Phylogeography of the neotropical Anopheles triannulatus complex (Diptera: Culicidae) supports deep structure and complex patterns

Parasites and Vectors

Volumn 6, Issue 1, 2013, Pages

  Moreno, Marta ^a,m   Bickersmith, Sara ^a   Harlow, Wesley ^a   Hildebrandt, Jessica ^a   McKeon, Sascha N ^a,b   Silva Do Nascimento, Teresa Fernandes ^c   Loaiza, Jose R ^d   Ruiz, Freddy ^e   Lourenço De Oliveira, Ricardo ^c   Sallum, Maria A M ^f   Bergo, Eduardo S ^g   Fritz, Gary N ^h   Wilkerson, Richard C ^e   Linton, Yvonne M ^e   Juri, Maria J Dantur ⁱ   Rangel, Yadira ^j   Póvoa, Marinete M ^k   Gutiérrez Builes, Lina A ^l   Correa, Margarita M ^l   Conn, Jan E ^a,b  

^a WADSWORTH CENTER   (United States)

^b STATE UNIVERSITY OF NEW YORK   (United States)

^c INSTITUTO OSWALDO CRUZ   (Brazil)

^d INSTITUTO DE INVESTIGACIONES CIENTÍFICAS Y SERVICIOS DE ALTA TECNOLOGÍA   (Panama)

^e WALTER REED ARMY INSTITUTE OF RESEARCH   (United States)

^f UNIVERSITY OF SÃO PAULO   (Brazil)

^g SUPERINTENDÊNCIA DE CONTROLE DE ENDEMIAS   (Brazil)

^h EASTERN ILLINOIS UNIVERSITY   (United States)

ⁱ UNIVERSIDAD NACIONAL DE TUCUMÁN   (Argentina)

^j UNIVERSIDAD CENTRAL DE VENEZUELA   (Venezuela)

^k INSTITUTO EVANDRO CHAGAS   (Brazil)

^l UNIVERSIDAD DE ANTIOQUIA   (Colombia)

^m UNIVERSITY OF CALIFORNIA   (United States)

more..

Author keywords

Anopheles halophylus; Anopheles triannulatus C; Anopheles triannulatus s.s.; COI gene; ITS2; phylogeography; White gene

Indexed keywords

RIBOSOME DNA; CYTOCHROME C OXIDASE; GENETIC MARKER; MITOCHONDRIAL DNA; MITOCHONDRIAL PROTEIN; RIBOSOMAL SPACER DNA;

ANOPHELES; ANOPHELES HALOPHYLUS; ANOPHELES TRIANNULATUS C; ANOPHELES TRIANNULATUS SS; ARTICLE; BAYES THEOREM; CLADISTICS; GEOGRAPHIC DISTRIBUTION; MOLECULAR PHYLOGENY; NEOTROPICS; NONHUMAN; NUCLEOTIDE SEQUENCE; PARSIMONY ANALYSIS; PHYLOGEOGRAPHY; POPULATION STRUCTURE; SYMPATRY; ANIMAL; CHEMISTRY; CLASSIFICATION; DISEASE CARRIER; DNA SEQUENCE; GENETIC MARKER; GENETIC VARIABILITY; GENETICS; HAPLOTYPE; HUMAN; MALARIA; MOLECULAR GENETICS; SOUTH AMERICA; TRANSMISSION;

ANOPHELES TRIANNULATUS; CULICIDAE; DIPTERA;

ANIMALS; ANOPHELES; BASE SEQUENCE; BAYES THEOREM; DNA, MITOCHONDRIAL; DNA, RIBOSOMAL SPACER; ELECTRON TRANSPORT COMPLEX IV; GENETIC MARKERS; GENETIC VARIATION; HAPLOTYPES; HUMANS; INSECT VECTORS; MALARIA; MITOCHONDRIAL PROTEINS; MOLECULAR SEQUENCE DATA; PHYLOGEOGRAPHY; SEQUENCE ANALYSIS, DNA; SOUTH AMERICA;

