Advertisement

Molecular and Biochemical Markers for Investigating the Vectorial Roles of Brazilian Sand Flies

  • Paul D. Ready
  • Felipe M. Vigoder
  • Elizabeth F. Rangel
Chapter

Abstract

This chapter reviews how molecular and biochemical methods have been developed in recent decades in order to incriminate sand flies as vectors of human diseases in Brazil, specifically of visceral and cutaneous leishmaniasis. There are references to relevant complementary research on non-vectors and sand flies from other countries and continents. Non-DNA techniques include multilocus enzyme electrophoresis and cuticular hydrocarbon analysis. The impacts of early DNA-based approaches are summarized, but most molecular examples refer to methods based on polymerase chain reaction. Many protocols depend on comparative sequence analysis, and this will increasingly involve high-throughput and whole genome sequencing. This chapter considers the complementary approaches necessary for identifying morphospecies, geographical populations characterized by distinct genetic lineages, and sympatric sibling species reproductively isolated by courtship behavior. Current and future challenges are considered, including the need to relate specific genotypes of individual sand flies to phenotypes of biomedical importance such as vector competence and insecticide resistance.

References

  1. Abdeladhim M, V Coutinho-Abreu I, Townsend S, Pasos-Pinto S, Sanchez L, Rasouli M, B Guimaraes-Costa A, Aslan H, Francischetti IM, Oliveira F, Becker I, Kamhawi S, Ribeiro JM, Jochim RC, Valenzuela JG (2016) Molecular diversity between salivary proteins from new world and old world sand flies with emphasis on Bichromomyia olmeca, the Sand Fly Vector of Leishmania mexicana in Mesoamerica. PLoS Negl Trop Dis 10(7):e0004771PubMedPubMedCentralCrossRefGoogle Scholar
  2. Adamson RE, Ward RD, Feliciangeli MD, Maingon R (1993) The application of random amplified polymorphic DNA for sandfly species identification. Med Vet Entomol 7(3):203–207PubMedCrossRefPubMedCentralGoogle Scholar
  3. Aires J, Casanova C, Vernal S, Nascimento M, Rodrigues S, Lerner EA, Roselino AM (2017) Maxadilan-simile expression in Nyssomyia neivai, a sandfly vector in an endemic region of Brazil, and its immunogenicity in patients with American tegumentary leishmaniasis. Mem Inst Oswaldo Cruz 112(2):116–122PubMedPubMedCentralCrossRefGoogle Scholar
  4. Alexander B, Barros VC, Souza SS, Teodoro LP, Soares ZR, Gontijo NF et al (2009) Susceptibility to chemical insecticides of two Brazilian populations of the visceral leishmaniasis vector Lutzomyia longipalpis (Diptera: Psychodidae). Trop Med Int Health 14(10):1272–1277PubMedCrossRefPubMedCentralGoogle Scholar
  5. Anderson JM, Oliveira F, Kamhawi S, Mans BJ, Reynoso D, Seitz AE, Lawyer P, Garfield M, Pham M, Valenzuela JG (2006) Comparative salivary gland transcriptomics of sandfly vectors of visceral leishmaniasis. BMC Genomics 7:52PubMedPubMedCentralCrossRefGoogle Scholar
  6. Andrade AJ, Andrade MR, Dias ES, Pinto MC, Eiras AE (2008) Are light traps baited with kairomones effective in the capture of Lutzomyia longipalpis and Lutzomyia intermedia? An evaluation of synthetic human odor as an attractant for phlebotomine sand flies (Diptera: Psychodidae: Phlebotominae). Mem Inst Oswaldo Cruz 103(4):337–343PubMedCrossRefPubMedCentralGoogle Scholar
  7. Araki AS, Vigoder FM, Bauzer LG, Ferreira GE, Souza NA, Araújo IB et al (2009) Molecular and behavioral differentiation among Brazilian populations of Lutzomyia longipalpis (Diptera: Psychodidae: Phlebotominae). PLoS Negl Trop Dis 3(1):e365PubMedPubMedCentralCrossRefGoogle Scholar
  8. Araki AS, Ferreira GE, Mazzoni CJ, Souza NA, Machado RC, Bruno RV et al (2013) Multilocus analysis of divergence and introgression in sympatric and allopatric sibling species of the Lutzomyia longipalpis complex in Brazil. PLoS Negl Trop Dis 7(10):e2495PubMedPubMedCentralCrossRefGoogle Scholar
  9. Aransay AM, Scoulica E, Tselentis Y, Ready PD (2000) Phylogenetic relationships of phlebotomine sandflies inferred from small subunit nuclear ribosomal DNA. Insect Mol Biol 9:157–168PubMedCrossRefPubMedCentralGoogle Scholar
  10. Aransay AM, Malarky G, Ready PD (2001) Isolation (with enrichment) and characterization of trinucleotide microsatellites from Phlebotomus perniciosus, a vector of Leishmania infantum. Mol Ecol Notes 1:176–178CrossRefGoogle Scholar
  11. Arrivilaga J, Feliciangeli MD (2001) Lutzomyia pseudolongipalpis: the first new species within the longipalpis (Diptera: Psychodidae: Phlebotominae) complex from La Rinconada, Curarigua, Lara state. Venez J Med Entomol 38:783–790CrossRefGoogle Scholar
  12. Arrivillaga JC, Norris DE, Feliciangeli MD, Lanzaro GC (2002) Phylogeography of the neotropical sandfly Lutzomyia longipalpis inferred from mitochondrial DNA sequences. Infect Genet Evol 2(2):83–95PubMedCrossRefPubMedCentralGoogle Scholar
  13. Arrivillaga J, Mutebi JP, Piñango H, Norris D, Alexander B, Feliciangeli MD et al (2003) The taxonomic status of genetically divergent populations of Lutzomyia longipalpis (Diptera: Psychodidae) based on the distribution of mitochondrial and isozyme variation. J Med Entomol 40(5):615–627PubMedCrossRefPubMedCentralGoogle Scholar
  14. Avise JC (2000) Phylogeography: The History and Formation of Species. Harvard University Press, Cambridge, MA, pp 1–447Google Scholar
  15. Azevedo RV, Dias DB, Bretãs JA, Mazzoni CJ, Souza NA, Albano RM, Wagner G, Davila AM, Peixoto AA (2012) The transcriptome of Lutzomyia longipalpis (Diptera: Psychodidae) male reproductive organs. PLoS One 7(4):e34495PubMedPubMedCentralCrossRefGoogle Scholar
  16. Bates PA, Depaquit J, Galati EAB, Kamhawi S, Maroli M, McDowell MA et al (2015) Recent advances in phlebotomine sand fly research related to leishmaniasis control. Parasit Vectors 8:131PubMedPubMedCentralCrossRefGoogle Scholar
  17. Bauzer LG, Gesto JS, Souza NA, Ward RD, Hamilton JG, Kyriacou CP et al (2002a) Molecular divergence in the period gene between two putative sympatric species of the Lutzomyia longipalpis complex. Mol Biol Evol 19(9):1624–1627PubMedCrossRefPubMedCentralGoogle Scholar
  18. Bauzer LG, Souza NA, Ward RD, Kyriacou CP, Peixoto AA (2002b) The period gene and genetic differentiation between three Brazilian populations of Lutzomyia longipalpis. Insect Mol Biol 11(4):315–323PubMedCrossRefPubMedCentralGoogle Scholar
