Genetic variability highlights the invasion route of the Lutzomyia longipalpis complex, the main vector of Visceral Leishmaniasis in Uruguay.
Lutzomyia longipalpis complex
infectious disease
molecular markers
mtDNA
phylogeography
Journal
Zoonoses and public health
ISSN: 1863-2378
Titre abrégé: Zoonoses Public Health
Pays: Germany
ID NLM: 101300786
Informations de publication
Date de publication:
08 2023
08 2023
Historique:
revised:
07
02
2023
received:
21
09
2022
accepted:
13
02
2023
medline:
4
7
2023
pubmed:
11
3
2023
entrez:
10
3
2023
Statut:
ppublish
Résumé
In the Americas, the sandfly Lutzomyia longipalpis is the main vector of the parasitic protozoa Leishmania infantum, the etiological agent of visceral leishmaniasis (VL). The Lu. longipalpis species complex is currently discontinuously distributed across the Neotropical region, from Mexico to the north of Argentina and Uruguay. During its continental spreading, it must have adapted to several biomes and temperature amplitudes, when founder events should have contributed to the high genetic divergence and geographical structure currently observed, reinforcing the speciation process. The first report of Lu. longipalpis in Uruguay was in 2010, calling the attention of Public Health authorities. Five years later, the parasite Le. infantum was recorded and in 2015 the first case of VL in canids was reported. Hitherto seven human cases by VL have been reported in Uruguay. Here, we publish the first DNA sequences from the mitochondrial genes ND4 and CYTB of Lu. longipalpis collected in Uruguay, and we used these molecular markers to investigate their genetic variability and population structure. We described four new ND4 haplotypes in a total of 98 (4/98) and one CYTB in a total of 77 (1/77). As expected, we were able to establish that the Lu. longipalpis collected in two localities (i.e. Salto and Bella Unión) from the north of Uruguay are closely related to the populations from neighbouring countries. We also propose that the possible route for the vector arrival to the region may have been through vegetation and forest corridors of the Uruguay River system, as well as it may have benefited from landscape modifications generated by commercial forestation. The ecological-scale processes shaping Lu. longipalpis populations, the identification of genetically homogeneous groups and the gene flow among them must be carefully investigated by using highly sensible molecular markers (i.e. genome wide SNPs) since it will help to the understanding of VL transmission and contribute to the planification of public policies on its control.
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
383-392Informations de copyright
© 2023 Wiley-VCH GmbH. Published by John Wiley & Sons Ltd.
Références
Abascal, F., Zardoya, R., & Telford, M. J. (2010). TranslatorX: Multiple alignment of nucleotide sequences guided by amino acid translations. Nucleic Acids Research, 38, 7-13. https://doi.org/10.1093/nar/gkq291
Alvar, J., Velez, I. D., Bern, C., Herrero, M., Desjeux, P., Cano, J., Jannin, J., den Boer, M., & WHO Leishmaniasis Control Team. (2012). Leishmaniasis worldwide and global estimates of its incidence. PLoS One, 7(5), e35671. https://doi.org/10.1371/journal.pone.0035671
Alvar, J., Yactayo, S., & Bern, C. (2006). Leishmaniasis and poverty. Trends in Parasitology, 22(12), 552-557. https://doi.org/10.1016/j.pt.2006.09.004
