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Published in: Malaria Journal 1/2014

Open Access 01-12-2014 | Research

Seasonal genetic partitioning in the neotropical malaria vector, Anopheles darlingi

Authors: Aline F Angêlla, Patrícia Salgueiro, Luiz HS Gil, José L Vicente, João Pinto, Paulo EM Ribolla

Published in: Malaria Journal | Issue 1/2014

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Abstract

Background

Anopheles darlingi is the main malaria mosquito vector in the Amazonia region. In spite of being considered a riverine, forest-dwelling species, this mosquito is becoming more abundant in peri-urban areas, increasing malaria risk. This has been associated with human-driven environmental changes such as deforestation.

Methods

Microsatellites were used to characterize A. darlingi from seven localities along the Madeira River, Rondônia (Brazil), collected in the early and late periods of the rainy season.

Results

Two genetically distinct subpopulations were detected: one (subpopulation A) was associated with the late rainfall period and seems to be ecologically closer to the typical forest A. darlingi; the other (subpopulation B) was associated with the early rainfall period and is probably more adapted to drier conditions by exploiting permanent anthropogenic breeding sites. Results suggest also a pattern of asymmetric introgression, with more subpopulation A alleles introgressed into subpopulation B. Both subpopulations (and admixed mosquitoes) presented similar malaria infection rates, highlighting the potential for perennial malaria transmission in the region.

Conclusions

The co-occurrence of two genetically distinct subpopulations of A. darlingi adapted to different periods of rainfall may promote a more perennial transmission of malaria throughout the year. These findings, in a context of strong environmental impact due to deforestation and dam construction, have serious implications for malaria epidemiology and control in the Amazonian region.
Appendix
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Literature
1.
go back to reference Hiwat H, Bretas G: Ecology of Anopheles darlingi Root with respect to vector importance: a review. Parasit Vectors. 2011, 4: 177-10.1186/1756-3305-4-177.PubMedCentralCrossRefPubMed Hiwat H, Bretas G: Ecology of Anopheles darlingi Root with respect to vector importance: a review. Parasit Vectors. 2011, 4: 177-10.1186/1756-3305-4-177.PubMedCentralCrossRefPubMed
3.
go back to reference Sinka ME, Rubio-Palis Y, Manguin S, Patil AP, Temperley WH, Gething PW, Van Boeckel T, Kabaria CW, Harbach RE, Hay SI: The dominant Anopheles vectors of human malaria in the Americas: occurrence data, distribution maps and bionomic précis. Parasit Vectors. 2010, 3: 72-10.1186/1756-3305-3-72.PubMedCentralCrossRefPubMed Sinka ME, Rubio-Palis Y, Manguin S, Patil AP, Temperley WH, Gething PW, Van Boeckel T, Kabaria CW, Harbach RE, Hay SI: The dominant Anopheles vectors of human malaria in the Americas: occurrence data, distribution maps and bionomic précis. Parasit Vectors. 2010, 3: 72-10.1186/1756-3305-3-72.PubMedCentralCrossRefPubMed
4.
go back to reference Loaiza JR, Bermingham E, Scott ME, Rovira JR, Conn JE: Species composition and distribution of adult Anopheles (Diptera; Culicidae) in Panama. J Med Entomol. 2008, 45: 841-851. 10.1603/0022-2585(2008)45[841:SCADOA]2.0.CO;2.PubMedCentralCrossRefPubMed Loaiza JR, Bermingham E, Scott ME, Rovira JR, Conn JE: Species composition and distribution of adult Anopheles (Diptera; Culicidae) in Panama. J Med Entomol. 2008, 45: 841-851. 10.1603/0022-2585(2008)45[841:SCADOA]2.0.CO;2.PubMedCentralCrossRefPubMed
5.
