1921
Volume 85, Issue 5
  • ISSN: 0002-9637
  • E-ISSN: 1476-1645

Abstract

Abstract.

Cryptic species and lineages characterize s.l. Gabaldón, an important malaria vector in South America. We investigated the phylogeographic structure across the range of this species with cytochrome oxidase subunit I () mitochondrial DNA sequences to estimate the number of clades and levels of divergence. Bayesian and maximum-likelihood phylogenetic analyses detected four groups distributed in two major monophyletic clades (I and II). Samples from the Amazon Basin were clustered in clade I, as were subclades II-A and II-B, whereas those from Bolivia/Colombia/Venezuela were restricted to one basal subclade (II-C). These data, together with a statistical parsimony network, confirm results of previous studies that is a species complex consisting of at least two cryptic taxa, one occurring in Colombia and Venezuela and the another occurring in the Amazon Basin. These data also suggest that additional incipient species may exist in the Amazon Basin. Divergence time and expansion tests suggested that these groups separated and expanded in the Pleistocene Epoch. In addition, the sequences clearly separated s.l. from the closely related species Causey, and three new records are reported for in Amazonian Brazil. These findings are relevant for vector control programs in areas where both species occur. Our analyses support dynamic geologic and landscape changes in northern South America, and infer particularly active divergence during the Pleistocene Epoch for New World anophelines.

Loading

Article metrics loading...

/content/journals/10.4269/ajtmh.2011.11-0150
2011-11-01
2017-09-26
Loading full text...

Full text loading...

/deliver/fulltext/14761645/85/5/857.html?itemId=/content/journals/10.4269/ajtmh.2011.11-0150&mimeType=html&fmt=ahah

