Typification of colombian specimens of Lutzomyia longipalpis (Diptera: Psychodidae) by “Barcoding”
Cytochrome Oxidase I Genetic distances Neighbor-joining
Main Article Content
Lutzomyia longipalpis, is the main vector of visceral leishmaniasis in the Neotropic and the taxonomic identification is relevant for epidemiologic studies and for the disease control. The evidence supporting the existence of a L. longipalpis species complex morphologically indistinguishable besides similarity with females belonging the Lutzomyia subgenus and longipalpis series, difficult taxonomical identification when there are not available males. In this study, we used the sequence proposed worldwide as DNA barcode to distinguish animal species to characterize specimens belonging to L. longipalpis from three Colombian localities (Neiva, El Callejón, Girón) and evaluate their usefulness in separating them from closely related species such as L. gomezi, L. cruciata and L. bifoliata. The amplified and sequenced fragment exhibited a length of 548 bp and 26 haplotypes for 33 individuals of L. longipalpis, one haplotype for L.gomezi, one haplotype for L. cruciata and two haplotypes for L. bifoliata were found. Genetic distances (K2P) between L. longipalpis haplotypes (0.05-0.07) and clusters in a NJ dendrogram, effectively separated L. longipalpis from individuals belonging to closely related species. Individuals of L. longipalpis were separated in two groups, one included haplotype from Neiva and El Callejón, and the other from Girón. The genetic distance found between the two groups of L. longipalpis were significantly higher than those found at the intraspecific level for species previously studied on the basis of the barcode sequence as L. trinidadensis (0.042) and L.panamensis (0.02).
HOYOS L., R., URIBE S., S., & VÉLEZ, I. (2012). Typification of colombian specimens of Lutzomyia longipalpis (Diptera: Psychodidae) by “Barcoding”. Revista Colombiana De Entomología, 38(1), 134–140. https://doi.org/10.25100/socolen.v38i1.8971
ARRIVILLAGA, J.; RANGEL, Y.; OVIEDO, M.; FELICIANGELI, M. 2000. Genetic diversity among Venezuelan populations of Lutzomyia longipalpis (Diptera: Psychodidae: Phlebotominae). Journal of Medical Entomology 37: 325-330.
ARRIVILLAGA, J.; NORRIS, D.; FELICIANGELI, M.; LANZARO, G. 2002. Phylogeography of the neotropical sand fly Lutzomyia longipalpis inferred from mitochondrial DNA sequences. Infection, Genetics and Evolution 2: 83-95.
ARRIVILLAGA, J.; MUTEBI, J.; PINANGO, H.; NORRIS, D.; ALEXANDER, B.; FELICIANGELI, M.; LANZARO, G. 2003. The taxonomic status of genetically divergent populations of Lutzomyia longipalpis (Diptera: Psychodidae) based on the distribution of mitochondrial and isozyme variation. Journal of Medical Entomology 40: 615-627.
AZPURUA, J.; CRUZ, D.; VALDERRAMA, A.; WINDSOR, D. 2010. Lutzomyia Sand Fly Diversity and Rates of Infection by Wolbachia and an Exotic leishmania Species on Barro Colorado Island, Panama. PLoS 4: 1-8.
BESANSKY, N.; SEVERSON, D.; FERDING, D. 2003. DNA barcoding of parasites and invertebrate disease vectors: what you don’t know can hurt you. TRENDS in Parasitology 19: 545-546.
BAUZER, L.; SOUZA, N.; MAINGON, R.; PEIXOTO, A. 2007. Lutzomyia longipalpis in Brazil: a complex or a single species? A mini-review. Memórias do Instituto Oswaldo Cruz 102 (1):1-12.
CASIRAGHI, M.; LABRA, M.; FERRI, M.; GALIMBERTI, A.; MATTIA, F. 2010. DNA barcoding: a six-question tour to improve users’ awareness about the method. Briefings in Bioinformatics 11: 440-453.