go back to reference Marinotti O, Cerqueira GC, de Almeida LG, Ferro MI, Loreto EL, Zaha A, Teixeira SM, Wespiser AR, Almeida E, Silva A, Schlindwein AD, Pacheco AC, Silva AL, Graveley BR, Walenz BP, Lima Bde A, Ribeiro CA, Nunes-Silva CG, de Carvalho CR, Soares CM, de Menezes CB, Matiolli C, Caffrey D, Araújo DA, de Oliveira DM, Golenbock D, Grisard EC, Fantinatti-Garboggini F, de Carvalho FM, Barcellos FG: The genome of Anopheles darlingi, the main neotropical malaria vector. Nucleic Acids Res. 2013, 41: 7387-7400. 10.1093/nar/gkt484.PubMedCentralCrossRefPubMed Marinotti O, Cerqueira GC, de Almeida LG, Ferro MI, Loreto EL, Zaha A, Teixeira SM, Wespiser AR, Almeida E, Silva A, Schlindwein AD, Pacheco AC, Silva AL, Graveley BR, Walenz BP, Lima Bde A, Ribeiro CA, Nunes-Silva CG, de Carvalho CR, Soares CM, de Menezes CB, Matiolli C, Caffrey D, Araújo DA, de Oliveira DM, Golenbock D, Grisard EC, Fantinatti-Garboggini F, de Carvalho FM, Barcellos FG: The genome of Anopheles darlingi, the main neotropical malaria vector. Nucleic Acids Res. 2013, 41: 7387-7400. 10.1093/nar/gkt484.PubMedCentralCrossRefPubMed
6.
go back to reference Moreno M, Marinotti O, Krzywinski J, Tadei WP, James AA, Achee NL, Conn JE: Complete mtDNA genomes of Anopheles darlingi and an approach to anopheline divergence time. Malar J. 2010, 9: 127-10.1186/1475-2875-9-127.PubMedCentralCrossRefPubMed Moreno M, Marinotti O, Krzywinski J, Tadei WP, James AA, Achee NL, Conn JE: Complete mtDNA genomes of Anopheles darlingi and an approach to anopheline divergence time. Malar J. 2010, 9: 127-10.1186/1475-2875-9-127.PubMedCentralCrossRefPubMed
7.
go back to reference Vittor AY, Gilman RH, Tielsch J, Glass G, Shields T, Lozano WS, Pinedo-Cancino V, Patz JA: The effect of deforestation on the human-biting rate of Anopheles darlingi, the primary vector of falciparum malaria in the Peruvian Amazon. Am J Trop Med Hyg. 2006, 74: 3-11.PubMed Vittor AY, Gilman RH, Tielsch J, Glass G, Shields T, Lozano WS, Pinedo-Cancino V, Patz JA: The effect of deforestation on the human-biting rate of Anopheles darlingi, the primary vector of falciparum malaria in the Peruvian Amazon. Am J Trop Med Hyg. 2006, 74: 3-11.PubMed
8.
go back to reference Charlwood J: Biological variation in Anopheles darlingi Root. Mem Inst Oswaldo Cruz. 1996, 91: 391-398.PubMed Charlwood J: Biological variation in Anopheles darlingi Root. Mem Inst Oswaldo Cruz. 1996, 91: 391-398.PubMed
9.
go back to reference Angêlla AF, Gil LHS, Silva LHP, Ribolla PEM: Population structure of the malaria vector Anopheles darlingi in Rondônia, Brazilian Amazon, based on mitochondrial DNA. Mem Inst Oswaldo Cruz. 2007, 102: 953-958. 10.1590/S0074-02762007000800010.CrossRefPubMed Angêlla AF, Gil LHS, Silva LHP, Ribolla PEM: Population structure of the malaria vector Anopheles darlingi in Rondônia, Brazilian Amazon, based on mitochondrial DNA. Mem Inst Oswaldo Cruz. 2007, 102: 953-958. 10.1590/S0074-02762007000800010.CrossRefPubMed
10.
go back to reference Manguin S, Wilkerson RC, Conn JE, Rubio-Palis Y, Danoff-Burg JA, Roberts DR: Population structure of the primary malaria vector in South America, Anopheles darlingi, using isozyme, random amplified polymorphic DNA, internal transcribed spacer 2, and morphologic markers. Am J Trop Med Hyg. 1999, 60: 364-376.PubMed Manguin S, Wilkerson RC, Conn JE, Rubio-Palis Y, Danoff-Burg JA, Roberts DR: Population structure of the primary malaria vector in South America, Anopheles darlingi, using isozyme, random amplified polymorphic DNA, internal transcribed spacer 2, and morphologic markers. Am J Trop Med Hyg. 1999, 60: 364-376.PubMed
11.
go back to reference Santos JM, Lobo JA, Tadei WP, Contel EPB: Intrapopulational genetic differentiation in Anopheles (N.) darlingi Root, 1926 (Diptera: Culicidae) in the amazon region. Genet Mol Biol. 1999, 22: 325-331. 10.1590/S1415-47571999000300007.CrossRef Santos JM, Lobo JA, Tadei WP, Contel EPB: Intrapopulational genetic differentiation in Anopheles (N.) darlingi Root, 1926 (Diptera: Culicidae) in the amazon region. Genet Mol Biol. 1999, 22: 325-331. 10.1590/S1415-47571999000300007.CrossRef
12.