Araki, A. S., Ferreira, G. E., Mazzoni, C. J., Souza, N. A., Machado, R. C., Bruno, R. V., & Peixoto, A. A. (2013). Multilocus analysis of divergence and introgression in sympatric and allopatric sibling species of the Lutzomyia longipalpis complex in Brazil. PLoS Neglected Tropical Diseases, 7(10), e2495. https://doi.org/10.1371/journal.pntd.0002495
Araki, A. S., Vigoder, F. M., Bauzer, L. G., Ferreira, G. E., Souza, N. A., Araujo, I. B., Hamilton, J. G. C., Brazil, R. P., & Peixoto, A. A. (2009). Molecular and behavioral differentiation among Brazilian populations of Lutzomyia longipalpis (Diptera: Psychodidae: Phlebotominae). PLoS Neglected Tropical Diseases, 3(1), e365. https://doi.org/10.1371/journal.pntd.0000365
Arrivillaga, J., Mutebi, J. P., Pinango, H., Norris, D., Alexander, B., Feliciangeli, M. D., & Lanzaro, G. C. (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(5), 615-627. https://doi.org/10.1603/0022-2585-40.5.615
Arrivillaga, J. C., & Feliciangeli, M. D. (2001). Lutzomyia pseudolongipalpis: The first new species within the longipalpis (Diptera: Psychodidae: Phlebotominae) complex from La Rinconada, Curarigua, Lara state, Venezuela. Journal of Medical Entomology, 38(6), 783-790. https://doi.org/10.1603/0022-2585-38.6.783
Arrivillaga, J. C., Norris, D. E., Feliciangeli, M. D., & Lanzaro, G. C. (2002). Phylogeography of the neotropical sand fly Lutzomyia longipalpis inferred from mitochondrial DNA sequences. Infection, Genetics and Evolution, 2(2), 83-95. https://doi.org/10.1016/s1567-1348(02)00087-4
Avise, J. C. (1994). Molecular markers, natural history and evolution. Chapman and Hall. https://doi.org/10.1007/978-1-4615-2381-9
Cheng, L., Connor, T. R., Siren, J., Aanensen, D. M., & Corander, J. (2013). Hierarchical and spatially explicit clustering of DNA sequences with BAPS software. Molecular Biology and Evolution, 30, 1224-1228. https://doi.org/10.1093/molbev/mst028
Coutinho-Abreu, I. V., Sonoda, I. V., Fonseca, J. A., Melo, M. A., Balbino, V. Q., & Ramalho-Ortigao, M. (2008). Lutzomyia longipalpis s.l. in Brazil and the impact of the Sao Francisco River in the speciation of this sand fly vector. Parasites & Vectors, 1(1), 16. https://doi.org/10.1186/1756-3305-1-37
Depaquit, J., Lienard, E., Verzeaux-Griffon, A., Ferte, H., Bounamous, A., Gantier, J. C., Hanafi, A., Jacobson, R. L., Maroli, M., Moin-Vaziri, V., Müller, F., Ozbel, Y., Svobodova, M., Volf, P., & Léger, N. (2008). Molecular homogeneity in diverse geographical populations of Phlebotomus papatasi (Diptera, Psychodidae) inferred from ND4 mtDNA and ITS2 rDNA epidemiological consequences. Infection, Genetics and Evolution, 8(2), 159-170. https://doi.org/10.1016/j.meegid.2007.12.001
Dujardin, J. P., Torrez, E. M., Le Pont, F., Hervas, D., & Sossa, D. (1997). Isozymic and metric variation in the Lutzomyia longipalpis complex. Medical and Veterinary Entomology, 11(4), 394-400. https://doi.org/10.1111/j.1365-2915.1997.tb00428.x
Esseghir, S., Ready, P. D., Killick-Kendrick, R., & Ben-Ismail, R. (1997). Mitochondrial haplotypes and phylogeography of Phlebotomus vectors of Leishmania major. Insect Molecular Biology, 6(3), 211-225. https://doi.org/10.1046/j.1365-2583.1997.00175.x
Fernández, M., Martínez, M., Pérez, A., Santini, M., Gould, I., & Salomón, O. D. (2015). Performance of light-emitting diode traps for collecting sand flies in entomological surveys in Argentina. Journal of Vector Ecology, 40(2), 373-378. https://doi.org/10.1111/jvec.12176
