Ecological niche partitioning between Anopheles gambiae molecular forms in Cameroon: the ecological side of speciation
Tóm tắt
Speciation among members of the Anopheles gambiae complex is thought to be promoted by disruptive selection and ecological divergence acting on sets of adaptation genes protected from recombination by polymorphic paracentric chromosomal inversions. However, shared chromosomal polymorphisms between the M and S molecular forms of An. gambiae and insufficient information about their relationship with ecological divergence challenge this view. We used Geographic Information Systems, Ecological Niche Factor Analysis, and Bayesian multilocus genetic clustering to explore the nature and extent of ecological and chromosomal differentiation of M and S across all the biogeographic domains of Cameroon in Central Africa, in order to understand the role of chromosomal arrangements in ecological specialisation within and among molecular forms. Species distribution modelling with presence-only data revealed differences in the ecological niche of both molecular forms and the sibling species, An. arabiensis. The fundamental environmental envelope of the two molecular forms, however, overlapped to a large extent in the rainforest, where they occurred in sympatry. The S form had the greatest niche breadth of all three taxa, whereas An. arabiensis and the M form had the smallest niche overlap. Correspondence analysis of M and S karyotypes confirmed that molecular forms shared similar combinations of chromosomal inversion arrangements in response to the eco-climatic gradient defining the main biogeographic domains occurring across Cameroon. Savanna karyotypes of M and S, however, segregated along the smaller-scale environmental gradient defined by the second ordination axis. Population structure analysis identified three chromosomal clusters, each containing a mixture of M and S specimens. In both M and S, alternative karyotypes were segregating in contrasted environments, in agreement with a strong ecological adaptive value of chromosomal inversions. Our data suggest that inversions on the second chromosome of An. gambiae are not causal to the evolution of reproductive isolation between the M and S forms. Rather, they are involved in ecological specialization to a similar extent in both genetic backgrounds, and most probably predated lineage splitting between molecular forms. However, because chromosome-2 inversions promote ecological divergence, resulting in spatial and/or temporal isolation between ecotypes, they might favour mutations in other ecologically significant genes to accumulate in unlinked chromosomal regions. When such mutations occur in portions of the genome where recombination is suppressed, such as the pericentromeric regions known as speciation islands in An. gambiae, they would contribute further to the development of reproductive isolation.
Tài liệu tham khảo
Coluzzi M, Petrarca V, Di Deco MA: Chromosomal inversion intergradation and incipient speciation in Anopheles gambiae. Bollettino di Zoologia. 1985, 52: 45-63.
Coluzzi M, Sabatini A, Della Torre A, Di Deco MA, Petrarca V: A polytene chromosome analysis of the Anopheles gambiae species complex. Science. 2002, 298 (5597): 1415-1418. 10.1126/science.1077769.
della Torre A, Costantini C, Besansky NJ, Caccone A, Petrarca V, Powell JR, Coluzzi M: Speciation within Anopheles gambiae – the glass is half full. Science. 2002, 298 (5591): 115-117. 10.1126/science.1078170.
Lehmann T, Licht M, Elissa N, Maega BT, Chimumbwa JM, Watsenga FT, Wondji CS, Simard F, Hawley WA: Population Structure of Anopheles gambiae in Africa. J Hered. 2003, 94 (2): 133-147. 10.1093/jhered/esg024.
Stump AD, Fitzpatrick MC, Lobo NF, Traoré S, Sagnon NF, Costantini C, Collins FH, Besansky NJ: Centromere-proximal differentiation and speciation in Anopheles gambiae. PNAS. 2005, 102 (44): 15930-15935. 10.1073/pnas.0508161102.
Stump AD, Shoener JA, Costantini C, Sagnon NF, Besansky NJ: Sex-linked differentiation between incipient species of Anopheles gambiae. Genetics. 2005, 169 (3): 1509-1519. 10.1534/genetics.104.035303.
Turner TL, Hahn MW, Nuzhdin SV: Genomic islands of speciation in Anopheles gambiae. PLoS Biol. 2005, 3 (9): e285-10.1371/journal.pbio.0030285.
Wondji C, Simard F, Fontenille D: Evidence for genetic differentiation between the molecular forms M and S within the Forest chromosomal form of Anopheles gambiae in an area of sympatry. Insect Mol Biol. 2002, 11 (1): 11-19. 10.1046/j.0962-1075.2001.00306.x.
della Torre A, Tu Z, Petrarca V: On the distribution and genetic differentiation of Anopheles gambiae s.s. molecular forms. Insect Biochem Mol Biol. 2005, 35 (7): 755-769. 10.1016/j.ibmb.2005.02.006.
