Skip to main content
Top
Published in: Malaria Journal 1/2015

Open Access 01-12-2015 | Research

Remarkable diversity of intron-1 of the para voltage-gated sodium channel gene in an Anopheles gambiae/Anopheles coluzzii hybrid zone

Authors: Federica Santolamazza, Beniamino Caputo, Davis C Nwakanma, Caterina Fanello, Vincenzo Petrarca, David J Conway, David Weetman, Joao Pinto, Emiliano Mancini, Alessandra della Torre

Published in: Malaria Journal | Issue 1/2015

Login to get access

Abstract

Background

Genomic differentiation between Anopheles gambiae and Anopheles coluzzii - the major malaria vectors in sub-Saharan Africa - is localized into large “islands” toward the centromeres of chromosome-X and the two autosomes. Linkage disequilibrium between these genomic islands was first detected between species-specific polymorphisms within ribosomal DNA genes (IGS-rDNA) on the X-chromosome and a single variant at position 702 of intron 1 (Int-1702) of the para Voltage-Gated Sodium Channel (VGSC) gene on chromosome arm 2 L. Intron-1 sequence data from West and Central Africa revealed two clearly distinct and species-specific haplogroups, each characterized by very low polymorphism, which has been attributed to a selective sweep. The aim of this study was to analyse Int-1 sequence diversity in A. gambiae and A. coluzzii populations from the Far-West of their range, in order to assess whether this selective-sweep signature could persist in a zone of high interspecific hybridization.

Methods

A 531 bp region of VGSC Int-1 was sequenced in 21 A. coluzzii, 31 A. gambiae, and 12 hybrids from The Gambia and Guinea Bissau, located within the Far-West geographical region, and in 53 A. gambiae s.l. samples from the rest of the range.

Results

Far-West samples exhibit dramatic Int-1 polymorphism, far higher within each country than observed throughout the rest of the species range. Moreover, patterning of haplotypes within A. coluzzii confirms previous evidence of a macro-geographic subdivision into a West and a Central African genetic cluster, and reveals a possible genetic distinction of A. coluzzii populations from the Far-West.