References

  1. Faran ME, , 1980. Mosquito studies (Diptera, Culicidae). XXXIV. A revision of the Albimanus section of the subgenus Nyssorhynchus of Anopheles . Contrib Am Entomol Inst 15: 1215.
  2. Elliott R, , 1972. The influence of vector behavior on malaria transmission. Am J Trop Med Hyg 21: 755763.
  3. Gabaldón A, , 1981. Anopheles nuneztovari: importante vector y agente de malaria refractaria en Venezuela. Bol Dir Malariol Saneam Amb XXI: 2838.
  4. Gutiérrez LA, González JJ, Gomes GF, Castro MI, Rosero DA, Luckhart S, Conn JE, Correa MM, , 2009. Species composition and natural infectivity of anthropophilic Anopheles (Diptera: Culicidae) in the states of Córdoba and Antioquia, northwestern Colombia. Mem Inst Oswaldo Cruz 104: 11171124.
  5. Arruda M, Carvalho MB, Nussenzweig RS, Maracic M, Ferreira AW, Cochrane AH, , 1986. 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 35: 873881.
  6. Hayes J, Calderon G, Falcon RI, Zambrand V, , 1987. Newly incriminated anopheline vector of human malaria parasites in Junin Department, Peru. J Am Mosq Control Assoc 3: 418422.
  7. Tadei WP, Dutary-Thatcher B, Santos JM, Scarpassa VM, Rodrigues IB, Rafael MS, , 1998. Ecologic observations on anopheline vectors of malaria in the Brazilian Amazon. Am J Trop Med Hyg 59: 325335.
  8. Póvoa MM, Wirtz RA, Lacerda RN, Miles MA, Warhurst D, , 2001. Malaria vectors in the municipality of Serra do Navio, State of Amapá, Amazon Region, Brazil. Mem Inst Oswaldo Cruz 96: 179184.[Crossref]
  9. Galardo AC, Arruda M, Couto ARA, Wirtz R, Lounibos LP, Zimmerman RH, , 2007. Malaria vector incrimination in three rural riverine villages in the Brazilian Amazon. Am J Trop Med Hyg 76: 461469.
  10. Tadei WP, Mascarenhas BM, Podestá MG, , 1983. Biologia de Anofelinos Amazônicos. VIII. Conhecimentos sobre a distribuição de espécies de Anopheles na região de Tucuruí-Marabá (Pará). Acta Amazon 13: 103140.[Crossref]
  11. Marrelli MT, Floeter-Winter LM, Malafronte RS, Tadei WP, Lourenço-de-Oliveira R, Flores-Mendonza C, Marinotti O, , 2005. Amazonian malaria vector anopheline relationships interpreted from ITS2 rDNA sequences. Med Vet Entomol 19: 208218.[Crossref]
  12. Krzywinski J, Li C, Morris M, Conn JE, Lima JB, Póvoa MM, Wilkerson RC, , 2011. Analysis of the evolutionary forces shaping mitochondrial genomes of a neotropical malaria vector complex. Mol Phyl Evol 58: 469477.[Crossref]
  13. Van Bortel W, Trung H, Sochantha T, Keokenchan K, Roelants P, Backeljau T, Coosemans M, , 2004. Ecoethological heterogeneity of the members of the Anopheles minimus complex (Diptera: Culicidae) in southeast Asia and its consequences for vector control. J Med Entomol 41: 366374.[Crossref]
  14. Lounibos LP, Conn JE, , 2000. Malaria vector heterogeneity in South America. Am Entomol 46: 238249.[Crossref]
  15. Wallace AR, , 1853. A Narrative of Travel on the Amazon and Rio Negro. London: Reeve and Co.
  16. Harback RE, , 2004. The classification of genus Anopheles (Diptera: Culicidae): a working hypothesis of phylogenetic relationships. Bull Entomol Res 94: 537553.
  17. Silva do Nascimento TF, Lourenço-de-Oliveira R, , 2002. Anopheles halophylus, a new species of the subgenus Nyssorhynchus [sic] (Diptera: Culicidae) from Brazil. Mem Inst Oswaldo Cruz 97: 801811.
  18. Calado DC, Foster PG, Bergo ES, Santos CLS, Galardo AK, Sallum MA, , 2008. 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 103: 791799.[Crossref]
  19. Kitzmiller JB, Kreutzer RD, Tallaferro E, , 1973. Chromosomal differences in populations of Anopheles nuneztovari . Bull World Health Organ 48: 435445.
  20. Conn J, Puertas YR, Seawright JA, , 1993. A new cytotype of Anopheles nuneztovari from western Venezuela and Colombia. J Am Mosq Control Assoc 9: 294301.
  21. Hribar LJ, , 1994. Geographic variation of male genitalia of Anopheles nuneztovari (Diptera: Culicidae). Mosq Syst 26: 132144.
  22. Fritz GN, Conn J, Cockburn AF, Seawright JA, , 1994. Sequence analysis of the ribosomal DNA internal transcribed spacer 2 from populations of Anopheles nuneztovari (Diptera: Culicidae). Mol Biol Evol 11: 406416.
  23. Linley JR, Lounibos LP, Conn J, Duzak D, Nishimura N, , 1996. 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 12: 275292.
  24. Scarpassa VM, Tadei WP, Suarez MF, , 1996. Allozyme differentiation among allopatric populations of Anopheles nuneztovari (Diptera: Culicidae). Braz J Genet 19: 265269.