Diabaté A, Dabire RK, Millogo N, Lehmann T: Evaluating the effect of postmating isolation between molecular forms of Anopheles gambiae (Diptera: Culicidae). J Med Entomol. 2007, 44 (1): 60-64. 10.1603/0022-2585(2007)44[60:ETEOPI]2.0.CO;2.
Tripet F, Touré YT, Taylor CE, Norris DE, Dolo G, Lanzaro GC: DNA analysis of transferred sperm reveals significant levels of gene flow between molecular forms of Anopheles gambiae. Mol Ecol. 2001, 10 (7): 1725-1732. 10.1046/j.0962-1083.2001.01301.x.
della Torre A, Fanello C, Akogbeto M, Dossou-yovo J, Favia G, Petrarca V, Coluzzi M: Molecular evidence of incipient speciation within Anopheles gambiae s.s. in West Africa. Insect Mol Biol. 2001, 10 (1): 9-18. 10.1046/j.1365-2583.2001.00235.x.
Edillo FE, Touré YT, Lanzaro GC, Dolo G, Taylor CE: Spatial and habitat distribution of Anopheles gambiae and Anopheles arabiensis (Diptera: Culicidae) in Banambani village, Mali. J Med Entomol. 2002, 39 (1): 70-77.
Wondji C, Frederic S, Petrarca V, Etang J, Santolamazza F, Della Torre A, Fontenille D: Species and populations of the Anopheles gambiae complex in Cameroon with special emphasis on chromosomal and molecular forms of Anopheles gambiae s.s. J Med Entomol. 2005, 42 (6): 998-1005. 10.1603/0022-2585(2005)042[0998:SAPOTA]2.0.CO;2.
Yawson AE, Weetman D, Wilson MD, Donnelly MJ: Ecological zones rather than molecular forms predict genetic differentiation in the malaria vector Anopheles gambiae s.s. in Ghana. Genetics. 2007, 175 (2): 751-761. 10.1534/genetics.106.065888.
Ayala FJ, Coluzzi M: Chromosome speciation: humans, Drosophila, and mosquitoes. PNAS. 2005, 102 (Suppl 1): 6535-6542. 10.1073/pnas.0501847102.
Masendu HT, Hunt RH, Govere J, Brooke BD, Awolola TS, Coetzee M: The sympatric occurrence of two molecular forms of the malaria vector Anopheles gambiae Giles sensu stricto in Kanyemba, in the Zambezi Valley, Zimbabwe. Trans R Soc Trop Med Hyg. 2004, 98 (7): 393-396. 10.1016/j.trstmh.2003.10.006.
Lehmann T, Diabate A: The molecular forms of Anopheles gambiae: A phenotypic perspective. Infect Genet Evol. 2008, 8 (5): 737-746. 10.1016/j.meegid.2008.06.003.
Diabaté A, Dabiré RK, Heidenberger K, Crawford J, Lamp WO, Culler LE, Lehmann T: Evidence for divergent selection between the molecular forms of Anopheles gambiae: role of predation. BMC Evol Biol. 2008, 8: 5-10.1186/1471-2148-8-5.
Diabaté A, Dabire RK, Kim EH, Dalton R, Millogo N, Baldet T, Simard F, Gimnig JE, Hawley WA, Lehmann T: Larval development of the molecular forms of Anopheles gambiae (Diptera: Culicidae) in different habitats: a transplantation experiment. J Med Entomol. 2005, 42 (4): 548-553. 10.1603/0022-2585(2005)042[0548:LDOTMF]2.0.CO;2.
Pombi M: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. PhD Thesis. 2004, Dept. Public Health, Univ. of Rome "La Sapienza", Rome, Italy,
Favia G, della Torre A, Bagayoko M, Lanfrancotti A, Sagnon N, Touré YT, Coluzzi M: Molecular identification of sympatric chromosomal forms of Anopheles gambiae and further evidence of their reproductive isolation. Insect Mol Biol. 1997, 6 (4): 377-383. 10.1046/j.1365-2583.1997.00189.x.