go back to reference Conn JE: Systematics and population level analysis of Anopheles darlingi. Mem Inst Oswaldo Cruz. 1998, 93: 647-650. 10.1590/S0074-02761998000500015.CrossRefPubMed Conn JE: Systematics and population level analysis of Anopheles darlingi. Mem Inst Oswaldo Cruz. 1998, 93: 647-650. 10.1590/S0074-02761998000500015.CrossRefPubMed
13.
go back to reference Mirabello L, Conn JE: Molecular population genetics of the malaria vector Anopheles darlingi in Central and South America. Heredity. 2006, 96: 311-321. 10.1038/sj.hdy.6800805.CrossRefPubMed Mirabello L, Conn JE: Molecular population genetics of the malaria vector Anopheles darlingi in Central and South America. Heredity. 2006, 96: 311-321. 10.1038/sj.hdy.6800805.CrossRefPubMed
14.
go back to reference Pedro PM, Sallum M: Spatial expansion and population structure of the neotropical malaria vector, Anopheles darlingi (Diptera: Culicidae). Biol J Linnean Soc. 2009, 97: 854-866. 10.1111/j.1095-8312.2009.01226.x.CrossRef Pedro PM, Sallum M: Spatial expansion and population structure of the neotropical malaria vector, Anopheles darlingi (Diptera: Culicidae). Biol J Linnean Soc. 2009, 97: 854-866. 10.1111/j.1095-8312.2009.01226.x.CrossRef
15.
go back to reference Conn JE, Vineis J, Bollback JP, Onyabe DY, Wilkerson C, Póvoa MM: Population structure of the malaria vector Anopheles darlingi in a malaria-endemic region of eastern Amazonian Brazil. Am J Trop Med Hyg. 2006, 74: 798-806.PubMed Conn JE, Vineis J, Bollback JP, Onyabe DY, Wilkerson C, Póvoa MM: Population structure of the malaria vector Anopheles darlingi in a malaria-endemic region of eastern Amazonian Brazil. Am J Trop Med Hyg. 2006, 74: 798-806.PubMed
16.
go back to reference Mirabello L, Vineis JH, Yanoviak SP, Scarpassa VM, Póvoa MM, Padilla N, Achee NL, Conn JE: Microsatellite data suggest significant population structure and differentiation within the malaria vector Anopheles darlingi in Central and South America. BMC Ecol. 2008, 8: 3-10.1186/1472-6785-8-3.PubMedCentralCrossRefPubMed Mirabello L, Vineis JH, Yanoviak SP, Scarpassa VM, Póvoa MM, Padilla N, Achee NL, Conn JE: Microsatellite data suggest significant population structure and differentiation within the malaria vector Anopheles darlingi in Central and South America. BMC Ecol. 2008, 8: 3-10.1186/1472-6785-8-3.PubMedCentralCrossRefPubMed
17.
go back to reference Scarpassa VM, Conn JE: Population genetic structure of the major malaria vector Anopheles darlingi (Diptera: Culicidae) from the Brazilian Amazon, using microsatellite markers. Mem Inst Oswaldo Cruz. 2007, 102: 319-327. 10.1590/S0074-02762007005000045.CrossRefPubMed Scarpassa VM, Conn JE: Population genetic structure of the major malaria vector Anopheles darlingi (Diptera: Culicidae) from the Brazilian Amazon, using microsatellite markers. Mem Inst Oswaldo Cruz. 2007, 102: 319-327. 10.1590/S0074-02762007005000045.CrossRefPubMed
18.
go back to reference Gil LHS, Alves FP, Zieler H, Salcedo JMV, Durlacher RR, Almeida Cunha RP, Tada MS, Camargo LMA, Camargo EP, Pereira Da Silva LH: Seasonal malaria transmission and variation of anopheline density in two distinct endemic areas in Brazilian Amazonia. J Med Entomol. 2003, 40: 636-641. 10.1603/0022-2585-40.5.636.CrossRefPubMed Gil LHS, Alves FP, Zieler H, Salcedo JMV, Durlacher RR, Almeida Cunha RP, Tada MS, Camargo LMA, Camargo EP, Pereira Da Silva LH: Seasonal malaria transmission and variation of anopheline density in two distinct endemic areas in Brazilian Amazonia. J Med Entomol. 2003, 40: 636-641. 10.1603/0022-2585-40.5.636.CrossRefPubMed
19.