  25. Scarpassa VM, Tadei WP, Suarez MF, , 1999. Population structure and genetic divergence in Anopheles nuneztovari (Diptera: Culicidae) from Brazil and Colombia. Am J Trop Med Hyg 60: 10101018.
  26. Conn JE, Mitchell SE, Cockburn AF, , 1998. Mitochondrial DNA analysis of the neotropical malaria vector Anopheles nuneztovari . Genome 41: 313327.[Crossref]
  27. Scarpassa VM, Geurgas S, Azeredo-Espin AM, Tadei WP, , 2000. Genetic divergence in mitochondrial DNA of Anopheles nuneztovari (Diptera: Culicidae) from Brazil and Colombia. Genet Mol Biol 23: 7178.[Crossref]
  28. Mirabello L, Conn JE, , 2008. Population analysis using the nuclear white gene detects pliocene/pleistocene lineage divergence within Anopheles nuneztovari in South America. Med Vet Entomol 22: 109119.[Crossref]
  29. Bergo ES, Souto RN, Galardo AK, Nagaki SS, Calado DC, Sallum MA, , 2007. Systematic notes on Anopheles meigen (Diptera: Culcidae) species in the state of Amapá, Brazil. Mem Inst Oswaldo Cruz 102: 373376.[Crossref]
  30. Queiroz K, , 2007. Species concepts and species delimitation. Syst Biol 56: 879886.[Crossref]
  31. Gabaldón A, , 1940. Estudios sobre anofelinos. Serie I. 1. Descripcion de Anopheles (Nyssorhynchus) nunez-tovari n. sp. y consideraciones sobre una sub-division del grupo Nyssorhynchus (Diptera: Culicidae). Publ Div Malariol 5: 37.
  32. Rozeboom LE, Gabaldón A, , 1941. A summary of the “tarsimaculatus” complex of Anopheles (Diptera: Culicidae). Am J Hyg 33: 88100.
  33. Floch H, Abonnenc E, , 1946. Sur A. nuneztovari et A. pessoai en Guyane Française table d'identification des Nyssorhynchus guyanais . Inst Pasteur de la Guyane et du Territoire de L'Inini 126: 15.
  34. Lane J, , 1953. Neotropical Culicidae. Volume. 1 São Paulo: Universidade de São Paulo.
  35. Causey OR, , 1945. Description of Anopheles (Nyssorhynchus) dunhami, a new species from the Upper Amazon Basin. J Natl Malar Soc 4: 231235.
  36. Peyton EL, , 1993. Anopheles (Nyssorhynchus) dunhami, resurrected from synonymy with Anopheles nuneztovari and validated as a senior synonym of Anopheles trinkae (Diptera: Culicidae). Mosq Syst 25: 151156.
  37. Lounibos LP, Wilkerson RC, Conn JE, Hribar LJ, Fritz GN, Danoff-Burg JA, , 1998. Morphological, molecular, and chromosomal discrimination of cryptic Anopheles (Nyssorhynchus) (Diptera: Culicidae) from South America. J Med Entomol 35: 830838.[Crossref]
  38. Trindade DB, Scarpassa VM, , 2002. 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 39: 613620.[Crossref]
  39. Ruiz F, Linton YM, Ponsonby DJ, Conn JE, Herrera M, Quinones ML, Vélez ID, Wilkerson RC, , 2010. Molecular of topotypic specimens confirms Anopheles (Nyssorhynchus) dunhami Causey (Diptera: Culicidae) in the Colombian Amazon. Mem Inst Oswaldo Cruz 105: 899903.
  40. Foley D, , 2010. A spreadsheet mapping approach for error checking and sharing collection point data. Biodiversity Inf 7: 137142.
  41. Sambrook J, Russell DW, , 2001. A Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
  42. Joy D, Conn JE, , 2001. Molecular and morphological phylogenetic analysis of an insular radiation in Pacific black flies (Simulium). Syst Biol 50: 1838.[Crossref]
  43. Clement M, Posada D, Crandall KA, , 2000. TCS: a computer program to estimate gene genealogies. Mol Ecol 9: 16571660.[Crossref]
  44. Crandall KA, Templeton AR, , 1993. Empirical tests of some predictions from coalescent theory with applications to intraspecific phylogeny reconstruction. Genetics 134: 959969.
  45. Jobb G, , 2008. Treefinder version of October 2008. Munich, Germany. Distributed by the author. Available at: www.treefinder.de.
  46. Posada D, , 2008. jModelTest: phylogenetic model averaging. Mol Biol Evol 25: 12531256.[Crossref]
  47. Ronquist F, Huelsenbeck JP, , 2003. Mr. Bayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 15721574.[Crossref]
  48. Rozas J, Sánches-DelBarrio JC, Messeguer X, Rozas R, , 2003. DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19: 24962497.[Crossref]
  49. Excoffier L, Laval G, Schneider S, , 2006. An Integrated Software Package for Population Genetics Data Analysis, Version 3.01. Computational and Molecular Population Genetics Laboratory, Institute of Zoology, University of Berne, Switzerland. Available at: http://cmpg.unibe.ch/software/arlequin3.