Conclusions

The results suggest a relaxation of selective pressures acting across the VGSC gene region in the hybrid zone. Genetic differentiation in the Far-West could be attributable to a founder effect within A. coluzzii, with subsequent extensive gene flow with secondarily-colonizing A. gambiae, potentially yielding a novel insight on the dynamic processes impacting genetic divergence of these key malaria vectors.
Appendix
Available only for authorised users
Literature
1.
go back to reference Feder JL, Egan SP, Nosil P. The genomics of speciation-with-gene-flow. Trends Genet. 2012;28:342–50.PubMedCrossRef Feder JL, Egan SP, Nosil P. The genomics of speciation-with-gene-flow. Trends Genet. 2012;28:342–50.PubMedCrossRef
2.
go back to reference Turner TL, Hahn MW. Genomic islands of speciation or genomic islands and speciation? Mol Ecol. 2010;19:848–50.PubMedCrossRef Turner TL, Hahn MW. Genomic islands of speciation or genomic islands and speciation? Mol Ecol. 2010;19:848–50.PubMedCrossRef
3.
go back to reference Coluzzi M. Spatial distribution of chromosomal inversions and speciation in anopheline mosquitoes. In: Barigozzi C, editor. Mechanisms of Speciation. New York: Alan R. Liss Inc; 1982. p. 143–53. Coluzzi M. Spatial distribution of chromosomal inversions and speciation in anopheline mosquitoes. In: Barigozzi C, editor. Mechanisms of Speciation. New York: Alan R. Liss Inc; 1982. p. 143–53.
4.
go back to reference Manoukis NC, Powell JR, Touré MB, Sacko A, Edillo FE, Coulibaly MB, et al. A test of the chromosomal theory of ecotypic speciation in Anopheles gambiae. Proc Natl Acad Sci USA. 2008;105:2940–5.PubMedCentralPubMedCrossRef Manoukis NC, Powell JR, Touré MB, Sacko A, Edillo FE, Coulibaly MB, et al. A test of the chromosomal theory of ecotypic speciation in Anopheles gambiae. Proc Natl Acad Sci USA. 2008;105:2940–5.PubMedCentralPubMedCrossRef
5.
go back to reference Coluzzi M, Sabatini A, della Torre A, Di Deco MA, Petrarca V. A polytene chromosome analysis of the Anopheles gambiae species complex. Science. 2002;298:1415–8.PubMedCrossRef Coluzzi M, Sabatini A, della Torre A, Di Deco MA, Petrarca V. A polytene chromosome analysis of the Anopheles gambiae species complex. Science. 2002;298:1415–8.PubMedCrossRef
7.
go back to reference della Torre A, Fanello C, Akogbeto M, Dossou-yovo J, Favia G, Petrarca V, et al. Molecular evidence of incipient speciation within Anopheles gambiae s.s. in West Africa. Insect Mol Biol. 2001;10:9–18.PubMedCrossRef della Torre A, Fanello C, Akogbeto M, Dossou-yovo J, Favia G, Petrarca V, et al. Molecular evidence of incipient speciation within Anopheles gambiae s.s. in West Africa. Insect Mol Biol. 2001;10:9–18.PubMedCrossRef
8.
go back to reference Della Torre A, Costantini C, Besansky NJ, Caccone A, Petrarca V, Powell JR, et al. Speciation within Anopheles gambiae: the glass is half full. Science. 2002;298:115–7.PubMedCrossRef Della Torre A, Costantini C, Besansky NJ, Caccone A, Petrarca V, Powell JR, et al. Speciation within Anopheles gambiae: the glass is half full. Science. 2002;298:115–7.PubMedCrossRef
9.
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;3619:246–74.CrossRef 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;3619:246–74.CrossRef
11.
go back to reference Lawniczak MK, Emrich SJ, Holloway AK, Regier AP, Olson M, White B, et al. Widespread divergence between incipient Anopheles gambiae species revealed by whole genome sequences. Science. 2010;330:512–4.PubMedCentralPubMedCrossRef Lawniczak MK, Emrich SJ, Holloway AK, Regier AP, Olson M, White B, et al. Widespread divergence between incipient Anopheles gambiae species revealed by whole genome sequences. Science. 2010;330:512–4.PubMedCentralPubMedCrossRef
12.
go back to reference Neafsey DE, Lawniczak MK, Park DJ, Redmond SN, Coulibaly MB, Traoré SF, et al. SNP genotyping defines complex gene-flow boundaries among African malaria vector mosquitoes. Science. 2010;330:514–7.PubMedCrossRef Neafsey DE, Lawniczak MK, Park DJ, Redmond SN, Coulibaly MB, Traoré SF, et al. SNP genotyping defines complex gene-flow boundaries among African malaria vector mosquitoes. Science. 2010;330:514–7.PubMedCrossRef
13.