go back to reference Gil LHS, Tada MS, Katsuragawa TH, Ribolla PEM, Pereira-Da-Silva LH: Urban and suburban malaria in Rondônia (Brazilian Western Amazon) II: Perennial transmissions with high anopheline densities are associated with human environmental changes. Mem Inst Oswaldo Cruz. 2007, 102: 271-276. 10.1590/S0074-02762007005000013.CrossRefPubMed Gil LHS, Tada MS, Katsuragawa TH, Ribolla PEM, Pereira-Da-Silva LH: Urban and suburban malaria in Rondônia (Brazilian Western Amazon) II: Perennial transmissions with high anopheline densities are associated with human environmental changes. Mem Inst Oswaldo Cruz. 2007, 102: 271-276. 10.1590/S0074-02762007005000013.CrossRefPubMed
20.
go back to reference Souza-Santos R: Seasonal distribution of malaria vectors in Machadinho d'Oeste, Rondônia State, Amazon Region, Brazil. Cad Saúde Pública. 2002, 18: 1813-1818. 10.1590/S0102-311X2002000600039.CrossRefPubMed Souza-Santos R: Seasonal distribution of malaria vectors in Machadinho d'Oeste, Rondônia State, Amazon Region, Brazil. Cad Saúde Pública. 2002, 18: 1813-1818. 10.1590/S0102-311X2002000600039.CrossRefPubMed
21.
go back to reference Moutinho PR, Gil LHS, Cruz RB, Ribolla PEM: Population dynamics, structure and behavior of Anopheles darlingi in a rural settlement in the Amazon rainforest of Acre. Brazil Malar J. 2011, 10: 174-10.1186/1475-2875-10-174.CrossRefPubMed Moutinho PR, Gil LHS, Cruz RB, Ribolla PEM: Population dynamics, structure and behavior of Anopheles darlingi in a rural settlement in the Amazon rainforest of Acre. Brazil Malar J. 2011, 10: 174-10.1186/1475-2875-10-174.CrossRefPubMed
23.
go back to reference Silva MJ, Saraiva FA, Araujo ML: Aspectos Climáticos de Porto Velho - Rondônia. XIII Congresso Brasileiro de Meteorologia. 2004, Fortaleza – CE: Meteorologia e o Desenvolvimento Sustentável Silva MJ, Saraiva FA, Araujo ML: Aspectos Climáticos de Porto Velho - Rondônia. XIII Congresso Brasileiro de Meteorologia. 2004, Fortaleza – CE: Meteorologia e o Desenvolvimento Sustentável
24.
go back to reference Consoli RAGB, Lourenço de Oliveira R: Principais mosquitos de importância sanitária no Brasil. 1994, Rio de Janeiro: Editora FIOCRUZ, 228- Consoli RAGB, Lourenço de Oliveira R: Principais mosquitos de importância sanitária no Brasil. 1994, Rio de Janeiro: Editora FIOCRUZ, 228-
25.
go back to reference Conn JE, Bollback JP, Onyabe DY, Robinson TN, Wilkerson RC, Póvoa MM: Isolation of polymorphic microsatellite markers from the malaria vector Anopheles darlingi. Mol Ecol Not. 2001, 1: 223-225. 10.1046/j.1471-8278.2001.00078.x.CrossRef Conn JE, Bollback JP, Onyabe DY, Robinson TN, Wilkerson RC, Póvoa MM: Isolation of polymorphic microsatellite markers from the malaria vector Anopheles darlingi. Mol Ecol Not. 2001, 1: 223-225. 10.1046/j.1471-8278.2001.00078.x.CrossRef
26.
go back to reference Calvo E, Pham V, Marinotto O, Andersen JF, Ribeiro JM: The salivary gland transcriptome of the neotropical malaria vector Anopheles darlingi reveals accelerated evolution of genes relevant to hematophagy. BMC Genomics. 2009, 10: 57-10.1186/1471-2164-10-57.PubMedCentralCrossRefPubMed Calvo E, Pham V, Marinotto O, Andersen JF, Ribeiro JM: The salivary gland transcriptome of the neotropical malaria vector Anopheles darlingi reveals accelerated evolution of genes relevant to hematophagy. BMC Genomics. 2009, 10: 57-10.1186/1471-2164-10-57.PubMedCentralCrossRefPubMed
27.