CREASE, T. J. 1999. The complete sequence for the mitochondrial genome of Daphnia pulex (Cladocera: Crustacea). Gene 233: 89-99.
CYWINSKA, A.; HANNAN, M.; KEVAN, P.; ROUGHLEY, R.; IRANPOUR, M.; HUNTER, F. 2010. Evaluation of DNA barcoding and identification of new Haplomorphs in Canadian deerflies and horseflies. Medical and Veterinary Entomology 24: 382-410.
FLÓREZ, M.; MARTÍNEZ, J.; GUTIÉRREZ, R.; LUNA, K.; SERRANO, H.; FERRO, C.; ANGULO, V.; SANDOVAL, M. 2006. Lutzomyia longipalpis (Diptera: Psychodidae) at a suburban focus of visceral leishmaniasis in the Chicamocha Canyon, Santander, Colombia. Biomédica 26: 109-120.
GALATI, E. 2009. Bioecologia e Identificação de Phlebotominae: Classificação, Morfologia e Terminologia e Identificação de Adultos. Vol I-II. Departamento de Epidemiologia, Faculdade de Saúde Pública. Universidade de São Paulo, 275 p.
GONZÁLEZ, C.; CABRERA, O. L.; MUNSTERMANN, L. E.; FERRO, C. 2006. Distribución de vectores de leishmania infantum en Colombia. Biomédica 26 (Suppl I): 64-72.
GRIMALDI, G.; TESH, R.; MACHAMON, D. 1989. A review on the geographic distribution and epidemiology of leishmaniasis in the new world. American Journal of Tropical Medicine and Hygiene 41: 687-725.
HALL, T. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41:95-98.
HEBERT, P.; CYWINSKA, A.; BALL, S.; DEWAARD, D. 2003. Biological identifications through DNA barcodes. Proceedings Royal Society of London 270: 313-321.
HOY, M. 2006. Insect molecular genetics: an introduction to principles and applications. Academic press, San Diego, 544 p.
JINBO, U.; KATO, T.; ITO, M. 2011. Current progress in DNA barcoding and future implications for entomology. Entomological Science 14: 107-124.
KUMAR, P.; RAJAVEL, A.; NATARAJAN, R.; JAMBULIGAM, P. 2007. DNA barcodes can distinguish species of Indian mosquitoes (Diptera: Culicidae). Journal of Medical Entomology 44: 1-7.
LAINSON, R.; RANGEL, E. 2005. Lutzomyia longipalpis and the eco-epidemiology of American visceral leishmaniasis; with particular reference to Brazil A Review -. Memórias do Instituto Oswaldo Cruz 100 (8): 811-827.
LANZARO, G.; WARBURG, A. 1995. Genetic variability in phlebotomine sandflies: possible implications for leishmaniasis epidemiology. Parasitology Today 11: 151-154.
LANZARO, G.; OSTROVSKA, K.; HERRERO, M.; LAWYER, P.; WARBURG, A. 1993. Lutzomyia longipalpis is a species complex: genetic divergence and interspecific hybrid sterility among three populations. American Journal of Tropical Medicine and Hygiene 48: 839-847.
LANZARO, G.; ALEXANDER, B.; MUTEBI, J.; MONTOYA, J.; WARBURG, A. 1998. Genetic variation among natural and laboratory colony populations of Lutzomyia longipalpis (Lutz & Neiva, 1912) (Diptera: Psychodidae) from Colombia. Memórias do Instituto Oswaldo Cruz 93: 65-69.
LANZARO, G.; LOPES, A.; RIBEIRO, J.; SHOEMAKER, C.; WARBURG, A.; SOARES, M.; TITUS, R. 1999. Variation in the salivary peptide, maxadilan, from species in the Lutzomyia longipalpis. Insect Molecular Biology 8: 267-275.
LARKIN, M.; BLACKSHIELDS, G.; BROWN, N.; CHENNA, R.; MCGETTIGAN, P.; MCWILLIAM, H.; VALENTIN, F.; WALLACE, I.; WILM, A.; LÓPEZ, R.; THOMPSON, J.; GIBSON, G.; HIGGINS, D. 2007. Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947-2948.
