Skip to main content Skip to main navigation menu Skip to site footer
Responsive image
Issue: Vol. 4175 No. 4: 17 Oct. 2016
Type: Article
Published: 2016-10-17
DOI: 10.11646/zootaxa.4175.4.7
Page range: 377–389
Abstract views: 98
PDF downloaded: 4

Use of DNA barcoding to distinguish the malaria vector Anopheles neivai in Colombia

Universidad Nacional de Colombia – Sede Medellín – Facultad de Ciencias – Escuela de Biociencias – Grupo de Investigación en Sistemática Molecular. Calle 53A 63-20, Medellín. Código Postal 050034 – Colombia.
Universidad Nacional de Colombia – Sede Medellín – Facultad de Ciencias – Escuela de Biociencias – Grupo de Investigación en Sistemática Molecular. Calle 53A 63-20, Medellín. Código Postal 050034 – Colombia.
Centers for Disease Control and Prevention (CDC). Division of Parasitic Diseases and Malaria, Entomology Branch. Atlanta, USA
Universidad Nacional de Colombia – Sede Medellín – Facultad de Ciencias – Escuela de Biociencias – Grupo de Investigación en Sistemática Molecular. Calle 53A 63-20, Medellín. Código Postal 050034 – Colombia.
Centers for Disease Control and Prevention (CDC). Division of Parasitic Diseases and Malaria, Entomology Branch. Atlanta, USA
Centers for Disease Control and Prevention (CDC). Division of Parasitic Diseases and Malaria, Entomology Branch. Atlanta, USA
Universidad Nacional de Colombia – Sede Medellín – Facultad de Ciencias – Escuela de Biociencias – Grupo de Investigación en Sistemática Molecular. Calle 53A 63-20, Medellín. Código Postal 050034 – Colombia.
Diptera DNA Barcode Malaria Kerteszia COI

Abstract

A reference 535 bp barcode sequence from a fragment of the mitochondrial gene cytochrome oxidase I (COI), acquired from specimens of An. neivai Howard, Dyar & Knab, 1913 from its type locality in Panama, was used as a tool for distinguishing this species from others in the subgenus Kerteszia. Comparisons with corresponding regions of COI between An. neivai and other species in the subgenus (An. bellator Dyar & Knab 1906, An. homunculus Komp 1937, An cruzii Dyar & Knab, 1908 and An. laneanus Corrêa & Cerqueira, 1944) produced K2P genetic distances of 8.3–12.6%, values well above those associated with intraspecific variation. In contrast, genetic distances among 55 specimens from five municipalities in the Colombian Pacific coastal state of Chocó were all within the range of 0–2.5%, with an optimized barcode threshold of 1.3%, the limit for unambiguous differentiation of An. neivai. Among specimens from the Chocó region, 18 haplotypes were detected, two of which were widely distributed over the municipalities sampled. The barcode sequence permits discrimination of An. neivai from sympatric species and indicates genetic variability within the species; aspects key to malaria surveillance and control as well as defining geographic distribution and dispersion patterns.

 

References

  1. Altschul, S.F., Gish, W., Miller, W., Myers, E.W. & Lipman, D.J. (1990) Basic local alignment search tool. Journal of Molecular Biology 215 (3), 403–10.
    http://dx.doi.org/10.1016/s0022-2836(05)80360-2

    Applied Biosystems. (2011) Sequence Scanner Software v1.0 Sequence Trace Viewer and Editor. Available from: https://www3.appliedbiosystems.com/cms/groups/mcb_marketing/documents/generaldocuments/cms_042188.pdf (accessed 1 July 2015)

    Arregui, G., Enríquez, S., Benítez-Ortiz, W. & Navarro, J.-C. (2015) Molecular Taxonomy of Anopheles from Ecuador, using mitochondrial DNA (Cytochrome c Oxidase I) and Maximum Parsimony optimization. Boletín de Malariología y Salud Ambiental, 55 (2), 128–136.

    Astaiza, R., Murillo, C. & Fajardo, P. (1988) Biología de Anopheles (Kerteszia) neivai H., D. & K., 1913 (Diptera: Culicidae) en la costa pacífica de Colombia. II Fluctuación de la población adulta. Revista de Saúde Pública, 22 (2), 101–108.
    http://dx.doi.org/10.1590/S0034-89101988000200005

    Brown, S.D.J., Collins, R.A., Boyer, S., Lefort, M.-C., Malumbres-Olarte, J., Vink, C.J. & Cruickshank, R.H. (2012) Spider: An R package for the analysis of species identity and evolution, with particular reference to DNA barcoding. Molecular Ecology Resources, 12, 562–565.
    http://dx.doi.org/10.1111/j.1755-0998.2011.03108.x

    Chaparro, P. & Padilla, J. (2012) Mortalidad por paludismo en Colombia, 1979-2008. Biomédica, 32 (Supplement 1), 95–105.