go back to reference Kimura M, Kaneko O, Liu Q, Zhou M, Kawamoto F, Wataya Y, Otani S, Yamaguchi Y, Tanabe K: Identification of the four species of human malaria parasites by nested PCR that targets variant sequences in the small subunit rRNA gene. Parasitol Int. 1997, 46: 91-95. 10.1016/S1383-5769(97)00013-5.CrossRef Kimura M, Kaneko O, Liu Q, Zhou M, Kawamoto F, Wataya Y, Otani S, Yamaguchi Y, Tanabe K: Identification of the four species of human malaria parasites by nested PCR that targets variant sequences in the small subunit rRNA gene. Parasitol Int. 1997, 46: 91-95. 10.1016/S1383-5769(97)00013-5.CrossRef
28.
go back to reference Goudet J: FSTAT (Version 1.2): A computer Program to calculate F-Statistics. J Hered. 1995, 86: 485-486. Goudet J: FSTAT (Version 1.2): A computer Program to calculate F-Statistics. J Hered. 1995, 86: 485-486.
29.
go back to reference Kalinowski ST: HP-RARE 1.0: a computer program for performing rarefaction on measures of allelic richness. Mol Ecol Not. 2004, 5: 187-189.CrossRef Kalinowski ST: HP-RARE 1.0: a computer program for performing rarefaction on measures of allelic richness. Mol Ecol Not. 2004, 5: 187-189.CrossRef
30.
go back to reference Excoffier L, Laval G, Schneider S: ARLEQUIN ver. 3.0: An integrated software package for population genetics data analysis. Evol Bioinform Online. 2005, 1: 47-50.PubMedCentral Excoffier L, Laval G, Schneider S: ARLEQUIN ver. 3.0: An integrated software package for population genetics data analysis. Evol Bioinform Online. 2005, 1: 47-50.PubMedCentral
31.
go back to reference Raymond M, Rousset F: GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered. 1995, 86: 248-249. Raymond M, Rousset F: GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered. 1995, 86: 248-249.
32.
go back to reference Rousset F: Genepop'007: a complete re-implementation of the genepop software for Windows and Linux. Mol Ecol Resour. 2008, 8: 103-106. 10.1111/j.1471-8286.2007.01931.x.CrossRefPubMed Rousset F: Genepop'007: a complete re-implementation of the genepop software for Windows and Linux. Mol Ecol Resour. 2008, 8: 103-106. 10.1111/j.1471-8286.2007.01931.x.CrossRefPubMed
33.
go back to reference Van Oosterhout C, Hutchinson W, Wills D, Shipley P: Micro-Checker: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Not. 2004, 4: 535-538. 10.1111/j.1471-8286.2004.00684.x.CrossRef Van Oosterhout C, Hutchinson W, Wills D, Shipley P: Micro-Checker: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Not. 2004, 4: 535-538. 10.1111/j.1471-8286.2004.00684.x.CrossRef
34.
go back to reference Weir B, Cockerham C: Estimating F-statistics for the analysis of population structure. Evolution. 1984, 38: 1358-1370. 10.2307/2408641.CrossRef Weir B, Cockerham C: Estimating F-statistics for the analysis of population structure. Evolution. 1984, 38: 1358-1370. 10.2307/2408641.CrossRef
35.
go back to reference Excoffier L, Smouse P, Quattro J: Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics. 1992, 131: 479-491.PubMedCentralPubMed Excoffier L, Smouse P, Quattro J: Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics. 1992, 131: 479-491.PubMedCentralPubMed
36.
go back to reference Pritchard J, Stephens M, Donnelly P: Inference of population structure using multilocus genotype data. Genetics. 2000, 155: 945-959.PubMedCentralPubMed Pritchard J, Stephens M, Donnelly P: Inference of population structure using multilocus genotype data. Genetics. 2000, 155: 945-959.PubMedCentralPubMed
37.
go back to reference Evanno G, Regnaut S, Goudet J: Detecting the number of clusters of individuals using the software Structure: a simulation study. Mol Ecol. 2005, 14: 2611-2620. 10.1111/j.1365-294X.2005.02553.x.CrossRefPubMed Evanno G, Regnaut S, Goudet J: Detecting the number of clusters of individuals using the software Structure: a simulation study. Mol Ecol. 2005, 14: 2611-2620. 10.1111/j.1365-294X.2005.02553.x.CrossRefPubMed
38.
go back to reference Earl D, von Holdt B: STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour. 2011, 4: 359-361.CrossRef Earl D, von Holdt B: STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour. 2011, 4: 359-361.CrossRef
39.