LÓPEZ, Y.; OSORIO, L.; ÁLVAREZ, G.; ROJAS, J.; JIMÉNEZ, F.; GÓMEZ, C. 1996. Sandfly Lutzomyia longipalpis in a cutaneous leishmaniasis focus in central Colombia. Memórias do Instituto Oswaldo Cruz 91: 415-419.
MARTINS, A.; FALCÃO, A.; SILVA, J.; DIAS, E. 1984. Nota sobre Lutzomyia (Lutzomyia) cruzi (Mangabeira.; 1938).; com a descrição da fêmea (Diptera.; Psychodidae.; Phlebotominae). Memórias do Instituto Oswaldo Cruz 79: 439-442.
MEIER, R.; SHIYANG, K.; VAIDYA, G.; NG, P. 2006. DNA barcoding and taxonomy in Diptera: A tale of high intraspecific variability and low identification success. Systematic Biology 55: 715-728.
MORITZ, C.; CICERO, C. 2004. DNA Barcoding: Promise and Pitfalls. PLoS Biology 2: 1529-1531.
MORRISON, A.; FERRO, C.; MORALES, A.; TESH, R.; WILSON, M. 1993. Dispersal of the sand fly Lutzomyia longipalpis (Diptera: Psychodidae) at an endemic focus of visceral leishmaniasis in Colombia. Journal of Medical Entomology 30: 427-435.
MUTEBI, J.; ROWTON, E.; HERRERO, M.; PONCE, C.; BELLI, A.; VALLE, S.; LANZARO, G. 1998. Genetic variability among populations of the sand fly Lutzomyia (Lutzomyia) longipalpis (Diptera: Psychodidae) from Central America. Journal Medical Entomology 35: 169-174.
NEI, M.; KUMAR, S. 2000. Molecular Evolution and Phylogenetics. Oxford University Press, New York, 333 p.
PORTER, C.; COLLINS, F. 1991. Species-diagnostic differences in a ribosomal DNA internal transcribed spacer from the sibling species Anopheles freeborni and Anopheles hermsi (Diptera: Culicidae). American Journal of Tropical Medicine and Hygiene 45: 271-279.
RIVERA, J.; CURRIE, D. 2009. Identification of Nearctic black flies using DNA barcodes (Diptera: Simuliidae). Molecular Ecology Resources 9: 224-236.
SONG, H.; BUHAY, J.; WHITING, M.; CRANDALL, K. 2008. Many species in one: DNA barcoding overestimates the number of species when nuclear mitochondrial pseudogenes are coamplified. PNAS 105: 13486-13491.
TAMURA, K.; DUDLEY, J.; NEI, M.; KUMAR, S. 2007. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA)
software version 4.0. Molecular Biology and Evolution 24: 1596-1599.
TRAVI, B.; ADLER, G.; LOZANO, M.; CADENA, H.; MONTOYA-LERMA, J. 2002. Impact of habitat degradation on phlebotominae (Diptera: Psychodidae) of tropical dry forests in Northern Colombia. Journal Medical of Entomology 39: 451-456.
URIBE, S. 1999. The status of the Lutzomyia longipalpis species complex and possible implications for leishmania transmission. Memórias do Instituto Oswaldo Cruz 94: 729-734.
URIBE, S.; LEHMANN, T.; ROWTON, E.; VÉLEZ, I.; PORTER, C. 2001. Speciation and population structure in the morphospecies Lutzomyia longipalpis (Lutz and Neiva) as derived from the mitochondrial ND4 gene. Molecular, Phylogenetic and Evolution 18: 84-93.
VIGODER, F.; ARAKI, A.; BAUZER, L.; SOUZA, N.; BRAZIL, R.; PEIXOTO, A. 2010. Lovesongs and period gene polymorphisms indicate Lutzomyia cruzi (Mangabeira, 1938) as a sibling species of the Lutzomyia longipalpis (Lutz and Neiva, 1912) complex. Infection, Genetics and Evolution 10: 734-739.
