of the Anopheles gambiae complex in Angola. American Journal of Tropical Medicine and Hygiene 78:169-175.
4. Caputo, B., D. Nwakanma, M. Jawara, M. Adiamoh, I. Dia, L. Konate, V. Petrarca et al. 2008. Anopheles gambiae complex along The Gambia river, with particular reference to the molecular forms of An. gambiae s.s. Malaria Journal 7:182.
5. Caputo, B., F. Santolamazza, J. L. Vicente, D. C. Nwakanma, M. Jawara, K. Palsson, T. Jaenson et al. 2011. The "far-west" of Anopheles gambiae molecular forms. PLoS ONE 6:e16415.
6. Chen, C., E. Durand, F. Forbes, and O. Francois 2007. Bayesian clustering algorithms ascertaining spatial population structure: a new computer program and a comparison study. Molecular Ecology Notes 7:747-756.
7. Choi, K. S., and H. Townson 2012. Evidence for X-linked introgression between molecular forms of Anopheles gambiae from Angola. Medical and Veterinary Entomology 26:218-227.
8. Coluzzi, M., A. Sabatini, V. Petrarca, and M. A. Di Deco 1979. Chromosomal differentiation and adaptation to human environments in the Anopheles gambiae complex. Transactions of the Royal Society of Tropical Medicine and Hygiene 73:483-497.
9. Coluzzi, M., A. Sabatini, A. della Torre, M. A. Di Deco, and V. Petrarca 2002. A polytene chromosome analysis of the Anopheles gambiae species complex. Science 298:1415-1418.
10. Costantini, C., D. Ayala, W. M. Guelbeogo, M. Pombi, C. Y. Some, I. H. Bassole, K. Ose et al. 2009. Living at the edge: biogeographic patterns of habitat segregation conform to speciation by niche expansion in Anopheles gambiae. BMC Ecology 9:16.
11. Crispo, E., J. S. Moore, J. A. Lee-Yaw, S. M. Gray, and B. C. Haller 2011. Broken barriers: human-induced changes to gene flow and introgression in animals: an examination of the ways in which humans increase genetic exchange among populations and species and the consequences for biodiversity. BioEssays 33:508-518.
12. Dabiré, K. R., A. Diabaté, M. Namountougou, K. H. Toé, A. Ouari, P. Kengne, C. Bass et al. 2009. Distribution of pyrethroid and DDT resistance and the L1014F kdr mutation in Anopheles gambiae s.l. from Burkina Faso West Africa. Transactions of the Royal Society of Tropical Medicine and Hygiene 103:1113-1120.
13. Deitz, K. C., G. Athrey, M. R. Reddy, H. J. Overgaard, A. Matias, J. Musa, A. della Torre et al. 2012. Genetic isolation within the malaria mosquito Anopheles melas. Molecular Ecology 21:4498-4513.
14. Diabaté, A., R. K. Dabiré, K. Heidenberger, J. Crawford, W. O. Lamp, L. E. Culler, and T. Lehmann 2008. Evidence for divergent selection between the molecular forms of Anopheles gambiae: role of predation. BMC Evolutionary Biology 8:5.
15. Donnelly, M. J., N. Cuamba, J. D. Charlwood, F. H. Collins, and H. Townson 1999. Population structure in the malaria vector, Anopheles arabiensis Patton, in East Africa. Heredity 83:408-417.
16. Donnelly, M. J., F. Simard, and T. Lehmann 2002. Evolutionary studies of malaria vectors. Trends in Parasitology 18:75-80.
17. Durand, E., F. Jay, O. E. Gaggiotti, and O. Francois 2009. Spatial inference of admixture proportions and secondary contact zones. Molecular Biology and Evolution 26:1963-1973.
18. Dyer, N. A., A. Furtado, J. Cano, F. Ferreira, M. O. Afonso, N. Ndong-Mabale, P. Ndong-Asumu et al. 2009. Evidence for a discrete evolutionary lineage within Equatorial Guinea suggests that the tsetse fly Glossina palpalis palpalis exists as a species complex. Molecular Ecology 18:3268-3282.
19. 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.
20. El Mousadik, A., and R. J. Petit 1996. High level of genetic differentiation for allelic richness among populations of the argan tree [Argania spinosa L. Skeels] endemic to Morocco. Theoretical and Applied Genetics 92:832-839.
21. Esnault, C., M. Boulesteix, J. B. Duchemin, A. A. Koffi, F. Chandre, R. Dabiré, V. Robert et al. 2008. High genetic differentiation between the M and S molecular forms of Anopheles gambiae in Africa. PLoS ONE 3:e1968.