  19. Bauzer LGSR, Souza NA, Maingon RDC, Peixoto AA (2007) Lutzomyia longipalpis in Brazil: a complex or a single species? A mini-review. Mem Inst Oswaldo Cruz 102(1):1–12PubMedCrossRefPubMedCentralGoogle Scholar
  20. Beati L, Caceres AG, Lee JA, Munstermann LE (2004) Systematics relationships among Lutzomyia sand flies (Diptera: Psychodidae) of Peru and Colombia based on the analysis of 12S and 28S ribosomal DNA sequences. Int J Parasitol 34:225–234PubMedCrossRefPubMedCentralGoogle Scholar
  21. Booth DR, Ready PD, Smith DF (1994) Isolation of non-LTR retrotransposon reverse transcriptase-like sequences from phlebotomine sandflies. Insect Mol Biol 3:89–96PubMedCrossRefPubMedCentralGoogle Scholar
  22. Booth DR, Ready PD, Smith DF (1996) Evolution of multiple families of non-LTR retrotransposons in phlebotomine sandflies. Genet Res 67:227–237PubMedCrossRefPubMedCentralGoogle Scholar
  23. Bottecchia M, Oliveira SG, Bauzer LG, Souza NA, Ward RD, Garner KJ et al (2004) Genetic divergence in the cacophony IVS6 intron among five Brazilian populations of Lutzomyia longipalpis. J Mol Evol 58(6):754–761PubMedCrossRefPubMedCentralGoogle Scholar
  24. Brandão-Filho SP, Balbino VQ, Marcondes CB, Brazil RP, Hamilton JG, Shaw JJ (2009) Should reproductively isolated populations of Lutzomyia longipalpis sensu lato receive taxonomically valid names? Mem Inst Oswaldo Cruz 104(8):1197–1200PubMedCrossRefPubMedCentralGoogle Scholar
  25. Bray DP, Bandi KK, Brazil RP, Oliveira AG, Hamilton JG (2009) Synthetic sex pheromone attracts the leishmaniasis vector Lutzomyia longipalpis (Diptera: Psychodidae) to traps in the field. J Med Entomol 46:428–434PubMedPubMedCentralCrossRefGoogle Scholar
  26. Bray DP, Carter V, Alves GB, Brazil RP, Bandi KK, Hamilton JG (2014) Synthetic sex pheromone in a long-lasting lure attracts the visceral leishmaniasis vector, Lutzomyia longipalpis, for up to 12 weeks in Brazil. PLoS Negl Trop Dis 8(3):e2723PubMedPubMedCentralCrossRefGoogle Scholar
  27. Brazil RP, Hamilton JGCH (2002) Isolation and identification of 9-methylgermacrene-B as the putative sex pheromone of Lutzomyia cruzi (Mangabeira, 1938) (Diptera: Psychodidae). Mem Inst Oswaldo Cruz 97(3):435–436PubMedCrossRefPubMedCentralGoogle Scholar
  28. Caillard T, Tibayrenc M, Le Pont F, Dujardin JP, Desjeux P, Ayala FJ (1986) Diagnosis by isozyme methods of two cryptic species, Psychodopygus carrerai and P. yucumensis (Diptera: Psychodidae). J Med Entomol 23:489–492PubMedCrossRefPubMedCentralGoogle Scholar
  29. Cameron MM, Acosta-Serrano A, Bern C, Boelaert M, den Boer M, Burza S, Chapman LA, Chaskopoulou A, Coleman M, Courtenay O, Croft S, Das P, Dilger E, Foster G, Garlapati R, Haines L, Harris A, Hemingway J, Hollingsworth TD, Jervis S, Medley G, Miles M, Paine M, Picado A, Poché R, Ready P, Rogers M, Rowland M, Sundar S, de Vlas SJ, Weetman D (2016) Understanding the transmission dynamics of Leishmania donovani to provide robust evidence for interventions to eliminate visceral leishmaniasis in Bihar, India. Parasit Vectors 9:25PubMedPubMedCentralCrossRefGoogle Scholar
  30. Campbell-Lendrum DH, Pinto MC, Brandão-Filho SP, de Souza AA, Ready PD, Davies CR (1999) Experimental comparison of anthropophily between geographically dispersed populations of Lutzomyia whitmani (Diptera: Psychodidae). Med Vet Entomol 13:299–309PubMedCrossRefPubMedCentralGoogle Scholar
  31. Campbell-Lendrum DH, Brandão-Filho SP, Pinto MC, Vexenat A, Ready PD, Davies CR (2000) Domesticity of Lutzomyia whitmani (Diptera: Psychodidae) populations: Field experiments indicate behavioural differences. Bull Entomol Res 90:41–48PubMedCrossRefPubMedCentralGoogle Scholar
  32. Campo D, Lehmann K, Fjeldsted C, Souaiaia T, Kao K, Nuzhdin SV (2013) Whole-genome sequencing of two North American Drosophila melanogaster populations reveals genetic differentiation and positive selection. Mol Ecol 22:5084–5097PubMedPubMedCentralCrossRefGoogle Scholar
  33. Carvalho BM, Rangel EF, Ready PD, Vale MM (2015) Ecological niche modelling predicts southward expansion of Lutzomyia (Nyssomyia) flaviscutellata (Diptera: Psychodidae: Phlebotominae), vector of Leishmania (Leishmania) amazonensis in South America, under climate change. PLoS One 10(11):e0143282PubMedPubMedCentralCrossRefGoogle Scholar
  34. Casanova C, Hamilton JGC, Trigo JR, Costa AIP (2006) Identification of sex pheromones of Lutzomyia longipalpis (Lutz & Neiva, 1912) populations from the state of São Paulo, Brazil. Mem Inst Oswaldo Cruz 101(1):113–115PubMedCrossRefPubMedCentralGoogle Scholar
  35. Casanova C, Colla-Jacques FE, Hamilton JG, Brazil RP, Shaw JJ (2015) Distribution of Lutzomyia longipalpis chemotype populations in São Paulo state, Brazil. PLoS Negl Trop Dis 9(3):e0003620PubMedPubMedCentralCrossRefGoogle Scholar
  36. Charlab R, Valenzuela JG, Rowton ED, Ribeiro JM (1999) Toward an understanding of the biochemical and pharmacological complexity of the saliva of a hematophagous sand fly Lutzomyia longipalpis. Proc Natl Acad Sci U S A 96(26):15155–15160PubMedPubMedCentralCrossRefGoogle Scholar
  37. Cohnstaedt LW, Beati L, Caceres AG, Ferro C, Munstermann LE (2011) Phylogenetics of the phlebotomine sand fly group Verrucarum (Diptera: Psychodidae: Lutzomyia). Am J Trop Med Hyg 84(6):913–922PubMedPubMedCentralCrossRefGoogle Scholar
  38. Collin N, Gomes R, Teixeira C, Cheng L, Laughinghouse A et al (2009) Sand fly salivary proteins induce strong cellular immunity in a natural reservoir of visceral leishmaniasis with adverse consequences for Leishmania. PLoS Pathog 5:e1000441PubMedPubMedCentralCrossRefGoogle Scholar
  39. Contreras Gutiérrez MA, Vivero RJ, Vélez ID, Porter CH, Uribe S (2014) DNA barcoding for the identification of sand fly species (Diptera, Psychodidae, Phlebotominae) in Colombia. PLoS One 9(1):e85496PubMedPubMedCentralCrossRefGoogle Scholar
  40. Day JC, Ready PD (1999) Relative abundance, isolation and structure of phlebotomine microsatellites. Insect Mol Biol 8(4):575–580PubMedCrossRefPubMedCentralGoogle Scholar
  41. de Moura TR, Oliveira F, Carneiro MW, Miranda JC, Clarêncio J, Barral-Netto M, Brodskyn C, Barral A, Ribeiro JM, Valenzuela JG, de Oliveira CI (2013) Functional transcriptomics of wild-caught Lutzomyia intermedia salivary glands: identification of a protective salivary protein against Leishmania braziliensis infection. PLoS Negl Trop Dis 7(5):e2242PubMedPubMedCentralCrossRefGoogle Scholar