VIVEROS, R.; BEJARANO, E.; PEREZ, A.; ESTRADA, L.; FLÓREZ, F.; TORRES, C.; MUSKUS, C. 2010. Presencia de Lutzomyia longipalpis (Diptera: Psychodidae) en los alrededores de un núcleo urbano del Caribe Colombiano. Biota Neotrópica 9: 277-280.
WARBURG, A.; SARAIVA, E.; LANZARO, G.; TITUS, R.; NEVA, F. 1994. Saliva of Lutzomyia longipalpis sibling species differs in its composition and capacity to enhance leishmaniasis. Philosophical Transactions of the Royal Society B: Biological Sciences 29: 223-230.
WARD, R.; RIBEIRO, A.; READY, P.; MURTAGH, A. 1983. Reproductive isolation between different forms of Lutzomyia longipalpis (Lutz & Neiva), (Diptera: Psychodidae), the vector of leishmania donovani chagasi Cunha & Chagas and its significance to kala-azar distribution in South America. Memórias do Instituto Oswaldo Cruz 78: 269-280.
WARD, R.; RIBEIRO, A.; RYAN, L.; FALCO, A.; RANGEL, E. 1985. The distribution of two morphological forms of Lutzomyia longipalpis (Lutz & Neiva) (Diptera: Psychodidae). Memórias do Instituto Oswaldo Cruz 80: 145-148.
WATTS, P.; HAMILTON, J.; WARD, R.; NOYES, H.; SOUZA, N.; KEMP, S.; FELICIANGELI, M.; BRAZIL, R.; MAINGON, R. 2005. Male sex pheromones and the phylogeographic structure of the Lutzomyia longipalpis species complex (Diptera: Psychodidae) from Brazil and Venezuela. American Journal of Tropical Medicine and Hygiene 73: 734-743.
XIA, X. 2002. DAMBE: Data Analysis in Molecular Biology and Evolution. New York, Kluwer Academic Express Editors, 284 p. YIN, H.; MUTEBI, J.; MARRIOTT, S.; LANZARO, G. 1999. Metaphase karyotypes and G-banding in sandflies of the Lutzomyia longipalpis complex. Medical & Veterinary Entomology 13: 72-77.
YIN, H.; NORRIS, D.; LANZARO, G. 2000. Sibling species in the Lutzomyia longipalpis complex differ in levels of mRNA expression for the salivary peptide, maxadilan. Insect Molecular Biology 9: 309-314.
YOUNG, D. 1979. A review of the bloodsucking psychodid flies of Colombia (Diptera: Phlebotominae and Sycoracinae). Institute of Food and Agricultural Sciences, Technical Bulletin 806: 1-266.
YOUNG, D.; DUNCAN, M. A. 1994. Guide to the identification and geographic distribution of Lutzomyia sand flies in Mexico, the West Indies, Central and South America (Diptera: Psychodidae). Memoirs of the American Entomological Institute 54: 1-881.
ARRIVILLAGA, J.; NORRIS, D.; FELICIANGELI, M.; LANZARO, G. 2002. Phylogeography of the neotropical sand fly Lutzomyia longipalpis inferred from mitochondrial DNA sequences. Infection, Genetics and Evolution 2: 83-95.
ARRIVILLAGA, J.; MUTEBI, J.; PINANGO, H.; NORRIS, D.; ALEXANDER, B.; FELICIANGELI, M.; LANZARO, G. 2003. The taxonomic status of genetically divergent populations of Lutzomyia longipalpis (Diptera: Psychodidae) based on the distribution of mitochondrial and isozyme variation. Journal of Medical Entomology 40: 615-627.
AZPURUA, J.; CRUZ, D.; VALDERRAMA, A.; WINDSOR, D. 2010. Lutzomyia Sand Fly Diversity and Rates of Infection by Wolbachia and an Exotic leishmania Species on Barro Colorado Island, Panama. PLoS 4: 1-8.