Flanley, C. M., Ramalho-Ortigao, M., Coutinho-Abreu, I. V., Mukbel, R., Hanafi, H. A., El-Hossary, S. S., Fawaz, E. E. Y., Hoel, D. F., Bray, A. W., Stayback, G., Shoue, D. A., Kamhawi, S., Karakuş, M., Jaouadi, K., Yaghoobie-Ershadi, M. R., Krüger, A., Amro, A., Kenawy, M. A., Dokhan, M. R., … McDowell, M. A. (2018). Population genetics analysis of Phlebotomus papatasi sand flies from Egypt and Jordan based on mitochondrial cytochrome b haplotypes. Parasites & Vectors, 11(1), 214. https://doi.org/10.1186/s13071-018-2785-9
Franco, F. A. L., Morillas-Marquez, F., Barón, S. D., Morales-Yuste, M., Galvez, R., Diaz, V., Pesson, B., Alves-Pires, C., Depaquit, J., Molina, R., Afonso, M. O., Gállego, M., Guernaoui, S., Bounamous, A., & Martín-Sáncheza, J. (2010). Genetic structure of Phlebotomus (Larroussius) ariasi populations, the vector of Leishmania infantum in the western Mediterranean: Epidemiological implications. International Journal of Parasitology, 40(11), 1335-1346. https://doi.org/10.1016/j.ijpara.2010.03.017
Galati, E. A. B. (2018). Classification morphology and terminology of adults and identification of American Taxa. In E. F. Rangel & R. Lainson (Eds.), Brazilian sand flies: Biology, taxonomy, medical importance and control (pp. 9-212). Springer.
Guindon, S., Dufayard, J. F., Lefort, V., Anisimova, M., Hordijk, W., & Gascuel, O. (2010). New algorithms and methods to estimate maximum-likelihood phylogenies: Assessing the performance of PhyML 3.0. Systematic Biology, 59, 307-321. https://doi.org/10.1093/sysbio/syq010
Gutierrez, M., Lopez, R., Ramos, A., Vélez, I., Gomez, R., Arrivillaga-Henríquez, J., & Uribe, S. (2021). DNA barcoding of Lutzomyia longipalpis species complex (Diptera: Psychodidae), suggests the existence of 8 candidate species. Acta Tropica, 221, 105983. https://doi.org/10.1016/j.actatropica.2021.105983
Hamarsheh, O., Presber, W., Abdeen, Z., Sawalha, S., Al-Lahem, A., & Schonian, G. (2007). Genetic structure of Mediterranean populations of the sandfly Phlebotomus papatasi by mitochondrial cytochrome b haplotype analysis. Medical and Veterinary Entomology, 21(3), 270-277. https://doi.org/10.1111/j.1365-2915.2007.00695.x
Hamilton, J. G., Maingon, R. D., Alexander, B., Ward, R. D., & Brazil, R. P. (2005). Analysis of the sex pheromone extract of individual male Lutzomyia longipalpis sandflies from six regions in Brazil. Medical and Veterinary Entomology, 19(4), 480-488. https://doi.org/10.1111/j.1365-2915.2005.00594.x
Hodgkinson, V. H., Birungi, J., Haghpanah, M., Joshi, S., & Munstermann, L. E. (2002). Rapid identification of mitochondrial cytochrome B haplotypes by single strand conformation polymorphism in Lutzomyia longipalpis (Diptera: Psychodidae) populations. Journal of Medical Entomology, 39(4), 689-694. https://doi.org/10.1603/0022-2585-39.4.689
Hodgkinson, V. H., Birungi, J., Quintana, M., Dietze, R., & Munstermann, L. E. (2003). Mitochondrial cytochrome b variation in populations of the visceral leishmaniasis vector Lutzomyia longipalpis across eastern Brazil. The American Journal of Tropical Medicine and Hygiene, 69(4), 386-392. https://doi.org/10.4269/ajtmh.2003.69.386
Jombart, T. (2008). Adegenet: A R package for the multivariate analysis of genetic markers. Bioinformatics, 24, 1403-1405. https://doi.org/10.1093/bioinformatics/btn129
Katoh, K., & Standley, D. M. (2013). MAFFT multiple sequence alignment software version 7: Improvements in performance and usability. Molecular Biology and Evolution, 30, 772-780. https://doi.org/10.1093/molbev/mst010
Keane, T. M., Creevey, C. J., Pentony, M. M., Naughton, T. J., & McInerney, J. O. (2006). Assessment of methods for amino acid matrix selection and their use on empirical data shows that ad hoc assumptions for choice of matrix are not justified. BMC Evolutionary Biology, 6, 29. https://doi.org/10.1186/1471-2148-6-29
