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PLoS Neglect Trop Dis 3: e365. Available: http:\/\/www.pubmedcentral.nih.gov\/articlerender.fcgi?artid=2628317&tool=pmcentrez&rendertype=abstract<\/ext-link>. Accessed 2013 Aug 16."},{"key":"ref2","unstructured":"Lainson R, Rangel EF (2005) Lutzomyia longipalpis<\/italic> and the eco-epidemiology of American visceral leishmaniasis, with particular reference to Brazil: a review. Mem Inst Oswaldo Cruz 100: 811\u2013827. Available: http:\/\/www.bioline.org.br\/pdf?oc05169<\/ext-link>. Accessed 2013 Aug 16."},{"key":"ref3","unstructured":"Kelly DW, Dye C (1997) Pheromones, kairomones and the aggregation dynamics of the sandfly Lutzomyia longipalpis<\/italic>. Anim Behav 53: 721\u2013731. Available: http:\/\/www.sciencedirect.com\/science\/article\/B6W9W-45MFNR4-13\/2\/b70fce000fc5ccde6ad07bef0f83fad7<\/ext-link>. Accessed 2013 Aug 16."},{"key":"ref4","unstructured":"Ward R, Phillips A, Burnet B, Marcondes C (1988) The Lutzomyia longipalpis<\/italic> complex: reprodution and distribution. MW Service, Biosystematics of Haematophagous Insects. Oxford: Oxford University Press. 258\u2013269."},{"key":"ref5","unstructured":"Spiegel CN, Jeanbourquin P, Guerin PM, Hooper AM, Claude S, et al<\/etal>.. (2005) (1S,3S,7R)-3-methyl-alpha-himachalene from the male sandfly Lutzomyia longipalpis<\/italic> (Diptera: Psychodidae) induces neurophysiological responses and attracts both males and females. J Insect Physiol 51: 1366\u20131375. Available: http:\/\/www.sciencedirect.com\/science\/article\/pii\/S0022191005001812<\/ext-link>. Accessed 2013 Aug 16."},{"key":"ref6","unstructured":"Souza NA, Vigoder FM, Araki AS, Ward RD, Kyriacou CP, et al<\/etal>.. (2004) Analysis of the copulatory courtship songs of Lutzomyia longipalpis<\/italic> in six populations from Brazil. J Med Entomol 41: 906\u2013913. Available: http:\/\/www.bioone.org\/doi\/pdf\/10.1603\/0022-2585-41.5.906<\/ext-link>. Accessed 2013 Aug 16."},{"key":"ref7","doi-asserted-by":"crossref","unstructured":"Ritchie MG (2007) Sexual Selection and Speciation. Ann Rev Ecol Evol Syst 38: 79\u2013102. Available: http:\/\/www.annualreviews.org\/doi\/abs\/10.1146\/annurev.ecolsys.38.091206.095733<\/ext-link>. Accessed 2013 Aug 16.","DOI":"10.1146\/annurev.ecolsys.38.091206.095733"},{"key":"ref8","doi-asserted-by":"crossref","unstructured":"Chapman RF (1998) The Insects: Structure and Function. 4th<\/sup> ed. New York: Cambridge University Press. 788 p.","DOI":"10.1017\/CBO9780511818202"},{"key":"ref9","unstructured":"Birkhead TR, Hosken DJ, Pitnick S, editors (2009) Sperm Biology: an evolutionary perspective. 1st<\/sup> ed. London: Academic Press, Elsevier. 642 p."},{"key":"ref10","unstructured":"Quicke DLJ, Ingram SN, Baillie HS, Gaitens PV (1992) Sperm structure and ultrastructure in the Hymenoptera (Insecta). Zool Scripta 21: 381\u2013402. Available: http:\/\/onlinelibrary.wiley.com\/doi\/10.1111\/j.1463-6409.1992.tb00339.x\/abstract<\/ext-link>. Accessed 2013 Aug 16."},{"key":"ref11","unstructured":"Valdez J (2001) Ultrastructure of the testis of the Mexican fruit fly (Diptera:Tephritidae). Ann Entomol Soc Am 94: 251\u2013256. Available: http:\/\/www.bioone.org\/doi\/pdf\/10.1603\/0013-8746(2001)094%5B0251%3AUOTTOT%5D2.0.CO%3B2<\/ext-link>. Accessed 2013 Aug 16."},{"key":"ref12","unstructured":"Dallacqua RP, Da Cruz-Landim C (2003) Ultrastructure of the ducts of the reproductive tract of males of Melipona bicolor bicolor lepeletier<\/italic> (Hymenoptera, Apinae, Meliponini). Anat Histol Embryol 32: 276\u2013281. Available: http:\/\/www.ncbi.nlm.nih.gov\/pubmed\/12969027<\/ext-link>. Accessed 2013 Aug 16."},{"key":"ref13","unstructured":"Casper A, Van Doren M (2006) The control of sexual identity in the Drosophila<\/italic> germline. Development 133: 2783\u20132791. Available: http:\/\/www.ncbi.nlm.nih.gov\/pubmed\/16835435<\/ext-link>. Accessed 2013 Aug 16."