Skip to main content
Top
Published in: Malaria Journal 1/2016

Open Access 01-12-2016 | Research

Evidence of new species for malaria vector Anopheles nuneztovari sensu lato in the Brazilian Amazon region

Authors: Vera Margarete Scarpassa, Antonio Saulo Cunha-Machado, José Ferreira Saraiva

Published in: Malaria Journal | Issue 1/2016

Login to get access

Abstract

Background

Anopheles nuneztovari sensu lato comprises cryptic species in northern South America, and the Brazilian populations encompass distinct genetic lineages within the Brazilian Amazon region. This study investigated, based on two molecular markers, whether these lineages might actually deserve species status.

Methods

Specimens were collected in five localities of the Brazilian Amazon, including Manaus, Careiro Castanho and Autazes, in the State of Amazonas; Tucuruí, in the State of Pará; and Abacate da Pedreira, in the State of Amapá, and analysed for the COI gene (Barcode region) and 12 microsatellite loci. Phylogenetic analyses were performed using the maximum likelihood (ML) approach. Intra and inter samples genetic diversity were estimated using population genetics analyses, and the genetic groups were identified by means of the ML, Bayesian and factorial correspondence analyses and the Bayesian analysis of population structure.

Results

The Barcode region dataset (N = 103) generated 27 haplotypes. The haplotype network suggested three lineages. The ML tree retrieved five monophyletic groups. Group I clustered all specimens from Manaus and Careiro Castanho, the majority of Autazes and a few from Abacate da Pedreira. Group II clustered most of the specimens from Abacate da Pedreira and a few from Autazes and Tucuruí. Group III clustered only specimens from Tucuruí (lineage III), strongly supported (97 %). Groups IV and V clustered specimens of A. nuneztovari s.s. and A. dunhami, strongly (98 %) and weakly (70 %) supported, respectively. In the second phylogenetic analysis, the sequences from GenBank, identified as A. goeldii, clustered to groups I and II, but not to group III. Genetic distances (Kimura-2 parameters) among the groups ranged from 1.60 % (between I and II) to 2.32 % (between I and III). Microsatellite data revealed very high intra-population genetic variability. Genetic distances showed the highest and significant values (P = 0.005) between Tucuruí and all the other samples, and between Abacate da Pedreira and all the other samples. Genetic distances, Bayesian (Structure and BAPS) analyses and FCA suggested three distinct biological groups, supporting the barcode region results.