BESANSKY, N.; SEVERSON, D.; FERDING, D. 2003. DNA barcoding of parasites and invertebrate disease vectors: what you don’t know can hurt you. TRENDS in Parasitology 19: 545-546.
BAUZER, L.; SOUZA, N.; MAINGON, R.; PEIXOTO, A. 2007. Lutzomyia longipalpis in Brazil: a complex or a single species? A mini-review. Memórias do Instituto Oswaldo Cruz 102 (1):1-12.
CASIRAGHI, M.; LABRA, M.; FERRI, M.; GALIMBERTI, A.; MATTIA, F. 2010. DNA barcoding: a six-question tour to improve users’ awareness about the method. Briefings in Bioinformatics 11: 440-453.
CREASE, T. J. 1999. The complete sequence for the mitochondrial genome of Daphnia pulex (Cladocera: Crustacea). Gene 233: 89-99.
CYWINSKA, A.; HANNAN, M.; KEVAN, P.; ROUGHLEY, R.; IRANPOUR, M.; HUNTER, F. 2010. Evaluation of DNA barcoding and identification of new Haplomorphs in Canadian deerflies and horseflies. Medical and Veterinary Entomology 24: 382-410.
FLÓREZ, M.; MARTÍNEZ, J.; GUTIÉRREZ, R.; LUNA, K.; SERRANO, H.; FERRO, C.; ANGULO, V.; SANDOVAL, M. 2006. Lutzomyia longipalpis (Diptera: Psychodidae) at a suburban focus of visceral leishmaniasis in the Chicamocha Canyon, Santander, Colombia. Biomédica 26: 109-120.
GALATI, E. 2009. Bioecologia e Identificação de Phlebotominae: Classificação, Morfologia e Terminologia e Identificação de Adultos. Vol I-II. Departamento de Epidemiologia, Faculdade de Saúde Pública. Universidade de São Paulo, 275 p.
GONZÁLEZ, C.; CABRERA, O. L.; MUNSTERMANN, L. E.; FERRO, C. 2006. Distribución de vectores de leishmania infantum en Colombia. Biomédica 26 (Suppl I): 64-72.
GRIMALDI, G.; TESH, R.; MACHAMON, D. 1989. A review on the geographic distribution and epidemiology of leishmaniasis in the new world. American Journal of Tropical Medicine and Hygiene 41: 687-725.
HALL, T. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41:95-98.
HEBERT, P.; CYWINSKA, A.; BALL, S.; DEWAARD, D. 2003. Biological identifications through DNA barcodes. Proceedings Royal Society of London 270: 313-321.
HOY, M. 2006. Insect molecular genetics: an introduction to principles and applications. Academic press, San Diego, 544 p.
JINBO, U.; KATO, T.; ITO, M. 2011. Current progress in DNA barcoding and future implications for entomology. Entomological Science 14: 107-124.
KUMAR, P.; RAJAVEL, A.; NATARAJAN, R.; JAMBULIGAM, P. 2007. DNA barcodes can distinguish species of Indian mosquitoes (Diptera: Culicidae). Journal of Medical Entomology 44: 1-7.
LAINSON, R.; RANGEL, E. 2005. Lutzomyia longipalpis and the eco-epidemiology of American visceral leishmaniasis; with particular reference to Brazil A Review -. Memórias do Instituto Oswaldo Cruz 100 (8): 811-827.
LANZARO, G.; WARBURG, A. 1995. Genetic variability in phlebotomine sandflies: possible implications for leishmaniasis epidemiology. Parasitology Today 11: 151-154.
LANZARO, G.; OSTROVSKA, K.; HERRERO, M.; LAWYER, P.; WARBURG, A. 1993. Lutzomyia longipalpis is a species complex: genetic divergence and interspecific hybrid sterility among three populations. American Journal of Tropical Medicine and Hygiene 48: 839-847.