  42. de Souza Freitas MT, Ríos-Velasquez CM, da Silva LG, Costa CR Jr, Marcelino A, Leal-Balbino TC, Balbino Vde Q, Pessoa FA (2016) Analysis of the genetic structure of allopatric populations of Lutzomyia umbratilis using the period clock gene. Acta Trop 154:149–154PubMedCrossRefPubMedCentralGoogle Scholar
  43. de Souza A, Ishikawa E, Braga R, Silveira F, Lainson R, Shaw J (1996) Psychodopygus complexus, a new vector of Leishmania braziliensis to humans in Pará State, Brazil. Trans R Soc Trop Med Hyg 90(2):112–113PubMedCrossRefPubMedCentralGoogle Scholar
  44. Depaquit J (2014) Molecular systematics applied to Phlebotomine sandflies: review and perspectives. Infect Genet Evol 28:744–756PubMedCrossRefPubMedCentralGoogle Scholar
  45. Dias ES, Fortes-Dias CL, Stiteler JM, Perkins PV, Lawyer PG (1998) Random amplified polymorphic DNA (RAPD) analysis of Lutzomyia longipalpis laboratory populations. Rev Inst Med Trop Sao Paulo 40:49–53PubMedCrossRefPubMedCentralGoogle Scholar
  46. Dillon RJ, Ivens AC, Churcher C, Holroyd N, Quail MA et al (2006) Analysis of ESTs from Lutzomyia longipalpis sand flies and their contribution toward understanding the insect-parasite relationship. Genomics 88:831–840PubMedPubMedCentralCrossRefGoogle Scholar
  47. Doehl JS, Sádlová J, Aslan H, Pružinová K, Metangmo S, Votýpka J, Kamhawi S, Volf P, Smith DF (2017) Leishmania HASP and SHERP genes are required for in vivo differentiation, parasite transmission and virulence attenuation in the host. PLoS Pathog 13(1):e1006130PubMedPubMedCentralCrossRefGoogle Scholar
  48. Dujardin JP, Le Pont F, Cruz M, Leon R, Tarrieu LF, Guderian R, Echeverria R, Tibayrenc M (1996) Cryptic speciation in Lutzomyia (Nyssomyia) trapidoi (Fairchild & Hertig) (Diptera: Psychodidae) detected by multilocus enzyme electrophoresis. Am J Trop Med Hyg 54(1):42–45PubMedCrossRefPubMedCentralGoogle Scholar
  49. Dvorak V, Halada P, Hlavackova K, Dokianakis E, Antoniou M, Volf P (2014) Identification of phlebotomine sand flies (Diptera: Psychodidae) by matrix-assisted laser desorption/ionization time of flight mass spectrometry. Parasit Vectors 7:21PubMedPubMedCentralCrossRefGoogle Scholar
  50. Esseghir S, Ready PD, Killick-Kendrick R, Ben-Ismail R (1997) Mitochondrial haplotypes and phylogeography of Phlebotomus vectors of Leishmania major. Insect Mol Biol 6:211–225PubMedCrossRefPubMedCentralGoogle Scholar
  51. Esseghir S, Ready PD, Ben-Ismail R (2000) Speciation of Phlebotomus sandflies of the subgenus Larroussius coincided with the late Miocene-Pliocene aridification of the Mediterranean subregion. Biol J Linn Soc 70:189–219CrossRefGoogle Scholar
  52. Ferreira TS, Minuzzi-Souza TT, Andrade AJ, Coelho TO, Rocha Dde A, Obara MT, Hecht M, Nitz N, Gurgel-Gonçalves R (2015) Molecular detection of Trypanosoma sp. and Blastocrithidia sp. (Trypanosomatidae) in phlebotomine sand flies (Psychodidae) in the Federal District of Brazil. Rev Soc Bras Med Trop 48(6):776–779CrossRefGoogle Scholar
  53. Gaio Ade O, Rodrigues RC, do Nascimento C, Secundino NF, Lemos FJ, Pimenta PF, Monesi N (2011) Use of the checkerboard DNA-DNA hybridization technique for bacteria detection in Aedes aegypti (Diptera:Culicidae) (L.) Parasit Vectors 4:237PubMedCrossRefPubMedCentralGoogle Scholar
  54. Galati EAB (1995) Philogenetic systematics of the Phlebotominae (Diptera, Psychodidae) with emphasis on American groups. Bol Mal Salud Amb 35(Suppl. 1):133–142Google Scholar
  55. Galati EAB (2003) Morfologia e taxonomia: classificação de Phlebotominae. In: Rangel EF, Lainson R (eds) Flebotomíneos do Brasil. Fiocruz, Rio de Janeiro, pp 23–51Google Scholar
  56. Galati EA, Fonseca MB, Marassá AM (2007) The subgenus Migonemyia Galati 1995 (Diptera, Psychodidae, Phlebotominae), with description of a new species Migonemyia vaniae: a review. Mem Inst Oswaldo Cruz 102(5):605–615PubMedCrossRefPubMedCentralGoogle Scholar
  57. Gesto JSM, Rivas GB, Pavan MG, Meireles-Filho ACA, Amoretty PR, Souza NA, Bruno RV, Peixoto AA (2015) Clocks do not tick in unison: isolation of Clock and vrille shed new light on the clockwork model of the sand fly Lutzomyia longipalpis. Parasit Vectors 8:505PubMedPubMedCentralCrossRefGoogle Scholar
  58. Giantsis IA, Chaskopoulou A, Bon MC (2016) Mild-vectolysis: a nondestructive DNA extraction method for vouchering sand flies and mosquitoes. J Med Entomol 53(3):692–695PubMedCrossRefPubMedCentralGoogle Scholar
  59. Gil LH, Basano SA, Souza AA, Silva MG, Barata I, Ishikawa EA, Camargo LM, Shaw JJ (2003) Recent observations on the sand fly (Diptera: Psychodidae) fauna of the State of Rondônia, Western Amazônia, Brazil: the importance of Psychdopygus davisi as a vector of zoonotic cutaneous leishmaniasis. Mem Inst Oswaldo Cruz 98(6):751–5PubMedCrossRefPubMedCentralGoogle Scholar
  60. Grace-Lema D, Yared S, Quitadamo A, Janies D, Wheeler WC, Balkew M, Hailu A, Warburg A, Clouse RM (2015) A phylogeny of sand flies (Diptera: Psychodidae: Phlebotominae), using recent Ethiopian collections and a broad selection of publicly available DNA sequence data. Syst Entomol 40(4):733–744CrossRefGoogle Scholar
  61. Hamilton JG, Ward RD (1991) Gas-chromatographic analysis of Lutzomyia longipalpis tergal pheromone gland extract. Parassitologia 33(Suppl):283–289PubMedPubMedCentralGoogle Scholar
  62. Hamilton JG, Ward RD (1994) Chemical analysis of a putative sex pheromone from Lutzomyia pessoai (Diptera: Psychodidae). Ann Trop Med Parasitol 88(4):405–412CrossRefPubMedGoogle Scholar
  63. Hamilton JG, Dougherty MJ, Ward RD (1994) Sex pheromone activity in a single component of tergal gland extract of Lutzomyia longipalpis (Diptera: Psychodidae) from Jacobina. J Chem Ecol 20:141–151PubMedCrossRefPubMedCentralGoogle Scholar
  64. Hamilton JGC, Dawson GW, Pickett JA (1996a) 9-Methyl-germacrene B: proposed structure for novel homosesquiterpene from the sex pheromone glands of Lutzomyia longipalpis (Diptera: Psychodidae) from Lapinha, Brazil. J Chem Ecol 22:1477–1491PubMedCrossRefPubMedCentralGoogle Scholar
  65. Hamilton JGC, Dawson GW, Pickett JA (1996b) 3-Methyl-a-himachalene: Proposed structure for novel homosesquiterpene sex pheromone of Lutzomyia longipalpis (Diptera: Psychodidae) from Jacobina, Brazil. J Chem Ecol 22:2331–2340PubMedCrossRefPubMedCentralGoogle Scholar
