Genetic analysis and population structure of Anopheles gambiae complex (Diptera: Culicidae) from different ecological zones of Burkina Faso.

Zoure, Abdou; Noël, Grégoire; Sombié, Aboubacar; Somda, Zéphirin; Badolo, Athanase; Francis, Frédéric

doi:10.1016/j.meegid.2020.104261

Article (Scientific journals)

Genetic analysis and population structure of Anopheles gambiae complex (Diptera: Culicidae) from different ecological zones of Burkina Faso.

Zoure, Abdou; Noël, Grégoire; Sombié, Aboubacar et al.

2020 • In Infection, Genetics and Evolution: Journal of Molecular Epidemiology and Evolutionary Genetics of Infectious Diseases

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https://hdl.handle.net/2268/247064

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10.1016/j.meegid.2020.104261

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32092481

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Keywords :

Anopheles gambia; rDNA; genetic structure

Abstract :

[en] The Anopheles gambiae complex is the most important vector for malaria in Sub-Saharan Africa, besides to other vectors such as Anopheles funestus. Malaria vector control must consider specific identification, the genetic diversity and the population structure of An. gambiae to design vector control strategies. The aim of this study was to determine the distribution of sibling species of the An. gambiae complex according to climatic regions related to cotton-growing or cotton-free areas by using polymerase chain reaction-restriction fragment length polymorphism (PCR-RFLP). Secondly, variation in mitochondrial cytochrome c oxidase 1 (COI) was used to assess the genetic structure within and between populations from our selected ecological zones. At the sibling species level, in all samples (n = 180), the following proportions of An. coluzzii (65.56%), An. gambiae s.s. (21.11%) and An. arabiensis (3.33%) were found. Hybrids between An. gambiae s.s. and An. coluzzii (7.78%) and hybrids between An. coluzzii and An. arabiensis (2.22%) were found as well. The phylogenetic tree and Integer Neighbour-Joining (IntNJ) haplotype network revealed no distinct genetic structure pattern related to climatic or agricultural conditions in Burkina Faso. The Fst (Wright’s F-statistic) values close to zero showed a free gene flow and an absence of differentiation in An. gambiae complex populations. Furthermore, neutrality indices calculated by Tajima’s D, Fu and Li's D*, Fu and Li's F*, Fu’s Fs tests suggested an excess of rare mutations in the investigated populations. Overall, this study found variations in the proportions of An. gambiae s.s., An. coluzzii and An. arabiensis according to climatic regions but without population 35 structuration of the An. gambiae complex. These results are scientific contributions that can be used as a basis for further in-depth study of the genetic diversity of the An. gambiae complex for epidemiologic risk assessment of malaria in Burkina Faso.

Disciplines :

Entomology & pest control

Author, co-author :

Zoure, Abdou ; Université de Liège - ULiège > Doct. sc. agro. & ingé. biol. (Paysage)

Noël, Grégoire ; Université de Liège - ULiège > Form. doct. sc. agro. & ingé. biol. (paysage)

Sombié, Aboubacar; Université Joseph KI-ZERBO

Somda, Zéphirin; Université Joseph KI-ZERBO

Badolo, Athanase; Université Joseph KI-ZERBO

Francis, Frédéric ; Université de Liège - ULiège > Département GxABT > Gestion durable des bio-agresseurs

Language :

English

Title :

Genetic analysis and population structure of Anopheles gambiae complex (Diptera: Culicidae) from different ecological zones of Burkina Faso.

Alternative titles :

[en] Belgique

Publication date :

2020

Journal title :

Infection, Genetics and Evolution: Journal of Molecular Epidemiology and Evolutionary Genetics of Infectious Diseases

ISSN :

1567-1348

eISSN :

1567-7257

Publisher :

Elsevier, Gembloux, Netherlands

Peer reviewed :

Peer Reviewed verified by ORBi

Funders :