    Clement, M., Posada, D. & Crandall, K. (2000) TCS: a computer program to estimate gene genealogies. Molecular Ecology, 9 (10), 1657–1659.
    http://dx.doi.org/10.1046/j.1365-294x.2000.01020.x

    Collins, F., Mendez, M., Rasmussen, M., Mehaffey, P., Besansky, N. & Finnerty, V. (1987) A ribosomal RNA gene probe differentiates member species of the Anopheles gambiae Complex. The American Journal of Tropical Medicine and Hygiene, 37 (1), 37–41.

    Collins, F.H. & Paskewitz, S.M. (1996) A review of the use of ribosomal DNA (rDNA) to differentiate among cryptic Anopheles species. Insect Molecular Biology, 5 (1), 1–9.
    http://dx.doi.org/10.1111/j.1365-2583.1996.tb00034.x

    Cywinska, A., Hunter, F.F. & Hebert, P.D.N. (2006) Identifying Canadian mosquito species through DNA barcodes. Medical and Veterinary Entomology, 20 (4), 413–424.
    http://dx.doi.org/10.1111/j.1365-2915.2006.00653.x

    Dantur Juri, M.J., Moreno, M., Prado Izaguirre, M.J., Navarro, J.-C., Zaidenberg, M.O., Almirón, W.R., Claps, G.L. & Conn, J.E. (2014) Demographic history and population structure of Anopheles pseudopunctipennis in Argentina based on the mitochondrial COI gene. Parasites & Vectors, 7 (1), 423.
    http://dx.doi.org/10.1186/1756-3305-7-423

    Edgar, R.C. (2004) MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32 (5), 1792–1797.
    http://dx.doi.org/10.1093/nar/gkh340

    Escovar, J., González, R. & Quiñones, M.L. (2013) Anthropophilic biting behaviour of Anopheles (Kerteszia) neivai Howard, Dyar & Knab associated with Fishermen’s activities in a malaria-endemic area in the Colombian Pacific. Memórias do Instituto Oswaldo Cruz, 108 (8), 1057–1064.
    http://dx.doi.org/10.1590/0074-0276130256

    Escovar, J., González, R., Quiñones, M.L., Wilkerson, R.C., Harrison, B. & Ruiz-lopez, F. (2012) Morphological and molecular identification of Anopheles (Kerteszia) present in two endemic foci of malaria in Colombia. Journal of the American Mosquito Control Association, 28 (2), 106–107.

    Folmer, O., Black, M., Hoeh, W., Lutz, R. & Vrijenhoek, R. (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294–299.

    Foster, P.G., Bergo, E.S., Bourke, B.P., Oliveira, T.M.P., Nagaki, S.S., Sant’Ana, D.C. & Sallum, M.A.M. (2013) Phylogenetic analysis and DNA-based species confirmation in Anopheles (Nyssorhynchus). Plos ONE, 8 (2), e54063.
    http://dx.doi.org/10.1371/journal.pone.0054063

    Gómez, G., Jaramillo, L. & Correa, M.M. (2013) Wing geometric morphometrics and molecular assessment of members in the Albitarsis Complex from Colombia. Molecular Ecology Resources, 2, 1082–1092.
    http://dx.doi.org/10.1111/1755-0998.12126

    González, R., Carrejo, N., Wilkerson, R.C., Alarcon, J., Alarcon-Ormasa, J., Ruiz, F., Bhatia, R., Loaiza, J. & Linton, Y.M. (2010) Confirmation of Anopheles (Anopheles) calderoni Wilkerson, 1991 (Diptera: Culicidae) in Colombia and Ecuador through molecular and morphological correlation with topotypic material. Memórias do Instituto Oswaldo Cruz, 105 (8), 1001–1009.
    http://dx.doi.org/10.1590/S0074-02762010000800009

    González, R. & Carrejo, N. (2009) Introducción al estudio taxonómico de Anopheles de Colombia: Claves y notas de distribución. Programa Editorial Universidad del Valle, Cali. 260 pp.