Conclusions

The two markers revealed three genetic lineages for A. nuneztovari s.l. in the Brazilian Amazon region. Lineages I and II may represent genetically distinct groups or species within A. goeldii. Lineage III may represent a new species, distinct from the A. goeldii group, and may be the most ancestral in the Brazilian Amazon. They may have differences in Plasmodium susceptibility and should therefore be investigated further.
Appendix
Available only for authorised users
Literature
1.
go back to reference Faran ME. Mosquito studies (Diptera, Culicidae). XXXIV. A revision of the Albimanus section of the subgenus Nyssorhynchus of Anopheles. Contrib Am Entomol Inst (Ann Arbor). 1980;15:1–215. Faran ME. Mosquito studies (Diptera, Culicidae). XXXIV. A revision of the Albimanus section of the subgenus Nyssorhynchus of Anopheles. Contrib Am Entomol Inst (Ann Arbor). 1980;15:1–215.
2.
go back to reference Fleming G. Biology y ecologia de los vectores de la malaria en las Americas PAHO/WHO. Washington: PNSP-86-72; 1986. p. 54 Fleming G. Biology y ecologia de los vectores de la malaria en las Americas PAHO/WHO. Washington: PNSP-86-72; 1986. p. 54
3.
go back to reference Sinka ME, Rubio-Palis Y, Manguin S, Patil AP, Temperley WH, Gething PW, et al. The dominant Anopheles vectors of human malaria in the Americas: occurrence data, distribution maps and bionomic précis. Parasit Vectors. 2010;3:72.CrossRefPubMedPubMedCentral Sinka ME, Rubio-Palis Y, Manguin S, Patil AP, Temperley WH, Gething PW, et al. The dominant Anopheles vectors of human malaria in the Americas: occurrence data, distribution maps and bionomic précis. Parasit Vectors. 2010;3:72.CrossRefPubMedPubMedCentral
4.
go back to reference Gabaldón A. Anopheles nuneztovari: importante vector y agente de malaria refractaria en Venezuela. Boletin de la Direccion de Malariologica y Saneamiento Ambiental. 1981;21:28–38. Gabaldón A. Anopheles nuneztovari: importante vector y agente de malaria refractaria en Venezuela. Boletin de la Direccion de Malariologica y Saneamiento Ambiental. 1981;21:28–38.
5.
go back to reference Gutiérrez LA, Gonzáles JJ, Gómez GF, Castro MI, Rosero DA, Luckhart S, et al. Species composition and natural infectivity of anthropophilic Anopheles (Diptera: Culicidae) in the states of Córdoba and Antioquia, Northwestern Colombia. Mem Inst Oswaldo Cruz. 2009;104:1117–24.PubMedPubMedCentral Gutiérrez LA, Gonzáles JJ, Gómez GF, Castro MI, Rosero DA, Luckhart S, et al. Species composition and natural infectivity of anthropophilic Anopheles (Diptera: Culicidae) in the states of Córdoba and Antioquia, Northwestern Colombia. Mem Inst Oswaldo Cruz. 2009;104:1117–24.PubMedPubMedCentral
6.
go back to reference Arruda M, Carvalho MB, Nussenzweig RS, Maracic M, Ferreira AW, Cochrane AH. Potential vectors of malaria and their different susceptibility to Plasmodium falciparum and Plasmodium vivax in northern Brazil identified by immunoassay. Am J Trop Med Hyg. 1986;35:873–81.PubMed Arruda M, Carvalho MB, Nussenzweig RS, Maracic M, Ferreira AW, Cochrane AH. Potential vectors of malaria and their different susceptibility to Plasmodium falciparum and Plasmodium vivax in northern Brazil identified by immunoassay. Am J Trop Med Hyg. 1986;35:873–81.PubMed
7.
go back to reference Tadei WP, Santos JMM, Scarpassa VM, Rodrigues IB. Incidência, distribuição e aspectos ecológicos de espécies de Anopheles (Diptera: Culicidae), em regiões naturais e sob impacto ambiental da Amazônia brasileira. In: Bases Científicas para Estratégias de Preservação e Desenvolvimento da Amazônia. Ferreira EJG, Santos GM, Leão ELM, Oliveira LA, editors. Vol. 2. Manaus: Instituto Nacional de Pesquisas da Amazônia. 1993, p. 167–196. Tadei WP, Santos JMM, Scarpassa VM, Rodrigues IB. Incidência, distribuição e aspectos ecológicos de espécies de Anopheles (Diptera: Culicidae), em regiões naturais e sob impacto ambiental da Amazônia brasileira. In: Bases Científicas para Estratégias de Preservação e Desenvolvimento da Amazônia. Ferreira EJG, Santos GM, Leão ELM, Oliveira LA, editors. Vol. 2. Manaus: Instituto Nacional de Pesquisas da Amazônia. 1993, p. 167–196.