IBD - Islamic Development Bank

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since 01 May 2020

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Bibliography

Abiodun, G.J., Maharaj, R., Witbooi, P., Okosun, K.O., Modelling the influence of temperature and rainfall on the population dynamics of Anopheles arabiensis. Malar. J. 15 (2016), 1–15, 10.1186/s12936-016-1411-6.
Benson, O., Falade, M.O., Molecular evolution and phylogenomics of the Anopheles gambiae complex. J. Mosq. Res. 3 (2013), 65–70, 10.5376/jmr.2013.03.0009.
Besansky, N.J., Powell, J.R., Caccone, A., Hamm, D.M., Scott, J.A., Collins, F.H., Molecular phylogeny of the Anopheles gambiae complex suggests genetic introgression between principal malaria vectors. Proc. Natl. Acad. Sci. U. S. A. 91 (1994), 6885–6888, 10.1073/pnas.91.15.6885.
Besansky, N.J., 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. Proc. Natl. Acad. Sci. U. S. A. 100 (2003), 10818–10823, 10.1073/pnas.1434337100.
Bomblies, A., Modeling the role of rainfall patterns in seasonal malaria transmission. Clim. Chang. 112 (2012), 673–685, 10.1007/s10584-011-0230-6.
Borja-Cacho, D., Matthews, J., The molecular forms of Anopheles gambiae: a phenotypic perspective. Infect. Genet. Evol. 6 (2008), 737–746, 10.1016/j.meegid.2008.06.003.
Borja-Cacho, D., Matthews, J., Population structure of Anopheles gambiae along the Kenyan coast. Acta Trop. 114 (2010), 103–108, 10.1016/j.actatropica.2010.01.011.
Bouckaert, R., Heled, J., Kuhnert, D., Vaughan, T., Wu, C., Xie, D., Suchard, M.A., Rambaut, A., Drummond, A.J., BEAST 2 : a software platform for Bayesian evolutionary analysis. PLoS Comput. Biol. 10 (2014), 1–6, 10.1371/journal.pcbi.1003537.
Carnevale, P., Robert, V., Les anophèles Biologie, transmission du Plasmodium et lutte antivectorielle. IRD éditions, 2009, 10.4000/books.irdeditions.10374.
Chen, H., Minakawa, N., Beier, J., Yan, G., Population genetic structure of Anopheles gambiae mosquitoes on Lake Victoria islands, west Kenya. Malar. J. 3 (2004), 1–8, 10.1186/1475-2875-3-48.
Coetzee, M., Craig, M., Le Sueur, D., Distribution of African malaria mosquitoes belonging to the Anopheles gambiae complex. Parasitol. Today 16 (2000), 74–77, 10.1016/S0169-4758(99)01563-X.
Coetzee, M., Hunt, R.H., Wilkerson, R., Torre, A. Della, Coulibaly, M.B., Besansky, N.J., Anopheles coluzzii and Anopheles amharicus, new members of the Anopheles gambiae complex. Zootaxa 3619 (2013), 246–274, 10.11646/zootaxa.3619.3.2.
Costantini, C., Ayala, D., Guelbeogo, W.M., Pombi, M., Some, C.Y., Bassole, I.H.N., Ose, K., Fotsing, M., Sagnon, N.F., Fontenille, D., Besansky, N.J., Simard, F., Living at the edge : biogeographic patterns of habitat segregation conform to speciation by niche expansion in Anopheles gambiae. BMC Ecol. 9 (2009), 1–27, 10.1186/1472-6785-9-16.
Crawford, J.E., Lazzaro, B.P., The demographic histories of the M and S molecular forms of Anopheles gambiae s.s. Mol. Biol. Evol. 27 (2010), 1739–1744, 10.1093/molbev/msq070.
Crawford, J.E., Riehle, M.M., Markianos, K., Bischoff, E., Guelbeogo, W.M., Gneme, A., Sagnon, N., Vernick, K.D., Nielsen, R., Lazzaro, B.P., Evolution of GOUNDRY, a cryptic subgroup of Anopheles gambiae s.l., and its impact on susceptibility to Plasmodium infection. Mol. Ecol. 25 (2016), 1494–1510, 10.1111/mec.13572.