Coluzzi M, Sabatini A, Petrarca V, Di Deco MA: Chromosomal differentiation and adaptation to human environments in the Anopheles gambiae complex. Trans R Soc Trop Med Hyg. 1979, 73 (5): 483-497. 10.1016/0035-9203(79)90036-1.
Touré Y, Petrarca V, Traore SF, Coulibaly A, Maiga HM, Sankare O, Sow M, Di Deco MA, Coluzzi M: Ecological studies in the chromosomal form Mopti of Anopheles gambiae s.str. in Mali, West Africa. Genetica. 1994, 94: 213-223. 10.1007/BF01443435.
Touré YT, Petrarca V, Traoré SF, Coulibaly A, Maiga HM, Sankaré O, Sow M, Di Deco MA, Coluzzi M: The distribution and inversion polymorphism of chromosomally recognized taxa of the Anopheles gambiae complex in Mali, West Africa. Parassitologia. 1998, 40 (4): 477-511.
Baldet T, Diabate A, Guiguemde TR: [Malaria transmission in 1999 in the rice field area of the Kou Valley (Bama), (Burkina Faso)]. Sante. 2003, 13 (1): 55-60.
Edillo FE, Tripét F, Touré YT, Lanzaro GC, Dolo G, Taylor CE: Water quality and immatures of the M and S forms of Anopheles gambiae s.s. and An. arabiensis in a Malian village. Malar J. 2006, 5: 35-10.1186/1475-2875-5-35.
Berzosa PJ, Cano J, Roche J, Rubio JM, Garcia L, Moyano E, Guerra A, Mateos JC, Petrarca V, Rosario VD: 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. J Vector Ecol. 2002, 27 (1): 102-106.
Pinto J, Sousa CA, Gil V, Ferreira C, Goncalves L, Lopes D, Petrarca V, Charlwood JD, do Rosario VE: Malaria in Sao Tome and Principe: parasite prevalences and vector densities. Acta Trop. 2000, 76 (2): 185-193. 10.1016/S0001-706X(00)00100-5.
Bockarie MJ, Service MW, Toure YT, Traore S, Barnish G, Greenwood BM: The ecology and behaviour of the forest form of Anopheles gambiae s.s. Parassitologia. 1993, 35 (Suppl): 5-8.
Antonio-Nkondjio C, Awono-Ambene P, Toto JC, Meunier JY, Zebaze-Kemleu S, Nyambam R, Wondji CS, Tchuinkam T, Fontenille D: High malaria transmission intensity in a village close to Yaounde, the capital city of Cameroon. J Med Entomol. 2002, 39 (2): 350-355.
Slotman MA, Tripet F, Cornel AJ, Meneses CR, Lee Y, Reimer LJ, Thiemann TC, Fondjo E, Fofana A, Traore SF: Evidence for subdivision within the M molecular form of Anopheles gambiae. Mol Ecol. 2007, 16 (3): 639-649. 10.1111/j.1365-294X.2006.03172.x.
Turner TL, Hahn MW: Locus- and population-specific selection and differentiation between incipient species of Anopheles gambiae. Mol Biol Evol. 2007, 24 (9): 2132-2138. 10.1093/molbev/msm143.
Antonio-Nkondjio C, Simard F, Awono-Ambene P, Ngassam P, Toto JC, Tchuinkam T, Fontenille D: Malaria vectors and urbanization in the equatorial forest region of south Cameroon. Trans R Soc Trop Med Hyg. 2005, 99 (5): 347-354. 10.1016/j.trstmh.2004.07.003.
Calzetta M, Santolamazza F, Carrara GC, Cani PJ, Fortes F, Di Deco MA, della Torre A, Petrarca V: Distribution and chromosomal characterization of the Anopheles gambiae complex in Angola. Am J Trop Med Hyg. 2008, 78 (1): 169-175.
Reimer LJ, Tripet F, Slotman M, Spielman A, Fondjo E, Lanzaro GC: An unusual distribution of the kdr gene among populations of Anopheles gambiae on the island of Bioko, Equatorial Guinea. Insect Mol Biol. 2005, 14 (6): 683-688. 10.1111/j.1365-2583.2005.00599.x.
Coluzzi M: Spatial distribution of chromosomal inversions and speciation in anopheline mosquitoes. Mechanisms of Speciation. Edited by: Barigozzi C. 1982, New York: Alan R. Liss, Inc, 143-153.
Kirkpatrick M, Barton N: Chromosome inversions, local adaptation and speciation. Genetics. 2006, 173 (1): 419-434. 10.1534/genetics.105.047985.
