Ecological niche partitioning between Anopheles gambiae molecular forms in Cameroon: The ecological side of speciation

BMC Ecology

Volumn 9, Issue , 2009, Pages

  Simard, Frédéric ^a,b,h   Ayala, Diego ^a   Kamdem, Guy Colince ^a,b   Pombi, Marco ^c   Etouna, Joachim ^d   Ose, Kenji ^e   Fotsing, Jean Marie ^e   Fontenille, Didier ^a   Besansky, Nora J ^f   Costantini, Carlo ^a,g  

^a INSTITUT DE RECHERCHE POUR LE DÉVELOPPEMENT   (France)

^b Laboratoire de Recherche sur le Paludisme Yaounde   (Cameroon)

^c SAPIENZA UNIVERSITY OF ROME   (Italy)

^d National Institute of Cartography   (Cameroon)

^e US140   (Guyana)

^f UNIVERSITY OF NOTRE DAME   (United States)

^g Institut de Recherche en Sciences de la Santé Direction Régionale de l'Ouest   (Burkina Faso)

^h IRD/IRSS DRO ^*  (Burkina Faso)

Author keywords

[No Author keywords available]

Indexed keywords

ANOPHELES GAMBIAE;

ANIMAL; ANOPHELES GAMBIAE; ARTICLE; BAYES THEOREM; BIOLOGICAL MODEL; CAMEROON; CHROMOSOME INVERSION; CLASSIFICATION; CLUSTER ANALYSIS; ECOLOGY; ECOSYSTEM; GENETIC POLYMORPHISM; GENETICS; GEOGRAPHIC INFORMATION SYSTEM; KARYOTYPING; MOLECULAR EVOLUTION; POPULATION GENETICS; SPECIES DIFFERENCE; SPECIES DIFFERENTIATION;

ANIMALS; ANOPHELES GAMBIAE; BAYES THEOREM; CAMEROON; CLUSTER ANALYSIS; ECOLOGY; ECOSYSTEM; EVOLUTION, MOLECULAR; GENETIC SPECIATION; GENETICS, POPULATION; GEOGRAPHIC INFORMATION SYSTEMS; INVERSION, CHROMOSOME; KARYOTYPING; MODELS, GENETIC; POLYMORPHISM, GENETIC; SPECIES SPECIFICITY;

EID: 67649143681     PISSN: None     EISSN: 14726785     Source Type: Journal    
DOI: 10.1186/1472-6785-9-17     Document Type: Article

References (92)