Dabiré, K.R., Diabaté, A., Djogbenou, L., Ouari, A., N'Guessan, R., Ouédraogo, J.B., Hougard, J.M., Chandre, F., Baldet, T., Dynamics of multiple insecticide resistance in the malaria vector Anopheles gambiae in a rice growing area in South-Western Burkina Faso. Malar. J. 7 (2008), 1–9, 10.1186/1475-2875-7-188.
Dabiré, R.K., Namountougou, M., Sawadogo, S.P., Yaro, L.B., Toé, H.K., Ouari, A., Gouagna, L.C., Simard, F., Chandre, F., Baldet, T., Bass, C., Diabaté, A., Population dynamics of Anopheles gambiae s.l. in Bobo-Dioulasso city: Bionomics, infection rate and susceptibility to insecticides. Parasit. Vectors 5 (2012), 1–9, 10.1186/1756-3305-5-127.
Darriet, F., Corbel, V., Influence des engrais de type NPK sur l'oviposition d'Aedes aegypti. Parasite 15 (2008), 89–92.
Darriet, F., Rossignol, M., Chandre, F., The combination of NPK fertilizer and deltamethrin insecticide favors the proliferation of pyrethroid-resistant Anopheles gambiae (Diptera: Culicidae). Parasite 19 (2012), 159–164, 10.1051/parasite/2012192159.
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. 10 (2001), 9–18, 10.1046/j.1365-2583.2001.00235.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. 35 (2005), 755–769, 10.1016/j.ibmb.2005.02.006.
Diallo, Mouctar, Sangaré, D., Traoré, A., Mariko, M., Diarra, S., Diallo, Moussa, Coulibaly, B., Dao, A., Doumbo, O., Traoré, C.F., Etude de l'impact des gites larvaires sur l'infectivite des gamétocytes de Plasmodium falciparum chez Anopheles gambiae sl en zone d'endémie palustre de Nanguilabougou–Mali. Mali Med. 30 (2015), 28–33.
Donnelly, M.J., Simard, F., Lehmann, T., Evolutionary studies of malaria vectors. Trends Parasitol. 18 (2002), 75–80, 10.1016/S1471-4922(01)02198-5.
Excoffier, L., Laval, G., Schneider, S., Arlequin (version 3. 0): an integrated software package for population genetics data analysis. Evol. Bioinformatics Online 1 (2005), 47–50.
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. 16 (2002), 461–464, 10.1046/j.1365-2915.2002.00393.x.
Favia, G., Lanfrancotti, A., Spanos, L., Sidén-Kiamos, I., Louis, C., Molecular characterization of ribosomal DNA polymorphisms discriminating among chromosomal forms of Anopheles gambiae s.s. Insect Mol. Biol. 10 (2001), 19–23, 10.1046/j.1365-2583.2001.00236.x.
Fontaine, M.C., Waterhouse, R.M., Steele, A., Pease, J.B., Neafsey, D.E., Sharakhov, I.V., Jiang, X., Hall, A.B., Kakani, E., Mitchell, S.N., Wu, Y., Smith, H.A., Hahn, M.W., Besansky, N.J., Extensive introgression in a malaria vector species complex revealed by phylogenomics. Science (80-.) 347 (2016), 1–20, 10.1126/science.1258524.Extensive.
Gillies, M.T., Coetzee, M., A Supplement to the Anophelinae of Africa South of the Sahara. Publ. South African Inst. Med. Res., 55, 1987, 63, 10.1046/j.1365-294X.1997.00177.x.
Gillies, M.T., De Meillon, B., The Anophelinae of Africa South of the Sahara (Ethiopian Zoogeographical Region). 1968, South African Institute for Medical Research, P.O. Box 1038, S. Africa, Johannesburg.
Hall, T.A., BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 41 (1999), 95–99.
Hanemaaijer, M.J., Houston, P.D., Collier, T.C., Norris, L.C., Fofana, A., Lanzaro, G.C., Cornel, A.J., Lee, Y., Mitochondrial genomes of Anopheles arabiensis, An. gambiae and An. coluzzii show no clear species division. F1000Research 7 (2019), 1–14, 10.12688/f1000research.13807.2.
Harbach, R.E., The classification of genus Anopheles (Diptera: Culicidae): a working hypothesis of phylogenetic relationships. Bull. Entomol. Res. 94 (2004), 537–553, 10.1079/BER2004321.