LANZARO, G.; ALEXANDER, B.; MUTEBI, J.; MONTOYA, J.; WARBURG, A. 1998. Genetic variation among natural and laboratory colony populations of Lutzomyia longipalpis (Lutz & Neiva, 1912) (Diptera: Psychodidae) from Colombia. Memórias do Instituto Oswaldo Cruz 93: 65-69.
LANZARO, G.; LOPES, A.; RIBEIRO, J.; SHOEMAKER, C.; WARBURG, A.; SOARES, M.; TITUS, R. 1999. Variation in the salivary peptide, maxadilan, from species in the Lutzomyia longipalpis. Insect Molecular Biology 8: 267-275.
LARKIN, M.; BLACKSHIELDS, G.; BROWN, N.; CHENNA, R.; MCGETTIGAN, P.; MCWILLIAM, H.; VALENTIN, F.; WALLACE, I.; WILM, A.; LÓPEZ, R.; THOMPSON, J.; GIBSON, G.; HIGGINS, D. 2007. Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947-2948.
LÓPEZ, Y.; OSORIO, L.; ÁLVAREZ, G.; ROJAS, J.; JIMÉNEZ, F.; GÓMEZ, C. 1996. Sandfly Lutzomyia longipalpis in a cutaneous leishmaniasis focus in central Colombia. Memórias do Instituto Oswaldo Cruz 91: 415-419.
MARTINS, A.; FALCÃO, A.; SILVA, J.; DIAS, E. 1984. Nota sobre Lutzomyia (Lutzomyia) cruzi (Mangabeira.; 1938).; com a descrição da fêmea (Diptera.; Psychodidae.; Phlebotominae). Memórias do Instituto Oswaldo Cruz 79: 439-442.
MEIER, R.; SHIYANG, K.; VAIDYA, G.; NG, P. 2006. DNA barcoding and taxonomy in Diptera: A tale of high intraspecific variability and low identification success. Systematic Biology 55: 715-728.
MORITZ, C.; CICERO, C. 2004. DNA Barcoding: Promise and Pitfalls. PLoS Biology 2: 1529-1531.
MORRISON, A.; FERRO, C.; MORALES, A.; TESH, R.; WILSON, M. 1993. Dispersal of the sand fly Lutzomyia longipalpis (Diptera: Psychodidae) at an endemic focus of visceral leishmaniasis in Colombia. Journal of Medical Entomology 30: 427-435.
MUTEBI, J.; ROWTON, E.; HERRERO, M.; PONCE, C.; BELLI, A.; VALLE, S.; LANZARO, G. 1998. Genetic variability among populations of the sand fly Lutzomyia (Lutzomyia) longipalpis (Diptera: Psychodidae) from Central America. Journal Medical Entomology 35: 169-174.
NEI, M.; KUMAR, S. 2000. Molecular Evolution and Phylogenetics. Oxford University Press, New York, 333 p.
PORTER, C.; COLLINS, F. 1991. Species-diagnostic differences in a ribosomal DNA internal transcribed spacer from the sibling species Anopheles freeborni and Anopheles hermsi (Diptera: Culicidae). American Journal of Tropical Medicine and Hygiene 45: 271-279.
RIVERA, J.; CURRIE, D. 2009. Identification of Nearctic black flies using DNA barcodes (Diptera: Simuliidae). Molecular Ecology Resources 9: 224-236.
SONG, H.; BUHAY, J.; WHITING, M.; CRANDALL, K. 2008. Many species in one: DNA barcoding overestimates the number of species when nuclear mitochondrial pseudogenes are coamplified. PNAS 105: 13486-13491.
TAMURA, K.; DUDLEY, J.; NEI, M.; KUMAR, S. 2007. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA)
software version 4.0. Molecular Biology and Evolution 24: 1596-1599.
TRAVI, B.; ADLER, G.; LOZANO, M.; CADENA, H.; MONTOYA-LERMA, J. 2002. Impact of habitat degradation on phlebotominae (Diptera: Psychodidae) of tropical dry forests in Northern Colombia. Journal Medical of Entomology 39: 451-456.