  66. Hamilton JG, Brazil RP, Campbell-Lendrum D, Davies CR, Kelly DW, Pessoa FA, de Queiroz RG (2002) Distribution of putative male sex pheromones among Lutzomyia sandflies (Diptera: Psychodidae). Ann Trop Med Parasitol 96(1):83–92PubMedCrossRefPubMedCentralGoogle Scholar
  67. Hamilton JG, Brazil RP, Maingon R (2004) A fourth chemotype of Lutzomyia longipalpis (Diptera: Psychodidae) from Jaiba, Minas Gerais state, Brazil. J Med Entomol 41(6):1021–1026PubMedCrossRefPubMedCentralGoogle Scholar
  68. Hamilton JG, Maingon RD, Alexander B, Ward RD, Brazil RP (2005) Analysis of the sex pheromone extracts of individual male Lutzomyia longipalpis sandflies from six regions in Brazil. Med Vet Entomol 19(4):480–488PubMedCrossRefPubMedCentralGoogle Scholar
  69. Hartl DL, Clark AG (2007) Principles of population genetics, 4th edn. Sunderland, Sinauer AssociatesGoogle Scholar
  70. Hebert PD, Ratnasingham S, de Waard JR (2003) Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. Proc Biol Sci 270(Suppl 1):S96–S99PubMedPubMedCentralCrossRefGoogle Scholar
  71. Hodgkinson VH, Birungi J, Haghpanah M, Joshi S, Munstermann LE (2002) Rapid identification of mitochondrial cytochrome B haplotypes by single strand conformation polymorphism in Lutzomyia longipalpis (Diptera: Psychodidae) populations. J Med Entomol 39:689–694PubMedCrossRefPubMedCentralGoogle Scholar
  72. Hodgkinson VH, Birungi J, Quintana M, Dietze R, Munstermann LE (2003) Mitochondrial cytochrome b variation in populations of the visceral leishmaniasis vector Lutzomyia longipalpis across eastern Brazil. Am J Trop Med Hyg 69(4):386–392PubMedPubMedCentralCrossRefGoogle Scholar
  73. Ishikawa EA, Ready PD, de Souza AA, Day JC, Rangel EF, Davies CR, Shaw JJ (1999) A mitochondrial DNA phylogeny indicates close relationships between populations of Lutzomyia whitmani (Diptera: Psychodidae, Phlebotominae) from the rain-forest regions of Amazônia and northeast Brazil. Mem Inst Oswaldo Cruz 94(3):339–345PubMedCrossRefPubMedCentralGoogle Scholar
  74. Jochim RC, Teixeira CR, Laughinghouse A, Mu J, Oliveira F et al (2008) The midgut transcriptome of Lutzomyia longipalpis: comparative analysis of cDNA libraries from sugar-fed, blood-fed, post-digested and Leishmania infantum chagasi-infected sand flies. BMC Genomics 9:15PubMedPubMedCentralCrossRefGoogle Scholar
  75. Johansson BG, Jones TM (2007) The role of chemical communication in mate choice. Biol Rev Camb Philos Soc 82(2):265–289PubMedCrossRefPubMedCentralGoogle Scholar
  76. Kocher A, Gantier JC, Holota H, Jeziorski C, Coissac E, Bañuls AL, Girod R, Gaborit P, Murienne J (2016) Complete mitochondrial genome of Lutzomyia (Nyssomyia) umbratilis (Diptera: Psychodidae), the main vector of Leishmania guyanensis. Mitochondrial DNA A DNA Mapp Seq Anal 27(6):4219–4221PubMedPubMedCentralGoogle Scholar
  77. Kocher A, Gantier JC, Gaborit P, Zinger L, Holota H, Valiere S, Dusfour I, Girod R, Bañuls AL, Murienne J (2017) Vector soup: high-throughput identification of Neotropical phlebotomine sand flies using metabarcoding. Mol Ecol Resour 17(2):172–182PubMedCrossRefPubMedCentralGoogle Scholar
  78. Kreutzer RD, Palau MT, Morales A, Ferro C, Feliciangeli D, Young DG (1990) Genetic relationships among phlebotomine sand flies (Diptera: Psychodidae) in the verrucarum species group. J Med Entomol 27(1):1–8PubMedCrossRefPubMedCentralGoogle Scholar
  79. Kuwahara K, Kato H, Gomez EA, Uezato H, Mimori T, Yamamoto Y, Calvopina M, Caceres AG, Iwata H, Hashiguchi Y (2009) Genetic diversity of ribosomal RNA internal transcribed spacer sequences in Lutzomyia species from areas endemic for New World cutaneous leishmaniasis. Acta Trop 112:131–136PubMedCrossRefPubMedCentralGoogle Scholar
  80. Kyriacou CP, Hall JC (1980) Circadian rhythm mutations in Drosophila affect short-term fluctuations in the male’s court- ship song. Proc Natl Acad Sci U S A 77:6729–6733PubMedPubMedCentralCrossRefGoogle Scholar
  81. Lampo M, Torgerson D, Márquez LM, Rinaldi M, García CZ, Arab A (1999) Occurrence of sibling species of Lutzomyia longipalpis (Diptera: Psychodidae) in Venezuela: first evidence from reproductively isolated sympatric populations. Am J Trop Med Hyg 61(6):1004–1009PubMedCrossRefPubMedCentralGoogle Scholar
  82. Lane RP, Phillips A, Molyneux DH, Procter C, Ward RD (1985) Chemical analysis of the abdominal glands of two forms of the Lutzomyia longipalpis: site of a possible sex pheromone? Ann Trop Med Parasit 79:225–229PubMedCrossRefPubMedCentralGoogle Scholar
  83. Lanzaro GC, Warburg A (1995) Genetic variability in phlebotomine sandf lies: possible implications for leishmaniasis epidemiology. Parasitol Today 11:151–154CrossRefGoogle Scholar
  84. Lanzaro GC, Ostrovska K, Herrero MV, Lawyer PG, Warburg A (1993) Lutzomyia longipalpis is a species complex: genetic divergence and interspecific hybrid sterility among three populations. Am J Trop Med Hyg 48(6):839–847PubMedCrossRefPubMedCentralGoogle Scholar
  85. Lanzaro GC, Lopes AH, Ribeiro JM, Shoemaker CB, Warburg A, Soares M et al (1999) Variation in the salivary peptide, maxadilan, from species in the Lutzomyia longipalpis complex. Insect Mol Biol 8(2):267–275PubMedCrossRefPubMedCentralGoogle Scholar
  86. Lerner EA, Ribeiro JM, Nelson RJ, Lerner MR (1991) Isolation of maxadilan, a potent vasodilatory peptide from the salivary glands of the sand fly Lutzomyia longipalpis. J Biol Chem 266(17):11234–11236PubMedPubMedCentralGoogle Scholar
  87. Lewis DJ, Young DG, Fairchild GB, Minter DM (1977) Proposals for a stable classification of the phlebotomine sandflies (Diptera: Psychodidae). Syst Entomol 2:319–332CrossRefGoogle Scholar
  88. Lima-Costa CR Jr, Freitas MT, Figueredo CAS Jr, Aragão NC, da Silva LG, Marcondes CB et al (2015) Genetic structuring and fixed polymorphisms in the period among natural populations of Lutzomyia longipalpis in Brazil. Parasit Vectors 8:193PubMedPubMedCentralCrossRefGoogle Scholar
  89. Lins RM, Oliveira SG, Souza NA, de Queiroz RG, Justiniano SC, Ward RD, Kyriacou CP, Peixoto AA (2002) Molecular evolution of the cacophony IVS6 region in sandflies. Insect Mol Biol 11:117–122PubMedCrossRefPubMedCentralGoogle Scholar