EID: 84874028963     PISSN: None     EISSN: 17563305     Source Type: Journal    
DOI: 10.1186/1756-3305-6-47     Document Type: Article

References (90)

1. Grimaldi D, Engel MS, Evolution of the insects Cambridge: Massachusetts, Cambridge University Press 2005
2. Speciation in Amazonian forest birds. Haffer J, Science 1969 165 131 137 10.1126/science.165.3889.131 17834730
3. The biogeography and population genetics of neotropical vector species. Conn JE, Mirabello L, Heredity 2007 99 245 256 10.1038/sj.hdy.6801002 17534382 (Pubitemid 47295861)
4. Diversification of rainforest faunas: an integrated molecular approach. Moritz C, Patton JL, Schneider CJ, Smith TB, Annu Rev Ecol Evol Syst 2000 31 533 563 10.1146/annurev.ecolsys.31.1.533 (Pubitemid 32122412)
5. Concordant phylogeographies of 2 malaria vectors attest to common spatial and demographic histories. Pedro PM, Uezu A, Sallum MA, J Hered 2010 101 618 627 10.1093/jhered/esq054 20511380
6. Review of genetic diversity in malaria vectors (culicidae: anophelinae). Loaiza JR, Bermingham E, Sanjur OI, Scott ME, Bickersmith SA, Conn JE, Infect Genet Evol 2012 12 1 12 10.1016/j.meegid.2011.08.004 21864721
7. Species concepts and species delimitation. de Queiroz K, Syst Biol 2007 56 956 974 10.1080/10635150701656378 18066930
8. Considerações sobre o gênero cellia theobald, com a descripção de uma nova espécie. Neiva A, Pinto C, Brazil Méd 1922 36 355 357 21780946
9. Mosquito studies (diptera, culicidae). XXXIV. A revision of the albimanus section of the subgenus nyssorhynchus of anopheles. Faran ME, Contrib Amer Entomol Inst 1980 15 1 215
10. A handbook of the Amazonian species of anopheles (nyssorhynchus) (diptera: culicidae). Faran ME, Linthicum KJ, Mosq Syst 1981 13 1 81
11. Anopheles triannulatus (Neiva and pinto): a new anopheles record from Trinidad, west indies. Chadee DD, Wilkerson RC, J Am Mosq Control Assoc 2005 21 316 317 10.2987/8756-971X(2005)21[316:ATNAPA]2.0.CO;2 16252524 (Pubitemid 41445262)
12. Disseminação da malária pela aviação. Biologia do anopheles gambiae e outros anofelineos no brasil. Pinto C, Mem Inst Oswaldo Cruz 1939 34 293 430
13. Contribuição ao conhecimento dos anofelinos do grupo nyssorhynchus de São paulo e regiões vizinhas (diptera: culicidae). Galvão ALA, Arq Zool Sao Paulo 1940 1 399 484
14. Observações sobre alguns anofelinos de salobra, mato grosso (diptera, culicidae). Galvão ALA, Lane J, Rev Biol Hyg 1941 11 10 18
15. Chave ilustrada p a identificação de ovos de trinta espécies de anofelinos brasileiros, com algumas descrições novas. Deane LM, Causey OR, Deane MP, Rev Serv Esp Saúde Públ 1947a 1 293 308
16. Chave ilustrada p a identificação de trinta e cinco espécies de anofelinos das regiões nordestina e amazônica do brasil pelos caractéres da fêmea, com notas sobre os transmissores da malária (diptera: culicidae). Deane LM, Causey OR, Deane MP, Rev Serv Esp Saúde Públ 1947b 1 309 336
17. Forattini OP, Entomologia médica, Volume 1 São Paulo, Brazil: Univ São Paulo 1962 23445207
18. Anopheline species complexes in brazil. Current knowledge of those related to malaria transmission. Rosa-Freitas MG, Lourenço-de-Oliveira R, Pinto JCC, Flores-Mendoza C, Nascimento TFS, Mem Inst Oswaldo Cruz 1998 93 651 655 10.1590/S0074-02761998000500016 9830533 (Pubitemid 128526865)
