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Brazilian Sand Flies pp 213–250Cite as

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

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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.

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References

  • 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):e0004771

    Article  PubMed  PubMed Central  Google Scholar 

  • 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):203–207

    Article  PubMed  CAS  Google Scholar 

  • 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):116–122

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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):1272–1277

    Article  PubMed  CAS  Google Scholar 

  • 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 7:52

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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):337–343

    Article  PubMed  Google Scholar 

  • 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):e365

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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):e2495

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Aransay AM, Scoulica E, Tselentis Y, Ready PD (2000) Phylogenetic relationships of phlebotomine sandflies inferred from small subunit nuclear ribosomal DNA. Insect Mol Biol 9:157–168

    Article  PubMed  CAS  Google Scholar 

  • 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 1:176–178

    Article  CAS  Google Scholar 

  • 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 38:783–790

    Article  Google Scholar 

  • 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):83–95

    Article  PubMed  CAS  Google Scholar 

  • 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):615–627

    Article  PubMed  CAS  Google Scholar 

  • Avise JC (2000) Phylogeography: The History and Formation of Species. Harvard University Press, Cambridge, MA, pp 1–447

    Google Scholar 

  • 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):e34495

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 8:131

    Article  PubMed  PubMed Central  Google Scholar 

  • 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):1624–1627

    Article  PubMed  CAS  Google Scholar 

  • 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):315–323

    Article  PubMed  CAS  Google Scholar 

  • 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):1–12

    Article  PubMed  Google Scholar 

  • 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 34:225–234

    Article  PubMed  CAS  Google Scholar 

  • Booth DR, Ready PD, Smith DF (1994) Isolation of non-LTR retrotransposon reverse transcriptase-like sequences from phlebotomine sandflies. Insect Mol Biol 3:89–96

    Article  PubMed  CAS  Google Scholar 

  • Booth DR, Ready PD, Smith DF (1996) Evolution of multiple families of non-LTR retrotransposons in phlebotomine sandflies. Genet Res 67:227–237

    Article  PubMed  CAS  Google Scholar 

  • 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):754–761

    Article  PubMed  CAS  Google Scholar 

  • 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):1197–1200

    Article  PubMed  Google Scholar 

  • 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 46:428–434

    Article  PubMed  CAS  Google Scholar 

  • 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):e2723

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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):435–436

    Article  PubMed  CAS  Google Scholar 

  • 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 23:489–492

    Article  PubMed  CAS  Google Scholar 

  • 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 9:25

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 13:299–309

    Article  PubMed  CAS  Google Scholar 

  • 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 90:41–48

    Article  PubMed  CAS  Google Scholar 

  • 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 22:5084–5097

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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):e0143282

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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):113–115

    Article  PubMed  CAS  Google Scholar 

  • 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):e0003620

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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):15155–15160

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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):913–922

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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:e1000441

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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):e85496

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Day JC, Ready PD (1999) Relative abundance, isolation and structure of phlebotomine microsatellites. Insect Mol Biol 8(4):575–580

    Article  PubMed  CAS  Google Scholar 

  • 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):e2242

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 154:149–154

    Article  PubMed  Google Scholar 

  • 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):112–113

    Article  PubMed  Google Scholar 

  • Depaquit J (2014) Molecular systematics applied to Phlebotomine sandflies: review and perspectives. Infect Genet Evol 28:744–756

    Article  PubMed  Google Scholar 

  • 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 40:49–53

    Article  PubMed  CAS  Google Scholar 

  • 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 88:831–840

    Article  PubMed  CAS  Google Scholar 

  • 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):e1006130

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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):42–45

    Article  PubMed  CAS  Google Scholar 

  • 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 7:21

    Article  PubMed  PubMed Central  Google Scholar 

  • Esseghir S, Ready PD, Killick-Kendrick R, Ben-Ismail R (1997) Mitochondrial haplotypes and phylogeography of Phlebotomus vectors of Leishmania major. Insect Mol Biol 6:211–225

    Article  PubMed  CAS  Google Scholar 

  • 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 70:189–219

    Article  Google Scholar 

  • 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):776–779

    Article  Google Scholar 

  • 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 4:237

    Article  PubMed  CAS  Google Scholar 

  • Galati EAB (1995) Philogenetic systematics of the Phlebotominae (Diptera, Psychodidae) with emphasis on American groups. Bol Mal Salud Amb 35(Suppl. 1):133–142