  90. Lins RMMA, Souza NA, Peixoto AA (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. Mem Inst Oswaldo Cruz 103(7):736–740PubMedCrossRefPubMedCentralGoogle Scholar
  91. Lins RM, Souza NA, Brazil RP, Maingon RD, Peixoto AA (2012) Fixed differences in the paralytic gene define two lineages within the Lutzomyia longipalpis complex producing different types of courtship songs. PLoS One 7(9):e44323PubMedPubMedCentralCrossRefGoogle Scholar
  92. Mahamdallie SS, Pesson B, Ready PD (2011) Multiple genetic divergences and population expansions of a Mediterranean sandfly, Phlebotomus ariasi, in Europe during the Pleistocene glacial cycles. Heredity 106:714–726PubMedCrossRefPubMedCentralGoogle Scholar
  93. Maingon RD, Ward RD, Hamilton JG, Noyes HA, Souza N, Kemp SJ et al (2003) Genetic identification of two sibling species of Lutzomyia longipalpis (Diptera: Psychodidae) that produce distinct male sex pheromones in Sobral, Ceará state, Brazil. Mol Ecol 12(7):1879–1894PubMedCrossRefPubMedCentralGoogle Scholar
  94. Maingon RD, Ward RD, Hamilton JG, Bauzer LG, Peixoto AA (2008) The Lutzomyia longipalpis species complex: does population sub-structure matter to Leishmania transmission? Trends Parasitol 24(1):12–17PubMedCrossRefPubMedCentralGoogle Scholar
  95. Marassá AM, Galati EA, Bergamaschi DP, Consales CA (2013) Blood feeding patterns of Nyssomyia intermedia and Nyssomyia neivai (Diptera, Psychodidae) in a cutaneous leishmaniasis endemic area of the Ribeira Valley, State of São Paulo, Brazil. Rev Soc Bras Med Trop 46(5):547–554PubMedCrossRefPubMedCentralGoogle Scholar
  96. Marcondes CB (1996) A redescription of Lutzomyia (Nyssomyia) intermedia (Lutz & Neiva, 1912), and resurrection of L. neivai (Pinto, 1926) (Diptera, Psychodidae, Phlebotominae). Mem Inst Oswaldo Cruz 91(4):457–462CrossRefGoogle Scholar
  97. Marcondes C, Day J, Ready PD (1997) Introgression between Lutzomyia intermedia and both Lu. Neivai and Lu. whitmani, and their roles as vectors of Leishmania braziliensis. Trans R Soc Trop Med Hyg 91:725–726PubMedCrossRefPubMedCentralGoogle Scholar
  98. Margonari CS, Fortes-Dias CL, Dias ES (2004) Genetic variability in geographical populations of Lutzomyia whitmani elucidated by RAPD-PCR. J Med Entomol 41:187–192PubMedCrossRefPubMedCentralGoogle Scholar
  99. Mathis A, Depaquit J, Dvořák V, Tuten H, Bañuls AL, Halada P, Zapata S, Lehrter V, Hlavačková K, Prudhomme J, Volf P, Sereno D, Kaufmann C, Pflüger V, Schaffner F (2015) Identification of phlebotomine sand flies using one MALDI-TOF MS reference database and two mass spectrometer systems. Parasit Vectors 8:266PubMedPubMedCentralCrossRefGoogle Scholar
  100. Mazzoni CJ, Gomes CA, Souza NA, de Queiroz RG, Justiniano SC, Ward RD, Kyriacou CP, Peixoto AA (2002) Molecular evolution of the period gene in sandflies. J Mol Evol 55:553–562PubMedCrossRefPubMedCentralGoogle Scholar
  101. Mazzoni CJ, Souza NA, Andrade-Coelho C, Kyriacou CP, Peixoto AA (2006) Molecular polymorphism, differentiation and introgression in the period gene between Lutzomyia intermedia and Lutzomyia whitmani. BMC Evol Biol 6:85PubMedPubMedCentralCrossRefGoogle Scholar
  102. Mazzoni CJ, Araki AS, Ferreira GE, Azevedo RV, Barbujani G, Peixoto AA (2008) Multilocus analysis of introgression between two sand fly vectors of leishmaniasis. BMC Evol Biol 8:141PubMedPubMedCentralCrossRefGoogle Scholar
  103. McAvin JC, Swanson KI, Chan AS, Quintana M, Coleman RE (2012) Leishmania detection in sand flies using a field-deployable real-time analytic system. Mil Med 177(4):460–466PubMedCrossRefPubMedCentralGoogle Scholar
  104. McIntyre S, Rangel EF, Ready PD, Carvalho BM (2017) Species-specific ecological niche modelling predicts different range contractions for Lutzomyia intermedia and a related vector of Leishmania braziliensis following climate change in South America. Parasit Vectors 10(1):157PubMedPubMedCentralCrossRefGoogle Scholar
  105. Meireles-Filho ACA, Kyriacou CP (2013) Circadian rhythms in insect disease vectors. Mem Inst Oswaldo Cruz 108(Suppl. 1):48–58PubMedPubMedCentralCrossRefGoogle Scholar
  106. Meireles-Filho ACA, Amoretty PR, Souza NA, Kyriacou CP, Peixoto AA (2006) Rhythmic expression of the cycle gene in a hematophagous insect vector. BMC Mol Biol 7:38PubMedPubMedCentralCrossRefGoogle Scholar
  107. Mendoza-Viveros L, Bouchard-Cannon P, Hegazi S, Cheng AH, Pastore S, Cheng H-YM (2017) Molecular modulators of the circadian clock: lessons from flies and mice. Cell Mol Life Sci 74:1035–1059PubMedCrossRefPubMedCentralGoogle Scholar
  108. Meneses CR, Cupolillo E, Monteiro F, Rangel EF (2005) Micro-geographical variation among male populations of the sandfly, Lutzomyia (Nyssomyia) intermedia, from an endemic area of American cutaneous leishmaniasis in the state of Rio de Janeiro, Brazil. Med Vet Entomol 19:38–47PubMedCrossRefPubMedCentralGoogle Scholar
  109. Miles M, Ward RD (1978) Preliminary isoenzyme studies on phlebotomine sandflies (Diptera: Psychodidae). Ann Trop Med Parasitol 72:398–400PubMedCrossRefPubMedCentralGoogle Scholar
  110. Milleron RS, Ribeiro JM, Elnaime D, Soong L, Lanzaro GC (2004) Negative effect of antibodies against maxadilan on the fitness of the sand fly vector of American visceral leishmaniasis. Am J Trop Med Hyg 70:278–285PubMedPubMedCentralCrossRefGoogle Scholar
  111. Monteiro CC, Villegas LE, Campolina TB, Pires AC, Miranda JC, Pimenta PF, Secundino NF (2016) Bacterial diversity of the American sand fly Lutzomyia intermedia using high-throughput metagenomic sequencing. Parasit Vectors 9:480PubMedPubMedCentralCrossRefGoogle Scholar
  112. Morton IE, Ward RD (1989) Laboratory response of female Lutzomyia longipalpis sandflies to a host and male pheromone source over distance. Med Vet Entomol 3:219–223PubMedPubMedCentralCrossRefGoogle Scholar
  113. Mukhopadhyay J, Ghosh K, Azevedo AC, Rangel EF, Munstermann LE (1998a) Genetic polymorphism of morphological and biochemical characters in a Natal, Brazil, population of Lutzomyia longipalpis (Diptera: Psychodidae). J Am Mosq Control Assoc 14(3):277–282PubMedPubMedCentralGoogle Scholar
  114. Mukhopadhyay J, Ghosh K, Rangel EF, Munstermann LE (1998b) Genetic variability in biochemical characters of Brazilian field populations of the Leishmania vector, Lutzomyia longipalpis (Diptera: Psychodidae). Am J Trop Med Hyg 59:893–901PubMedCrossRefPubMedCentralGoogle Scholar