Harbach, R.E., The Phylogeny and Classiffication of Anopheles, Anopheles Mosquitoes-New Insights iIto Malaria Vectors. 2013, 10.5772/3392.
Harbach, R.E., Kitching, I.J., The phylogeny of anophelinae revisited: inferences about the origin and classification of Anopheles (Diptera: Culicidae). Zool. Scr. 45 (2016), 34–47, 10.1111/zsc.12137.
Harrison, J.C., Langdale, J.A., A step by step guide to phylogeny reconstruction. Plant J. 45 (2006), 561–572, 10.1111/j.1365-313X.2005.02611.x.
Hauchart, V., Le Burkina Faso, un producteur de coton face à la mondialisation et à la dépendance économique. Regard sur un Sud. Cybergeo Eur. J. Geogr., 2007, 0–10, 10.4000/cybergeo.2665.
Hegde, S., Rasgon, J.L., Hughes, G.L., The microbiome modulates arbovirus transmission in mosquitoes. Curr. Opin. Virol. 15 (2015), 97–102, 10.1016/j.coviro.2015.08.011.
Hien, A.S., Soma, D.D., Hema, O., Bayili, B., Namountougou, M., Gnankiné, O., Baldet, T., Diabaté, A., Dabiré, K.R., Evidence that agricultural use of pesticides selects pyrethroid resistance within Anopheles gambiae s.l. populations from cotton growing areas in Burkina Faso, West Africa. PLoS One 12 (2017), 1–15, 10.1371/journal.pone.0173098.
Huson, D.H., Bryant, D., Application of phylogenetic networks in evolutionary studies. Mol. Biol. Evol. 23 (2006), 254–267, 10.1093/molbev/msj030.
IFPRI, R., Diagnostic du secteur agricole de pays: dépenses publiques. 2010, 2010.
INSD, Annuaire statistiques 2014. Institut national de la statistique et de la démographie. 2015, Ouagadougou, Burkina Faso.
Ishimura, R., Nagy, G., Dotu, I., Zhou, H., Yang, X., Senju, S., Nishimura, Y., Chuang, J.H., Susan, L., Population Genetic Structure of Anopheles Arabiensis (Diptera: Culicidae) in a Rice Growing Area of Central Kenya. J. Med. Entomol. 345 (2015), 455–459, 10.1126/science.1249749.Ribosome.
Kabore, B., Kam, S., Ouedraogo, G.W.P., Bathiebo, D.J., Etude de l'évolution climatique au Burkina Faso de 1983 à 2012 : cas des villes de Bobo dioulasso. Ouagadougou et Dori. Arab. J. Earth Sci. 4 (2017), 50–59.
Kamali, M., Marek, P.E., Peery, A., Antonio-Nkondjio, C., Ndo, C., Tu, Z., Simard, F., Sharakhov, I.V., Multigene phylogenetics reveals temporal diversification of major African malaria vectors. PLoS One 9 (2014), 1–9, 10.1371/journal.pone.0093580.
Kyalo, D., Amratia, P., Mundia, C.W., Mbogo, C.M., Coetzee, M., Snow, R.W., A geo-coded inventory of anophelines in the Afrotropical Region south of the Sahara: 1898–2016. Wellcome Open Res., 2, 2017, 57, 10.12688/wellcomeopenres.12187.1.
Lanfear, R., Calcott, B., Ho, S.Y.W., Guindon, S., PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses research article. Mol. Biol. Evol. 29 (2012), 1695–1701, 10.1093/molbev/mss020.
Lanfear, R., Frandsen, P.B., Wright, A.M., Senfeld, T., Calcott, B., PartitionFinder 2: new methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Mol. Biol. Evol. 34 (2016), 772–773, 10.1093/molbev/msw260.
Lanzaro, G.C., Tripet, F., Gene flow among populations of Anopheles gambiae: a critical review. Crit. Rev. 61 (2009), 713–722, 10.1002/iub.196.
Larkin, M.A., Blackshields, G., Brown, N.P., Chenna, R., Mcgettigan, P.A., Mcwilliam, H., Valentin, F., Wallace, I.M., Wilm, A., Lopez, R., Thompson, J.D., Gibson, T.J., Higgins, D.G., Clustal W and Clustal X version 2. 0. Bioinformatics 23 (2007), 2947–2948, 10.1093/bioinformatics/btm404.