8.
go back to reference Tadei WP, Dutary-Thatcher B, Santos JMM, Scarpassa VM, Rodrigues IB, Rafael MS. Ecologic observations on anopheline vectors of malaria in the Brazilian Amazon. Am J Trop Med Hyg. 1998;59:325–35.PubMed Tadei WP, Dutary-Thatcher B, Santos JMM, Scarpassa VM, Rodrigues IB, Rafael MS. Ecologic observations on anopheline vectors of malaria in the Brazilian Amazon. Am J Trop Med Hyg. 1998;59:325–35.PubMed
9.
go back to reference Tadei WP, Dutary-Thatcher B. Malaria vectors in the Brazilian Amazon: Anopheles of the subgenus Nyssorhynchus. Rev Inst Med Trop S Paulo. 2000;42:87–94.CrossRefPubMed Tadei WP, Dutary-Thatcher B. Malaria vectors in the Brazilian Amazon: Anopheles of the subgenus Nyssorhynchus. Rev Inst Med Trop S Paulo. 2000;42:87–94.CrossRefPubMed
10.
go back to reference Póvoa MM, Wirtz RA, Lacerda RNL, Miles MA, Warhurst D. Malaria vectors in the municipality of Serra do Navio, State of Amapá, Amazon Region. Brazil. Mem Inst Oswaldo Cruz. 2001;96:179–84.CrossRefPubMed Póvoa MM, Wirtz RA, Lacerda RNL, Miles MA, Warhurst D. Malaria vectors in the municipality of Serra do Navio, State of Amapá, Amazon Region. Brazil. Mem Inst Oswaldo Cruz. 2001;96:179–84.CrossRefPubMed
11.
go back to reference Silva-Vasconcelos A, Kató MYN, Mourão EM, Souza RTL, Lacerda RNL, Sibajev A, et al. Biting indices, host-seeking activity and natural infection rates of anopheline species in Boa Vista, Roraima, Brazil from 1996 to 1998. Mem Inst Oswaldo Cruz. 2002;97:151–61.CrossRefPubMed Silva-Vasconcelos A, Kató MYN, Mourão EM, Souza RTL, Lacerda RNL, Sibajev A, et al. Biting indices, host-seeking activity and natural infection rates of anopheline species in Boa Vista, Roraima, Brazil from 1996 to 1998. Mem Inst Oswaldo Cruz. 2002;97:151–61.CrossRefPubMed
12.
go back to reference Galardo ACR, Arruda M, Couto ARA, Wirtz R, Lounibos LP, Zimmerman RH. Malaria vectors incrimination in three rural riverine villages in the Brazilian Amazon. Am J Trop Med Hyg. 2007;76:461–9.PubMed Galardo ACR, Arruda M, Couto ARA, Wirtz R, Lounibos LP, Zimmerman RH. Malaria vectors incrimination in three rural riverine villages in the Brazilian Amazon. Am J Trop Med Hyg. 2007;76:461–9.PubMed
13.
go back to reference Rios-Velásques CM, Martins-Campos KM, Simões RC, Izzo T, Santos EV, Pessoa FAC, et al. Experimental Plasmodium vivax infection of key Anopheles species from the Brazilian Amazon. Malar J. 2013;12:460.CrossRef Rios-Velásques CM, Martins-Campos KM, Simões RC, Izzo T, Santos EV, Pessoa FAC, et al. Experimental Plasmodium vivax infection of key Anopheles species from the Brazilian Amazon. Malar J. 2013;12:460.CrossRef
14.
go back to reference Elliott R. The influence of vector behavior on malaria transmission. Am J Trop Med Hyg. 1972;21:755–63.PubMed Elliott R. The influence of vector behavior on malaria transmission. Am J Trop Med Hyg. 1972;21:755–63.PubMed
15.
go back to reference Kitzmiller JB, Kreutzer RD, Tallaferro E. Chromosomal differences in populations of Anopheles nuneztovari. Bull World Health Org. 1973;48:435–45.PubMedPubMedCentral Kitzmiller JB, Kreutzer RD, Tallaferro E. Chromosomal differences in populations of Anopheles nuneztovari. Bull World Health Org. 1973;48:435–45.PubMedPubMedCentral
16.
go back to reference Conn J, Puertas YR, Seawright JA. A new cytotype of Anopheles nuneztovari from Western Venezuela and Colombia. J Am Mosq Control Assoc. 1993;9:294–301.PubMed Conn J, Puertas YR, Seawright JA. A new cytotype of Anopheles nuneztovari from Western Venezuela and Colombia. J Am Mosq Control Assoc. 1993;9:294–301.PubMed
17.
go back to reference Fritz GN, Conn J, Cockburn AF, Seawright JA. Sequence analysis of the ribosomal DNA internal transcribed spacer 2 from populations of Anopheles nuneztovari (Diptera: Culicidae). Mol Biol Evol. 1994;11:406–16.PubMed Fritz GN, Conn J, Cockburn AF, Seawright JA. Sequence analysis of the ribosomal DNA internal transcribed spacer 2 from populations of Anopheles nuneztovari (Diptera: Culicidae). Mol Biol Evol. 1994;11:406–16.PubMed
18.