    Google Scholar 

  • Galati EAB (2003) Morfologia e taxonomia: classificação de Phlebotominae. In: Rangel EF, Lainson R (eds) Flebotomíneos do Brasil. Fiocruz, Rio de Janeiro, pp 23–51

    Google Scholar 

  • 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):605–615

    Article  PubMed  Google Scholar 

  • 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 8:505

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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):692–695

    Article  PubMed  Google Scholar 

  • 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):751–5

    Article  PubMed  Google Scholar 

  • 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):733–744

    Article  Google Scholar 

  • Hamilton JG, Ward RD (1991) Gas-chromatographic analysis of Lutzomyia longipalpis tergal pheromone gland extract. Parassitologia 33(Suppl):283–289

    PubMed  Google Scholar 

  • Hamilton JG, Ward RD (1994) Chemical analysis of a putative sex pheromone from Lutzomyia pessoai (Diptera: Psychodidae). Ann Trop Med Parasitol 88(4):405–412

    Article  CAS  PubMed  Google Scholar 

  • 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 20:141–151

    Article  PubMed  CAS  Google Scholar 

  • 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 22:1477–1491

    Article  PubMed  CAS  Google Scholar 

  • 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 22:2331–2340

    Article  PubMed  CAS  Google Scholar 

  • 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):83–92

    Article  PubMed  CAS  Google Scholar 

  • 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):1021–1026

    Article  PubMed  CAS  Google Scholar 

  • 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):480–488

    Article  PubMed  CAS  Google Scholar 

  • Hartl DL, Clark AG (2007) Principles of population genetics, 4th edn. Sunderland, Sinauer Associates

    Google Scholar 

  • 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–S99

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 39:689–694

    Article  PubMed  CAS  Google Scholar 

  • 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):386–392

    Article  PubMed  CAS  Google Scholar 

  • 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):339–345

    Article  PubMed  CAS  Google Scholar 

  • 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 9:15

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Johansson BG, Jones TM (2007) The role of chemical communication in mate choice. Biol Rev Camb Philos Soc 82(2):265–289

    Article  PubMed  Google Scholar 

  • 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):4219–4221

    PubMed  CAS  Google Scholar 

  • 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):172–182

    Article  PubMed  CAS  Google Scholar 

  • 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):1–8

    Article  PubMed  CAS  Google Scholar 

  • 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 112:131–136

    Article  PubMed  CAS  Google Scholar 

  • 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 77:6729–6733

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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):1004–1009

    Article  PubMed  CAS  Google Scholar 

  • 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 79:225–229

    Article  PubMed  CAS  Google Scholar 

  • Lanzaro GC, Warburg A (1995) Genetic variability in phlebotomine sandf lies: possible implications for leishmaniasis epidemiology. Parasitol Today 11:151–154

    Article  Google Scholar 

  • 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):839–847

    Article  PubMed  CAS  Google Scholar 

  • 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):267–275

    Article  PubMed  CAS  Google Scholar 

  • 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):11234–11236

    PubMed  CAS  Google Scholar 

  • Lewis DJ, Young DG, Fairchild GB, Minter DM (1977) Proposals for a stable classification of the phlebotomine sandflies (Diptera: Psychodidae). Syst Entomol 2:319–332

    Article  Google Scholar 

  • 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 8:193

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 11:117–122

    Article  PubMed  CAS  Google Scholar 

  • 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):736–740

    Article  PubMed  CAS  Google Scholar 

  • 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):e44323

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 106:714–726

    Article  PubMed  CAS  Google Scholar 

  • 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):1879–1894

    Article  PubMed  CAS  Google Scholar 

  • 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):12–17

    Article  PubMed  Google Scholar 

  • 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):547–554

    Article  PubMed  Google Scholar 

  • 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):457–462

    Article  Google Scholar 

  • 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 91:725–726

    Article  PubMed  CAS  Google Scholar 

  • Margonari CS, Fortes-Dias CL, Dias ES (2004) Genetic variability in geographical populations of Lutzomyia whitmani elucidated by RAPD-PCR. J Med Entomol 41:187–192

    Article  PubMed  CAS  Google Scholar 

  • 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 8:266

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 55:553–562

    Article  PubMed  CAS  Google Scholar 

  • 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 6:85

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 8:141

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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):460–466

