Taxonomic status of the malaria vector Anopheles (Nyssorhynchus) triannulatus (Neiva & Pinto) in Cáceres, Antioquia, Colombia

Authors

Keywords:

Anopheles triannulatus, barcoding, COI, Colombia.

Abstract

Introduction: Anopheles triannulatus is a species complex of public health importance in South America, by its role as a secondary malaria vector in Brazil, Perú and Venezuela.

Objective: To elucidate the taxonomic status of An. triannulatus in Caceres, Antioquia, Colombia, with specimens collected in the village Los Azules.

Methods: The specimens were identified by morphological keys and DNA barcoding (COI, mtDNA). A Neighbor-Joining tree using Kimura-2-parameter (NJ-K2P) model was generated.

Results: A total of 251 mosquitoes of the genus Anopheles were collected, of which 233 were An. triannulatus with five haplotypes (H1, H2, H3, H4 and H5).

Conclusion: Using the DNA barcoding region, we confirmed that An. triannulatus is a species complex in Colombia, with at least three lineages. However, future studies of adult morphology, immature stages, ecology and the use of further molecular markers are necessary to determine the exact number of species present in this mosquito complex of public health importance.

Downloads

Download data is not yet available.

Author Biographies

Wilber Adolfo Gómez-Vargas, Universidad CES, Instituto Colombiano de Medicina Tropical (ICMT-CES). Colombia.

Docente e investigador

Juan Fernando Ríos-Cadavid, Universidad CES, Instituto Colombiano de Medicina Tropical (ICMT-CES), Secretaría Seccional de Salud y Protección Social de Antioquia.

Investigador

John Freddy Ruiz-López, Universidad de Antioquia, Programa de Estudio y Control de Enfermedades Tropicales. Colombia.

Investigador

References

World Health Organization. World Malaria Report 2019. Geneva; 2019 [acceso 03/08/2020]. Disponible en: https://apps.who.int/iris/bitstream/handle/10665/330011/9789241565721-eng.pdf

Sinka ME, Bangs MJ, Manguin S, Rubio-Palis Y, Chareonviriyaphap T, Coetzee M, et al. A global map of dominant malaria vectors. Parasit Vectors. 2012;5:69. DOI: https://dx.doi.org/10.1186/1756-3305-5–69

Montoya-Lerma J, Solarte YA, Giraldo-Calderón GI, Quiñones ML, Ruiz-López F, Wilkerson RC, et al. Malaria vector species in Colombia: A review. Mem Inst Oswaldo Cruz. 2011;106(S1):223-38. DOI: https://dx.doi.org/10.1590/S0074-02762011

Harrison BA, Ruiz-Lopez F, Falero GC, Savage HM, Pecor JE, Wilkerson RC. 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. 2012;3218:1-17.

Ruiz-Lopez F, Wilkerson RC, Ponsonby DJ, Herrera M, Sallum MAM, Velez ID, et al. Systematics of the Oswaldoi Complex (Anopheles, Nyssorhynchus) in South America. Parasit Vectors. 2013;6:324. DOI: https://dx.doi.org/10.1186/1756-3305-6–324

Hribar J. Geographic Variation of Male Genitalia of Anopheles nuneztovari (Diptera:Culicidae). Mosq Syst. 1994;26(3):132-44.

Fritz GN, Conn J, Cockburn A, Seawright J. Sequence analysis of the ribosomal DNA internal transcribed spacer2 from populations of Anopheles nuneztovari (Diptera: Culicidae). Mol Biol Evol. 1994;11(3):406-16.

Coetzee M, Estrada-Franco JG, Wunderlich CA, Hunt RH. Cytogenetic evidence for a species complex within Anopheles pseudopunctipennis Theobald (Diptera: Culicidae). Am J Trop Med Hyg. 1999;60(4):649-53. DOI: https://dx.doi.org/10.4269/ajtmh.1999.60

Urrea-Aguirre PA, Correa-Ochoa MM, Naranjo-Díaz NJ. Variabilidad genética de Anopheles punctimacula s.l. en dos localidades de la zona endémica para la malaria: El Bajo Cauca y Alto Sinú. Hechos microbiológicos. 2014;5(2):51-62.

Rodríguez-Zabala J, González R, Correa MM, Gómez GF. Análisis morfométrico de dos poblaciones de Anopheles (Anopheles) calderoni (Diptera: Culicidae) del suroccidente colombiano. Rev Mex Biodivers. 2016;87(3):966-71. DOI: https://dx.doi.org/10.1016/j.rmb.2016.06

López-Rubio A, Suaza-Vasco J, Marcet PL, Ruíz-Molina N, Cáceres L, Porter C, et al. Use of DNA barcoding to distinguish the malaria vector Anopheles neivai in Colombia. Zootaxa. 2016;4175(4):377-89. DOI: https://dx.doi.org/10.11646/zootaxa.4175

Silva Do Nascimento TF, Lourenco-de-Oliveira R. Anopheles halophylus, a new species of the subgenus Nyssorhynchus (Diptera: Culicidae) from Brazil. Mem Inst Oswaldo Cruz. 2002;97(6):801-11. DOI: https://dx.doi.org/S0074-0276200200060001

Aramburú-Guarda J, Ramal-Asayag C, Witzig R. Malaria reemergence in the Peruvian Amazon Region. Emerg Infect Dis. 1999;5(2):209-15. DOI: https://dx.doi.org/10.3201/eid0502.990204

Benarroch E. Studies of malaria in Venezuela. Am J Hyg. 1931;14:690-3.