go back to reference Conn JE, Mitchell SE, Cockburn AF. Mitochondrial DNA analysis of the neotropical malaria vector Anopheles nuneztovari. Genome. 1998;41:313–27.CrossRef Conn JE, Mitchell SE, Cockburn AF. Mitochondrial DNA analysis of the neotropical malaria vector Anopheles nuneztovari. Genome. 1998;41:313–27.CrossRef
19.
go back to reference Hribar LJ. Geographic variation of male genitalia of Anopheles nuneztovari (Diptera: Culicidae). Mosq Syst. 1994;26:132–44. Hribar LJ. Geographic variation of male genitalia of Anopheles nuneztovari (Diptera: Culicidae). Mosq Syst. 1994;26:132–44.
20.
go back to reference Linley JR, Lounibos LP, Conn J, Duzak D, Nishimura N. A description and morphometric comparison of eggs from eight geographic populations of the South American malaria vector Anopheles (Nyssorhynchus) nuneztovari (Diptera: Culicidae). J Am Mosq Control Assoc. 1996;12:275–92.PubMed Linley JR, Lounibos LP, Conn J, Duzak D, Nishimura N. A description and morphometric comparison of eggs from eight geographic populations of the South American malaria vector Anopheles (Nyssorhynchus) nuneztovari (Diptera: Culicidae). J Am Mosq Control Assoc. 1996;12:275–92.PubMed
21.
go back to reference Scarpassa VM, Tadei WP, Suarez MF. Allozyme differentiation among allopatric populations of Anopheles nuneztovari (Diptera: Culicidae). Braz J Genet. 1996;19:265–9. Scarpassa VM, Tadei WP, Suarez MF. Allozyme differentiation among allopatric populations of Anopheles nuneztovari (Diptera: Culicidae). Braz J Genet. 1996;19:265–9.
22.
go back to reference Scarpassa VM, Tadei WP, Suarez MF. Population structure and genetic divergence in Anopheles nuneztovari (Diptera: Culicidae) from Brazil and Colombia. Am J Trop Med Hyg. 1999;60:1010–8.PubMed Scarpassa VM, Tadei WP, Suarez MF. Population structure and genetic divergence in Anopheles nuneztovari (Diptera: Culicidae) from Brazil and Colombia. Am J Trop Med Hyg. 1999;60:1010–8.PubMed
23.
go back to reference Scarpassa VM, Geurgas S, Azeredo-Espin AML, Tadei WP. Genetic divergence in mitochondrial DNA of Anopheles nuneztovari (Diptera: Culicidae) from Brazil and Colombia. Genet Mol Biol. 2000;23:71–8.CrossRef Scarpassa VM, Geurgas S, Azeredo-Espin AML, Tadei WP. Genetic divergence in mitochondrial DNA of Anopheles nuneztovari (Diptera: Culicidae) from Brazil and Colombia. Genet Mol Biol. 2000;23:71–8.CrossRef
24.
go back to reference Mirabello L, Conn JE. Population analysis using the nuclear white gene detects Pliocene/Pleistocene lineage divergence within Anopheles nuneztovari in South America. Med Vet Entomol. 2008;22:109–19.CrossRefPubMed Mirabello L, Conn JE. Population analysis using the nuclear white gene detects Pliocene/Pleistocene lineage divergence within Anopheles nuneztovari in South America. Med Vet Entomol. 2008;22:109–19.CrossRefPubMed
25.
go back to reference Calado DC, Foster PG, Bergo ES, Santos CLS, Galardo AKR, Sallum MAM. Resurrection of Anopheles goeldii from synonymy with Anopheles nuneztovari (Diptera: Culicidae) and a new record for Anopheles dunhami in the Brazilian Amazon. Mem Inst Oswaldo Cruz. 2008;103:791–9.CrossRefPubMed Calado DC, Foster PG, Bergo ES, Santos CLS, Galardo AKR, Sallum MAM. Resurrection of Anopheles goeldii from synonymy with Anopheles nuneztovari (Diptera: Culicidae) and a new record for Anopheles dunhami in the Brazilian Amazon. Mem Inst Oswaldo Cruz. 2008;103:791–9.CrossRefPubMed
26.
go back to reference Scarpassa VM. Divergência genética entre populações alopátricas de Anopheles nuneztovari Gabaldón, 1940 (Diptera: Culicidae) do Brasil e Colômbia. Doutoral Thesis. Instituto Nacional de Pesquisas da Amazônia, Manaus, Brazil. 1996;p. 171. Scarpassa VM. Divergência genética entre populações alopátricas de Anopheles nuneztovari Gabaldón, 1940 (Diptera: Culicidae) do Brasil e Colômbia. Doutoral Thesis. Instituto Nacional de Pesquisas da Amazônia, Manaus, Brazil. 1996;p. 171.
27.
go back to reference Sant’Ana DC, Bergo ES, Sallum MAM. Anopheles goeldii Rozeboom and Gabaldón (Diptera: Culicidae): a species of the Nuneztovari Complex of Anopheles Meigen. Rev Brasil Entomol. 2015;59:68–76.CrossRef Sant’Ana DC, Bergo ES, Sallum MAM. Anopheles goeldii Rozeboom and Gabaldón (Diptera: Culicidae): a species of the Nuneztovari Complex of Anopheles Meigen. Rev Brasil Entomol. 2015;59:68–76.CrossRef