    Gutiérrez, L., Orrego, L.M., Gómez, G.F., López, A., Luckhart, S., Conn, J.E. & Correa, M.M. (2010) A new mtDNA COI gene lineage closely related to Anopheles janconnae of the Albitarsis complex in the Caribbean region of Colombia. Memórias do Instituto Oswaldo Cruz, 105 (8), 1019–1025.
    http://dx.doi.org/10.1590/S0074-02762010000800011

    Gutierrez, L.A., Gomez, G.F., Gonzalez, J.J., Castro, M.I., Luckhart, S., Conn, J.E. & Correa, M.M. (2010) Microgeographic Genetic Variation of the Malaria Vector Anopheles darlingi Root (Diptera: Culicidae) from Cordoba and Antioquia, Colombia. American Journal of Tropical Medicine and Hygiene, 83 (1), 38–47.
    http://dx.doi.org/10.4269/ajtmh.2010.09-0381

    Gutiérrez, L.A., Naranjo, N., Jaramillo, L.M., Muskus, C., Luckhart, S., Conn, J.E. & Correa, M.M. (2008) Natural infectivity of Anopheles species from the Pacific and Atlantic Regions of Colombia. Acta Tropica, 107, 99–105.
    http://dx.doi.org/10.1016/j.actatropica.2008.04.019

    Hajibabaei, M., Janzen, D.H., Burns, J.M., Hallwachs, W. & Hebert, P.D.N. (2006) DNA barcodes distinguish species of tropical Lepidoptera. Proceedings of the National Academy of Sciences of the United States of America, 103, 968–971.
    http://dx.doi.org/10.1073/pnas.0510466103

    Hall, T.A. (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series, 41, 95–98.

    Harbach, R.E. (2013) The Phylogeny and classification of Anopheles. In: Manguin, S. (Ed), Anopheles mosquitoes - New insights into malaria vectors. InTech, Rijeka, pp. 55.

    Harrison, B.A., Ruiz-Lopez, F., Falero, G.C., Savage, H.M., Pecor, J.E. & Wilkerson, R.C. (2012) Anopheles (Kerteszia) lepidotus (Diptera: Culicidae), not the malaria vector we thought it was: Revised male and female morphology; larva, pupa,and male genitalia characters; and molecular verification. Zootaxa, 3218, 1–17.

    Hebert, P.D.N., Cywinska, A., Ball, S.L., Jeremy, R. & DeWaard, J.R. (2003) Biological identifications through DNA barcodes. Proceedings of the Royal Society B Biological Sciences, 270 (1512), 313–321.
    http://dx.doi.org/10.1098/rspb.2002.2218

    Hebert, P.D.N., Stoeckle, M.Y., Zemlak, T.S. & Francis, C.M. (2004) Identification of Birds through DNA Barcodes. PLoS Biology, 2 (10), 1657–1663.
    http://dx.doi.org/10.1371/journal.pbio.0020312

    Hlaing, T., Tun-Lin, W., Somboon, P., Socheat, D., Setha, T., Min, S., Chang, M.S. & Walton, C. (2009) Mitochondrial pseudogenes in the nuclear genome of Aedes aegypti mosquitoes: implications for past and future population genetic studies. BMC Genetics, 10, 11.
    http://dx.doi.org/10.1186/1471-2156-10-11

    INS (Instituto Nacional de Salud). (2015) Boletín Epidemiológico Semanal. Estadísticas del sistema de vigilancia en salud pública- SIVIGILA. Available from: http://www.ins.gov.co/boletin-epidemiologico/Boletn Epidemiolgico/2015 Boletin epidemiologico Semana 52.pdf (accessed 10 January 2016)

    Jaramillo, L.M., Gutiérrez, L.A., Luckhart, S., Conn, J.E. & Correa, M.M. (2011) Molecular evidence for a single taxon, Anopheles nuneztovari s.l., from two endemic malaria regions in Colombia. Memórias do Instituto Oswaldo Cruz, 106 (8), 1017–23.
    http://dx.doi.org/10.1590/S0074-02762011000800020

    Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M., Sturrock, S., Buxton, S., Cooper, A., Markowitz, S., Duran, C., Thierer, T., Ashton, B., Meintjes, P. & Drummond, A. (2012) Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics, 28 (12) 1647–1649.
    http://dx.doi.org/10.1093/bioinformatics/bts199

    Kimura, M. (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution, 16 (2), 111–120.
    http://dx.doi.org/10.1007/BF01731581

    Kumar, N.P., Krishnamoorthy, N., Sahu, S.S., Rajavel, A.R., Sabesan, S. & Jambulingam, P. (2013) DNA Barcodes indicate members of the Anopheles fluviatilis (Diptera: Culicidae) species complex to be conspecific in India. Molecular Ecology Resources, 13 (3), 354–361.
    http://dx.doi.org/10.1111/1755-0998.12076