Khalid, N. M., Marium, M., Aboud, A., Alrabba, M., Elnaiem, A., & Tripet, F. (2012). Evidence for genetic differentiation at the microgeographic scale in Phlebotomus papatasi populations from Sudan. Parasites & Vectors, 5, 249. https://doi.org/10.1186/1756-3305-5-249
Kuhls, K., Alam, M. Z., Cupolillo, E., Ferreira, G. E. M., Mauricio, I. L., Oddone, R., Feliciangeli, M. D., Wirth, T., Miles, M. A., & Schönian, G. (2011). Comparative microsatellite typing of new world Leishmania infantum reveals low heterogeneity among populations and its recent Old World origin. PLoS Neglected Tropical Diseases, 5(6), e1155. https://doi.org/10.1371/journal.pntd.0001155
Lainson, R., & Rangel, E. F. (2005). Lutzomyia longipalpis and the eco-epidemiology of American visceral leishmaniasis, with particular reference to Brazil: a review. Memórias do Instituto Oswaldo Cruz, 100, 811-827. https://doi.org/10.1590/s0074-02762005000800001
Lampo, M., Torgerson, D., Marquez, L. M., Rinaldi, M., Garcia, C. Z., & Arab, A. (1999). Occurrence of sibling species of Lutzomyia longipalpis (Diptera: Psychodidae) in Venezuela: First evidence from reproductively isolated sympatric populations. The American Journal of Tropical Medicine and Hygiene, 61(6), 1004-1009. https://doi.org/10.4269/ajtmh.1999.61.1004
Lanzaro, G. C., Alexander, B., Mutebi, J. P., Montoya-Lerma, 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(1), 65-69. https://doi.org/10.1590/s0074-02761998000100013
Lanzaro, G. C., Lopes, A. H., Ribeiro, J. M., Shoemaker, C. B., Warburg, A., Soares, M., & Titus, R. G. (1999). Variation in the salivary peptide, maxadilan, from species in the Lutzomyia longipalpis complex. Insects Molecular Biology, 8(2), 267-275. https://doi.org/10.1046/j.1365-2583.1999.820267.x
Lanzaro, G. C., Ostrovska, K., Herrero, M. V., Lawyer, P. G., & Warburg, A. (1993). Lutzomyia longipalpis is a species complex: Genetic divergence and interspecific hybrid sterility among three populations. The American Journal of Tropical Medicine and Hygiene, 48(6), 839-847. https://doi.org/10.4269/ajtmh.1993.48.839
Lanzaro, G. C., & Warburg, A. (1995). Genetic variability in phlebotomine sand flies: Possible implications for leishmaniasis epidemiology. Parasitology Today, 11, 151-154. https://doi.org/10.1016/0169-4758(95)80137-5
Leigh, J. W., & Bryant, D. (2015). PopART: Full-feature software for haplotype network construction. Methods in Ecology and Evolution, 6(9), 1110-1116. https://doi.org/10.1111/2041-210X.12410
Lins, R. M., Souza, N. A., & Peixoto, A. A. (2008). Genetic divergence between two sympatric species of the Lutzomyia longipalpis complex in the paralytic gene, a locus associated with insecticide resistance and lovesong production. Memórias Do Instituto Oswaldo Cruz, 103(7), 736-740. https://doi.org/10.1590/s0074-02762008000700019
Lutz, A., & Neiva, A. (1912). Contribuição para o conhecimentodas espécies do gênero Phlebotomus existente no Brasil. Memórias do Instituto Oswaldo Cruz, 4(1), 84-95. https://doi.org/10.1590/S0074-02761912000100006
Maia-Elkhoury, A. N. S., Valadas, S. Y. O. B., Puppim-Buzanovsky, L., Rocha, F., & Sanchez-Vazquez, M. J. (2017). SisLeish: A multi-country standardized information system to monitor the status of Leishmaniasis in the Americas. PLoS Neglected Tropical Diseases, 11(9), e0005868. https://doi.org/10.1371/journal.pntd.0005868
Mangabeira, O. (1969). Sobre a sistemática e biologia dos flebótomos do Ceará. Revista Brasileira de Malariologia e Doenças Tropicais, 21, 3-26.