28.
go back to reference Foster PG, Bergo ES, Bourke BP, Oliveira TMP, Nagaki SS, Sant’Ana DC, et al. Phylogenetic analysis and DNA-based species confirmation in Anopheles (Nyssorhynchus). PLoS One. 2013;8:e54063.CrossRefPubMedPubMedCentral Foster PG, Bergo ES, Bourke BP, Oliveira TMP, Nagaki SS, Sant’Ana DC, et al. Phylogenetic analysis and DNA-based species confirmation in Anopheles (Nyssorhynchus). PLoS One. 2013;8:e54063.CrossRefPubMedPubMedCentral
29.
go back to reference Lounibos LP, Wilkerson RC, Conn JE, Hribar LJ, Fritz GN, Danoff-Burg JA. Morphological, molecular, and chromosomal discrimination of cryptic Anopheles (Nyssorhynchus) (Diptera: Culicidae) from South America. J Med Entomol. 1998;35:830–8.CrossRefPubMed Lounibos LP, Wilkerson RC, Conn JE, Hribar LJ, Fritz GN, Danoff-Burg JA. Morphological, molecular, and chromosomal discrimination of cryptic Anopheles (Nyssorhynchus) (Diptera: Culicidae) from South America. J Med Entomol. 1998;35:830–8.CrossRefPubMed
30.
go back to reference Trindade DB, Scarpassa VM. Genetic differentiation and diagnostic loci among Anopheles (Nyssorhynchus) rangeli, An. (Nys.) nuneztovari and An. (Nys.) dunhami (Diptera: Culicidae) from the Brazilian Amazon. J Med Entomol. 2002;39:613–20.CrossRefPubMed Trindade DB, Scarpassa VM. Genetic differentiation and diagnostic loci among Anopheles (Nyssorhynchus) rangeli, An. (Nys.) nuneztovari and An. (Nys.) dunhami (Diptera: Culicidae) from the Brazilian Amazon. J Med Entomol. 2002;39:613–20.CrossRefPubMed
31.
go back to reference Scarpassa VM, Conn JE. Mitochondrial DNA detects a complex evolutionary history with Pleistocene Epoch divergence for the Neotropical malaria vector Anopheles nuneztovari sensu lato. Am J Trop Med Hyg. 2011;85:857–67.CrossRefPubMedPubMedCentral Scarpassa VM, Conn JE. Mitochondrial DNA detects a complex evolutionary history with Pleistocene Epoch divergence for the Neotropical malaria vector Anopheles nuneztovari sensu lato. Am J Trop Med Hyg. 2011;85:857–67.CrossRefPubMedPubMedCentral
32.
go back to reference Ruiz F, Linton Y-M, Ponsonby DJ, Conn JE, Herrera M, Quiñones ML, et al. Molecular comparison of topotypic specimens confirms Anopheles (Nyssorhynchus) dunhami Causey (Diptera: Culicidae) in the Colombian Amazon. Mem Inst Oswaldo Cruz. 2010;105:899–903.PubMedPubMedCentral Ruiz F, Linton Y-M, Ponsonby DJ, Conn JE, Herrera M, Quiñones ML, et al. Molecular comparison of topotypic specimens confirms Anopheles (Nyssorhynchus) dunhami Causey (Diptera: Culicidae) in the Colombian Amazon. Mem Inst Oswaldo Cruz. 2010;105:899–903.PubMedPubMedCentral
33.
go back to reference Causey OR. Description of Anopheles (Nyssorhynchus) dunhami, a new species from the Upper Amazon Basin. J Nat Malar Soc. 1945;4:231–5. Causey OR. Description of Anopheles (Nyssorhynchus) dunhami, a new species from the Upper Amazon Basin. J Nat Malar Soc. 1945;4:231–5.
34.
go back to reference Loaiza JR, Bermingham E, Sanjur OI, Scott ME, Bickersmith SA, Conn JE. Review of genetic diversity in malaria vectors (Culicidae: Anophelinae). Infect Genet Evol. 2012;12:1–12.CrossRefPubMed Loaiza JR, Bermingham E, Sanjur OI, Scott ME, Bickersmith SA, Conn JE. Review of genetic diversity in malaria vectors (Culicidae: Anophelinae). Infect Genet Evol. 2012;12:1–12.CrossRefPubMed
35.
go back to reference Hebert PDN, Ratnasingham S, deWaard JR. Biological identification through DNA barcode. Proc R Soc Lond B. 2003;270:313–22.CrossRef Hebert PDN, Ratnasingham S, deWaard JR. Biological identification through DNA barcode. Proc R Soc Lond B. 2003;270:313–22.CrossRef
36.
go back to reference Ruiz-Lopes F, Wilkerson RC, Conn JE, Mckeon SN, Levin DM, Quiñones ML, et al. DNA barcoding reveals both known and novel taxa in the Albitarsis group (Anopheles: Nyssorhynchus) of Neotropical malaria vectors. Parasit Vectors. 2012;5:44.CrossRef Ruiz-Lopes F, Wilkerson RC, Conn JE, Mckeon SN, Levin DM, Quiñones ML, et al. DNA barcoding reveals both known and novel taxa in the Albitarsis group (Anopheles: Nyssorhynchus) of Neotropical malaria vectors. Parasit Vectors. 2012;5:44.CrossRef