    Kumar, N.P., Rajavel, A.R., Natarajan, R. & Jambulingam, P. (2007) DNA barcodes can distinguish species of Indian mosquitoes (Diptera: Culicidae). Journal of Medical Entomology, 44 (1), 1–7.
    http://dx.doi.org/10.1603/0022-2585(2007)44[1:DBCDSO]2.0.CO;2

    Lehr, M.A., Kilpatrick, C.W., Wilkerson, R.C. & Conn, J.E. (2005) Cryptic species in the Anopheles (Nyssorhynchus) albitarsis (Diptera: Culicidae) complex: incongruence between random amplified polymorphic DNA-polymerase chain reaction identification and analysis of mitochondrial DNA COI gene sequences. Annals of the Entomological Society of America, 98 (6), 908–917.
    http://dx.doi.org/10.1603/0013-8746(2005)098[0908:CSITAN]2.0.CO;2

    Librado, P. & Rozas, J. (2009) DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics, 25 (11), 1451–1452.
    http://dx.doi.org/10.1093/bioinformatics/btp187

    Linton, Y.-M.M. (2009) Mosquito Barcoding Initiative. The first barcode release paper. Third International Barcode of Life Conference. Available from: https://vimeo.com/8996184 (accessed 11 September 2015)

    Lorenz, C., Patané, J.S.L. & Suesdek, L. (2015) Morphogenetic characterisation, date of divergence, and evolutionary relationships of malaria vectors Anopheles cruzii and Anopheles homunculus. Infection, Genetics and Evolution, 35, 144–152.
    http://dx.doi.org/10.1016/j.meegid.2015.08.011

    Mirabello, L. & Conn, J.E. (2006) Molecular population genetics of the malaria vector Anopheles darlingi in Central and South America. Heredity, 96, 1–11.
    http://dx.doi.org/10.1038/sj.hdy.6800805

    Montoya-Lerma, J., Murillo, C. & Solarte, Y. (1987) Variación fenotípica de Anopheles (K) neivai (Diptera: Culicidae) en la costa Pacífica de Colombia. Colombia Médica, 8 (1), 25–27.

    Murillo, C., Astaiza, R. & Fajardo, P. (1988) Biología de Anopheles (Kerteszia) neivai h., d. & k., 1913 (Diptera: Culicidae) en la costa pacífica de Colombia. I fluctuación de la población larval y características de sus criaderos. Revista de Saúde Pública, 22 (2), 94–100.
    http://dx.doi.org/10.1590/S0034-89101988000200004

    Oliveira, T.M.P., Foster, P.G., Bergo, E.S., Nagaki, S.S., Sanabani, S.S., Marinotti, O., Marinotti, P.N. & Sallum, M.A.M. (2016) Mitochondrial genomes of Anopheles (Kerteszia) (Diptera: Culicidae) from the Atlantic Forest, Brazil. Journal of Medical Entomology, 1–8. [published online]

    Park, D.-S., Suh, S.-J., Oh, H.-W. & Hebert, P.D.N. (2010) Recovery of the mitochondrial COI barcode region in diverse Hexapoda through tRNA-based primers. BMC Genomics, 11, 423.
    http://dx.doi.org/10.1186/1471-2164-11-423

    Paradis, E. (2012) Analysis of Phylogenetics and Evolution with R. Springer, New York, 386 pp.

    Pecor, J. & Gaffigan, T. (1997) Collecting, rearing, preserving, mounting and shipping techniques for mosquitoes. Available from: http://wrbu.si.edu/Techniques.html (accessed 12 August 2015)

    R Developement Core Team (2015) R: A Language and Environment for Statistical Computing. Available from: http://www.r-project.org (accessed 5 October 2015)

    Ratnasingham, S. & Hebert, P.D.N. (2007) BOLD: The Barcode of Life Data System (http://www.barcodinglife.org). Molecular Ecology Notes, 7 (3), 355–364.

    Rona, L.D.P., Carvalho-Pinto, C.J. de & Peixoto, A. (2012) Speciation in brazilian Atlantic Forest mosquitoes: A mini-review of the Anopheles cruzii species complex. In: Fusté, C. (Ed.), Studies in population genetics. INTECH Open Access Publisher, Rijeka, pp. 105–116.
    http://dx.doi.org/10.5772/35693

    Rona, L.D.P., Carvalho-Pinto, C.J., Gentile, C., Grisard, E.C. & Peixoto, A. (2009) Assessing the molecular divergence between Anopheles (Kerteszia) cruzii populations from Brazil using the timeless gene: further evidence of a species complex. Malaria Journal, 8, 60.
    http://dx.doi.org/10.1186%2F1475-2875-8-60