22. Estoup, A., P. Jarne, and J.-M. Cornuet 2002. Homoplasy and mutation model at microsatellite loci and their consequences for population genetics analysis. Molecular Ecology 11:1591-1604.
23. Etang, J., J. L. Vicente, P. Nwane, M. Chouaibou, I. Morlais, V. E. do Rosario, F. Simard et al. 2009. Polymorphism of intron-1 in the voltage-gated sodium channel gene of Anopheles gambiae s.s. populations from Cameroon with emphasis on insecticide knockdown resistance mutations. Molecular Ecology 18:3076-3086.
24. Evanno, G., J. Goudet, and S. Regnaut 2005. Detecting the number of clusters of individuals using the software structure: a simulation study. Molecular Ecology 14:2611-2620.
25. Favia, G., A. della Torre, M. Bagayoko, A. Lanfrancotti, N. Sagnon, Y. T. Touré, and M. Coluzzi 1997. Molecular identification of sympatric chromosomal forms of Anopheles gambiae and further evidence of their reproductive isolation. Insect Molecular Biology 6:377-383.
26. François, O., S. Ancelet, and G. Guillot 2006. Bayesian clustering using hidden Markov random fields in spatial population genetics. Genetics 174:805-816.
27. Frantz, A. C., S. Cellina, A. Krier, L. Schley, and T. Burke 2009. Using spatial Bayesian methods to determine the genetic structure of a continuously distributed population: clusters or isolation by distance? Journal of Applied Ecology 46:493-505.
28. Gimonneau, G., J. Bouyer, S. Morand, N. J. Besansky, A. Diabate, and F. Simard 2010. A behavioral mechanism underlying ecological divergence in the malaria mosquito Anopheles gambiae. Behavioral Ecology 21:1087-1092.
29. Gimonneau, G., M. Pombi, M. Choisy, S. Morand, R. K. Dabiré, and F. Simard 2012. Larval habitat segregation between the molecular forms of the mosquito Anopheles gambiae in a rice field area of Burkina Faso, West Africa. Medical and Veterinary Entomology 26:9-17.
30. Goudet, J. 1995. FSTAT version 1.2: a computer software to calculate F-statistics. Journal of Heredity 86:485-486.
31. Guillot, G., R. Leblois, A. Coulon, and A. C. Frantz 2009. Statistical methods in spatial genetics. Molecular Ecology 18:4734-4756.
32. Holm, S. 1979. A simple sequentially rejective multiple test procedure. Scandinavian Journal of Statistics 6:65-70.
33. Jakobsson, M., and N. A. Rosenberg 2007. CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23:1801-1806.
34. Kamdem, C., B. Tene Fossog, F. Simard, J. Etouna, C. Ndo, P. Kengne, P. Boussès et al. 2012. Anthropogenic habitat disturbance and ecological divergence between incipient species of the malaria mosquito Anopheles gambiae. PLoS ONE 7:e39453.
35. Kaufmann, C., and H. Briegel 2004. Flight performance of the malaria vectors Anopheles gambiae and Anopheles atroparvus. Journal of Vector Ecology 29:140-153.
36. Lanzaro, G. C., Y. T. Touré, J. Carnahan, L. Zheng, G. Dolo, S. Traoré, V. Petrarca et al. 1998. Complexities in the genetic structure of Anopheles gambiae populations in west Africa as revealed by microsatellite DNA analysis. Proceedings of the National Academy of Sciences of the United States of America 95:14260-14265.
37. Lawniczak, M. K., S. J. Emrich, A. K. Holloway, A. P. Regier, M. Olson, B. White, S. Redmond et al. 2010. Widespread divergence between incipient Anopheles gambiae species revealed by whole genome sequences. Science 330:512-514.
38. Lee, Y., A. J. Cornel, C. R. Meneses, A. Fofana, A. G. Andrianarivo, R. D. McAbee, E. Fondjo et al. 2009. Ecological and genetic relationships of the Forest-M form among chromosomal and molecular forms of the malaria vector Anopheles gambiae sensu stricto. Malaria Journal 8:75.
39. Lehmann, T., W. A. Hawley, H. Grebert, M. Danga, F. Atieli, and F. H. Collins 1999. The rift valley complex as a barrier to gene flow for Anopheles gambiae in Kenya. Journal of Heredity 90:613-621.