  115. Munstermann LE, Morrison AC, Ferro C, Pardo R, Torres M (1998) Genetic structure of local populations of Lutzomyia longipalpis (Diptera: Psychodidae) in central Colombia. J Med Entomol 35:82–89PubMedCrossRefPubMedCentralGoogle Scholar
  116. Mutebi JP, Rowton E, Herrero MV, Ponce C, Belli A, Valle S et al (1998) Genetic variability among populations of the sand fly Lutzomyia (Lutzomyia) longipalpis (Diptera: Psychodidae) from Central America. J Med Entomol 35(2):169–174PubMedCrossRefPubMedCentralGoogle Scholar
  117. Mutebi JP, Alexander B, Sherlock I, Wellington J, Souza AA, Shaw J et al (1999) Breeding structure of the sandfly Lutzomyia longipalpis (Lutz & Neiva) in Brazil. Am J Trop Med Hyg 61:149–157PubMedCrossRefPubMedCentralGoogle Scholar
  118. Neitzke-Abreu HC, Reinhold-Castro KR, Venazzi MS, Scodro RB, Dias Ade C, Silveira TG, Teodoro U, Lonardoni MV (2014) Detection of Leishmania (Viannia) in Nyssomyia neivai and Nyssomyia whitmani by multiplex polymerase chain reaction, in Southern Brazil. Rev Inst Med Trop Sao Paulo 56(5):391–395PubMedPubMedCentralCrossRefGoogle Scholar
  119. Oliveira SG, Bottecchia M, Bauzer LGSR, Souza NA, Ward RD, Kyriacou CP et al (2001) Courtship song genes and speciation in sand flies. Mem Inst Oswaldo Cruz 96(3):403–405PubMedCrossRefPubMedCentralGoogle Scholar
  120. Oliveira F, Kamhawi S, Seitz AE, Pham VM, Guigal PM, Fischer L, Ward J, Valenzuela JG (2006) From transcriptome to immunome: identification of DTH inducing proteins from a Phlebotomus ariasi salivary gland cDNA library. Vaccine 24(3):374–390PubMedCrossRefPubMedCentralGoogle Scholar
  121. Oliveira F, Lawyer PG, Kamhawi S, Valenzuela JG (2008) Immunity to distinct sand fly salivary proteins primes the anti-Leishmania immune response towards protection or exacerbation of disease. PLoS Negl Trop Dis 2(4):e226PubMedPubMedCentralCrossRefGoogle Scholar
  122. Peixoto AA, Hall JC (1998) Analysis of temperature- sensitive mutants reveals new genes involved in the courtship song of Drosophila. Genetics 148:827–838PubMedPubMedCentralGoogle Scholar
  123. Pesson B, Ready JS, Benabdennbi I, Martin-Sanchez J, Esseghir S et al (2004) Sandflies of the Phlebotomus perniciosus complex: mitochondrial introgression and a new sibling species of P. longicuspis in the Moroccan Rif. Med Vet Entomol 18:25–37PubMedCrossRefPubMedCentralGoogle Scholar
  124. Phillips A, Ward R, Ryan L (1986) Chemical analysis of compounds extracted from the tergal “spots” of “Lutzomyia longipalpis” from Brazil. Acta Trop 43:271–276PubMedPubMedCentralGoogle Scholar
  125. Pinto MC, Campbell-Lendrum DH, Lozovei AL, Teodoro U, Davies CR (2001) Phlebotomine sandfly responses to carbon dioxide and human odour in the field. Med Vet Entomol 15(2):132–139PubMedCrossRefPubMedCentralGoogle Scholar
  126. Pinto IS, das Chagas BD, Rodrigues AAF, Ferreira AL, Rezende HR, Bruno RV et al (2015) DNA barcoding of neotropical sand flies (Diptera, Psychodidae, Phlebotominae): species identification and discovery within Brazil. PLoS One 10(10):e0140636PubMedCentralCrossRefGoogle Scholar
  127. Pita-Pereira D, Souza GD, Zwetsch A, Alves CR, Britto C, Rangel EF (2009) First report of Lutzomyia (Nyssomyia) neivai (Diptera: Psychodidae: Phlebotominae) naturally infected by Leishmania (Viannia) braziliensis in a periurban area of south Brazil using a multiplex polymerase chain reaction assay. Am J Trop Med Hyg 80(4):593–595PubMedPubMedCentralCrossRefGoogle Scholar
  128. Pittendrigh B, Reenan R, ffrench-Constant RH, Ganetzky B (1997) Point mutations in the Drosophila sodium channel gene para associated with resistance to DDT and pyrethroid insecticides. Mol Gen Genet 256:602–610PubMedCrossRefPubMedCentralGoogle Scholar
  129. Puillandre N, Lambert A, Brouillet S, Achaz G (2012) ABGD, Automatic Barcode Gap Discovery for primary species delimitation. Mol Ecol 21(8):1864–1877PubMedCrossRefPubMedCentralGoogle Scholar
  130. Ranasinghe S, Rogers ME, Hamilton JG, Bates PA, Maingon RD (2008) A real-time PCR assay to estimate Leishmania chagasi load in its natural sand fly vector Lutzomyia longipalpis. Trans R Soc Trop Med Hyg 102(9):875–882PubMedPubMedCentralCrossRefGoogle Scholar
  131. Rangel EF, Lainson R (2009) Proven and putative vectors of American cutaneous leishmaniasis in Brazil: aspects of their biology and vectorial competence. Mem Inst Oswaldo Cruz 104:937–954PubMedPubMedCentralCrossRefGoogle Scholar
  132. Rangel EF, Lainson R, Souza AA, Ready P, Azevedo AC (1996) Variation between geographical populations of Lutzomyia (Nyssomyia) whitmani (Antunes & Coutinho, 1939) sensu lato (Diptera: Psychodidae: Phlebotominae) in Brazil. Mem Inst Oswaldo Cruz 91(1):43–50PubMedCrossRefPubMedCentralGoogle Scholar
  133. Ready PD (2011) Should sandfly taxonomy predict vectorial and ecological traits? J Vector Ecol 36:S17–S32PubMedCrossRefPubMedCentralGoogle Scholar
  134. Ready PD (2013) Biology of phlebotomine sand flies as vectors of disease agents. Annu Rev Entomol 58:227–250PubMedCrossRefPubMedCentralGoogle Scholar
  135. Ready PD, Rangel R (2003) Caracteres Isoenzimáticos e Moleculares: espécies crípticas. In: Rangel EF, Lainson R (eds) Flebotomíneos do Brasil. Editora Fiocruz, Rio de JaneiroGoogle Scholar
  136. Ready PD, Silva RMR (1984) An alloenzymic comparison of Psychodopygus wellcomei (Diptera: Psychodidae) – an incriminated vector of Leishmania braziliensis in Pará State, Brazil – and the sympatric morphospecies Ps. complexus (Diptera: Psychodidae). Cahiers Orstom ser Entomol Med Parasitol 22:3–8Google Scholar
  137. Ready PD, Lainson R, Shaw JJ (1984) Habitat and seasonality of Psychodopygus wellcomei help incriminate it as a vector of Leishmania braziliensis in Amazonia and northeast Brazil. Trans R Soc Trop Med Hyg 78:543–544PubMedCrossRefPubMedCentralGoogle Scholar
  138. Ready PD, Lainson R, Shaw JJ, Ward RD (1986) The ecology of Lutzomyia umbratilis Ward & Fraiha (Diptera: Psychodidae), the major vector to man of Leishmania braziliensis guyanensis in north-eastern Amazonian Brazil. Bull Entom Res 76:21–40CrossRefGoogle Scholar
  139. Ready PD, Smith DF, Killick-Kendrick R (1988) DNA hybridizations on squash-blotted sandflies to identify both Phlebotomus papatasi and infecting Leishmania major. Med Vet Entomol 2(2):109–116PubMedCrossRefPubMedCentralGoogle Scholar