    Rosa-Freitas, M.G., Lourenço-de-Oliveira, R., Carvalho-Pinto, C.J. de, Flores-Mendoza, C. & Silva-do-Nascimento, T.F. (1998) Anopheline species complexes in Brazil. Current knowledge of those related to malaria transmission. Memórias do Instituto Oswaldo Cruz, 93 (5), 651–655.
    http://dx.doi.org/10.1590/S0074-02761998000500016

    Rosero, D.A., Jaramillo, L.M., Gutiérrez, L. a., Conn, J.E. & Correa, M.M. (2012) Genetic diversity of Anopheles triannulatus s.l. (Diptera: Culicidae) from Northwestern and Southeastern Colombia. American Journal of Tropical Medicine and Hygiene, 87 (5), 910–920.
    http://dx.doi.org/10.4269/ajtmh.2012.12-0285

    Rozo-Lopez, P. & Mengual, X. (2015) Mosquito species (Diptera, Culicidae) in three ecosystems from the Colombian Andes: identification through DNA barcoding and adult morphology. ZooKeys, 513, 39–64.
    http://dx.doi.org/10.3897/zookeys.513.9561

    Rubio-Palis, Y. (1991) Vector biology and malaria transmission in western Venezuela. University of London, London, 261 pp.

    Ruiz-Lopez, F., Linton, Y.M., Ponsonby, D.J., Conn, J.E., Herrera, M., Quiñones, M.L., Vélez, I.D. & Wilkerson, R.C. (2010) Molecular comparison of topotypic specimens confirms Anopheles (Nyssorhynchus) dunhami Causey (Diptera: Culicidae) in the Colombian Amazon. Memórias do Instituto Oswaldo Cruz, 105 (7), 899–903.

    Ruiz-Lopez, F., Wilkerson, R.C., Conn, J.E., McKeon, S.N., Levin, D.M., Quiñones, M.L., Póvoa, M.M. & Linton, Y.-M.M. (2012) DNA barcoding reveals both known and novel taxa in the Albitarsis Group (Anopheles: Nyssorhynchus) of Neotropical malaria vectors. Parasites & Vectors, 5 (1), 44.
    http://dx.doi.org/10.1186/1756-3305-5-44

    SEM (Servicio de Erradicación de la Malaria. Ministerio de Salud Pública. República de Colombia) (1957) Plan de erradicación de la Malaria en Colombia. Vol. II. Ministerio. de Salud. Pública. Bogotá, 635 pp.

    Silva-do-Nascimento, T.F., Pitaluga, L.D.R., Peixoto, A.A. & Lourenço-de-Oliveira, R. (2011) Molecular divergence in the timeless and cpr genes among three sympatric cryptic species of the Anopheles triannulatus complex. Memórias do Instituto Oswaldo Cruz, 106 (Supplement 1), 218–22.
    http://dx.doi.org/10.1590/S0074-02762011000900027

    Sinka, M.E., Rubio-Palis, Y., Manguin, S., Patil, A.P., Temperley, W.H., Gething, P.W., Van Boeckel, T., Kabaria, C.W., Harbach, R.E. & Hay, S.I. (2010) The dominant Anopheles vectors of human malaria in the Americas: occurrence data, distribution maps and bionomic précis. Parasites & Vectors, 3 (4), 72.
    http://dx.doi.org/10.1186/1756-3305-3-72

    Stone, A., Knight, K.L. & Starcke, H. (1959) A Synoptic Catalog of the mosquitoes of the World (Diptera: Culicidae). The Thomas Say Foundation, Entomological Society of America, Washington D.C., 358 pp.

    Tamura, K., Stecher, G., Peterson, D., Filipski, A. & Kumar, S. (2013) MEGA6: Molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution, 30 (12), 2725–2729.
    http://dx.doi.org/10.1093/molbev/mst197

    Uribe, S.I., Lehmann, T., Rowton, E.D., Vélez B., I.D. & Porter, C.H. (2001) Speciation and population structure in the morphospecies Lutzomyia longipalpis (Lutz & Neiva) as derived from the mitochondrial ND4 gene. Molecular Phylogenetics and Evolution, 18 (1), 84–93.
    http://dx.doi.org/10.1006/mpev.2000.0863

    Uribe, S.I., Porter, C.H. & Vélez, I.D. (1998) Amplificación y obtención de secuencias de rRNA mitocondrial en Lutzomyia spp (Diptera: Psychodidae) vectores de Leishmaniosis. Revista Colombiana de Entomología, 23 (3–4), 177–185.

    Zavortink, T.J. (1973) Mosquito studies (Diptera, Culicidae) XXIX. A review of the subgenus Kerteszia of Anopheles. Contributions of the American Entomological Institute, 9 (3), 1–54.