go back to reference White BJ, Cheng C, Simard F, Costantini C, Besansky NJ. Genetic association of physically unlinked islands of genomic divergence in incipient species of Anopheles gambiae. Mol Ecol. 2010;19:925–39.PubMedCentralPubMedCrossRef White BJ, Cheng C, Simard F, Costantini C, Besansky NJ. Genetic association of physically unlinked islands of genomic divergence in incipient species of Anopheles gambiae. Mol Ecol. 2010;19:925–39.PubMedCentralPubMedCrossRef
14.
go back to reference Via S, West J. The genetic mosaic suggests a new role for hitchhiking in ecological speciation. Mol Ecol. 2008;17:4334–45.PubMedCrossRef Via S, West J. The genetic mosaic suggests a new role for hitchhiking in ecological speciation. Mol Ecol. 2008;17:4334–45.PubMedCrossRef
15.
go back to reference Feder JL, Nosil P. The efficacy of divergence hitchhiking in generating genomic islands during ecological speciation. Evolution. 2010;64:1729–47.PubMedCrossRef Feder JL, Nosil P. The efficacy of divergence hitchhiking in generating genomic islands during ecological speciation. Evolution. 2010;64:1729–47.PubMedCrossRef
16.
go back to reference Cruickshank TE, Hahn MW. Re-analysis suggests that genomic islands of speciation are due to reduced diversity, not reduced gene flow. Mol Ecol. 2014;23:3133–57.PubMedCrossRef Cruickshank TE, Hahn MW. Re-analysis suggests that genomic islands of speciation are due to reduced diversity, not reduced gene flow. Mol Ecol. 2014;23:3133–57.PubMedCrossRef
17.
go back to reference Caputo B, Santolamazza F, Vicente JL, Nwakanma DC, Jawara M, Palsson K, et al. The “far-west” of Anopheles gambiae molecular forms. PLoS One. 2011;6:e16415.PubMedCentralPubMedCrossRef Caputo B, Santolamazza F, Vicente JL, Nwakanma DC, Jawara M, Palsson K, et al. The “far-west” of Anopheles gambiae molecular forms. PLoS One. 2011;6:e16415.PubMedCentralPubMedCrossRef
18.
go back to reference Nieman CC, Sanford MR, Dinis J, Martins C, Rodrigues A, Cornel AJ, et al. Asymmetric introgression between the M and S forms of the malaria vector, Anopheles gambiae, maintains divergence despite extensive hybridization. Mol Ecol. 2011;20:4983–94.PubMedCentralPubMedCrossRef Nieman CC, Sanford MR, Dinis J, Martins C, Rodrigues A, Cornel AJ, et al. Asymmetric introgression between the M and S forms of the malaria vector, Anopheles gambiae, maintains divergence despite extensive hybridization. Mol Ecol. 2011;20:4983–94.PubMedCentralPubMedCrossRef
19.
go back to reference Weetman D, Wilding CS, Steen K, Pinto J, Donnelly MJ. Gene flow-dependent genomic divergence between Anopheles gambiae M and S forms. Mol Biol Evol. 2012;29:279–91.PubMedCentralPubMedCrossRef Weetman D, Wilding CS, Steen K, Pinto J, Donnelly MJ. Gene flow-dependent genomic divergence between Anopheles gambiae M and S forms. Mol Biol Evol. 2012;29:279–91.PubMedCentralPubMedCrossRef
20.
go back to reference Nwakanma DC, Neafsey DE, Jawara M, Adiamoh M, Lund E, Rodrigues A, et al. Breakdown in the process of incipient speciation in Anopheles gambiae. Genetics. 2013;193:1221–31.PubMedCentralPubMedCrossRef Nwakanma DC, Neafsey DE, Jawara M, Adiamoh M, Lund E, Rodrigues A, et al. Breakdown in the process of incipient speciation in Anopheles gambiae. Genetics. 2013;193:1221–31.PubMedCentralPubMedCrossRef
21.
go back to reference Lee Y, Marsden CD, Norris LC, Collier TC, Main BJ, Fofana A, et al. Spatiotemporal dynamics of gene flow and hybrid fitness between the M and S forms of the malaria mosquito, Anopheles gambiae. Proc Natl Acad Sci USA. 2013;110:19854–9.PubMedCentralPubMedCrossRef Lee Y, Marsden CD, Norris LC, Collier TC, Main BJ, Fofana A, et al. Spatiotemporal dynamics of gene flow and hybrid fitness between the M and S forms of the malaria mosquito, Anopheles gambiae. Proc Natl Acad Sci USA. 2013;110:19854–9.PubMedCentralPubMedCrossRef
22.
go back to reference Weill M, Chandre F, Brengues C, Manguin S, Akogbeto M, Pasteur N, et al. The kdr mutation occurs in the Mopti form of Anopheles gambiae s.s. through introgression. Insect Mol Biol. 2000;9:451–5.PubMedCrossRef Weill M, Chandre F, Brengues C, Manguin S, Akogbeto M, Pasteur N, et al. The kdr mutation occurs in the Mopti form of Anopheles gambiae s.s. through introgression. Insect Mol Biol. 2000;9:451–5.PubMedCrossRef