Marinho, D. S., Casas, C. N. P. R., Pereira, C. D. D. A., & Leite, I. C. (2015). Health economic evaluations of visceral Leishmaniasis treatments: A systematic review. PLoS Neglected Tropical Diseases, 9(2), e0003527. https://doi.org/10.1371/journal.pntd.0003527
Moo-Llanes, D., Pech-May, A., Ibarra-Cerdena, C. N., Rebollar-Tellez, E. A., & Ramsey, J. (2019). Inferring distributional shifts from Pleistocene to future scenarios of epidemiologically important north and central American sand flies (Diptera: Psychodidae). Medical and Veterinary Entomology, 33(1), 31-43. https://doi.org/10.1111/mve.12326
Morrison, A. C., Ferro, C., Morales, A., Tesh, R. B., & Wilson, M. L. (1993). Dispersal of the sand fly Lutzomyia longipalpis (Diptera: Psychodidae) at an endemic focus of visceral leishmaniasis in Colombia. Journal of Medical Entomology, 30(2), 427-435. https://doi.org/10.1093/jmedent/30.2.427
MSP. (2021). Boletines Epidemiológicos. Miniesterio de Salud Publica Uruguay. https://www.gub.uy/ministerio-salud-publica/tematica/boletines-epidemiologicos
PAHO. (2018). Leishmaniasis Report #6. https://iris.paho.org/bitstream/handle/10665.2/34856/LeishReport6_eng.pdf?ua=1
Paradis, E. (2010). Pegas: An R package for population genetics with an integrated modular approach. Bioinformatics, 26(3), 419-420. https://doi.org/10.1093/bioinformatics/btp696
Paradis, E., Claude, J., & Strimmer, K. (2004). APE: Analyses of Phylogenetics and evolution in R language. Bioinformatics, 20(2), 289-290. https://doi.org/10.1093/bioinformatics/btp696
Paradis, E., & Schliep, K. (2019). Ape 5.0: An environment for modern phylogenetics and evolutionary analyzes in R. Bioinformatics, 35, 526-528. https://doi.org/10.1093/bioinformatics/bty633
Pech-May, A., Marina, C. F., Vazquez-Dominguez, E., Berzunza-Cruz, M., Rebollar-Tellez, E. A., Narvaez-Zapata, J. A., Moo-Llanes, D., Ibáñez-Bernal, S., Ramsey, J. M., & Becker, I. (2013). Genetic structure and divergence in populations of Lutzomyia cruciata, a phlebotomine sand fly (Diptera: Psychodidae) vector of Leishmania mexicana in southeastern Mexico. Infection, Genetics and Evolution, 16, 254-262. https://doi.org/10.1016/j.meegid.2013.02.004
Pech-May, A., Ramsey, J. M., González Ittig, R. E., Giuliani, M., Berrozpe, P., Quintana, M. G., & Salomón, O. D. (2018). Genetic diversity, phylogeography and molecular clock of the Lutzomyia longipalpis complex (Diptera: Psychodidae). PLoS Neglected Tropical Diseases, 12(7), e0006614. https://doi.org/10.1371/journal.pntd.0006614
Peterson, A. T., Campbell, L. P., Moo-Llanes, D. A., Travi, B., Gonzalez, C., Ferro, M. C., Melim Ferreira, G. E., Brandão-Filho, S. P., Cupolillo, E., Ramsey, J., Chernaki Leffer, A. M., Pech-May, A., & Shaw, J. J. (2017). Influences of climate change on the potential distribution of Lutzomyia longipalpis sensu lato (Psychodidae: Phlebotominae). International Journal for Parasitology, 47(10-11), 667-674. https://doi.org/10.1016/j.ijpara.2017.04.007