1. Chromosomal inversion intergradation and incipient speciation in Anopheles gambiae. M Coluzzi V Petrarca MA Di Deco, Bollettino di Zoologia 1985 52 45 63
2. A polytene chromosome analysis of the Anopheles gambiae species complex. M Coluzzi A Sabatini A Della Torre MA Di Deco V Petrarca, Science 2002 298 5597 1415 1418 10.1126/science.1077769 12364623
3. Speciation within Anopheles gambiae the glass is half full. A della Torre C Costantini NJ Besansky A Caccone V Petrarca JR Powell M Coluzzi, Science 2002 298 5591 115 117 10.1126/science.1078170 12364784
4. Population Structure of Anopheles gambiae in Africa. T Lehmann M Licht N Elissa BT Maega JM Chimumbwa FT Watsenga CS Wondji F Simard WA Hawley, J Hered 2003 94 2 133 147 10.1093/jhered/esg024 12721225
5. Centromere-proximal differentiation and speciation in Anopheles gambiae. AD Stump MC Fitzpatrick NF Lobo S Traoré NF Sagnon C Costantini FH Collins NJ Besansky, PNAS 2005 102 44 15930 15935 16247019 10.1073/pnas. 0508161102
6. Sex-linked differentiation between incipient species of Anopheles gambiae. AD Stump JA Shoener C Costantini NF Sagnon NJ Besansky, Genetics 2005 169 3 1509 1519 15654109 10.1534/genetics.104.035303
7. Genomic islands of speciation in Anopheles gambiae. TL Turner MW Hahn SV Nuzhdin, PLoS Biol 2005 3 9 e285 16076241 10.1371/journal.pbio.0030285
8. Evidence for genetic differentiation between the molecular forms M and S within the Forest chromosomal form of Anopheles gambiae in an area of sympatry. C Wondji F Simard D Fontenille, Insect Mol Biol 2002 11 1 11 19 10.1046/j.0962-1075.2001.00306.x 11841498
9. On the distribution and genetic differentiation of Anopheles gambiae s.s. molecular forms. A della Torre Z Tu V Petrarca, Insect Biochem Mol Biol 2005 35 7 755 769 10.1016/j.ibmb.2005.02.006 15894192
10. Evaluating the effect of postmating isolation between molecular forms of Anopheles gambiae (Diptera: Culicidae). A Diabaté RK Dabire N Millogo T Lehmann, J Med Entomol 2007 44 1 60 64 10.1603/0022-2585(2007)44[60:ETEOPI]2.0. CO;2 17294921
11. DNA analysis of transferred sperm reveals significant levels of gene flow between molecular forms of Anopheles gambiae. F Tripet YT Touré CE Taylor DE Norris G Dolo GC Lanzaro, Mol Ecol 2001 10 7 1725 1732 10.1046/j.0962-1083.2001.01301.x 11472539
12. Molecular evidence of incipient speciation within Anopheles gambiae s.s. in West Africa. A della Torre C Fanello M Akogbeto J Dossou-yovo G Favia V Petrarca M Coluzzi, Insect Mol Biol 2001 10 1 9 18 10.1046/j.1365-2583.2001. 00235.x 11240632
13. Spatial and habitat distribution of Anopheles gambiae and Anopheles arabiensis (Diptera: Culicidae) in Banambani village, Mali. FE Edillo YT Touré GC Lanzaro G Dolo CE Taylor, J Med Entomol 2002 39 1 70 77 11931274 (Pubitemid 135694289)
14. Species and populations of the Anopheles gambiae complex in Cameroon with special emphasis on chromosomal and molecular forms of Anopheles gambiae s.s. C Wondji S Frederic V Petrarca J Etang F Santolamazza A Della Torre D Fontenille, J Med Entomol 2005 42 6 998 1005 10.1603/0022-2585(2005)042[0998:SAPOTA]2.0. CO;2 16465741 (Pubitemid 41719337)
15. Ecological zones rather than molecular forms predict genetic differentiation in the malaria vector Anopheles gambiae s.s. in Ghana. AE Yawson D Weetman MD Wilson MJ Donnelly, Genetics 2007 175 2 751 761 17110481 10.1534/genetics.106.065888
16. Chromosome speciation: humans, Drosophila, and mosquitoes. FJ Ayala M Coluzzi, PNAS 2005 102 Suppl 1 6535 6542 15851677 10.1073/pnas.0501847102
17. The sympatric occurrence of two molecular forms of the malaria vector Anopheles gambiae Giles sensu stricto in Kanyemba, in the Zambezi Valley, Zimbabwe. HT Masendu RH Hunt J Govere BD Brooke TS Awolola M Coetzee, Trans R Soc Trop Med Hyg 2004 98 7 393 396 10.1016/j.trstmh.2003.10.006 15138074
18. The molecular forms of Anopheles gambiae: A phenotypic perspective. T Lehmann A Diabate, Infect Genet Evol 2008 8 5 737 746 10.1016/j.meegid.2008.06. 003 18640289