37.
go back to reference Ruiz-Lopes F, Wilkerson RC, Ponsonby DJ, Herrera M, Sallum MAM, Veléz ID, et al. Systematic of the Oswaldoi complex (Anopheles, Nyssorhynchus) in South America. Parasit Vectors. 2013;6:324.CrossRef Ruiz-Lopes F, Wilkerson RC, Ponsonby DJ, Herrera M, Sallum MAM, Veléz ID, et al. Systematic of the Oswaldoi complex (Anopheles, Nyssorhynchus) in South America. Parasit Vectors. 2013;6:324.CrossRef
38.
go back to reference Foley DH, Wilkerson RC, Cooper RD, Volovsek ME, Bryan JH. A molecular phylogeny of Anopheles annulipes (Diptera: Culicidae) sensu lato: The most species-rich anopheline complex. Mol Phylogenet Evol. 2007;43:283–97.CrossRefPubMed Foley DH, Wilkerson RC, Cooper RD, Volovsek ME, Bryan JH. A molecular phylogeny of Anopheles annulipes (Diptera: Culicidae) sensu lato: The most species-rich anopheline complex. Mol Phylogenet Evol. 2007;43:283–97.CrossRefPubMed
39.
go back to reference Austin JD, Bertin A, Bórques JP, Cardoza TB, Douglas KC, Ellwood SR, et al. Molecular ecology resources primer development consortium, Permanent Genetics Resources added to Molecular Ecology Resources Database 1 Feb 2011–31 Mar 2011. Mol Ecol Res. 2011;11:757–8 (Print).CrossRef Austin JD, Bertin A, Bórques JP, Cardoza TB, Douglas KC, Ellwood SR, et al. Molecular ecology resources primer development consortium, Permanent Genetics Resources added to Molecular Ecology Resources Database 1 Feb 2011–31 Mar 2011. Mol Ecol Res. 2011;11:757–8 (Print).CrossRef
41.
go back to reference Cova-Garcia P. Notas sobre los anofelinos de Venezuela y su identificación. Ed. Grafos, Caracas. 1961. Cova-Garcia P. Notas sobre los anofelinos de Venezuela y su identificación. Ed. Grafos, Caracas. 1961.
42.
go back to reference Sambrook J, Russell DW. A Laboratory Manual 2001. New York: Cold Spring Harbor Laboratory Press. Sambrook J, Russell DW. A Laboratory Manual 2001. New York: Cold Spring Harbor Laboratory Press.
43.
go back to reference Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R. DNA primers for amplification of mitochondrial Cytochrome C Oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol. 1994;3:294–9.PubMed Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R. DNA primers for amplification of mitochondrial Cytochrome C Oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol. 1994;3:294–9.PubMed
44.
go back to reference Schuelke M. An economic method for the fluorescent labeling of PCR fragments. Nat Biotechnol. 2000;18:233–4.CrossRefPubMed Schuelke M. An economic method for the fluorescent labeling of PCR fragments. Nat Biotechnol. 2000;18:233–4.CrossRefPubMed
45.
go back to reference Hall TA. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser. 1999;41:95–8. Hall TA. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser. 1999;41:95–8.
48.
go back to reference Librado P, Rozas J. DnaSP v. 5: a software for comprehen-sive analysis of DNA polymorphism data. Bioinformatics. 2009;25:1451–2.CrossRefPubMed Librado P, Rozas J. DnaSP v. 5: a software for comprehen-sive analysis of DNA polymorphism data. Bioinformatics. 2009;25:1451–2.CrossRefPubMed
49.
go back to reference Clement M, Posada D, Crandall KA. TCS: a computer program to estimate gene genealogies. Mol Ecol. 2000;9:1657–60.CrossRefPubMed Clement M, Posada D, Crandall KA. TCS: a computer program to estimate gene genealogies. Mol Ecol. 2000;9:1657–60.CrossRefPubMed
50.
52.
go back to reference Excoffier L, Laval G, Schneider S. An integrated software package for population genetics data analysis, Version 3.01. Computational and Molecular Population Genetics Lab. Institute of Zoology, University of Berne, Switzerland. 2006. http://www.cmpg.unibe.ch/software/arlequin3. Accessed 18 Jul 2014. Excoffier L, Laval G, Schneider S. An integrated software package for population genetics data analysis, Version 3.01. Computational and Molecular Population Genetics Lab. Institute of Zoology, University of Berne, Switzerland. 2006. http://​www.​cmpg.​unibe.​ch/​software/​arlequin3. Accessed 18 Jul 2014.