go back to reference Jakobsson M, Rosenberg NA: CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics. 2007, 23: 1801-1806. 10.1093/bioinformatics/btm233.CrossRefPubMed Jakobsson M, Rosenberg NA: CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics. 2007, 23: 1801-1806. 10.1093/bioinformatics/btm233.CrossRefPubMed
40.
go back to reference Vaha J-P, Primmer CR: Efficiency of model-based Bayesian methods for detecting hybrid individuals under different hybridization scenarios and with different numbers of loci. Mol Ecol. 2006, 15: 63-72.CrossRefPubMed Vaha J-P, Primmer CR: Efficiency of model-based Bayesian methods for detecting hybrid individuals under different hybridization scenarios and with different numbers of loci. Mol Ecol. 2006, 15: 63-72.CrossRefPubMed
41.
go back to reference Anderson EC, Thompson EA: A model-based method for identifying species hybrids using multilocus genetic data. Genetics. 2002, 160: 217-1229. Anderson EC, Thompson EA: A model-based method for identifying species hybrids using multilocus genetic data. Genetics. 2002, 160: 217-1229.
42.
go back to reference Piry S, Luikart G, Cornuet J: BOTTLENECK: a computer program for detecting recent reductions in the effective population size using allele frequency data. J Hered. 1999, 90: 502-503. 10.1093/jhered/90.4.502.CrossRef Piry S, Luikart G, Cornuet J: BOTTLENECK: a computer program for detecting recent reductions in the effective population size using allele frequency data. J Hered. 1999, 90: 502-503. 10.1093/jhered/90.4.502.CrossRef
43.
go back to reference Cornuet J-M, Luikart G: Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics. 1996, 144: 2001-2014.PubMedCentralPubMed Cornuet J-M, Luikart G: Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics. 1996, 144: 2001-2014.PubMedCentralPubMed
44.
go back to reference Holm S: A simple sequentially rejective multiple test procedure. Scand J Statist. 1979, 6: 65-70. Holm S: A simple sequentially rejective multiple test procedure. Scand J Statist. 1979, 6: 65-70.
45.
go back to reference Coetzee M, Hunt RH, Wilkerson R, della Torre A, Coulibaly MB, Besansky NJ: Anopheles coluzzii and Anopheles amharicus, new members of the Anopheles gambiae complex. Zootaxa. 2013, 3619: 246-274.CrossRefPubMed Coetzee M, Hunt RH, Wilkerson R, della Torre A, Coulibaly MB, Besansky NJ: Anopheles coluzzii and Anopheles amharicus, new members of the Anopheles gambiae complex. Zootaxa. 2013, 3619: 246-274.CrossRefPubMed
46.
go back to reference 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.PubMedCentralCrossRefPubMed 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.PubMedCentralCrossRefPubMed
47.
go back to reference Simard F, Ayala D, Kamdem GC, Pombi M, Etouna J, Ose K, Fotsing J-M, Fontenille D, Besansky NJ, Costantini C: Ecological niche partitioning between Anopheles gambiae molecular forms in Cameroon: the ecological side of speciation. BMC Ecol. 2009, 9: 17-10.1186/1472-6785-9-17.PubMedCentralCrossRefPubMed Simard F, Ayala D, Kamdem GC, Pombi M, Etouna J, Ose K, Fotsing J-M, Fontenille D, Besansky NJ, Costantini C: Ecological niche partitioning between Anopheles gambiae molecular forms in Cameroon: the ecological side of speciation. BMC Ecol. 2009, 9: 17-10.1186/1472-6785-9-17.PubMedCentralCrossRefPubMed
48.
go back to reference Kamdem C, Tene Fossog B, Simard F, Etouna J, Ndo C, Kengne P, Boussès P, Etoa FX, Awono-Ambene P, Fontenille D, Antonio-Nkondjio C, Besansky NJ, Costantini C: Anthropogenic habitat disturbance and ecological divergence between incipient species of the malaria mosquito Anopheles gambiae. PLoS One. 2012, 7: e39453-10.1371/journal.pone.0039453.PubMedCentralCrossRefPubMed Kamdem C, Tene Fossog B, Simard F, Etouna J, Ndo C, Kengne P, Boussès P, Etoa FX, Awono-Ambene P, Fontenille D, Antonio-Nkondjio C, Besansky NJ, Costantini C: Anthropogenic habitat disturbance and ecological divergence between incipient species of the malaria mosquito Anopheles gambiae. PLoS One. 2012, 7: e39453-10.1371/journal.pone.0039453.PubMedCentralCrossRefPubMed
49.