Lee, Y., Cornel, A.J., Meneses, C.R., Fofana, A., Andrianarivo, A.G., Mcabee, R.D., Fondjo, E., Traoré, S.F., Lanzaro, G.C., Ecological and genetic relationships of the Forest-M form among chromosomal and molecular forms of the malaria vector Anopheles gambiae sensu stricto. Malar. J. 8 (2009), 1–15, 10.1186/1475-2875-8-75.
Lehmann, T., Hawley, W.A., Kamau, L., Fontenille, D., Simard, F., Collins, F.H., Genetic differentiation of Anopheles gambiae populations from East and West Africa: Comparison of microsatellite and allozyme loci. Heredity (Edinb). 77 (1996), 192–200, 10.1038/hdy.1996.124.
Lehmann, T., Licht, M., Elissa, N., Maega, B.T.A., Chimumbwa, J.M., Watsenga, F.T., Wondji, C.S., Simard, F., Hawley, W.A., Population structure of Anopheles gambiae in Africa. J. Hered. 94 (2003), 133–147, 10.1093/jhered/esg024.
Leigh, J.W., Bryant, D., POPART : full-feature software for haplotype network construction. Methods Ecol. Evol. 6 (2015), 1110–1116, 10.1111/2041-210X.12410.
Levine, R.S., Peterson, A.T., Benedict, M.Q., Geographic and ecologic distributions of the Anopheles gambiae complex predicted using a genetic algorithm. Am. J. Trop. Med. Hyg. 70 (2004), 105–109 70/2/105 pii.
Librado, P., Rozas, J., DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25 (2009), 1451–1452.
Maddison, D., Swofford, D.L., Maddison, W., NEXUS: an Extensible File Format for Systematic Information NEXUS: an extensible file format for systematic information. Syst. Biol. 46 (1997), 590–621, 10.1093/sysbio/46.4.590.
Markianos, K., Bischoff, E., Mitri, C., Guelbeogo, W.M., Gneme, A., Eiglmeier, K., Holm, I., Sagnon, N., Vernick, K.D., Riehle, M.M., Genetic structure of a local population of the Anopheles gambiae complex in Burkina Faso. PLoS One 11 (2016), 1–16, 10.1371/journal.pone.0145308.
Matthews, S.D., Meehan, L.J., Onyabe, D.Y., Vineis, J., Nock, I., Ndams, I., Conn, J.E., Evidence for late Pleistocene population expansion of the malarial mosquitoes, Anopheles arabiensis and Anopheles gambiae in Nigeria. Med. Vet. Entomol. 21 (2007), 358–369, 10.1111/j.1365-2915.2007.00703.x.
Miles, A., Harding, N.J., Bottà, G., Clarkson, C.S., Antão, T., Kozak, K., Schrider, D.R., Kern, A.D., Redmond, S., Sharakhov, I., Pearson, R.D., Bergey, C., Fontaine, M.C., Donnelly, M.J., Lawniczak, M.K.N., Ayala, D., Besansky, N.J., Burt, A., Caputo, B., Torre, A. Della, Godfray, H.C.J., Hahn, M.W., Midega, J., Neafsey, D.E., O'Loughlin, S., Pinto, J., Riehle, M.M., Vernick, K.D., Weetman, D., Wilding, C.S., White, B.J., Troco, A.D., Diabaté, A., Costantini, C., Rohatgi, K.R., Elissa, N., Coulibaly, B., Dinis, J., Mbogo, C., Bejon, P., Mawejje, H.D., Stalker, J., Rockett, K., Drury, E., Mead, D., Jeffreys, A., Hubbart, C., Rowlands, K., Isaacs, A.T., Jyothi, D., Malangone, C., Vauterin, P., Jeffery, B., Wright, I., Hart, L., Kluczyński, K., Cornelius, V., Macinnis, B., Henrichs, C., Giacomantonio, R., Kwiatkowski, D.P., Genetic diversity of the African malaria vector Anopheles gambiae. Nature 552 (2017), 96–100, 10.1038/nature24995.
Minakawa, N., Sonye, G., The effects of climatic factors on the distribution and abundance of malaria vectors in Kenya. J. Med. Entomol. 39 (2002), 833–841, 10.1603/0022-2585-39.6.833.
Mohanty, A., Swain, S., Kar, S.K., Hazra, R.K., Analysis of the phylogenetic relationship of Anopheles species, subgenus Cellia (Diptera: Culicidae) and using it to define the relationship of morphologically similar species. Infect. Genet. Evol. 9 (2009), 1204–1224, 10.1016/j.meegid.2009.06.021.