19. Anopheles halophylus, a new species of the subgenus nyssorhynchus (diptera: culicidae) from brazil. Silva-do-Nascimento TF, Lourenço-de- Oliveira R, Mem Inst Oswaldo Cruz 2002 97 801 811 12386701
20. Molecular confirmation of the specific status of anopheles halophylus (diptera: culicidae) and evidence of a new criptic species within An. Triannulatus in central brazil. Silva-do-Nascimento TF, Wilkerson RC, Lourenço-de-Oliveira R, Monteiro FA, J Med Entomol 2006 43 455 459 10.1603/0022-2585(2006)43[455:MCOTSS]2.0.CO;2 16739400 (Pubitemid 44734934)
21. Molecular divergence in the timeless and cpr genes among three sympatric cryptic species of the anopheles triannulatus complex. Silva-do-Nascimento TF, Pitaluga LD, Peixoto AA, Lourenço-de-Oliveira R, Mem Inst Oswaldo Cruz 2011 106 218 222 21881777
22. Diverse population dynamics of the three anopheles species belonging to the triannulatus complex (diptera: culicidae). Silva-do-Nascimento TF, Lourenço-de-Oliveira R, Mem Inst Oswaldo Cruz 2007 102 975 982 10.1590/S0074-02762007000800013 18209937
23. Contribuição ao estudo epidemiológico da malária em trechos da rodovia transamazônica, brasil. Dixon K, Roberts DR, Llewellyn CH, Rev Inst Med Trop São Paulo 1979 21 287 292 (Pubitemid 10101074)
24. Malaria vector incrimination in three rural riverine village in the Brazilian Amazon. Galardo A, Arruda M, D'almeida A, Wirtz R, Lounibus P, Zimmerman R, AmJTrop Med Hyg 2007 76 461 469 (Pubitemid 351627737)
25. An ecorregional classification for the state of roraima, brazil: the importance of landscape in malaria biology. Rosa-Freitas M, Tsouris P, Peterson A, Honorio NA, de Barros FS, de Aguiar DB, Gurgel Hda C, de Arruda ME, Vasconcelos SD, Luitgards-Moura JF, Mem Inst Oswaldo Cruz 2007 102 349 357 10.1590/S0074-02762007005000052 17568941 (Pubitemid 46869333)
26. Malaria vectors in the Brazilian Amazon anopheles of the subgenus nyssorhynchus. Tadei WP, Dutary-Thatcher B, Rev Inst Med Trop S Paulo 2000 42 87 94 10.1590/S0036-46652000000200005 10810323
27. Malaria re-emergence in the Peruvian Amazon region. Aramburú GJ, Ramal AC, Witzig R, Emerg Infec Dis 1999 5 209 215 10.3201/eid0502.9902 (Pubitemid 29200618)
28. Studies of malaria in venezuela. Benarroch EI, Am J Hyg 1931 14 690 693
29. Notas sobre a distribuição e a biologia dos anofelinos das regiões nordestina e amazônica do brasil. Deane LM, Causey OR, Deane MP, Rev Serv Esp Saúde Públ 1948 1 827 965
30. Anopheline species, some of their habits and relation to malaria in endemic areas of rondônia state, amazon region of brazil. Lourenço-de-Oliveira R, Guimarães AE, Arlé M, Silva TF, Castro MG, Motta MA, Deane LM, Mem Inst Oswaldo Cruz 1989 84 501 514 2487447
31. Simian malaria at two sites in the Brazilian Amazon. II. Vertical distribution and frequency of anopheline species inside and outside the forest. Lourenço-de-Oliveira R, Luz SLB, Mem Inst Oswaldo Cruz 1996 91 687 694 10.1590/S0074-02761996000600005 9283645 (Pubitemid 126479334)