  140. Ready PD, Lainson R, Shaw JJ, Souza AA (1991) DNA probes for distinguishing Psychodopygus wellcomei from Psychodopygus complexus (Diptera: Psychodidae). Mem Inst Oswaldo Cruz 86:41–49PubMedCrossRefPubMedCentralGoogle Scholar
  141. Ready PD, Day JC, de Souza AA, Rangel EF, Davies CR (1997) Mitochondrial DNA characterization of populations of Lutzomyia whitmani (Diptera: Psychodidae) incriminated in the peri-domestic and silvatic transmission of Leishmania species in Brazil. Bull Entomol Res 87:187–195CrossRefGoogle Scholar
  142. Ready PD, de Souza AA, Rebelo JM, Day JC, Silveira FT, Campbell-Lendrum D, Davies CR, Costa JM (1998) Phylogenetic species and domesticity of Lutzomyia whitmani at the southeast boundary of Amazonian Brazil. Trans R Soc Trop Med Hyg 92(2):159–160PubMedCrossRefPubMedCentralGoogle Scholar
  143. Ribolla PE, Gushi LT, Pires E Cruz Mdo S, Costa CH, Costa DL, Lima Júnior MS, Dorval ME, Gutierrez de Oliveira A, da Cunha Santos MF, Fonseca Camargo-Neves VL, Fortaleza CM, Alonso DP (2016) Leishmania infantum genetic diversity and Lutzomyia longipalpis Mitochondrial Haplotypes in Brazil. Biomed Res Int 16:9249217Google Scholar
  144. Richardson BJ, Baverstock PR, Adams M (1990) Allozyme electrophoresis. A handbook for animal systematics and population studies. Academic Press, New YorkGoogle Scholar
  145. Ritchie MG, Halsey EJ, Gleason JM (1999) Drosophila song as a species-specific mating signal and the behavioural importance of Kyriacou & Hall cycles in D. melanogaster song. Anim Behav 58:649–657PubMedCrossRefPubMedCentralGoogle Scholar
  146. Romero-Ricardo L, Lastre-Meza N, Pérez-Doria A, Bejarano EE (2016) DNA barcoding to identify species of phlebotomine sand fly (Diptera: Psychodidae) in the mixed leishmaniasis focus of the Colombian Caribbean. Acta Trop 159:125–131PubMedCrossRefPubMedCentralGoogle Scholar
  147. Ryan L, Phillips A, Milligan P, Lainson R, Molyneux DH, Shaw JJ (1986) Separation of female Psychodopygus wellcomei and P. complexus (Diptera: Psychodidae) by cuticular hydrocarbon analysis. Acta Trop 43:85–89PubMedPubMedCentralGoogle Scholar
  148. Sakai T, Ishida N (2001) Circadian rhythms of female mating activity governed by clock genes in Drosophila. Proc Natl Acad Sci USA 98:9221–9225PubMedPubMedCentralCrossRefGoogle Scholar
  149. Sant'Anna MR, Jones NG, Hindley JA, Mendes-Sousa AF, Dillon RJ, Cavalcante RR, Alexander B, Bates PA (2008) Blood meal identification and parasite detection in laboratory-fed and field-captured Lutzomyia longipalpis by PCR using FTA databasing paper. Acta Trop 107(3):230–237PubMedPubMedCentralCrossRefGoogle Scholar
  150. Scarpassa VM, Alencar RB (2012) Lutzomyia umbratilis, the main vector of Leishmania guyanensis, represents a novel species complex? PLoS One 7:e37341PubMedPubMedCentralCrossRefGoogle Scholar
  151. Scarpassa VM, Alencar RB (2013) Molecular taxonomy of the two Leishmania vectors Lutzomyia umbratilis and Lutzomyia anduzei (Diptera: Psychodidae) from the Brazilian Amazon. Parasit Vectors 6:258PubMedPubMedCentralCrossRefGoogle Scholar
  152. Scarpassa VM, Figueiredo Ada S, Alencar RB (2015) Genetic diversity and population structure in the Leishmania guyanensis vector Lutzomyia anduzei (Diptera, Psychodidae) from the Brazilian Amazon. Infect Genet Evol 31:312–320PubMedCrossRefPubMedCentralGoogle Scholar
  153. Simon C, Frati F, Beckenbach A, Crespi B, Liu H, Flook P (1994) Evolution, Weighting, and Phylogenetic Utility of Mitochondrial Gene Sequences and a Compilation of Conserved Polymerase Chain Reaction Primers. Ann Entomol Soc Am 87(6):651–701CrossRefGoogle Scholar
  154. Smith LA, Peixoto AA, Kramer EM, Villella A, Hall JC (1998) Courtship and visual defects of cacophony mutants reveal functional complexity of a calcium-channel α-1 subunit in Drosophila. Genetics 149:1407–1426PubMedPubMedCentralGoogle Scholar
  155. Soares VY, Silva JC, Silva KR, Pires e Cruz Mdo S, Santos MP, Ribolla PE, Alonso DP, Coelho LF, Costa DL, Costa CH (2014) Identification of blood meal sources of Lutzomyia longipalpis using polymerase chain reaction-restriction fragment length polymorphism analysis of the cytochrome B gene. Mem Inst Oswaldo Cruz 109(3):379–383PubMedPubMedCentralCrossRefGoogle Scholar
  156. Soto SI, Lehmann T, Rowton ED, Vélez BID, Porter CH (2001) Speciation and population structure in the morphospecies Lutzomyia longipalpis (Lutz & Neiva) as derived from the mitochondrial ND4 gene. Mol Phylogenet Evol 18(1):84–93PubMedCrossRefPubMedCentralGoogle Scholar
  157. Souza NA, Vigoder FM, Araki AS, Ward RD, Kyriacou CP, Peixoto AA (2004) Analysis of the copulatory courtship songs of Lutzomyia longipalpis in six populations from Brazil. J Med Entomol 41:906–913PubMedPubMedCentralCrossRefGoogle Scholar
  158. Souza NA, Andrade-Coelho CA, Vigoder FM, Ward RD, Peixoto AA (2008) Reproductive isolation between sympatric and allopatric Brazilian populations of Lutzomyia longipalpis s.l. (Diptera: Psychodidae). Mem Inst Oswaldo Cruz 103(2):216–219PubMedCrossRefPubMedCentralGoogle Scholar
  159. Souza NA, Andrade-Coelho CA, Silva VC, Ward RD, Peixoto AA (2009) Life cycle differences among Brazilian sandflies of the Lutzomyia longipalpis sibling species complex. Med Vet Entomol 23(3):287–292PubMedCrossRefPubMedCentralGoogle Scholar
  160. Souza NA, Brazil RP, Araki AS (2017) The current status of the Lutzomyia longipalpis (Diptera: Psychodidae: Phlebotominae) species complex. Mem Inst Oswaldo Cruz 112(3):161–174PubMedPubMedCentralCrossRefGoogle Scholar
  161. Spiegel CN, Dias DBS, Araki AS, Hamilton JGC, Brazil RP, Jones TM (2016) The Lutzomyia longipalpis complex: a brief natural history of aggregation-sex pheromone communication. Parasit Vectors 9:580PubMedPubMedCentralCrossRefGoogle Scholar
  162. Tabbabi A, Rhim A, Ghrab J, Martin O, Aoun K, Bouratbine A, Ready PD (2014) Phlebotomus (Paraphlebotomus) riouxi: a synonym of Phlebotomus chabaudi without any proven vectorial role in Tunisia and Algeria. Med Vet Entomol 28S(1):51–59CrossRefGoogle Scholar
  163. Telleria EL, Sant’anna MR, Ortigão-Farias JR, Pitaluga AN, Dillon VM et al (2012) Caspar-like gene depletion reduces Leishmania infection in the sand fly host Lutzomyia longipalpis. J Biol Chem e:28Google Scholar