Namountougou, M., Simard, F., Baldet, T., Diabaté, A., Ouédraogo, J.B., Martin, T., Dabiré, R.K., Multiple insecticide resistance in Anopheles gambiae s.l. Populations from Burkina Faso, West Africa. PLoS One, 7, 2012, 10.1371/journal.pone.0048412.
Nei, M., Molecular Evolutionary Genetics. 1987.
Ng'Habi, K.R., Knols, B.G., Lee, Y., Ferguson, H.M., Lanzaro, G.C., Population genetic structure of Anopheles arabiensis and Anopheles gambiae in a malaria endemic region of southern Tanzania. Malar. J., 10, 2011, 289, 10.1186/1475-2875-10-289.
Norris, L.C., Norris, D.E., Phylogeny of anopheline (Diptera: Culicidae) species in southern Africa, based on nuclear and mitochondrial genes. J. Vector Ecol. 40 (2015), 16–27, 10.1111/jvec.12128.Phylogeny.
Oshaghi, M.A., Yaaghoobi, F., Abaie, M.R., Pattern of mitochondrial DNA variation between and within Anopheles stephensi (Diptera: Culicidae) biological forms suggests extensive gene flow. Acta Trop. 99 (2006), 226–233, 10.1016/j.actatropica.2006.08.005.
Pates, H.V., Curtis, C.F., Takken, W., Hybridization studies to modify the host preference of Anopheles gambiae. Med. Vet. Entomol. 28 (2014), 68–74, 10.1111/mve.12070.
Pinto, J., Egyir-Yawson, A., Vicente, J., Gomes, B., Santolamazza, F., Moreno, M., Charlwood, J., Simard, F., Elissa, N., Weetman, D., Donnelly, M., Caccone, A., Della Torre, A., 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. Evol. Appl. 6 (2013), 910–924, 10.1111/eva.12075.
Pombi, M., Kengne, P., Gimonneau, G., Tene-Fossog, B., Ayala, D., Kamdem, C., Santolamazza, F., Guelbeogo, W.M., Sagnon, N., Petrarca, V., Fontenille, D., Besansky, N.J., Antonio-Nkondjio, C., Dabiré, R.K., Della Torre, A., Simard, F., Costantini, C., Dissecting functional components of reproductive isolation among closely related sympatric species of the Anopheles gambiae complex. Evol. Appl. 10 (2017), 1102–1120, 10.1111/eva.12517.
Posada, D., Using MODELTEST and PAUP ⁎ to select a model of nucleotide substitution. Curr. Protoc. Bioinformatics 00 (2003), 6.5.1–6.5.14, 10.1002/0471250953.bi0605s00.
Prugnolle, F., Durand, P., Jacob, K., Razakandrainibe, F., Arnathau, C., Villarreal, D., Rousset, F., de Meeûs, T., Renaud, F., A comparison of Anopheles gambiae and Plasmodium falciparum genetic structure over space and time. Microbes Infect. 10 (2008), 269–275, 10.1016/j.micinf.2007.12.021.
Rambaut, A., Figtree 1.4.3. 2017 Available from http//tree.bio.ed.ac.uk/software/figtree/. (accessed 18 Aug. 2017).
Ratnasingham, S., Hebert, P.D.N., BARCODING, BOLD : The Barcode of Life Data System (www.barcodinglife.org). Mol. Ecol. Notes 7 (2007), 355–364, 10.1111/j.1471-8286.2006.01678.x.
Raymond, M., Rousset, F., An exact test for population differenciation. Evolution (N. Y). 49 (2013), 1280–1283.
Riehle, M.M., Guelbeogo, W.M., Gneme, A., Eiglmeier, K., Bischoff, E., Garnier, T., Snyder, G.M., Li, X., Markianos, K., Sagnon, N.F., Vernick, K.D., A cryptic subgroup of Anopheles gambiae is highly susceptible to human malaria parasites. Science (80-.) 331 (2011), 596–598, 10.1126/science.1196759.A.
Robert, V., Petrarca, V., Carnevale, P., Zoulani, A., Coluzzi, M., Analyse Cytogénétique Du Complexe Anopheles gambiae Dans La Région De Bobo-Dioulasso (Burkina Faso)1. Ann. Parasitol. Hum. Comp. 64 (1989), 290–311, 10.1051/parasite/1989644290.