32. Bloodmeal hosts of anopheles species (diptera: culicidae) in a malaria-endemic area of the Brazilian Amazon. Zimmerman RH, Galardo AK, Lounibos LP, Arruda M, Wirtz R, J Med Entomol 2006 43 947 956 10.1603/0022-2585(2006) 43[947:BHOASD]2.0.CO;2 17017232 (Pubitemid 44734894)
33. Improved molecular technique for the differentiation of neotropical anopheline species. Matson R, Rios CT, Chavez CB, Gilman RH, Florin D, Sifuentes VL, Greffa RC, Yori PP, Fernandez R, Portocarrero DV, Vinetz JM, Kosek M, AmJTrop Med Hyg 2008 78 492 498 (Pubitemid 351845202)
34. Avise JC, Phylogeography: The history and formation of species Massachusetts: Harvard University Press 2000
35. A molecular phylogeny of mosquitoes in the anopheles barbirostris subgroup reveals cryptic species: implications for identification of disease vectors. Paredes-Esquivel C, Donnelly MJ, Harbach RE, Townson H, Mol Phyl Evol 2009 50 141 151 10.1016/j.ympev.2008.10.011
36. Microgeographic genetic variation of the malaria vector anopheles darlingi (diptera: culicidae) from Cordoba and Antioquia, Colombia. Gutierrez LA, Gomez GF, Gonzales JJ, Castro MI, Luckhart S, Conn JE, Correa MM, AmJTrop Med Hyg 2010 83 38 47
37. Molecular systematics of anopheles: from subgenera to subpopulations. Krzywinski J, Besansky NJ, Annu Rev Entomol 2003 48 111 139 10.1146/annurev. ento.48.091801.112647 12208816 (Pubitemid 37365388)
38. Phylogenetic relationships among species of anopheles (nyssorhynchus) (diptera, culicidae) based on nuclear and mitochondrial gene sequences. Bourke BP, Foster PG, Bergo ES, Calado DC, Sallum MA, Acta Trop 2010 114 88 96 10.1016/j.actatropica.2010.01.009 20117069
39. Intraspecific concerted evolution of the rDNA ITS1 in anopheles farauti sensu stricto (diptera: culicidae) reveals recent patterns of population structure. Bower JE, Dowton M, Cooper RD, Beebe NW, J Mol Evol 2008 67 397 411 10.1007/s00239-008-9161-x 18818859
40. Discrimination of seven anopheles species from San Pedro de uraba, Antioquia, Colombia, by polymerase chain reaction-restriction fragment length polymorphism analysis of its sequences. Zapata MA, Cienfuegos AV, Quiros OI, Quinones ML, Luckhart S, Correa MM, AmJTrop Med Hyg 2007 77 67 72 (Pubitemid 351844353)
41. The insect cytochrome oxidase I gene: evolutionary patterns and conserved primers for phylogenetic studies. Lunt DH, Zhang DX, Szymura JM, Hewitt GM, Insect Mol Biol 1996 5 153 165 10.1111/j.1365-2583.1996.tb00049.x 8799733 (Pubitemid 126439989)
42. Mirabello L, Molecular population genetics of the malaria vector nopheles darlingi throughout central and south America using mitochondrial, nuclear and microsatellites markers State University of New York at Albany, Biomedical Sciences Department: Ph.D. thesis 2007
43. Population analysis using the nuclear white gene detects Pliocene/Pleistocene lineage divergence within anopheles nuneztovari in south America. Mirabello L, Conn JE, Med Vet Entomol 2008 22 109 119 10.1111/j.1365-2915.2008.00731.x 18498609 (Pubitemid 351733113)
44. Identification of anopheles (nyssorhynchus) albitarsis complex species (diptera: culicidae) using rDNA internal transcribed spacer 2-based polymerase chain reaction primers. Li C, Wilkerson RC, Mem Inst Oswaldo Cruz 2005 100 495 500 16184227 (Pubitemid 41424076)