    Article  PubMed  Google Scholar 

  • 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):157

    Article  PubMed  PubMed Central  Google Scholar 

  • Meireles-Filho ACA, Kyriacou CP (2013) Circadian rhythms in insect disease vectors. Mem Inst Oswaldo Cruz 108(Suppl. 1):48–58

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 7:38

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 74:1035–1059

    Article  PubMed  CAS  Google Scholar 

  • 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 19:38–47

    Article  PubMed  CAS  Google Scholar 

  • Miles M, Ward RD (1978) Preliminary isoenzyme studies on phlebotomine sandflies (Diptera: Psychodidae). Ann Trop Med Parasitol 72:398–400

    Article  PubMed  CAS  Google Scholar 

  • 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 70:278–285

    Article  PubMed  Google Scholar 

  • 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 9:480

    Article  PubMed  PubMed Central  Google Scholar 

  • Morton IE, Ward RD (1989) Laboratory response of female Lutzomyia longipalpis sandflies to a host and male pheromone source over distance. Med Vet Entomol 3:219–223

    Article  PubMed  CAS  Google Scholar 

  • 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):277–282

    PubMed  CAS  Google Scholar 

  • 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 59:893–901

    Article  PubMed  CAS  Google Scholar 

  • 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 35:82–89

    Article  PubMed  CAS  Google Scholar 

  • 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):169–174

    Article  PubMed  CAS  Google Scholar 

  • 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 61:149–157

    Article  PubMed  CAS  Google Scholar 

  • 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):391–395

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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):403–405

    Article  PubMed  CAS  Google Scholar 

  • 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):374–390

    Article  PubMed  CAS  Google Scholar 

  • 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):e226

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Peixoto AA, Hall JC (1998) Analysis of temperature- sensitive mutants reveals new genes involved in the courtship song of Drosophila. Genetics 148:827–838

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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 18:25–37

    Article  PubMed  CAS  Google Scholar 

  • Phillips A, Ward R, Ryan L (1986) Chemical analysis of compounds extracted from the tergal “spots” of “Lutzomyia longipalpis” from Brazil. Acta Trop 43:271–276

    PubMed  CAS  Google Scholar 

  • 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):132–139

    Article  PubMed  CAS  Google Scholar 

  • 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):e0140636

    Article  PubMed Central  CAS  Google Scholar 

  • 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):593–595

    Article  PubMed  Google Scholar 

  • 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 256:602–610

    Article  PubMed  CAS  Google Scholar 

  • Puillandre N, Lambert A, Brouillet S, Achaz G (2012) ABGD, Automatic Barcode Gap Discovery for primary species delimitation. Mol Ecol 21(8):1864–1877

    Article  PubMed  CAS  Google Scholar 

  • 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):875–882

    Article  PubMed  CAS  Google Scholar 

  • 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 104:937–954

    Article  PubMed  Google Scholar 

  • 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):43–50

    Article  PubMed  CAS  Google Scholar 

  • Ready PD (2011) Should sandfly taxonomy predict vectorial and ecological traits? J Vector Ecol 36:S17–S32

    Article  PubMed  Google Scholar 

  • Ready PD (2013) Biology of phlebotomine sand flies as vectors of disease agents. Annu Rev Entomol 58:227–250

    Article  PubMed  CAS  Google Scholar 

  • Ready PD, Rangel R (2003) Caracteres Isoenzimáticos e Moleculares: espécies crípticas. In: Rangel EF, Lainson R (eds) Flebotomíneos do Brasil. Editora Fiocruz, Rio de Janeiro

    Google Scholar 

  • 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 22:3–8

    Google Scholar 

  • 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 78:543–544

    Article  PubMed  CAS  Google Scholar 

  • 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 76:21–40

    Article  Google Scholar 

  • 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):109–116

    Article  PubMed  CAS  Google Scholar 

  • Ready PD, Lainson R, Shaw JJ, Souza AA (1991) DNA probes for distinguishing Psychodopygus wellcomei from Psychodopygus complexus (Diptera: Psychodidae). Mem Inst Oswaldo Cruz 86:41–49

    Article  PubMed  CAS  Google Scholar 

  • 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 87:187–195

    Article  CAS  Google Scholar 

  • 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):159–160

    Article  PubMed  CAS  Google Scholar 

  • 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 16:9249217

    Google Scholar 

  • Richardson BJ, Baverstock PR, Adams M (1990) Allozyme electrophoresis. A handbook for animal systematics and population studies. Academic Press, New York