40. Lehmann, T., M. Licht, N. Elissa, B. T. Maega, J. M. Chimumbwa, F. T. Watsenga, C. S. Wondji et al. 2003. Population Structure of Anopheles gambiae in Africa. Journal of Heredity 94:133-147.
41. Lynd, A., D. Weetman, S. Barbosa, A. Egyir Yawson, S. Mitchell, J. Pinto, I. Hastings et al. 2010. Field, genetic, and modeling approaches show strong positive selection acting upon an insecticide resistance mutation in Anopheles gambiae s.s. Molecular Biology and Evolution 27:1117-1125.
42. Marsden, C. D., Y. Lee, C. C. Nieman, M. R. Sanford, J. Dinis, C. Martins, A. Rodrigues et al. 2011. Asymmetric introgression between the M and S forms of the malaria vector, Anopheles gambiae, maintains divergence despite extensive hybridization. Molecular Ecology 20:4983-4994.
43. Martinez-Torres, D., F. Chandre, M. S. Williamson, F. Darriet, J. B. Bergé, A. L. Devonshire, P. Guillet et al. 1998. Molecular characterization of pyrethroid knockdown resistance kdr in the major malaria vector Anopheles gambiae s.s. Insect Molecular Biology 7:179-184.
44. Moreno, M., P. Salgueiro, J. L. Vicente, J. Cano, P. J. Berzosa, A. de Lucio, F. Simard et al. 2007. Genetic population structure of Anopheles gambiae in Equatorial Guinea. Malaria Journal 6:137.
45. Ndo, C., C. Antonio-Nkondjio, A. Cohuet, D. Ayala, P. Kengne, I. Morlais, P. H. Awono-Ambene et al. 2010. Population genetic structure of the malaria vector Anopheles nili in sub-Saharan Africa. Malaria Journal 9:161.
46. Neafsey, D. E., M. K. Lawniczak, D. J. Park, S. N. Redmond, M. B. Coulibaly, S. F. Traoré, N. Sagnon et al. 2010. SNP genotyping defines complex gene-flow boundaries among African malaria vector mosquitoes. Science 330:514-517.
47. Nei, M. 1987. Molecular Evolutionary Genetics. Columbia University Press, New York.
48. Nielsen, E. E., L. A. Bach, and P. Kotlicki 2006. Hybridlab version 1.0: a programme for generating simulated hybrids from population samples. Molecular Ecology Notes 6:971-973.
49. Oliveira, E., P. Salgueiro, K. Palsson, J. L. Vicente, A. P. Arez, T. G. Jaenson, A. Caccone et al. 2008. High levels of hybridization between molecular forms of Anopheles gambiae from Guinea Bissau. Journal of Medical Entomology 45:1057-1063.
50. 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.
51. Pinto, J., M. J. Donnelly, C. A. Sousa, V. Gil, C. Ferreira, N. Elissa, V. E. do Rosário et al. 2002. Genetic structure of Anopheles gambiae Diptera: Culicidae in São Tomé and Príncipe West Africa: implications for malaria control. Molecular Ecology 11:2183-2187.
52. Pinto, J., A. Lynd, J. L. Vicente, F. Santolamazza, N. P. Randle, G. Gentile, M. Moreno et al. 2007. Multiple origins of knockdown resistance mutations in the Afrotropical mosquito vector Anopheles gambiae. PLoS ONE 2:e1243.
53. Pritchard, J. K., M. Stephens, and P. Donnelly 2000. Inference of population structure using multilocus genotype data. Genetics 155:945-959.
54. Raymond, M., and F. Rousset 1995. GENEPOP version 1.2: population genetics software for exact tests and ecumenicism. Journal of Heredity 86:248-249.
55. Ridl, F. C., C. Bass, M. Torrez, D. Govender, V. Ramdeen, L. Yellot, A. E. Edu et al. 2008. A pre-intervention study of malaria vector abundance in Rio Muni, Equatorial Guinea: their role in malaria transmission and the incidence of insecticide resistance alleles. Malaria Journal 7:194.
56. Riehle, M. M., W. M. Guelbeogo, A. Gneme, K. Eiglmeier, I. Holm, E. Bischoff, T. Garnier et al. 2011. A cryptic subgroup of Anopheles gambiae is highly susceptible to human malaria parasites. Science 331:596-598.
57. Rousset, F. 1997. Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145:1219-1228.
58. Santolamazza, F., M. Calzetta, J. Etang, E. Barrese, I. Dia, A. Caccone, M. J. Donnelly et al. 2008. Distribution of knock-down resistance mutations in Anopheles gambiae molecular forms in west and west-central Africa. Malaria Journal 7:74.