45. BioEdit: a user-friendly biological sequence alignment editor and analysis program for windows 95/98/NT. Hall TA, Nucl Acids Symp Ser 1999 41 95 98
46. JModelTest: phylogenetic model averaging. Posada D, Mol Biol Evol 2008 25 1253 1256 10.1093/molbev/msn083 18397919 (Pubitemid 351882013)
47. MRBAYES: Bayesian inference of phylogenetic trees. Huelsenbeck JP, Ronquist F, Bioinformatics 2001 17 754 755 10.1093/bioinformatics/17.8.754 11524383 (Pubitemid 32851390)
48. Partitioned Bayesian analyses, partition choice, and the phylogenetic relationships of scincid lizards. Brandley MC, Schmitz A, Reeder TW, Syst Biol 2005 54 373 390 10.1080/10635150590946808 16012105 (Pubitemid 41040438)
49. DnaSP v. 5: a software for comprehensive analysis of DNA polymorphism data. Librado P, Rozas J, Bioinformatics 2009 25 1451 1452 10.1093/ bioinformatics/btp187 19346325
50. A simulated annealing approach to define the genetic structure of populations. Dupanloup I, Schneider S, Excoffier L, Mol Ecol 2002 11 2571 2581 10.1046/j.1365-294X.2002.01650.x 12453240 (Pubitemid 35436677)
51. Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Excoffier L, Smouse PE, Quattro JM, Genetics 1992 131 479 491 1644282
52. Isolation by distance, web service. Jensen JL, Bohonak AJ, Kelley ST, BMC Genet 2005 6 13 v.3.16 15760479
53. Ersts PJ, Geographic distance matrix generator (version 1.2.3) American Museum of Natural History, Center for Biodiversity and Conservation http://biodiversityinformatics.amnh.org/open-source/gdmg
54. Multiple regression and correlation extensions of the mantel test of matrix correspondence. Smouse PE, Long JC, Sokal RR, Syst Zool 1986 35 627 632 10.2307/2413122
55. Median-joining networks for inferring intraspecific phylogenies. Bandelt HJ, Forster P, Röhl A, Mol Biol Evol 1999 16 37 48 10.1093/oxfordjournals. molbev.a026036 10331250 (Pubitemid 29024937)
56. A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data III. Cladogram estimation. Templeton AR, Crandall KA, Sing CF, Genetics 1992 132 619 633 1385266
57. TCS: a computer program to estimate gene genealogies. Clement M, Posada D, Crandall KA, Mol Ecol 2000 9 1657 1660 10.1046/j.1365-294x.2000.01020.x 11050560
58. Rates of nucleotide substitution in drosophila mitochondrial DNA and nuclear DNA are similar. Powell JR, Caccone A, Amato GD, Yoon C, Proc Natl Acad Sci USA 1986 83 9090 9093 10.1073/pnas.83.23.9090 3097641 (Pubitemid 17223541)
59. Genetic structure and colonization processes in European populations of the common vole, microtus arvalis. Heckel G, Burri R, Fink S, Desmet JF, Excoffier L, Evolution 2005 59 2231 2242 16405166 (Pubitemid 41552995)
60. Rapid morphological radiation and convergence among races of the butterfly heliconius erato inferred from patterns of mitochondrial DNA evolution. Brower AV, Proc Natl Acad Sci USA 1994 91 6491 6495 10.1073/pnas.91.14.6491 8022810 (Pubitemid 24200687)
61. Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Excoffier L, Laval G, Schneider S, Evol Bioinform 2005 1 47 50
62. Phylogeny of anophelinae (diptera: culicidae) based on nuclear ribosomal and mitochondrial DNA sequences. Sallum MAM, Schultz TR, Foster PG, Aronstein K, Wirtz RA, Wilkerson RC, Syst Entomol 2002 27 361 382 10.1046/j.1365-3113.2002. 00182.x (Pubitemid 34838115)