  50. Tajima F, , 1989. Statistical method for testing the neutral mutation hypothesis by DNA polymorphisms. Genetics 123: 585595.
  51. Fu YX, Li WH, , 1993. Statistical tests of neutrality of mutations. Genetics 133: 693709.
  52. Fu YX, , 1997. Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147: 915925.
  53. Ramos-Onsins SE, Rozas J, , 2002. Statistical properties of new neutrality tests against population growth. Mol Biol Evol 19: 20922100.[Crossref]
  54. Swofford DL, , 2003. PAUP (Phylogenetic Analysis Using Parsimony) and Others Methods, Version 4. Sunderland, MA: Sinauer Associates.
  55. Tamura K, Dudley J, Nei M, Kumar S, , 2007. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software, version 4.0. Mol Biol Evol 24: 15961599.[Crossref]
  56. Brown A, , 1994. Rapid morphological radiation and convergence among races of the butterfly Heliconius erato inferred from patterns of mitochondrial DNA evolution. Proc Natl Acad Sci USA 91: 64916495.[Crossref]
  57. Tamura K, , 1992. The rate and pattern of nucleotide substitution in Drosophila mitochondrial DNA. Mol Biol Evol 9: 814825.
  58. Hasan AU, Suguri S, Fujimoto C, Itaki RL, Harada M, Kawabata M, Bugoro H, Albino B, Tsukahara T, Hombhanje F, Masta A, , 2008. Phylogeography and dispersion pattern of Anopheles farauti senso stricto mosquitoes in Melanesia. Mol Phyl Evol 46: 792800.[Crossref]
  59. Walton C, Handley JM, TunLin W, Collins FH, Harbach RE, Baimai V, Butlin RK, , 2000. Population structure and population history of Anopheles dirus mosquitoes in southeast Asia. Mol Biol Evol 17: 962974.[Crossref]
  60. Moreno J, Rubio-Palis Y, Sánchez V, Mariany D, , 2004. Primer registro de Anopheles (Nyssorhynchus) nuneztovari Gabaldón, 1940 (Diptera: Culicidae) en el estado Bolívar, Venezuela y sus implicaciones eco-epidemiológicas. Entomotropica 19: 5558.
  61. MacKeon SN, Lehr MA, Wilkerson RC, Ruiz JF, Sallum MA, Lima JB, Póvoa MM, Conn JE, , 2010. Lineage divergence detected in the malaria vector Anopheles marajoara (Diptera: Culicidae) in Amazonian Brazil. Malar J 9: 271.[Crossref]
  62. Scarpassa VM, Conn JE, , 2006. Molecular differentiation in natural populations of Anopheles oswaldoi sensu lato (Diptera: Culicidae) from the Brazilian Amazon, using sequences of the COI gene from mitochondrial DNA. Genet Mol Res 5: 493502.
  63. Loaiza JR, Scott ME, Bermingham E, Rovira J, Conn JE, , 2010. Evidence for Pleistocene population divergence and expansion of Anopheles albimanus in southern Central America. Am J Trop Med Hyg 82: 156164.[Crossref]
  64. Onyabe DY, Conn JE, , 1999. Intragenomic heterogeneity of a ribosomal DNA spacer (ITS2) varies regionally in the neotropical malaria vector Anopheles nuneztovari (Diptera: Culicidae). Insect Mol Biol 8: 435442.[Crossref]
  65. Kambhampati S, Rai KS, , 1991. Mitochondrial DNA variation within and among populations of the mosquito Aedes albopictus . Genome 34: 288292.[Crossref]
  66. Pedro MP, Sallum MA, , 2009. Spatial expansion and population structure of the neotropical malaria vector, Anopheles darlingi (Diptera: Culicidae). Biol J Linn Soc Lond 97: 854866.[Crossref]
  67. Pedro MP, Uezu A, Sallum MA, , 2010. Concordant phylogeographies of 2 malaria vectors attest to common spatial and demographic histories. J Hered 54: 110.
  68. Roussetti DF, Mann de Toledo P, Góes AM, , 2005. New geological framework for Western Amazonia (Brazil) and implications for biogeography and evolution. Quat Res 63: 7889.[Crossref]
  69. Dick CW, Roubik DW, Gruber KF, Bermingham E, , 2004. Long-distance gene flow and cross-Andean dispersal of lowland rainforest bees (Apidae: Euglossini) revealed by comparative mitochondrial DNA phylogeography. Mol Ecol 13: 37753785.[Crossref]
  70. Mayle FE, Beerling DJ, Gosling WD, Bush MB, , 2004. Responses of Amazonian ecosystems to climatic and atmospheric carbon dioxide changes since the last glacial maximum. Philos Trans R Soc Lond B Biol Sci 359: 499514.[Crossref]
http://instance.metastore.ingenta.com/content/journals/10.4269/ajtmh.2011.11-0150
Loading
/content/journals/10.4269/ajtmh.2011.11-0150
Loading

Data & Media loading...

  • Received : 15 Mar 2011
  • Accepted : 07 Aug 2011

Most Cited This Month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error