53.
go back to reference Tajima F. Statistical method for testing the neutral mutation hypothesis by DNA polymorphisms. Genetics. 1999;123:585–95. Tajima F. Statistical method for testing the neutral mutation hypothesis by DNA polymorphisms. Genetics. 1999;123:585–95.
55.
go back to reference Fu YX. Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics. 1997;147:915–25.PubMedPubMedCentral Fu YX. Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics. 1997;147:915–25.PubMedPubMedCentral
56.
go back to reference Brown A. Rapid morphological radiation and convergence among races of the butterfly Heliconius erato inferred from patterns of mitochondrial DNA evolution. Proc Natl Acad Sci USA. 1994;91:6491–5.CrossRef Brown A. Rapid morphological radiation and convergence among races of the butterfly Heliconius erato inferred from patterns of mitochondrial DNA evolution. Proc Natl Acad Sci USA. 1994;91:6491–5.CrossRef
57.
go back to reference Van Oosterhout C, Hutchinson WF, Willis DPM, Shipley P. Micro-checker: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes. 2004;4:535–8.CrossRef Van Oosterhout C, Hutchinson WF, Willis DPM, Shipley P. Micro-checker: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes. 2004;4:535–8.CrossRef
58.
go back to reference Peakall R, Smouse PE. GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research-an update. Bioinformatics. 2012;28:2537–9.CrossRefPubMedPubMedCentral Peakall R, Smouse PE. GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research-an update. Bioinformatics. 2012;28:2537–9.CrossRefPubMedPubMedCentral
60.
go back to reference Pritchard JK, Stephens M, Donnelly P. Inference of population structure using multilocus genotype data. Genetics. 2000;155:945–59.PubMedPubMedCentral Pritchard JK, Stephens M, Donnelly P. Inference of population structure using multilocus genotype data. Genetics. 2000;155:945–59.PubMedPubMedCentral
61.
go back to reference Falush D, Stephens M, Pritchard JK. Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics. 2003;164:1567–87.PubMedPubMedCentral Falush D, Stephens M, Pritchard JK. Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics. 2003;164:1567–87.PubMedPubMedCentral
62.
go back to reference Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F. GENETIX 4.05, logiciel sous Windows TM pour la génétique des populations. Laboratoire Génome, Populations, Interactions, CNRS UMR 5000, Université de Montpellier II, Montpellier (France) 1996–2004. http://kimura.univ-montp2.fr/genetix/. Accessed at 17 Jul 2015. Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F. GENETIX 4.05, logiciel sous Windows TM pour la génétique des populations. Laboratoire Génome, Populations, Interactions, CNRS UMR 5000, Université de Montpellier II, Montpellier (France) 1996–2004. http://​kimura.​univ-montp2.​fr/​genetix/​. Accessed at 17 Jul 2015.
63.
go back to reference Corander J, Marttinen P, Sirén J, Tang J. Enhanced Bayesian modelling in BAPS software for learning genetic structures of populations. BMC Bioinformatics. 2008;9:539.CrossRefPubMedPubMedCentral Corander J, Marttinen P, Sirén J, Tang J. Enhanced Bayesian modelling in BAPS software for learning genetic structures of populations. BMC Bioinformatics. 2008;9:539.CrossRefPubMedPubMedCentral
64.
go back to reference Holm S. A simple sequential rejective multiple test procedure. Scandinavian J Statistics. 1979;6:65–70. Holm S. A simple sequential rejective multiple test procedure. Scandinavian J Statistics. 1979;6:65–70.
65.
go back to reference Krzywinski J, Besansky NJ. Molecular systematics of Anopheles: from subgenera to subpopulations. Annu Rev Entomol. 2003;48:111–39.CrossRefPubMed Krzywinski J, Besansky NJ. Molecular systematics of Anopheles: from subgenera to subpopulations. Annu Rev Entomol. 2003;48:111–39.CrossRefPubMed
66.
go back to reference Mayr E. Systematics and the origin of species. New York: Columbia University Press; 1942. Mayr E. Systematics and the origin of species. New York: Columbia University Press; 1942.
67.