59. Schwartz, M. K., and K. S. Mckelvey 2009. Why sampling scheme matters: the effect of sampling scheme on landscape genetic results. Conservation Genetics 10:441-452.
60. Scott, J. A., W. G. Brogdon, and F. H. Collins. 1993. Identification of single specimens of the Anopheles gambiae complex by the polymerase chain reaction. American Journal of Tropical Medicine and Hygiene 49:520-529.
61. Simard, F., D. Ayala, G. C. Kamdem, M. Pombi, J. Etouna, K. Ose, J. M. Fotsing et al. 2009. Ecological niche partitioning between Anopheles gambiae molecular forms in Cameroon: the ecological side of speciation. BMC Ecology 9:17.
62. Slotman, M. A., M. M. Mendez, A. D. Torre, G. Dolo, Y. T. Touré, and A. Caccone 2006. Genetic differentiation between the BAMAKO and SAVANNA chromosomal forms of Anopheles gambiae as indicated by amplified fragment length polymorphism analysis. American Journal of Tropical Medicine and Hygiene 74:641-648.
63. Slotman, M. A., F. Tripet, A. J. Cornel, C. R. Meneses, Y. Lee, L. J. Reimer, T. C. Thiemann et al. 2007. Evidence for subdivision within the M molecular form of Anopheles gambiae. Molecular Ecology 16:639-649.
64. Taylor, C., Y. T. Touré, J. Carnahan, D. E. Norris, G. Dolo, S. F. Traoré, F. E. Edillo et al. 2001. Gene flow among populations of the malaria vector, Anopheles gambiae, in Mali, West Africa. Genetics 157:743-750.
65. della Torre, A., C. Fanello, M. Akogbeto, J. Dossou-yovo, G. Favia, V. Petrarca, and M. Coluzzi 2001. Molecular evidence of incipient speciation within Anopheles gambiae s.s. in West Africa. Insect Molecular Biology 10:9-18.
66. della Torre, A., C. Costantini, N. J. Besansky, A. Caccone, V. Petrarca, J. R. Powell, and M. Coluzzi 2002. Speciation within Anopheles gambiae-the glass is half full. Science 298:115-117.
67. della Torre, A., Z. Tu, and V. Petrarca 2005. On the distribution and genetic differentiation of Anopheles gambiae s.s. molecular forms. Insect Biochemistry and Molecular Biology 35:755-769.
68. Turner, T. L., M. W. Hahn, and S. V. Nuzhdin 2005. Genomic islands of speciation in Anopheles gambiae. PLoS Biology 3:e285.
69. UNEP 2010. Africa water atlas. United Nations Environment Programme. Progress Press Limited, Malta. http://na.unep.net/atlas/africaWater/book.php (accessed on January 2013).
70. Vähä, J. P., and C. R. Primmer 2006. Efficiency of model-based Bayesian methods for detecting hybrid individuals under different hybridization scenarios and with different numbers of loci. Molecular Ecology 15:63-72.
71. 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.
72. Weetman, D., C. S. Wilding, K. Steen, J. C. Morgan, F. Simard, and M. J. Donnelly 2010. Association mapping of insecticide resistance in wild Anopheles gambiae populations: major variants identified in a low-linkage disequilbrium genome. PLoS ONE 5:e13140.
73. Weetman, D., C. S. Wilding, K. Steen, J. Pinto, and M. J. Donnelly 2012. Gene flow-dependent genomic divergence between Anopheles gambiae M and S forms. Molecular Biology and Evolution 29:279-291.
74. Weir, B. S., and C. C. Cockerham 1984. Estimating F-statistics for the analysis of population structure. Evolution 38:1358-1370.
75. White, B. J., C. Cheng, F. Simard, C. Costantini, and N. J. Besansky 2010. Genetic association of physically unlinked islands of genomic divergence in incipient species of Anopheles gambiae. Molecular Ecology 19:925-939.
76. White, B. J., M. K. Lawniczak, C. Cheng, M. B. Coulibaly, M. D. Wilson, N. Sagnon, C. Costantini et al. 2011. Adaptive divergence between incipient species of Anopheles gambiae increases resistance to Plasmodium. Proceedings of the National Academy of Sciences of the United States of America 108:244-249.
77. Yawson, A. E., D. Weetman, M. D. Wilson, and M. J. Donnelly 2007. Ecological zones rather than molecular forms predict genetic differentiation in the malaria vector Anopheles gambiae s.s. in Ghana. Genetics 175:751-761.