URIBE, S. 1999. The status of the Lutzomyia longipalpis species complex and possible implications for leishmania transmission. Memórias do Instituto Oswaldo Cruz 94: 729-734.
URIBE, S.; LEHMANN, T.; ROWTON, E.; VÉLEZ, I.; PORTER, C. 2001. Speciation and population structure in the morphospecies Lutzomyia longipalpis (Lutz and Neiva) as derived from the mitochondrial ND4 gene. Molecular, Phylogenetic and Evolution 18: 84-93.
VIGODER, F.; ARAKI, A.; BAUZER, L.; SOUZA, N.; BRAZIL, R.; PEIXOTO, A. 2010. Lovesongs and period gene polymorphisms indicate Lutzomyia cruzi (Mangabeira, 1938) as a sibling species of the Lutzomyia longipalpis (Lutz and Neiva, 1912) complex. Infection, Genetics and Evolution 10: 734-739.
VIVEROS, R.; BEJARANO, E.; PEREZ, A.; ESTRADA, L.; FLÓREZ, F.; TORRES, C.; MUSKUS, C. 2010. Presencia de Lutzomyia longipalpis (Diptera: Psychodidae) en los alrededores de un núcleo urbano del Caribe Colombiano. Biota Neotrópica 9: 277-280.
WARBURG, A.; SARAIVA, E.; LANZARO, G.; TITUS, R.; NEVA, F. 1994. Saliva of Lutzomyia longipalpis sibling species differs in its composition and capacity to enhance leishmaniasis. Philosophical Transactions of the Royal Society B: Biological Sciences 29: 223-230.
WARD, R.; RIBEIRO, A.; READY, P.; MURTAGH, A. 1983. Reproductive isolation between different forms of Lutzomyia longipalpis (Lutz & Neiva), (Diptera: Psychodidae), the vector of leishmania donovani chagasi Cunha & Chagas and its significance to kala-azar distribution in South America. Memórias do Instituto Oswaldo Cruz 78: 269-280.
WARD, R.; RIBEIRO, A.; RYAN, L.; FALCO, A.; RANGEL, E. 1985. The distribution of two morphological forms of Lutzomyia longipalpis (Lutz & Neiva) (Diptera: Psychodidae). Memórias do Instituto Oswaldo Cruz 80: 145-148.
WATTS, P.; HAMILTON, J.; WARD, R.; NOYES, H.; SOUZA, N.; KEMP, S.; FELICIANGELI, M.; BRAZIL, R.; MAINGON, R. 2005. Male sex pheromones and the phylogeographic structure of the Lutzomyia longipalpis species complex (Diptera: Psychodidae) from Brazil and Venezuela. American Journal of Tropical Medicine and Hygiene 73: 734-743.
XIA, X. 2002. DAMBE: Data Analysis in Molecular Biology and Evolution. New York, Kluwer Academic Express Editors, 284 p. YIN, H.; MUTEBI, J.; MARRIOTT, S.; LANZARO, G. 1999. Metaphase karyotypes and G-banding in sandflies of the Lutzomyia longipalpis complex. Medical & Veterinary Entomology 13: 72-77.
YIN, H.; NORRIS, D.; LANZARO, G. 2000. Sibling species in the Lutzomyia longipalpis complex differ in levels of mRNA expression for the salivary peptide, maxadilan. Insect Molecular Biology 9: 309-314.
YOUNG, D. 1979. A review of the bloodsucking psychodid flies of Colombia (Diptera: Phlebotominae and Sycoracinae). Institute of Food and Agricultural Sciences, Technical Bulletin 806: 1-266.
YOUNG, D.; DUNCAN, M. A. 1994. Guide to the identification and geographic distribution of Lutzomyia sand flies in Mexico, the West Indies, Central and South America (Diptera: Psychodidae). Memoirs of the American Entomological Institute 54: 1-881.
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