go back to reference Ridley M. Evolution. 3rd edition. Malden: Blackwell Publishing; 2004. Ridley M. Evolution. 3rd edition. Malden: Blackwell Publishing; 2004.
68.
go back to reference Coyne JA, Orr HA. Speciation. Sunderland: Sinauer Associates Inc; 2004. Coyne JA, Orr HA. Speciation. Sunderland: Sinauer Associates Inc; 2004.
69.
go back to reference Moreno M, Bickersmith S, Harlow W, Hildebrandt J, McKeon SN, Silva-do- Nascimento TF, et al. Phylogeography of the neotropical Anopheles triannulatus complex (Diptera: Culicidae) supports deep structure and complex patterns. Parasit Vectors. 2013;6:47.CrossRefPubMedPubMedCentral Moreno M, Bickersmith S, Harlow W, Hildebrandt J, McKeon SN, Silva-do- Nascimento TF, et al. Phylogeography of the neotropical Anopheles triannulatus complex (Diptera: Culicidae) supports deep structure and complex patterns. Parasit Vectors. 2013;6:47.CrossRefPubMedPubMedCentral
70.
go back to reference Bourke BP, Oliveira TP, Suesdek L, Bergo ES, Sallum MAM. A multi-locus approach to barcoding in the Anopheles strodei subgroup (Diptera: Culicidae). Parasit Vectors. 2013;6:111.CrossRefPubMedPubMedCentral Bourke BP, Oliveira TP, Suesdek L, Bergo ES, Sallum MAM. A multi-locus approach to barcoding in the Anopheles strodei subgroup (Diptera: Culicidae). Parasit Vectors. 2013;6:111.CrossRefPubMedPubMedCentral
71.
go back to reference McKeon SN, Lehr MA, Wilkerson RC, Ruiz JF, Sallum MA, Lima JB, et al. Lineage divergence detected in the malaria vector Anopheles marajoara (Diptera: Culicidae) in Amazonian Brazil. Malar J. 2010;9:271.CrossRefPubMedPubMedCentral McKeon SN, Lehr MA, Wilkerson RC, Ruiz JF, Sallum MA, Lima JB, et al. Lineage divergence detected in the malaria vector Anopheles marajoara (Diptera: Culicidae) in Amazonian Brazil. Malar J. 2010;9:271.CrossRefPubMedPubMedCentral
72.
go back to reference Scarpassa VM, Alencar RB. Molecular taxonomy of the two Leishmania vectors Lutzomyia umbratilis and Lutzomyia anduzei (Diptera: Psychodidae) from the Brazilian Amazon. Parasit Vectors. 2013;6:258.CrossRefPubMedPubMedCentral Scarpassa VM, Alencar RB. Molecular taxonomy of the two Leishmania vectors Lutzomyia umbratilis and Lutzomyia anduzei (Diptera: Psychodidae) from the Brazilian Amazon. Parasit Vectors. 2013;6:258.CrossRefPubMedPubMedCentral
73.
go back to reference Funk W, Caldwell J, Peden C, Padial JM, De la Riva I, Cannatella DC. Tests of biogeographic hypotheses for diversification in the Amazon forest frog, Physalaemus petersi. Mol Phyl Evol. 2007;44:825–37.CrossRef Funk W, Caldwell J, Peden C, Padial JM, De la Riva I, Cannatella DC. Tests of biogeographic hypotheses for diversification in the Amazon forest frog, Physalaemus petersi. Mol Phyl Evol. 2007;44:825–37.CrossRef
74.
go back to reference Hayes F, Sewlal J. The Amazon River as a dispersal barrier to passerine birds: effects of river width, habitat and taxonomy. J Biogeography. 2004;31:1809–18.CrossRef Hayes F, Sewlal J. The Amazon River as a dispersal barrier to passerine birds: effects of river width, habitat and taxonomy. J Biogeography. 2004;31:1809–18.CrossRef
76.
go back to reference Pedro PM, Sallum MAM. Spatial expansion and population structure of the neotropical malaria vector, Anopheles darlingi (Diptera: Culicidae). Biol J Linnean Soc. 2009;97:854–66.CrossRef Pedro PM, Sallum MAM. Spatial expansion and population structure of the neotropical malaria vector, Anopheles darlingi (Diptera: Culicidae). Biol J Linnean Soc. 2009;97:854–66.CrossRef
77.
go back to reference Conn JE, Vineis J, Bollback J, Onyabe DY. 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 J, Onyabe DY. 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
Metadata
Title
Evidence of new species for malaria vector Anopheles nuneztovari sensu lato in the Brazilian Amazon region
Authors
Vera Margarete Scarpassa
Antonio Saulo Cunha-Machado
José Ferreira Saraiva
Publication date
01-12-2016
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2016
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/s12936-016-1217-6

Other articles of this Issue 1/2016

Malaria Journal 1/2016 Go to the issue