63. Phylogenetic relationships among onychophora from Australasia inferred from the mitochondrial cytochrome oxidase subunit I gene. Gleeson DM, Rowell DM, Tait NN, Briscoe DA, Higgins AV, Mol Phylogenet Evol 1998 10 237 248 10.1006/mpev.1998.0512 9878234 (Pubitemid 128350028)
64. An index of substitution saturation and its application. Xia X, Xie Z, Salemi M, Chen L, Wang Y, Mol Phylogenet Evol 2003 26 1 7 10.1016/S1055-7903(02) 00326-3 12470932 (Pubitemid 36029247)
65. Root probabilities for intraspecific gene trees under neutral coalescent theory. Castelloe J, Templeton AR, Mol Phylogenet Evol 1994 3 102 113 10.1006/mpev.1994.1013 8075830
66. Bayesian phylogenetic analysis of combined data. Nylander JAA, Ronquist F, Huelsenbeck JP, Nieves Aldrey JL, Syst Biol 2004 53 47 67 10.1080/10635150490264699 14965900 (Pubitemid 38370420)
67. Studies on Brazilian mosquitoes. I. Anophelines of the nyssorhynchus group. Root FM, Am J Hyg 1926 6 684 717
68. Frequent intron loss in the white gene: a cautionary tale for phylogeneticists. Krzywinski J, Besansky NJ, Mol Biol Evol 2002 19 362 366 10.1093/oxfordjournals.molbev.a004091 11861897 (Pubitemid 34184608)
69. Intron retention identifies a malaria vector within the anopheles (nyssorhynchus) albitarsis complex (diptera: culicidae). Merritt TJ, Young CR, Vogt RG, Wilkerson RC, Quattro JM, Mol Phylogenet Evol 2005 35 719 724 10.1016/j.ympev.2005.03.009 15878139 (Pubitemid 40607963)
70. Avise JC, Molecular markers, natural history, and evolution Massachusetts: Second ed Sinauer 2004
71. Inferring phylogenies from mtDNA variation: mitochondrial gene trees versus nuclear gene trees. Moore WS, Evolution 1995 49 718 726 10.2307/2410325
72. Molecular phylogenetics and biogeography of the neocellia series of anopheles mosquitoes in the oriental region. Morgan K, O'Loughlin SM, Mun-Yik F, Linton YM, Somboon P, Min S, Htun PT, Nambanya S, Weerasinghe I, Sochanta T, Prakash A, Walton C, Mol Phylogenet Evol 2009 52 588 601 10.1016/j.ympev.2009. 01.022 19603555
73. Molecular phylogenetics of tsetse flies (diptera: glossinidae) based on mitochondrial (COI, 16S, ND2) and nuclear ribosomal DNA sequences, with an emphasis on the palpalis group. Dyer NA, Lawton SP, Ravel S, Choi KS, Lehane MJ, Robinson AS, Okedi LM, Hall MJ, Solano P, Donnelly MJ, Mol Phylogenet Evol 2008 49 227 239 10.1016/j.ympev.2008.07.011 18692147
74. Biological identifications through DNA barcodes. Hebert PDN, Cywinska A, Ball SL, deWaard JR, Proc R Soc Lond B Biol Sci 2003 270 313 321 10.1098/rspb.2002.2218 (Pubitemid 36228536)
75. Phylogeography of the neotropical sand fly lutzomyia longipalpis inferred from mitochondrial DNA sequences. Arrivillaga JC, Norris DE, Feliciangeli MD, Lanzaro GC, Infect Genet Evol 2002 2 83 95 10.1016/S1567-1348(02)00087-4 12797984 (Pubitemid 35299505)
76. Gene flow among anopheles albimanus populations in central America, south America, and the Caribbean assessed by microsatellites and mitochondrial DNA. Molina-Cruz A, de Mérida AM, Mills K, Rodríguez F, Schoua C, Yurrita MM, Molina E, Palmieri M, Black WC 4th, AmJTrop Med Hyg 2004 71 350 359 (Pubitemid 39223513)