go back to reference Fossog Tene B, Poupardin R, Costantini C, Awono-Ambene P, Wondji CS, Ranson H, Antonio-Nkondjio C: Resistance to DDT in an urban setting: common mechanisms implicated in both M and S forms of Anopheles gambiae in the city of Yaoundé, Cameroon. PLoS One. 2013, 8: e61408-10.1371/journal.pone.0061408.PubMedCentralCrossRefPubMed Fossog Tene B, Poupardin R, Costantini C, Awono-Ambene P, Wondji CS, Ranson H, Antonio-Nkondjio C: Resistance to DDT in an urban setting: common mechanisms implicated in both M and S forms of Anopheles gambiae in the city of Yaoundé, Cameroon. PLoS One. 2013, 8: e61408-10.1371/journal.pone.0061408.PubMedCentralCrossRefPubMed
50.
go back to reference Gomes B, Sousa CA, Novo MT, Freitas FB, Alves R, Côrte-Real AR, Salgueiro P, Donnelly MJ, Almeida APJ, Pinto J: Asymmetric introgression between sympatric molestus and pipiens forms of Culex pipiens (Diptera: Culicidae) in the Comporta region, Portugal. BMC Evol Biol. 2009, 9: 262-10.1186/1471-2148-9-262.PubMedCentralCrossRefPubMed Gomes B, Sousa CA, Novo MT, Freitas FB, Alves R, Côrte-Real AR, Salgueiro P, Donnelly MJ, Almeida APJ, Pinto J: Asymmetric introgression between sympatric molestus and pipiens forms of Culex pipiens (Diptera: Culicidae) in the Comporta region, Portugal. BMC Evol Biol. 2009, 9: 262-10.1186/1471-2148-9-262.PubMedCentralCrossRefPubMed
51.
go back to reference Gomes B, Kioulos E, Papa A, Almeida AP, Vontas J, Pinto J: Distribution and hybridization of Culex pipiens forms in Greece during the West Nile virus outbreak of 2010. Infect Genet Evol. 2013, 16: 218-225.CrossRefPubMed Gomes B, Kioulos E, Papa A, Almeida AP, Vontas J, Pinto J: Distribution and hybridization of Culex pipiens forms in Greece during the West Nile virus outbreak of 2010. Infect Genet Evol. 2013, 16: 218-225.CrossRefPubMed
52.
go back to reference Marsden CD, Lee Y, Nieman CC, Sanford MR, Dinis J, Martins C, Rodrigues A, Cornel AJ, Lanzaro GC: Asymmetric introgression between the M and S forms of the malaria vector, Anopheles gambiae, maintains divergence despite extensive hybridization. Mol Ecol. 2011, 20: 4983-4994. 10.1111/j.1365-294X.2011.05339.x.PubMedCentralCrossRefPubMed Marsden CD, Lee Y, Nieman CC, Sanford MR, Dinis J, Martins C, Rodrigues A, Cornel AJ, Lanzaro GC: Asymmetric introgression between the M and S forms of the malaria vector, Anopheles gambiae, maintains divergence despite extensive hybridization. Mol Ecol. 2011, 20: 4983-4994. 10.1111/j.1365-294X.2011.05339.x.PubMedCentralCrossRefPubMed
53.
go back to reference Gow JL, Peichel CL, Taylor EB: Contrasting hybridization rates between sympatric three-spined sticklebacks highlight the fragility of reproductive barriers between evolutionarily young species. Mol Ecol. 2006, 15: 739-752. 10.1111/j.1365-294X.2006.02825.x.CrossRefPubMed Gow JL, Peichel CL, Taylor EB: Contrasting hybridization rates between sympatric three-spined sticklebacks highlight the fragility of reproductive barriers between evolutionarily young species. Mol Ecol. 2006, 15: 739-752. 10.1111/j.1365-294X.2006.02825.x.CrossRefPubMed
54.
go back to reference Nosil P: Speciation with gene flow could be common. Mol Ecol. 2008, 17: 2103-2106. 10.1111/j.1365-294X.2008.03715.x.CrossRefPubMed Nosil P: Speciation with gene flow could be common. Mol Ecol. 2008, 17: 2103-2106. 10.1111/j.1365-294X.2008.03715.x.CrossRefPubMed
55.