23.
go back to reference Gentile G, Santolamazza F, Fanello C, Petrarca V, Caccone A, della Torre A. Variation in an intron sequence of the voltage-gated sodium channel gene correlates with genetic differentiation between Anopheles gambiae s.s. molecular forms. Insect Mol Biol. 2004;13:371–7.PubMedCrossRef Gentile G, Santolamazza F, Fanello C, Petrarca V, Caccone A, della Torre A. Variation in an intron sequence of the voltage-gated sodium channel gene correlates with genetic differentiation between Anopheles gambiae s.s. molecular forms. Insect Mol Biol. 2004;13:371–7.PubMedCrossRef
24.
go back to reference Scott JA, Brogdon WG, Collins FH. Identification of single specimens of the Anopheles gambiae complex by the polymerase chain reaction. Am J Trop Med Hyg. 1993;49:520–9.PubMed Scott JA, Brogdon WG, Collins FH. Identification of single specimens of the Anopheles gambiae complex by the polymerase chain reaction. Am J Trop Med Hyg. 1993;49:520–9.PubMed
25.
go back to reference 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;16:461–4.PubMedCrossRef 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;16:461–4.PubMedCrossRef
26.
go back to reference Santolamazza F, Mancini E, Simard F, Qi Y, Tu Z, della Torre A. Insertion polymorphisms of SINE200 retrotransposons within speciation islands of Anopheles gambiae molecular forms. Malar J. 2008;7:163.PubMedCentralPubMedCrossRef Santolamazza F, Mancini E, Simard F, Qi Y, Tu Z, della Torre A. Insertion polymorphisms of SINE200 retrotransposons within speciation islands of Anopheles gambiae molecular forms. Malar J. 2008;7:163.PubMedCentralPubMedCrossRef
27.
go back to reference Martinez-Torres D, Chandre F, Williamson MS, Darriet F, Berge JB, Devonshire AL, et al. Molecular characterization of pyrethroid knockdown resistance (kdr) in the major malaria vector Anopheles gambiae s.s. Insect Mol Biol. 1998;7:179–84.PubMedCrossRef Martinez-Torres D, Chandre F, Williamson MS, Darriet F, Berge JB, Devonshire AL, et al. Molecular characterization of pyrethroid knockdown resistance (kdr) in the major malaria vector Anopheles gambiae s.s. Insect Mol Biol. 1998;7:179–84.PubMedCrossRef
28.
go back to reference Ranson H, Jensen B, Vulule JM, Wang X, Hemingway J, Collins FH. Identification of a point mutation in the voltage-gated sodium channel gene of Kenyan Anopheles gambiae associated with resistance to DDT and pyrethroids. Insect Mol Biol. 2000;9:491–7.PubMedCrossRef Ranson H, Jensen B, Vulule JM, Wang X, Hemingway J, Collins FH. Identification of a point mutation in the voltage-gated sodium channel gene of Kenyan Anopheles gambiae associated with resistance to DDT and pyrethroids. Insect Mol Biol. 2000;9:491–7.PubMedCrossRef
29.
go back to reference Lynd A, Ranson H, McCall PJ, Randle NP, Black WC, Walker ED, et al. A simplified high-throughput method for pyrethroid knock-down resistance (kdr) detection in Anopheles gambiae. Malar J. 2005;4:16.PubMedCentralPubMedCrossRef Lynd A, Ranson H, McCall PJ, Randle NP, Black WC, Walker ED, et al. A simplified high-throughput method for pyrethroid knock-down resistance (kdr) detection in Anopheles gambiae. Malar J. 2005;4:16.PubMedCentralPubMedCrossRef
30.
go back to reference Staden R, Beal KF, Bonfield JK. The Staden package. Methods Mol Biol. 2000;132:115–30.PubMed Staden R, Beal KF, Bonfield JK. The Staden package. Methods Mol Biol. 2000;132:115–30.PubMed
31.
32.
33.
go back to reference Librado P, Rozas J. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics. 2009;25:1451–2.PubMedCrossRef Librado P, Rozas J. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics. 2009;25:1451–2.PubMedCrossRef
34.
go back to reference Tajima F. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics. 1989;123:585–95.PubMedCentralPubMed Tajima F. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics. 1989;123:585–95.PubMedCentralPubMed
36.
go back to reference Clement M, Posada D, Crandall KA. TCS: a computer program to estimate gene genealogies. Mol Ecol. 2000;9:1657–9.PubMedCrossRef Clement M, Posada D, Crandall KA. TCS: a computer program to estimate gene genealogies. Mol Ecol. 2000;9:1657–9.PubMedCrossRef
37.