77. Phylogeography and dispersion pattern of anopheles farauti senso stricto mosquitoes in Melanesia. Hasan AU, Suguri S, Fujimoto C, Itaki RL, Harada M, Kawabata M, Bugoro H, Albino B, Tsukahara T, Hombhanje F, Masta A, Mol Phylogenet Evol 2008 46 792 800 10.1016/j.ympev.2007.09.018 18357645 (Pubitemid 351222721)
78. Uplift history of the central and northern Andes: a review. Gregory-Wodzicki KM, Geolog Society Am Bull 2000 112 1091 1105 10.1130/0016-7606(2000)112<1091:UHOTCA>2.0.CO;2 (Pubitemid 32832321)
79. Multiple mantel tests and isolation by distance, taking into account long-term historical divergence. Telles MPC, Diniz-Filho JAF, Gen Mol Res 2005 4 742 748
80. Spatial expansion and population structure of the neotropical malaria vector, anopheles darlingi. Pedro P, Sallum MAM, Biol J Linnean Soc 2009 97 854 866 10.1111/j.1095-8312.2009.01226.x
81. Molecular evidence for the occurrence of a new sibling species within the anopheles (kerteszia) cruzii complex in south-east brazil. Rona LD, Carvalho-Pinto CJ, Peixoto AA, Malaria J 2010 26 9 33
82. Müller P, Die herpetofauna der insel von São sebastião (brasilien) Saarbrücken: Verlag Saarbrücker Zeitung 1968 1 82
83. Genetic structure of natural populations of the sand fly lutzomyia longipalpis (diptera: psychodidae) from the Brazilian northeastern region. Queiroz Balbino V, Coutinho-Abreu IV, Sonoda IV, Melo MA, de Andrade PP, de Castro JA, Rebêlo JM, Carvalho SM, Ramalho-Ortigão M, Acta Trop 2006 98 15 24 10.1016/j.actatropica.2006.01.007 16480941
84. Forest refuges: evidence from woody angiosperms. Prance GT, Biological diversification in the tropics New York, USA: Columbia University Press, Prance GT, 1982 137 157
85. Evidence for Pleistocene population divergence and expansion of anopheles albimanus in southern central America. Loaiza JR, Scott ME, Bermingham E, Rovira J, Conn JE, AmJTrop Med Hyg 2010 82 156 164 10.4269/ajtmh.2010.09-0423
86. Statistical-method for testing the neutral mutation hypothesis by DNA polymorphism. Tajima F, Genetics 1989 123 585 595 2513255 (Pubitemid 19274682)
87. Evaluation of a PCR-RFLP-ITS2 assay for discrimination of anopheles species in northern and western Colombia. Cienfuegos AV, Rosero DA, Naranjo N, Luckhart S, Conn JE, Correa MM, Acta Trop 2011 118 128 133 10.1016/j. actatropica.2011.02.004 21345325
88. Late Pleistocene environmental changes lead to unstable demography and population divergence of anopheles albimanus in the northern neotropics. Loaiza JR, Scott ME, Bermingham E, Sanjur OI, Wilkerson R, Rovira J, Gutiérrez LA, Correa MM, Grijalva MJ, Birnberg L, Bickersmith S, Conn JE, Mol Phylogenet Evol 2010 57 1341 1346 10.1016/j.ympev.2010.09.016 20888924
89. Population structure of aedes albopictus (skuse): the mosquito which is colonizing Mediterranean countries. Urbanelli S, Bellini R, Carrieri M, Sallicandro P, Celli G, Heredity 2000 84 331 337 10.1046/j.1365-2540.2000.00676. x 10762403 (Pubitemid 30236597)
90. Zoogeografia de los anofelinos en Venezuela: I. Los dos vectores secundarios y los no vectores. Gabaldon A, Cova Garcia P, Tijeretazos Sobre Malar 1946 10 78 127