Manoukis NC, Powell JR, Toure MB, Sacko A, Edillo FE, Coulibaly MB, Traore SF, Taylor CE, Besansky NJ: A test of the chromosomal theory of ecotypic speciation in Anopheles gambiae. Proc Natl Acad Sci USA. 2008, 105 (8): 2940-2945. 10.1073/pnas.0709806105.
Noor MA, Garfield DA, Schaeffer SW, Machado CA: Divergence between the Drosophila pseudoobscura and D. persimilis genome sequences in relation to chromosomal inversions. Genetics. 2007, 177 (3): 1417-1428. 10.1534/genetics.107.070672.
Besansky NJ, Krzywinski J, Lehmann T, Simard F, Kern M, Mukabayire O, Fontenille D, Touré Y, Sagnon N: Semipermeable species boundaries between Anopheles gambiae and Anopheles arabiensis: evidence from multilocus DNA sequence variation. PNAS. 2003, 100 (19): 10818-10823. 10.1073/pnas.1434337100.
Wang-Sattler R, Blandin S, Ning Y, Blass C, Dolo G, Toure YT, delle Torre A, Lanzaro GC, Steinmetz LM, Kafatos FC: Mosaic genome architecture of the Anopheles gambiae species complex. PLoS ONE. 2007, 2 (11): e1249-10.1371/journal.pone.0001249.
Djogbenou L, Chandre F, Berthomieu A, Dabire R, Koffi A, Alout H, Weill M: Evidence of introgression of the ace-1(R) mutation and of the ace-1 duplication in West African Anopheles gambiae s. s. PLoS ONE. 2008, 3 (5): e2172-10.1371/journal.pone.0002172.
Weill M, Chandre F, Brengues C, Manguin S, Akogbeto M, Pasteur N, Guillet P, Raymond M: The kdr mutation occurs in the Mopti form of Anopheles gambiae s.s. through introgression. Insect Mol Biol. 2000, 9 (5): 451-455. 10.1046/j.1365-2583.2000.00206.x.
Costantini C, Ayala D, Guelbeogo WG, Pombi M, Some CY, Bassole IHN, Ose K, Fotsing J-M, Sagnon NF, Fontenille D: Living at the edge: biogeographic patterns of habitat segregation conform to speciation by niche expansion in Anopheles gambiae. BMC Ecology. 2009, 9: 16-10.1186/1472-6785-9-16.
Hirzel AH, Hausser J, Chessel D, Perrin N: Ecological-Niche Factor Analysis: how to compute Habitat-Suitability maps without absence data?. Ecology. 2002, 83 (7): 2027-2036.
Olivry JC: Fleuves et Rivières du Cameroun. 1986, Paris, France: ORSTOM, 9:
Costantini C, Li SG, della Torre A, Sagnon NF, Coluzzi M, Taylor CE: Density, survival and dispersal of Anopheles gambiae complex mosquitoes in a west African Sudan savanna village. Med Vet Entomol. 1996, 10 (3): 203-219. 10.1111/j.1365-2915.1996.tb00733.x.
Gillies MT, de Meillon B: The Anophelinae of Africa, South of the Sahara. 1968, Johannesburg: The South African Institute for Medical Research, 54:
Gillies MT, Coetzee MC: A Supplement to the Anophelinae of Africa South of the Sahara (Afrotropical region). 1987, Johannesburg: The South African Institute for Medical Research
Fanello C, Santolamazza F, della Torre A: Simultaneous identification of species and molecular forms of the Anopheles gambiae complex by PCR-RFLP. Med Vet Entomol. 2002, 16 (4): 461-464. 10.1046/j.1365-2915.2002.00393.x.
Cornel AJ, Collins FH: PCR of the ribosomal DNA intergenic spacer regions as a method for identifying mosquitoes in the Anopheles gambiae complex. Methods Mol Biol. 1996, 50: 321-332.
Hirzel AH, Posse B, Oggier PA, Crettenand Y, Glenz C, Arlettaz R: Ecological requirements of reintroduced species and the implications for release policy: the case of the bearded vulture. J Appl Ecol. 2004, 41: 1103-1116. 10.1111/j.0021-8901.2004.00980.x.