go back to reference Excoffier L, Laval G, Schneider S. Arlequin (version 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 (version 3.0): an integrated software package for population genetics data analysis. Evol Bioinform Online. 2005;1:47–50.PubMedCentral
38.
go back to reference Santolamazza F, Caputo B, Calzetta M, Vicente JL, Mancini E, Petrarca V, et al. Comparative analyses reveal discrepancies among results of commonly used methods for Anopheles gambiae molecular form identification. Malar J. 2011;10:215.PubMedCentralPubMedCrossRef Santolamazza F, Caputo B, Calzetta M, Vicente JL, Mancini E, Petrarca V, et al. Comparative analyses reveal discrepancies among results of commonly used methods for Anopheles gambiae molecular form identification. Malar J. 2011;10:215.PubMedCentralPubMedCrossRef
39.
go back to reference Etang J, Vicente JL, Nwane P, Chouaibou M, Morlais I, Do Rosario VE, et al. Polymorphism of intron-1 in the voltage-gated sodium channel gene of Anopheles gambiae s.s. populations from Cameroon with emphasis on insecticide knockdown resistance mutations. Mol Ecol. 2009;18:3076–86.PubMedCrossRef Etang J, Vicente JL, Nwane P, Chouaibou M, Morlais I, Do Rosario VE, et al. Polymorphism of intron-1 in the voltage-gated sodium channel gene of Anopheles gambiae s.s. populations from Cameroon with emphasis on insecticide knockdown resistance mutations. Mol Ecol. 2009;18:3076–86.PubMedCrossRef
40.
go back to reference Clarkson CS, Weetman D, Essandoh J, Yawson AE, Maslen G, Manske M, et al. Adaptive introgression between Anopheles sibling species eliminates a major genomic island but not reproductive isolation. Nature Comm. 2014;5:4248.CrossRef Clarkson CS, Weetman D, Essandoh J, Yawson AE, Maslen G, Manske M, et al. Adaptive introgression between Anopheles sibling species eliminates a major genomic island but not reproductive isolation. Nature Comm. 2014;5:4248.CrossRef
41.
go back to reference Pinto J, Lynd A, Vicente JL, Santolamazza F, Randle NP, Moreno G, et al. Multiple origins of knockdown resistance mutations in the Afrotropical mosquito vector Anopheles gambiae. PLoS One. 2007;2:e1243.PubMedCentralPubMedCrossRef Pinto J, Lynd A, Vicente JL, Santolamazza F, Randle NP, Moreno G, et al. Multiple origins of knockdown resistance mutations in the Afrotropical mosquito vector Anopheles gambiae. PLoS One. 2007;2:e1243.PubMedCentralPubMedCrossRef
42.
go back to reference Santolamazza F, Calzetta M, Etang J, Barrese E, Dia I, Caccone A, et al. Distribution of knock-down resistance mutations in Anopheles gambiae (Diptera: Culicidae) molecular forms in west and west-central Africa. Malar J. 2008;7:74.PubMedCentralPubMedCrossRef Santolamazza F, Calzetta M, Etang J, Barrese E, Dia I, Caccone A, et al. Distribution of knock-down resistance mutations in Anopheles gambiae (Diptera: Culicidae) molecular forms in west and west-central Africa. Malar J. 2008;7:74.PubMedCentralPubMedCrossRef
43.
go back to reference Slotman MA, Tripet F, Cornel AJ, Meneses CR, Lee Y, Reimer LJ, et al. Evidence for subdivision within the M molecular form of Anopheles gambiae. Mol Ecol. 2007;16:639–49.PubMedCrossRef Slotman MA, Tripet F, Cornel AJ, Meneses CR, Lee Y, Reimer LJ, et al. Evidence for subdivision within the M molecular form of Anopheles gambiae. Mol Ecol. 2007;16:639–49.PubMedCrossRef
44.
go back to reference Pinto J, Egyir-Yawson A, Vicente J, Gomes B, Santolamazza F, Moreno M, et al. 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. 2013;6:910–24.PubMedCentralPubMedCrossRef Pinto J, Egyir-Yawson A, Vicente J, Gomes B, Santolamazza F, Moreno M, et al. 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. 2013;6:910–24.PubMedCentralPubMedCrossRef
Metadata
Title
Remarkable diversity of intron-1 of the para voltage-gated sodium channel gene in an Anopheles gambiae/Anopheles coluzzii hybrid zone
Authors
Federica Santolamazza
Beniamino Caputo
Davis C Nwakanma
Caterina Fanello
Vincenzo Petrarca
David J Conway
David Weetman
Joao Pinto
Emiliano Mancini
Alessandra della Torre
Publication date
01-12-2015
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2015
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/s12936-014-0522-1

Other articles of this Issue 1/2015

Malaria Journal 1/2015 Go to the issue