19. Evidence for divergent selection between the molecular forms of Anopheles gambiae: role of predation. A Diabaté RK Dabiré K Heidenberger J Crawford WO Lamp LE Culler T Lehmann, BMC Evol Biol 2008 8 5 18190719 10.1186/1471-2148-8-5
20. Larval development of the molecular forms of Anopheles gambiae (Diptera: Culicidae) in different habitats: a transplantation experiment. A Diabaté RK Dabire EH Kim R Dalton N Millogo T Baldet F Simard JE Gimnig WA Hawley T Lehmann, J Med Entomol 2005 42 4 548 553 10.1603/0022-2585(2005)042[0548:LDOTMF] 2.0.CO;2 16119542 (Pubitemid 41040455)
21. Anopheles gambiae larval habitats in an arid savanna village of Burkina Faso: characterization of bionomical parameters and potential markers of ecological niche partitioning among three sympatric taxa of the complex. M Pombi, PhD Thesis Dept. Public Health, Univ. of Rome "La Sapienza", Rome, Italy 2004
22. Molecular identification of sympatric chromosomal forms of Anopheles gambiae and further evidence of their reproductive isolation. G Favia A della Torre M Bagayoko A Lanfrancotti N Sagnon YT Touré M Coluzzi, Insect Mol Biol 1997 6 4 377 383 10.1046/j.1365-2583.1997.00189.x 9359579 (Pubitemid 27452952)
23. Chromosomal differentiation and adaptation to human environments in the Anopheles gambiae complex. M Coluzzi A Sabatini V Petrarca MA Di Deco, Trans R Soc Trop Med Hyg 1979 73 5 483 497 10.1016/0035-9203(79)90036-1 394408
24. Ecological studies in the chromosomal form Mopti of Anopheles gambiae s.str. in Mali, West Africa. Y Touré V Petrarca SF Traore A Coulibaly HM Maiga O Sankare M Sow MA Di Deco M Coluzzi, Genetica 1994 94 213 223 10.1007/BF01443435 7896141
25. The distribution and inversion polymorphism of chromosomally recognized taxa of the Anopheles gambiae complex in Mali, West Africa. YT Touré V Petrarca SF Traoré A Coulibaly HM Maiga O Sankaré M Sow MA Di Deco M Coluzzi, Parassitologia 1998 40 4 477 511 10645562 (Pubitemid 128521680)
26. [Malaria transmission in 1999 in the rice field area of the Kou Valley (Bama), (Burkina Faso)]. T Baldet A Diabate TR Guiguemde, Sante 2003 13 1 55 60 12925325 (Pubitemid 36723073)
27. Water quality and immatures of the M and S forms of Anopheles gambiae s.s. and An. arabiensis in a Malian village. FE Edillo F Tripét YT Touré GC Lanzaro G Dolo CE Taylor, Malar J 2006 5 35 16646991 10.1186/1475-2875-5-35
28. Malaria vectors in Bioko Island (Equatorial Guinea): PCR determination of the members of Anopheles gambiae Giles complex (Diptera: Culicidae) and pyrethroid knockdown resistance (kdr) in An. gambiae sensu stricto. PJ Berzosa J Cano J Roche JM Rubio L Garcia E Moyano A Guerra JC Mateos V Petrarca VD Rosario, J Vector Ecol 2002 27 1 102 106 12125862 (Pubitemid 135747894)
29. Malaria in Sao Tome and Principe: parasite prevalences and vector densities. J Pinto CA Sousa V Gil C Ferreira L Goncalves D Lopes V Petrarca JD Charlwood VE do Rosario, Acta Trop 2000 76 2 185 193 10.1016/S0001-706X(00) 00100-5 10936578
30. The ecology and behaviour of the forest form of Anopheles gambiae s.s. MJ Bockarie MW Service YT Toure S Traore G Barnish BM Greenwood, Parassitologia 1993 35 Suppl 5 8 8233612
31. High malaria transmission intensity in a village close to Yaounde, the capital city of Cameroon. C Antonio-Nkondjio P Awono-Ambene JC Toto JY Meunier S Zebaze-Kemleu R Nyambam CS Wondji T Tchuinkam D Fontenille, J Med Entomol 2002 39 2 350 355 11931035 (Pubitemid 135695972)
32. Evidence for subdivision within the M molecular form of Anopheles gambiae. MA Slotman F Tripet AJ Cornel CR Meneses Y Lee LJ Reimer TC Thiemann E Fondjo A Fofana SF Traore, Mol Ecol 2007 16 3 639 649 10.1111/j.1365-294X.2006. 03172.x 17257119
33. Locus- and population-specific selection and differentiation between incipient species of Anopheles gambiae. TL Turner MW Hahn, Mol Biol Evol 2007 24 9 2132 2138 10.1093/molbev/msm143 17636041