Ready, P. D., Day, J., De Souza, A. A., Rangel, E. F., & Davies, C. R. (1997). Mitochondrial DNA characterization of populations of Lutzomyia whitmani (Diptera: Psychodidae) incriminated in the peridomestic and sylvatic transmission of Leishmania species in Brazil. Bulletin of Entomological Research, 87, 187-195. https://doi.org/10.1590/s0074-02761999000300010
Ready, P. D., de Souza, A. A., Rebelo, J. M., Day, J. C., Silveira, F. T., Campbell-Lendrum, D., Davies, C. R., & Costa, J. M. (1998). Phylogenetic species and domesticity of Lutzomyia whitmani at the southeast boundary of Amazonian Brazil. Transactions of the Royal Society of Tropical Medicine and Hygiene., 92(2), 159-160. https://doi.org/10.1016/s0035-9203(98)90726-x
Reynolds, J., Weir, B. S., & Cockerham, C. C. (1983). Estimation of the coancestry coefficient: Basis for a short-term genetic distance. Genetics, 105, 767-779. https://doi.org/10.1093/genetics/105.3.767
Salomón, O., Sinagra, A., Nevot, M., Barberian, G., Paulin, P., Estevez, J. O., Riarte, A., & Estevez, J. (2008). First visceral leishmaniasis focus in Argentina. Memórias Do Instituto Oswaldo Cruz, 103(1), 109-111. https://doi.org/10.1590/s0074-02762008000100018
Salomón, O. D., Araki, A. S., Hamilton, J. G., Acardi, S. A., & Peixoto, A. A. (2010). Sex pheromone and period gene characterization of Lutzomyia longipalpis sensu lato (Lutz & Neiva) (Diptera: Psychodidae) from Posadas, Argentina. Memórias Do Instituto Oswaldo Cruz, 105(7), 928-930. https://doi.org/10.1590/s0074-02762010000700016
Salomón, O. D., Basmajdian, Y., Fernandez, M. S., & Santini, M. S. (2011). Lutzomyia longipalpis in Uruguay: The first report and the potential of visceral leishmaniasis transmission. Memórias Do Instituto Oswaldo Cruz, 106(3), 381-382. https://doi.org/10.1590/s0074-02762011000300023
Santini, M. S., Utgés, M. E., Berrozpe, P., MantecaAcosta, M., Casas, N., Heuer, P., & Salomón, O. D. (2015). Lutzomyia longipalpis presence and abundance distribution at different micro-spatial scales in an urban scenario. PLoS Neglected Tropical Diseases, 9(8), e0003951. https://doi.org/10.1371/journal.pntd.0003951
Satragno, D., Faral-Tello, P., Canneva, B., Verger, L., Lozano, A., Vitale, E., Greif, G., Soto, C., Robello, C., & Basmadjián, Y. (2017). Autochthonous outbreak and expansion of canine visceral leishmaniasis, Uruguay. Emerging Infectious Diseases, 23(3), 536-538. https://doi.org/10.3201/eid2303.160377
Scarpassa, V. M., Cunha-Machado, A. S., & Alencar, R. B. (2021). Multiple evolutionary lineages for the main vector of Leishmania guyanensis, Lutzomyia umbratilis (Diptera: Psychodidae), in the Brazilian Amazon. Scientific Reports, 11(1), 15323. https://doi.org/10.1038/s41598-021-93072-4
Scarpassa, V. M., Figueiredo, A. S., & Alencar, R. B. (2015). Genetic diversity and population structure in the Leishmania guyanensis vector Lutzomyia anduzei (Diptera, Psychodidae) from the Brazilian Amazon. Infection, Genetics and Evolution, 31, 312-320. https://doi.org/10.1016/j.meegid.2015.02.007
Slatkin, M. (1987). Gene flow and the geographic structure of natural populations. Science, 236, 787-792. https://doi.org/10.1126/science.3576198