    Google Scholar 

  • 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 58:649–657

    Article  PubMed  CAS  Google Scholar 

  • 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 159:125–131

    Article  PubMed  Google Scholar 

  • 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 43:85–89

    PubMed  CAS  Google Scholar 

  • Sakai T, Ishida N (2001) Circadian rhythms of female mating activity governed by clock genes in Drosophila. Proc Natl Acad Sci USA 98:9221–9225

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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):230–237

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Scarpassa VM, Alencar RB (2012) Lutzomyia umbratilis, the main vector of Leishmania guyanensis, represents a novel species complex? PLoS One 7:e37341

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 6:258

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 31:312–320

    Article  PubMed  Google Scholar 

  • 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):651–701

    Article  CAS  Google Scholar 

  • 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 149:1407–1426

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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):379–383

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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):84–93

    Article  PubMed  CAS  Google Scholar 

  • 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 41:906–913

    Article  PubMed  Google Scholar 

  • 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):216–219

    Article  PubMed  Google Scholar 

  • 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):287–292

    Article  PubMed  CAS  Google Scholar 

  • 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):161–174

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 9:580

    Article  PubMed  PubMed Central  Google Scholar 

  • 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):51–59

    Article  Google Scholar 

  • 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:28

    Google Scholar 

  • 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 70:907–913

    Article  PubMed  CAS  Google Scholar 

  • 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 84:205–218

    Article  PubMed  CAS  Google Scholar 

  • 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 18:67–70

    Google Scholar 

  • 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 97:5313–5316

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Titus RG, Ribeiro JM (1988) Salivary gland lysates from the sand fly Lutzomyia longipalpis enhance Leishmania infectivity. Science 239(4845):1306–1308

    Article  PubMed  CAS  Google Scholar 

  • 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 69:484–493

    Article  PubMed  CAS  Google Scholar 

  • 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):3717–3729

    Article  PubMed  CAS  Google Scholar 

  • 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):734–739

    Article  PubMed  CAS  Google Scholar 

  • Vigoder FM, Souza NA, Peixoto AA (2010b) Copulatory courtship song in Lutzomyia migonei (Diptera: psychodidae). Mem Inst Oswaldo Cruz 105(8):1065–1067

    Article  PubMed  Google Scholar 

  • Vigoder FM, Souza NA, Peixoto AA (2011) Acoustic signals in the sand fly Lutzomyia (Nyssomyia) intermedia (Diptera: Psychodidae). Parasit Vectors 4:76

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 8:290

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 27:429–438

    Article  PubMed  Google Scholar 

  • 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):223–230

    Article  CAS  Google Scholar 

  • Ward RD, Morton IE (1991) Pheromones in mate choice and sexual isolation between siblings of Lutzomyia longipalpis (Diptera:Psychodidae). Parassitologia 33(Suppl):527–533

    PubMed  Google Scholar 

  • 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):269–280

    Article  Google Scholar 

  • 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 257–269

    Google Scholar 

  • 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 2:60–61

    Google Scholar 

  • 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):734–743

    Article  PubMed  CAS  Google Scholar 

  • 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):85

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 8:472

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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):72–77

    Article  PubMed  CAS  Google Scholar 

  • 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):309–314

    Article  PubMed  CAS  Google Scholar 

  • 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 54:1–881

    Google Scholar 

  • 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 12:966–977

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. London School of Hygiene and Tropical Medicine, and Natural History Museum, London, UK

    Paul D. Ready

  2. Instituto de Biologia, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil

    Felipe M. Vigoder

  3. Instituto Oswaldo Cruz, Fundação Oswaldo Cruz, Rio de Janeiro, Brazil

    Elizabeth F. Rangel

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  1. Paul D. Ready
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  2. Felipe M. Vigoder
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  3. Elizabeth F. Rangel
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Correspondence to Paul D. Ready .

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Editors and Affiliations

  1. Instituto Oswaldo Cruz, Fundação Oswaldo Cruz, Rio de Janeiro, Brazil

    Elizabeth F. Rangel

  2. Instituto de Ciências Biomédicas, Universidade de São Paulo, São Paulo, Brazil

    Jeffrey J. Shaw

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Ready, P.D., Vigoder, F.M., Rangel, E.F. (2018). Molecular and Biochemical Markers for Investigating the Vectorial Roles of Brazilian Sand Flies. In: Rangel, E., Shaw, J. (eds) Brazilian Sand Flies . Springer, Cham. https://doi.org/10.1007/978-3-319-75544-1_3

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