Sokal RR, Rohlf JF: Biometry. 1981, New York: W.H. Freeman & Co, 2
Hirzel AH, Hausser J, Perrin N: Biomapper 1.0-4.0. Lab of Conservation Biology. 2007, Department of Ecology and Evolution, University of Lausanne, Switzerland
Eastman JR: IDRISI 32-22. The Idrisi Project. 2002, Worcester, MA: Clark Laboratories
Hutchinson GE: Concluding remarks. Cold Spring Harbor Symposia on Quantitative Biology. 1957, 415-427.
Braunisch V, Bollmann K, Graf R, Hirzel AH: Living on the edge – Modelling habitat suitability for species at the edge of their fundamental niche. Ecol Model. 2008, 214 (2–4): 153-167. 10.1016/j.ecolmodel.2008.02.001.
Sattler T, Bontadina F, Hirzel AH, Arlettaz R: Ecological niche modelling of two cryptic bat species calls for a reassessment of their conservation status. J Appl Ecol. 2007, 44 (6): 1188-1199. 10.1111/j.1365-2664.2007.01328.x.
MacArthur RH: On the relative abundance of bird species. Proc Natl Acad Sci USA. 1957, 43 (3): 293-295. 10.1073/pnas.43.3.293.
Hirzel AH, Le Lay G, Helfer V, Randin C, Guisan A: Evaluating the ability of habitat suitability models to predict species presences. Ecol Model. 2006, 199: 142-152. 10.1016/j.ecolmodel.2006.05.017.
Hirzel AH, Arlettaz R: Modeling habitat suitability for complex species distributions by environmental-distance geometric mean. Environmental management. 2003, 32 (5): 614-623. 10.1007/s00267-003-0040-3.
Boyce MS, Vernier PR, Nielsen SE, Schmiegelow FKA: Evaluating resource selection functions. Ecol Model. 2002, 157: 281-300. 10.1016/S0304-3800(02)00200-4.
Hurlbert SH: The measurement of niche overlap and some relatives. Ecology. 1978, 59 (1): 67-77. 10.2307/1936632.
Leps J, Smilauer P: Multivariate Analysis of Ecological Data using CANOCO. 2003, Cambridge: Cambridge University Press
della Torre A: Polytene chromosome preparation from Anopheline mosquitoes. Molecular Biology of Insect Disease Vectors: a Methods Manual. Edited by: Crampton JM, Beard CB, Louis C. 1997, London: Chapman & Hall, 329-336.
Falush D, Stephens M, Pritchard J: Inference of population structure using multilocus genotype data: dominant markers and null alleles. Mol Ecol Notes. 2007, 7 (4): 574-578. 10.1111/j.1471-8286.2007.01758.x.
Falush D, Stephens M, Pritchard JK: Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics. 2003, 164 (4): 1567-1587.
Pritchard JK, Stephens M, Donnelly P: Inference of population structure using multilocus genotype data. Genetics. 2000, 155 (2): 945-959.
Antonio-Nkondjio C, Kerah CH, Simard F, Awono-Ambene P, Chouaibou M, Tchuinkam T, Fontenille D: Complexity of the malaria vectorial system in Cameroon: contribution of secondary vectors to malaria transmission. J Med Entomol. 2006, 43 (6): 1215-1221. 10.1603/0022-2585(2006)43[1215:COTMVS]2.0.CO;2.
Hirzel AH, Helfer V, Metral F: Assessing habitat-suitability models with a virtual species. Ecol Model. 2001, 145: 111-121. 10.1016/S0304-3800(01)00396-9.
Coluzzi M: Heterogeneities of the malaria vectorial system in tropical Africa and their significance in malaria epidemiology and control. Bull World Health Organ. 1984, 62 (Suppl): 107-113.
Pombi M, Caputo B, Simard F, Di Deco MA, Coluzzi M, Della Torre A, Costantini C, Besansky NJ, Petrarca V: Chromosomal plasticity and evolutionary potential in the malaria vector Anopheles gambiae sensu stricto: insights from three decades of rare paracentric inversions. BMC Evol Biol. 2008, 8 (1): 309-10.1186/1471-2148-8-309.
Powell JR, Petrarca V, della Torre A, Caccone A, Coluzzi M: Population structure, speciation, and introgression in the Anopheles gambiae complex. Parassitologia. 1999, 41 (1–3): 101-113.
Bryan JH, Di Deco MA, Petrarca V, Coluzzi M: Inversion polymorphism and incipient speciation in Anopheles gambiae s.str. in The Gambia, West Africa. Genetica. 1982, 59: 167-176. 10.1007/BF00056539.