  164. Terayama Y, Kato H, Gomez EA, Uezato H, Calvopina M, Iwata H, Hashiguchi Y (2008) Molecular typing of sand fly species (Diptera, Psychodidae, Phlebotominae) from areas endemic for Leishmaniasis in Ecuador by PCR-RFLP of 18S ribosomal RNA gene. J Vet Med Sci 70:907–913PubMedCrossRefPubMedCentralGoogle Scholar
  165. Testa JM, Montoya-Lerma J, Cadena H, Oviedo M, Ready PD (2002) Molecular identification of vectors of Leishmania in Colombia: mitochondrial introgression in the Lutzomyia townsendi series. Acta Trop 84:205–218PubMedCrossRefPubMedCentralGoogle Scholar
  166. Tibayrenc M, Carriou ML, Corneau B, Pajot FX (1980) Etude allozymique chez Lutzomyia umbratilis (Diptera, Psychodidae), vecteur de la leishmaniose en Guyane française. Cahiers Orstom ser Entomol Med Parasitol 18:67–70Google Scholar
  167. Ting CT, Tsaur SC, Wu CI (2000) The phylogeny of closely related species as revealed by the genealogy of a speciation gene, Odysseus. Proc Natl Acad Sci USA 97:5313–5316PubMedPubMedCentralCrossRefGoogle Scholar
  168. Titus RG, Ribeiro JM (1988) Salivary gland lysates from the sand fly Lutzomyia longipalpis enhance Leishmania infectivity. Science 239(4845):1306–1308PubMedPubMedCentralCrossRefGoogle Scholar
  169. Torgerson DG, Lampo M, Velazquez Y, Woo PT (2003) Genetic relationships among some species groups within the genus Lutzomyia (Diptera: Psychodidae). Am J Trop Med Hyg 69:484–493PubMedPubMedCentralCrossRefGoogle Scholar
  170. Valenzuela JG, Garfield M, Rowton ED, Pham VM (2004) Identification of the most abundant secreted proteins from the salivary glands of the sand fly Lutzomyia longipalpis, vector of Leishmania chagasi. J Exp Biol 207(21):3717–3729PubMedCrossRefPubMedCentralGoogle Scholar
  171. Vigoder FM, Araki AS, Bauzer LG, Souza NA, Brazil RP, Peixoto AA (2010a) Lovesongs and period gene polymorphisms indicate Lutzomyia cruzi (Mangabeira, 1938) as a sibling species of the Lutzomyia longipalpis (Lutz and Neiva, 1912) complex. Infect Genet Evol 10(6):734–739PubMedCrossRefPubMedCentralGoogle Scholar
  172. Vigoder FM, Souza NA, Peixoto AA (2010b) Copulatory courtship song in Lutzomyia migonei (Diptera: psychodidae). Mem Inst Oswaldo Cruz 105(8):1065–1067PubMedCrossRefPubMedCentralGoogle Scholar
  173. Vigoder FM, Souza NA, Peixoto AA (2011) Acoustic signals in the sand fly Lutzomyia (Nyssomyia) intermedia (Diptera: Psychodidae). Parasit Vectors 4:76PubMedPubMedCentralCrossRefGoogle Scholar
  174. Vigoder FM, Souza NA, Brazil RP, Bruno RV, Costa LP, Ritchie MG et al (2015) Phenotypic differentiation in love song traits among sibling species of the Lutzomyia longipalpis complex in Brazil. Parasit Vectors 8:290PubMedPubMedCentralCrossRefGoogle Scholar
  175. Vivero RJ, Contreras-Gutierrez MA, Bejarano EE (2007) Analisis de la estructura primaria y secundaria del ARN de transferencia mitocondrial para serina en siete especies de Lutzomyia. Biomedica 27:429–438PubMedCrossRefPubMedCentralGoogle Scholar
  176. Warburg A, Saraiva E, Lanzaro GC, Titus RG, Neva F (1994) Saliva of Lutzomyia longipalpis sibling species differs in its composition and capacity to enhance leishmaniasis. Philos Trans R Soc Lond Ser B Biol Sci 345(1312):223–230CrossRefGoogle Scholar
  177. Ward RD, Morton IE (1991) Pheromones in mate choice and sexual isolation between siblings of Lutzomyia longipalpis (Diptera:Psychodidae). Parassitologia 33(Suppl):527–533PubMedPubMedCentralGoogle Scholar
  178. Ward RD, Ribeiro AL, Ready PD, 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. Mem Inst Oswaldo Cruz 78(3):269–280CrossRefGoogle Scholar
  179. Ward RD, Phillips A, Burnet B, Marcondes CB (1988) The Lutzomyia longipalpis complex: reproduction and distribution. In: Service MW (ed) Biosystematics of haematophagous insects. Systematics Association Special, Clarendon Press, Oxford, UK, pp 257–269Google Scholar
  180. Watts PC, Boyland E, Noyes HA, Maingon RDC, Kemp SJ (2001) Polymorphic dinucleotide microsatellite loci in the sandfly Lutzomyia longipalpis (Diptera: Phlebotominae). Mol Ecol Notes 2:60–61Google Scholar
  181. Watts PC, Hamilton JG, Ward RD, Noyes HA, Souza NA, Kemp SJ et al (2005) Male sex pheromones and the phylogeographic structure of the Lutzomyia longipalpis species complex (Diptera: Psychodidae) from Brazil and Venezuela. Am J Trop Med Hyg 73(4):734–743PubMedPubMedCentralCrossRefGoogle Scholar
  182. Wiebe A, Longbottom J, Gleave K, Shearer FM, Sinka ME, Massey NC, Cameron E, Bhatt S, Gething PW, Hemingway J, Smith DL, Coleman M, Moyes CL (2017) Geographical distributions of African malaria vector sibling species and evidence for insecticide resistance. Malar J 16(1):85PubMedPubMedCentralCrossRefGoogle Scholar
  183. Ye F, Liu T, King SD, You P (2015) Mitochondrial genomes of two phlebotomine sand flies, Phlebotomus chinensis and Phlebotomus papatasi (Diptera: Nematocera), the first representatives from the family Psychodidae. Parasit Vectors 8:472PubMedPubMedCentralCrossRefGoogle Scholar
  184. Yin H, Mutebi JP, Marriott S, Lanzaro GC (1999) Metaphase karyotypes and G-banding in sandflies of the Lutzomyia longipalpis complex. Med Vet Entomol 13(1):72–77PubMedCrossRefPubMedCentralGoogle Scholar
  185. Yin H, Norris DE, Lanzaro GC (2000) Sibling species in the Lutzomyia longipalpis complex differ in levels of mRNA expression for the salivary peptide, maxadilan. Insect Mol Biol 9(3):309–314PubMedCrossRefPubMedCentralGoogle Scholar
  186. Young DG, Duncan MA (1994) Guide to the identification and geographic distribution of Lutzomyia sand flies in Mexico, the West Indies, Central and South America (Diptera: Psychodidae). Mem Amer Ent Inst 54:1–881Google Scholar
  187. Zapata S, Leon R, Sauvage F, Augot D, Trueba G, Cruaud C, Couloux A, Teran R, Depaquit J (2012) Morphometric and molecular characterization of the series Guyanensis (Diptera, Psychodidae, Psychodopygus) from the Ecuadorian Amazon Basin with description of a new species. Infect Genet Evol 12:966–977PubMedCrossRefPubMedCentralGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Paul D. Ready
    • 1
  • Felipe M. Vigoder
    • 2
  • Elizabeth F. Rangel
    • 3
  1. 1.London School of Hygiene and Tropical Medicine, and Natural History MuseumLondonUK
  2. 2.Instituto de BiologiaUniversidade Federal do Rio de JaneiroRio de JaneiroBrazil
  3. 3.Instituto Oswaldo Cruz, Fundação Oswaldo CruzRio de JaneiroBrazil

Personalised recommendations