Saitou, N., Nei, M., The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4 (1987), 406–425.
Sallum, M.A., Schultz, T.R., Foster, P.G., Aronstein, K., Wirtz, R.A., Wilkerson, R.C., Phylogeny of Anophelinae (Diptera: Culicidae) based on nuclear ribosomal and mitochondrial DNA sequences. Syst. Entomol. 27 (2002), 361–382, 10.1111/jvec.12128.
Scott, J.A., Brogdon, W.G., Collins, F.H., Identification of single specimens of the Anopheles gambiae complex by the polymerase chain reaction. Am. J. Trop. Med. Hyg. 49 (1993), 520–529, 10.4269/ajtmh.1993.49.520.
Simard, F., Ayala, D., Kamdem, G.C., Pombi, M., Etouna, J., Ose, K., Fotsing, J.M., Fontenille, D., Besansky, N.J., Costantini, C., Ecological niche partitioning between Anopheles gambiae molecular forms in Cameroon: the ecological side of speciation. BMC Ecol., 9, 2009, 10.1186/1472-6785-9-17.
Stevenson, J.C., Norris, D.E., Implicating cryptic and novel anophelines as malaria vectors in Africa. Insects 8 (2017), 1–18, 10.3390/insects8010001.
Sum, J.-S., Lee, W.-C., Amir, A., Braima, K.A., Jeffery, J., Abdul-Aziz, N.M., Fong, M.-Y., Lau, Y.-L., Phylogenetic study of six species of Anopheles mosquitoes in Peninsular Malaysia based on inter-transcribed spacer region 2 (ITS2) of ribosomal DNA. Parasit. Vectors, 7, 2014, 309, 10.1186/1756-3305-7-309.
Tajima, F., Evolutionary relationship of DNA sequences in finite populations. Genetics 105 (1983), 437–460.
Tamura, K., Nei, M., Kumar, S., Prospects for inferring very large phylogenies by using the neighbor-joining method. Proc. Natl. Acad. Sci. 101 (2004), 11030–11035.
Taylor, C., Touré, Y.T., Carnahan, J., Norris, D.E., Dolo, G., Traoré, S.F., Edillo, F.E., Lanzaro, G.C., Gene flow among populations of the malaria vector, Anopheles gambiae, in Mali, West Africa. Genetics 157 (2001), 743–750.
Wang, G., Li, C., Zheng, W., Song, F., Guo, X., Wu, Z., Luo, P., Yang, Y., He, L., Zhao, T., An evaluation of the suitability of COI and COII gene variation for reconstructing the phylogeny of, and identifying cryptic species in, anopheline mosquitoes (Diptera Culicidae). Mitochondrial DNA Part A DNA Mapping. Seq. Anal. 28 (2017), 769–777, 10.1080/24701394.2016.1186665.
Weetman, D., Steen, K., Rippon, E.J., Mawejje, H.D., Donnelly, M.J., Wilding, C.S., Contemporary gene flow between wild An. gambiae s.s. and An. arabiensis. Parasit. Vectors 7 (2014), 1–9, 10.1186/1756-3305-7-345.
WHO, World Malaria Report 2018. 2018, World Health Organization, Geneva, Switzerland.
Wiebe, A., Longbottom, J., Gleave, K., Shearer, F.M., Sinka, M.E., Massey, N.C., Cameron, E., Bhatt, S., Gething, P.W., Hemingway, J., Smith, D.L., Coleman, M., Moyes, C.L., Geographical distributions of African malaria vector sibling species and evidence for insecticide resistance. Malar. J. 16 (2017), 1–10, 10.1186/s12936-017-1734-y.
Wilcox, T.P., Zwickl, D.J., Heath, T.A., Hillis, D.M., Phylogenetic relationships of the dwarf boas and a comparison of Bayesian and bootstrap measures of phylogenetic support. Mol. Phylogenet. Evol. 25 (2002), 361–371, 10.1016/S1055-7903(02)00244-0.
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. 11 (2002), 11–19, 10.1046/j.0962-1075.2001.00306.x.
Yawson, A.E., Weetman, D., Wilson, M.D., Donnelly, M.J., Ecological zones rather than molecular forms predict genetic differentiation in the malaria vector Anopheles gambiae s.s. in Ghana. Genetics 175 (2007), 751–761, 10.1534/genetics.106.065888.