Pearce JL, Boyce MS: Modelling distribution and abundance with presence-only data. J Appl Ecol. 2006, 43: 405-412. 10.1111/j.1365-2664.2005.01112.x.
Torr SJ, Della Torre A, Calzetta M, Costantini C, Vale GA: 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. Med Vet Entomol. 2008, 22 (2): 93-108. 10.1111/j.1365-2915.2008.00723.x.
Govere J, Braack LE, Durrheim DN, Hunt RH, Coetzee M: Repellent effects on Anopheles arabiensis biting humans in Kruger Park, South Africa. Med Vet Entomol. 2001, 15 (3): 287-292. 10.1046/j.0269-283x.2001.00309.x.
Soberon J, Peterson TA: Interpretation of models of fundamental ecological niches and species' distributional areas. Biodiversity Informatics. 2005, 2: 1-10.
Guisan A, Zimmermann NE: Predictive habitat distribution models in ecology. Ecol Model. 2000, 135: 147-186. 10.1016/S0304-3800(00)00354-9.
Kristan M, Fleischmann H, della Torre A, Stich A, Curtis CF: Pyrethroid resistance/susceptibility and differential urban/rural distribution of Anopheles arabiensis and An. gambiae s.s. malaria vectors in Nigeria and Ghana. Med Vet Entomol. 2003, 17 (3): 326-332. 10.1046/j.1365-2915.2003.00449.x.
Moreno M, Salgueiro P, Vicente JL, Cano J, Berzosa PJ, de Lucio A, Simard F, Caccone A, Do Rosario VE, Pinto J: Genetic population structure of Anopheles gambiae in Equatorial Guinea. Malar J. 2007, 6: 137-10.1186/1475-2875-6-137.
Pulliam HR: On the relationship between niche and distribution. Ecol Letters. 2000, 3: 349-361. 10.1046/j.1461-0248.2000.00143.x.
Gillies MT: Studies on the dispersion and survival of Anopheles gambiae Giles in East Africa, by means of marking and release experiments. Bulletin of Entomological Research. 1961, 52: 99-127.
Manga L, Fondjo E, Carnevale P, Robert V: Importance of low dispersion of Anopheles gambiae (Diptera, Culicidae) on malaria transmission in hilly towns in South Cameroon. J Med Entomol. 1993, 30 (5): 936-938.
Midega JT, Mbogo CM, Mwnambi H, Wilson MD, Ojwang G, Mwangangi JM, Nzovu JG, Githure JI, Yan G, Beier JC: Estimating dispersal and survival of Anopheles gambiae and Anopheles funestus along the Kenyan coast by using mark-release-recapture methods. J Med Entomol. 2007, 44 (6): 923-929. 10.1603/0022-2585(2007)44[923:EDASOA]2.0.CO;2.
Sabatinelli G, Rossi P, Belli A: Étude sur la dispersion d'Anopheles gambiae s.l. dans une zone urbaine à Ouagadougou (Burkina Faso). Parassitologia. 1986, 28 (1): 33-39.
Toure YT, Dolo G, Petrarca V, Traore SF, Bouare M, Dao A, Carnahan J, Taylor CE: Mark-release-recapture experiments with Anopheles gambiae s.l. in Banambani Village, Mali, to determine population size and structure. Med Vet Entomol. 1998, 12 (1): 74-83. 10.1046/j.1365-2915.1998.00071.x.
Trape JF, Lefebvre-Zante E, Legros F, Ndiaye G, Bouganali H, Druilhe P, Salem G: Vector density gradients and the epidemiology of urban malaria in Dakar, Senegal. Am J Trop Med Hyg. 1992, 47 (2): 181-189.
Lincoln R, Boxshall G, Clark P: A Dictionary of Ecology, Evolution and Systematics. 1998, Cambridge: Cambridge University Press, 2
Pombi M, Stump AD, Della Torre A, Besansky NJ: Variation in recombination rate across the X chromosome of Anopheles gambiae. Am J Trop Med Hyg. 2006, 75 (5): 901-903.
Cassone BJ, Mouline K, Hahn MW, White BJ, Pombi M, Simard F, Costantini C, Besansky NJ: Differential gene expression in incipient species of Anopheles gambiae. Mol Ecol. 2008, 17 (10): 2491-2504. 10.1111/j.1365-294X.2008.03774.x.