34. Malaria vectors and urbanization in the equatorial forest region of south Cameroon. C Antonio-Nkondjio F Simard P Awono-Ambene P Ngassam JC Toto T Tchuinkam D Fontenille, Trans R Soc Trop Med Hyg 2005 99 5 347 354 10.1016/j.trstmh.2004.07.003 15780341
35. Distribution and chromosomal characterization of the Anopheles gambiae complex in Angola. M Calzetta F Santolamazza GC Carrara PJ Cani F Fortes MA Di Deco A della Torre V Petrarca, Am J Trop Med Hyg 2008 78 1 169 175 18187801 (Pubitemid 351844512)
36. An unusual distribution of the kdr gene among populations of Anopheles gambiae on the island of Bioko, Equatorial Guinea. LJ Reimer F Tripet M Slotman A Spielman E Fondjo GC Lanzaro, Insect Mol Biol 2005 14 6 683 688 10.1111/j.1365-2583.2005.00599.x 16313568
37. Spatial distribution of chromosomal inversions and speciation in anopheline mosquitoes. M Coluzzi, Mechanisms of Speciation New York: Alan R. Liss, Inc, Barigozzi C, 1982 143 153
38. Chromosome inversions, local adaptation and speciation. M Kirkpatrick N Barton, Genetics 2006 173 1 419 434 16204214 10.1534/genetics.105.047985
39. A test of the chromosomal theory of ecotypic speciation in Anopheles gambiae. NC Manoukis JR Powell MB Toure A Sacko FE Edillo MB Coulibaly SF Traore CE Taylor NJ Besansky, Proc Natl Acad Sci USA 2008 105 8 2940 2945 18287019 10.1073/pnas.0709806105
40. Divergence between the Drosophila pseudoobscura and D. persimilis genome sequences in relation to chromosomal inversions. MA Noor DA Garfield SW Schaeffer CA Machado, Genetics 2007 177 3 1417 1428 18039875 10.1534/genetics.107.070672
41. Semipermeable species boundaries between Anopheles gambiae and Anopheles arabiensis: evidence from multilocus DNA sequence variation. NJ Besansky J Krzywinski T Lehmann F Simard M Kern O Mukabayire D Fontenille Y Touré N Sagnon, PNAS 2003 100 19 10818 10823 12947038 10.1073/pnas.1434337100
42. Mosaic genome architecture of the Anopheles gambiae species complex. R Wang-Sattler S Blandin Y Ning C Blass G Dolo YT Toure A delle Torre GC Lanzaro LM Steinmetz FC Kafatos, PLoS ONE 2007 2 11 e1249 18043756 10.1371/journal.pone. 0001249
43. Evidence of introgression of the ace-1(R) mutation and of the ace-1 duplication in West African Anopheles gambiae s. s. L Djogbenou F Chandre A Berthomieu R Dabire A Koffi H Alout M Weill, PLoS ONE 2008 3 5 e2172 18478097 10.1371/journal.pone.0002172
44. The kdr mutation occurs in the Mopti form of Anopheles gambiae s.s. through introgression. M Weill F Chandre C Brengues S Manguin M Akogbeto N Pasteur P Guillet M Raymond, Insect Mol Biol 2000 9 5 451 455 10.1046/j.1365-2583.2000.00206.x 11029663
45. Living at the edge: biogeographic patterns of habitat segregation conform to speciation by niche expansion in Anopheles gambiae. C Costantini D Ayala WG Guelbeogo M Pombi CY Some IHN Bassole K Ose J-M Fotsing NF Sagnon D Fontenille, BMC Ecology 2009 9 16 10.1186/1472-6785-9-16 19460144
46. Ecological-Niche Factor Analysis: how to compute Habitat-Suitability maps without absence data? AH Hirzel J Hausser D Chessel N Perrin, Ecology 2002 83 7 2027 2036 (Pubitemid 36524791)
47. Fleuves et Rivières du Cameroun. JC Olivry, Paris, France: ORSTOM 1986 9
48. Density, survival and dispersal of Anopheles gambiae complex mosquitoes in a west African Sudan savanna village. C Costantini SG Li A della Torre NF Sagnon M Coluzzi CE Taylor, Med Vet Entomol 1996 10 3 203 219 10.1111/j.1365-2915.1996.tb00733.x 8887330
49. The Anophelinae of Africa, South of the Sahara. MT Gillies B de Meillon, Johannesburg: The South African Institute for Medical Research 1968 54
50. A Supplement to the Anophelinae of Africa South of the Sahara (Afrotropical region). MT Gillies MC Coetzee, Johannesburg: The South African Institute for Medical Research 1987
51. Simultaneous identification of species and molecular forms of the Anopheles gambiae complex by PCR-RFLP. C Fanello F Santolamazza A della Torre, Med Vet Entomol 2002 16 4 461 464 10.1046/j.1365-2915.2002.00393.x 12510902