go back to reference Pinho C, Hey J: Divergence with gene flow: models and data. Annu Rev Ecol Evol Syst. 2010, 41: 215-230. 10.1146/annurev-ecolsys-102209-144644.CrossRef Pinho C, Hey J: Divergence with gene flow: models and data. Annu Rev Ecol Evol Syst. 2010, 41: 215-230. 10.1146/annurev-ecolsys-102209-144644.CrossRef
56.
go back to reference Charlwood JD: Observations on the bionomics of Anopheles darlingi Root (Diptera; Culicidae) from Brazil. Bull Entomol Res. 1980, 70: 685-692. 10.1017/S0007485300007975.CrossRef Charlwood JD: Observations on the bionomics of Anopheles darlingi Root (Diptera; Culicidae) from Brazil. Bull Entomol Res. 1980, 70: 685-692. 10.1017/S0007485300007975.CrossRef
57.
go back to reference Vittor AY, Pan W, Gilman RH, Tielsch J, Sánchez-Lozano W, Salas-Cobos E, Flores S, Patz JA: Linking deforestation to malaria in the Amazon: characterization of the breeding habitat of the principal malaria vector, Anopheles darlingi. Am J Trop Med Hyg. 2009, 81: 5-12.PubMedCentralPubMed Vittor AY, Pan W, Gilman RH, Tielsch J, Sánchez-Lozano W, Salas-Cobos E, Flores S, Patz JA: Linking deforestation to malaria in the Amazon: characterization of the breeding habitat of the principal malaria vector, Anopheles darlingi. Am J Trop Med Hyg. 2009, 81: 5-12.PubMedCentralPubMed
58.
go back to reference Hahn MB, Gangnon RE, Barcellos C, Asner GP, Patz JA: Influence of deforestation, logging, and fire on malaria in the Brazilian Amazon. Plos ONE. 2014, 9: e85725-10.1371/journal.pone.0085725.PubMedCentralCrossRefPubMed Hahn MB, Gangnon RE, Barcellos C, Asner GP, Patz JA: Influence of deforestation, logging, and fire on malaria in the Brazilian Amazon. Plos ONE. 2014, 9: e85725-10.1371/journal.pone.0085725.PubMedCentralCrossRefPubMed
59.
go back to reference Povoa MM, Conn JE, Schlichting CD, Amaral JC, Sequra MN, Da Silva AN, Dos Santos CC, Lacerda RN, De Souza RT, Galiza D, Santa Rosa EP, Wirtz RA: Malaria vectors, epidemiology, and the re-emergence of Anopheles darlingi in Belem, Para, Brazil. J Med Entomol. 2003, 40: 379-386. 10.1603/0022-2585-40.4.379.CrossRefPubMed Povoa MM, Conn JE, Schlichting CD, Amaral JC, Sequra MN, Da Silva AN, Dos Santos CC, Lacerda RN, De Souza RT, Galiza D, Santa Rosa EP, Wirtz RA: Malaria vectors, epidemiology, and the re-emergence of Anopheles darlingi in Belem, Para, Brazil. J Med Entomol. 2003, 40: 379-386. 10.1603/0022-2585-40.4.379.CrossRefPubMed
60.
go back to reference Harris AF, Matias-Arnez A, Hill N: Biting time of Anopheles darlingi in the Bolivian Amazon and implications for control of malaria. Trans R Soc Trop Med Hyg. 2006, 100: 45-47. 10.1016/j.trstmh.2005.07.001.CrossRefPubMed Harris AF, Matias-Arnez A, Hill N: Biting time of Anopheles darlingi in the Bolivian Amazon and implications for control of malaria. Trans R Soc Trop Med Hyg. 2006, 100: 45-47. 10.1016/j.trstmh.2005.07.001.CrossRefPubMed
61.
go back to reference Keiser J, Castro MCD, Maltese MF, Bos R, Tanner M, Singer BH, Utzinger J: Effect of irrigation and large dams on the burden of malaria on a global and regional scale. Am J Trop Med Hyg. 2005, 72: 392-406.PubMed Keiser J, Castro MCD, Maltese MF, Bos R, Tanner M, Singer BH, Utzinger J: Effect of irrigation and large dams on the burden of malaria on a global and regional scale. Am J Trop Med Hyg. 2005, 72: 392-406.PubMed
Metadata
Title
Seasonal genetic partitioning in the neotropical malaria vector, Anopheles darlingi
Authors
Aline F Angêlla
Patrícia Salgueiro
Luiz HS Gil
José L Vicente
João Pinto
Paulo EM Ribolla
Publication date
01-12-2014
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2014
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/1475-2875-13-203

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