Soto, S. I., Lehmann, T., Rowton, E. D., Velez, B. I., & Porter, C. H. (2011). 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. https://doi.org/10.1006/mpev.2000.0863
Thomaz-Soccol, V., Gonçalves, A. L., Piecknick, C. A., Baggio, R. A., Boeger, W. A., Buchman, T. L., Michaliszyn, M., Rodrigues Dos Santos, D., Celestino, A., Aquino, J., Jr., de Souza Leandro, A., de Souza, L., da Paz, O., Limont, M., Bisetto, A., Jr., Shaw, J. J., Yadon, Z. E., & Salomon, O. D. (2018). Hidden danger: Unexpected scenario in the vector-parasite dynamics of leishmaniases in the Brazil side of triple border (Argentina, Brazil and Paraguay). PLoS Neglected Tropical Diseases, 12(4), e0006336. https://doi.org/10.1371/journal.pntd.0006336
Torgerson, D. G., Lampo, M., Velazquez, Y., & Woo, P. T. (2003). Genetic relationships among some species groups within the genus Lutzomyia (Diptera: Psychodidae). The American Journal of Tropical Medicine and Hygiene, 69(5), 484-493. https://doi.org/10.4269/ajtmh.2003.69.484
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. https://doi.org/10.1590/s0074-02761999000600005
Valderrama, A., Tavares, M. G., & Andrade Filho, J. D. (2014). Phylogeography of the Lutzomyia gomezi (Diptera: Phlebotominae) on the Panama isthmus. Parasites & Vectors, 7, 9. https://doi.org/10.1186/1756-3305-7-9
Ward, R. D., Phillips, A., Burnet, B., & Marcondes, C. (1988). The Lutzomyia longipalpis complex reproduction and distribution. In Service, M.W. (Ed.), Biosystematics of haematophagous insects (pp. 257-269). Oxford University Press, ISBN 0-19-857709-5.
Ward, R. D., Ribeiro, A. L., Ready, P. D., & 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 Kalaazar distribution on South America. Memórias Do Instituto Oswaldo Cruz, 78(1983), 269-280. https://doi.org/10.1590/S0074-02761983000300005
Watts, P. C., Hamilton, J. G., Ward, R. D., Noyes, H. A., Souza, N. A., Kemp, S. J., Feliciangeli, M. D., Brazil, R., & Maingoni, R. D. C. (2005). Male sex pheromones and the phylogeographic structure of the Lutzomyia longipalpis species complex (Diptera: Psychodidae) from Brazil and Venezuela. The American Journal of Tropical Medicine and Hygiene, 73(4), 734-743. https://doi.org/10.4269/ajtmh.2005.73.734
WHO. (2019). Leishmaniasis Fact sheet, March 2019. World Health Organization. https://www.who.int/es/news-room/fact-sheets/detail/leishmaniasis.
Yin, H., Norris, D. E., & Lanzaro, G. C. (2000). Sibling species in the Llutzomyia longipalpis complex differ in levels of mRNA expression for the salivary peptide, maxadilan. Insect Molecular Biology, 9(3), 309-314. https://doi.org/10.1046/j.1365-2583.2000.00190.x
Young, D. G., & Duran, 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) (p. 881). Memoirs of the Entomological Institute No. 54, Associate Publishers ISBN 1-5666-054-2.
Yu, G., Smith, D. K., Zhu, H., Guan, Y., & Lam, T. T. Y. (2017). Ggtree: An R package for visualization and annotation of phylogenetic trees with their covariates and other associated data. Methods in Ecology and Evolution, 8, 28-36. https://doi.org/10.1111/2041-210X.12628