52. PCR of the ribosomal DNA intergenic spacer regions as a method for identifying mosquitoes in the Anopheles gambiae complex. AJ Cornel FH Collins, Methods Mol Biol 1996 50 321 332 8751368
53. Ecological requirements of reintroduced species and the implications for release policy: the case of the bearded vulture. AH Hirzel B Posse PA Oggier Y Crettenand C Glenz R Arlettaz, J Appl Ecol 2004 41 1103 1116 10.1111/j.0021-8901.2004.00980.x
54. Biometry. RR Sokal JF Rohlf, New York: W.H. Freeman & Co 2 1981
55. Biomapper 1.0-4.0. AH Hirzel J Hausser N Perrin, Lab of Conservation Biology Department of Ecology and Evolution, University of Lausanne, Switzerland 2007
56. IDRISI 32-22. JR Eastman, The Idrisi Project Worcester, MA: Clark Laboratories 2002
57. Concluding remarks. GE Hutchinson, Cold Spring Harbor Symposia on Quantitative Biology 1957 415 427
58. Living on the edge Modelling habitat suitability for species at the edge of their fundamental niche. V Braunisch K Bollmann R Graf AH Hirzel, Ecol Model 2008 214 2 4 153 167 10.1016/j.ecolmodel.2008.02.001
59. Ecological niche modelling of two cryptic bat species calls for a reassessment of their conservation status. T Sattler F Bontadina AH Hirzel R Arlettaz, J Appl Ecol 2007 44 6 1188 1199 10.1111/j.1365-2664.2007.01328.x
60. On the relative abundance of bird species. RH MacArthur, Proc Natl Acad Sci USA 1957 43 3 293 295 16590018 10.1073/pnas.43.3.293
61. Evaluating the ability of habitat suitability models to predict species presences. AH Hirzel G Le Lay V Helfer C Randin A Guisan, Ecol Model 2006 199 142 152 10.1016/j.ecolmodel.2006.05.017
62. Modeling habitat suitability for complex species distributions by environmental-distance geometric mean. AH Hirzel R Arlettaz, Environmental management 2003 32 5 614 623 10.1007/s00267-003-0040-3 15015699
63. Evaluating resource selection functions. MS Boyce PR Vernier SE Nielsen FKA Schmiegelow, Ecol Model 2002 157 281 300 10.1016/S0304-3800(02)00200-4
64. The measurement of niche overlap and some relatives. SH Hurlbert, Ecology 1978 59 1 67 77 10.2307/1936632
65. Multivariate Analysis of Ecological Data using CANOCO. J Leps P Smilauer, Cambridge: Cambridge University Press 2003 12964131
66. Polytene chromosome preparation from Anopheline mosquitoes. A della Torre, Molecular Biology of Insect Disease Vectors: a Methods Manual London: Chapman & Hall, Crampton JM, Beard CB, Louis C, 1997 329 336
67. Inference of population structure using multilocus genotype data: dominant markers and null alleles. D Falush M Stephens J Pritchard, Mol Ecol Notes 2007 7 4 574 578 18784791 10.1111/j.1471-8286.2007.01758.x
68. Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. D Falush M Stephens JK Pritchard, Genetics 2003 164 4 1567 1587 12930761 (Pubitemid 37102217)
69. Inference of population structure using multilocus genotype data. JK Pritchard M Stephens P Donnelly, Genetics 2000 155 2 945 959 10835412 (Pubitemid 30397141)
70. Complexity of the malaria vectorial system in Cameroon: contribution of secondary vectors to malaria transmission. C Antonio-Nkondjio CH Kerah F Simard P Awono-Ambene M Chouaibou T Tchuinkam D Fontenille, J Med Entomol 2006 43 6 1215 1221 10.1603/0022-2585(2006)43[1215:COTMVS]2.0.CO;2 17162956
71. Assessing habitat-suitability models with a virtual species. AH Hirzel V Helfer F Metral, Ecol Model 2001 145 111 121 10.1016/S0304-3800(01)00396-9
72. Heterogeneities of the malaria vectorial system in tropical Africa and their significance in malaria epidemiology and control. M Coluzzi, Bull World Health Organ 1984 62 Suppl 107 113 6335681 (Pubitemid 15165253)
73. Chromosomal plasticity and evolutionary potential in the malaria vector Anopheles gambiae sensu stricto: insights from three decades of rare paracentric inversions. M Pombi B Caputo F Simard MA Di Deco M Coluzzi A Della Torre C Costantini NJ Besansky V Petrarca, BMC Evol Biol 2008 8 1 309 19000304 10.1186/1471-2148-8-309