Silva-do-Nascimento TF, Lourenço-de-Oliveira R. Diverse population dynamics of three Anopheles species belonging to the Triannulatus Complex (Diptera: Culicidae). Mem Inst Oswaldo Cruz. 2007;102(8):975-82. DOI: https://dx.doi.org/10.1590/S0074-02762007

Rosa-Freitas MG, Tsouris P, Peterson AT, Honório NA, De Barros FSM, De Aguiar DB, et al. An ecoregional classification for the state of Roraima, Brazil. The importance of landscape in malaria biology. Mem Inst Oswaldo Cruz. 2007;102(3):349-57. DOI: https://dx.doi.org/10.1590/S0074-02762007

Galardo AKR, Arruda M, D’Almeida Couto AAR, Wirtz R, Lounibos LP, Zimmerman RH. Malaria vector incrimination in three rural riverine villages in the Brazilian amazon. Am J Trop Med Hyg. 2007;76(3):461-69. DOI: https://dx.doi.org/10.4269/ajtmh.2007.76

Rosero DA, Jaramillo LM, Gutiérrez LA, Conn JE, Correa MM. Genetic diversity of Anopheles triannulatus s.l. (Diptera: Culicidae) from Northwestern and Southeastern Colombia. Am J Trop Med Hyg. 2012;87(5):910-20. DOI: https://dx.doi.org/10.4269/ajtmh.2012.12-0.

Montoya C, Bascuñán P, Rodríguez-Zabala J, Correa MM. Abundance, composition and natural infection of Anopheles mosquitoes from two malaria-endemic regions of Colombia. Biomédica. 2017;37(S2):98-105. DOI: https://dx.doi.org/10.7705/biomedica.v34i2

González R, Carrejo NS. Introducción al estudio taxonómico de Anopheles de Colombia. Claves y notas de distribución. 2nd ed. Cali, Colombia: Editorial Universidad del Valle; 2009.

Faran ME. Mosquitoes studies (Diptera, Culicidae) XXXIV. A revision of the Albimanus Section of the subgenus Nyssorhynchus of Anopheles. 1980;15(7):213.

Faran M, Linthicum K. A handbook of the Amazonian species of Anopheles (Nyssorhynchus) (Diptera: Culicidae). Mosq Syst. 1981;13(1):1-81.

Secretaría Seccional de Salud y Protección Social de Antioquia. Eventos de interés en salud pública por subregiones y municipios. Antioquia 2007 – 2018. Medellín; 2019 [acceso 09/08/2020]. Disponible en: http://dssa.gov.co/index.php/estadisticas/eventos-en-salud-publica/item/71-eventos-de-interes-en-salud-publica-por-subregiones-y-municipios-antioquia-2007-2016

Ruiz F, Linton YM, 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(7):899-903. DOI: https://dx.doi.org/10.1590/S0074-02762010

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(5):294-9. DOI: https://dx.doi.org/10.1071/ZO9660275

Kimura M. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol. 1980;16(1330):111-20.

Ahumada ML, Orjuela LI, Pareja PX, Conde M, Cabarcas DM, Cubillos EFG, et al. Spatial distributions of Anopheles species in relation to malaria incidence at 70 localities in the highly endemic Northwest and South Pacific coast regions of Colombia. Malar J. 2016;15:407. DOI: https://dx.doi.org/10.1186/s12936-016-1421–4

González MA. Códigos de barras de ADN - tras las huellas de las especies. Hipótesis Apunt Científicos Uniandinos. 2012;12:51-6.

Hebert PDN, Cywinska A, Ball SL, DeWaard JR. Biological identifications through DNA barcodes. Proc R Soc B Biol Sci. 2003;270(1512):313-21. DOI: https://dx.doi.org/10.1098/rspb.2002.2218

Ruiz F, Quiñones ML, Erazo HF, Calle DA, Alzate JF, Linton YM. Molecular differentiation of Anopheles (Nyssorhynchus) benarrochi and An. (N.) oswaldoi from Southern Colombia. Memorias Inst Oswaldo Cruz. 2005;100(2):155-60.

Ruiz-Lopez 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. Parasites and Vectors. 2012;5:44. DOI: https://dx.doi.org/10.1186/1756-3305-5–44

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. DOI: https://dx.doi.org/10.1186/1756-3305-6–47 .

Atencia M, Toro-Cantillo A, Hoyos-López R. Diversidad genética y estructura poblacional de Anopheles triannulatus s.l. en Córdoba, Colombia, determinadas mediante el método de región de código de barras de ADN. Biomédica. 2018;38:117-26. DOI: https://dx.doi.org/10.7705/biomedica.v38i0

Instituto Nacional de Salud. Informe vigilancia entomológica de malaria, Colombia 2018. Bogota D.C.; 2019 [acceso 03/08/2020]. Disponible en: https://www.ins.gov.co/buscador-eventos/Informacin de laboratorio/Informe-vigilancia-entomologica-Malaria-Colombia-2018.pdf

Published

2024-10-11

How to Cite

1.
Gutiérrez-Arbbelaéz P, Gómez-Vargas WA, Ríos-Cadavid JF, Ruiz-López JF. Taxonomic status of the malaria vector Anopheles (Nyssorhynchus) triannulatus (Neiva & Pinto) in Cáceres, Antioquia, Colombia. Rev Cuba Med Tropical [Internet]. 2024 Oct. 11 [cited 2025 Feb. 21];76. Available from: https://revmedtropical.sld.cu/index.php/medtropical/article/view/958

Issue

Section

Artículos originales