74. Population structure, speciation, and introgression in the Anopheles gambiae complex. JR Powell V Petrarca A della Torre A Caccone M Coluzzi, Parassitologia 1999 41 1 3 101 113 10697841 (Pubitemid 129640238)
75. Inversion polymorphism and incipient speciation in Anopheles gambiae s.str. in The Gambia, West Africa. JH Bryan MA Di Deco V Petrarca M Coluzzi, Genetica 1982 59 167 176 10.1007/BF00056539
76. Modelling distribution and abundance with presence-only data. JL Pearce MS Boyce, J Appl Ecol 2006 43 405 412 10.1111/j.1365-2664.2005.01112.x
77. Towards a fuller understanding of mosquito behaviour: use of electrocuting grids to compare the odour-orientated responses of Anopheles arabiensis and An. quadriannulatus in the field. SJ Torr A Della Torre M Calzetta C Costantini GA Vale, Med Vet Entomol 2008 22 2 93 108 10.1111/j.1365-2915.2008.00723.x 18498608
78. Repellent effects on Anopheles arabiensis biting humans in Kruger Park, South Africa. J Govere LE Braack DN Durrheim RH Hunt M Coetzee, Med Vet Entomol 2001 15 3 287 292 10.1046/j.0269-283x.2001.00309.x 11583446
79. Interpretation of models of fundamental ecological niches and species' distributional areas. J Soberon TA Peterson, Biodiversity Informatics 2005 2 1 10
80. Predictive habitat distribution models in ecology. A Guisan NE Zimmermann, Ecol Model 2000 135 147 186 10.1016/S0304-3800(00)00354-9
81. Pyrethroid resistance/susceptibility and differential urban/rural distribution of Anopheles arabiensis and An. gambiae s.s. malaria vectors in Nigeria and Ghana. M Kristan H Fleischmann A della Torre A Stich CF Curtis, Med Vet Entomol 2003 17 3 326 332 10.1046/j.1365-2915.2003.00449.x 12941018
82. Genetic population structure of Anopheles gambiae in Equatorial Guinea. M Moreno P Salgueiro JL Vicente J Cano PJ Berzosa A de Lucio F Simard A Caccone VE Do Rosario J Pinto, Malar J 2007 6 137 17937805 10.1186/1475-2875-6-137
83. On the relationship between niche and distribution. HR Pulliam, Ecol Letters 2000 3 349 361 10.1046/j.1461-0248.2000.00143.x
84. Studies on the dispersion and survival of Anopheles gambiae Giles in East Africa, by means of marking and release experiments. MT Gillies, Bulletin of Entomological Research 1961 52 99 127
85. Importance of low dispersion of Anopheles gambiae (Diptera, Culicidae) on malaria transmission in hilly towns in South Cameroon. L Manga E Fondjo P Carnevale V Robert, J Med Entomol 1993 30 5 936 938 8254644
86. Estimating dispersal and survival of Anopheles gambiae and Anopheles funestus along the Kenyan coast by using mark-release-recapture methods. JT Midega CM Mbogo H Mwnambi MD Wilson G Ojwang JM Mwangangi JG Nzovu JI Githure G Yan JC Beier, J Med Entomol 2007 44 6 923 929 10.1603/0022-2585(2007)44[923: EDASOA]2.0.CO;2 18047189
87. tude sur la dispersion d'Anopheles gambiae s.l. dans une zone urbaine Ouagadougou (Burkina Faso). G Sabatinelli P Rossi A Belli, Parassitologia 1986 28 1 33 39 3455531
88. Mark-release-recapture experiments with Anopheles gambiae s.l. in Banambani Village, Mali, to determine population size and structure. YT Toure G Dolo V Petrarca SF Traore M Bouare A Dao J Carnahan CE Taylor, Med Vet Entomol 1998 12 1 74 83 10.1046/j.1365-2915.1998.00071.x 9513942
89. Vector density gradients and the epidemiology of urban malaria in Dakar, Senegal. JF Trape E Lefebvre-Zante F Legros G Ndiaye H Bouganali P Druilhe G Salem, Am J Trop Med Hyg 1992 47 2 181 189 1354414
90. A Dictionary of Ecology, Evolution and Systematics. R Lincoln G Boxshall P Clark, Cambridge: Cambridge University Press 2 1998
91. Variation in recombination rate across the X chromosome of Anopheles gambiae. M Pombi AD Stump A Della Torre NJ Besansky, Am J Trop Med Hyg 2006 75 5 901 903 17123984 (Pubitemid 351627537)
92. Differential gene expression in incipient species of Anopheles gambiae. BJ Cassone K Mouline MW Hahn BJ White M Pombi F Simard C Costantini NJ Besansky, Mol Ecol 2008 17 10 2491 2504 10.1111/j.1365-294X.2008.03774.x 18430144