},{"key":"ref14","doi-asserted-by":"crossref","unstructured":"Giebultowicz JM, Riemann JG, Raina AK, Ridgway RL (1989) Circadian system controlling release of sperm in the insect testes. Science 245: 1098\u20131100. Available: http:\/\/www.sciencemag.org\/content\/245\/4922\/1098.refs<\/ext-link>. Accessed 2013 Aug 16.","DOI":"10.1126\/science.245.4922.1098"},{"key":"ref15","doi-asserted-by":"crossref","unstructured":"Gillott C (2003) Male accessory gland secretions: modulators of female reproductive physiology and behavior. Annu Rev Entomol 48: 163\u2013184. Available: http:\/\/www.ncbi.nlm.nih.gov\/pubmed\/12208817<\/ext-link>. Accessed 2013 Aug 16.","DOI":"10.1146\/annurev.ento.48.091801.112657"},{"key":"ref16","doi-asserted-by":"crossref","unstructured":"Wolfner MF (1997) Tokens of love: functions and regulation of Drosophila<\/italic> male accessory gland products. Insect Biochem Mol Biol 27: 179\u2013192. Available: http:\/\/www.sciencedirect.com\/science\/article\/pii\/S0965174896000847<\/ext-link>. Accessed 2013 Aug 16.","DOI":"10.1016\/S0965-1748(96)00084-7"},{"key":"ref17","doi-asserted-by":"crossref","unstructured":"Avila FW, Sirot LK, LaFlamme BA, Rubinstein CD, Wolfner MF (2011) Insect seminal fluid proteins: identification and function. Annu Rev Entomol 56: 21\u201340. Available: http:\/\/www.ncbi.nlm.nih.gov\/pubmed\/20868282<\/ext-link>. Accessed 2013 Aug 16.","DOI":"10.1146\/annurev-ento-120709-144823"},{"key":"ref18","unstructured":"Baldini F, Gabrieli P, Rogers DW, Catteruccia F (2012) Function and composition of male accessory gland secretions in Anopheles gambiae<\/italic>: a comparison with other insect vectors of infectious diseases. Pathogens and global health 106: 82\u201393. Available: http:\/\/www.ncbi.nlm.nih.gov\/pubmed\/22943543<\/ext-link>. Accessed 2013 Aug 16."},{"key":"ref19","unstructured":"Helinski MEH, Deewatthanawong P, Sirot LK, Wolfner MF, Harrington LC (2012) Duration and dose-dependency of female sexual receptivity responses to seminal fluid proteins in Aedes albopictus<\/italic> and Ae. aegypti<\/italic> mosquitoes. J Insect Physiol. Available: http:\/\/www.ncbi.nlm.nih.gov\/pubmed\/22796224<\/ext-link>. Accessed 2013 Aug 16."},{"key":"ref20","doi-asserted-by":"crossref","unstructured":"Gioti A, Wigby S, Wertheim B, Schuster E, Martinez P, et al<\/etal>.. (2012) Sex peptide of Drosophila melanogaster males is a global regulator of reproductive processes in females. Proc R Soc B 279: 4423\u20134432. Available: http:\/\/www.ncbi.nlm.nih.gov\/pubmed\/22977156<\/ext-link>. Accessed 2013 Aug 16.","DOI":"10.1098\/rspb.2012.1634"},{"key":"ref21","unstructured":"Yamane T, Miyatake T, Kimura Y (2008) Female mating receptivity after injection of male-derived extracts in Callosobruchus maculatus<\/italic>. J Insect Physiol 54: 1522\u20131527. Available: http:\/\/www.sciencedirect.com\/science\/article\/B6T3F-4TDK70Y-1\/2\/89510363a227e16e0df9619d1f282a74<\/ext-link>. Accessed 2013 Aug 16."},{"key":"ref22","unstructured":"Tram U, Wolfner MF (1998) Seminal fluid regulation of female sexual attractiveness in Drosophila melanogaster<\/italic>. Proc Natl Acad Sci USA 95: 4051\u20134054. Available: hhttp:\/\/www.ncbi.nlm.nih.gov\/pmc\/articles\/PMC19961\/<\/ext-link>. Accessed 2013 Aug 16."},{"key":"ref23","unstructured":"Maroli M, Bettini S, Tricoli D, Khoury C, Perrotti E (1991) Studies on mating plug of two sandfly species, Phlebotomus perniciosus<\/italic> and Phlebotomus papatasi<\/italic> (Diptera: Psychodidae). Parassitologia 33 Suppl: 405\u2013411. Available: http:\/\/www.ncbi.nlm.nih.gov\/pubmed\/1841236<\/ext-link>. Accessed 2013 Aug 16."},{"key":"ref24","unstructured":"Azevedo RVDM, Dias DBS, Bretas JAC, Mazzoni CJ, Souza NA, et al<\/etal>.. (2012) The transcriptome of Lutzomyia longipalpis<\/italic> (Diptera: Psychodidae) male reproductive organs. PLoS ONE 7: e34495. Available: http:\/\/dx.plos.org\/10.1371\/journal.pone.0034495<\/ext-link>. Accessed 2013 Aug 16."},{"key":"ref25","unstructured":"Fausto AM, Gambellini G, Taddei AR, Maroli M, Mazzini M (2000) Ultrastructure of the seminal vesicle of Phlebotomus perniciosus<\/italic> Newstead (Diptera, Psychodidae). Tissue Cell 32: 228\u2013237. Available: http:\/\/www.ncbi.nlm.nih.gov\/pubmed\/11037793<\/ext-link>. Accessed 2013 Aug 16."},{"key":"ref26","unstructured":"Modi GB, Tesh RB (1983) A simple technique for mass rearing Lutzomyia longipalpis<\/italic> and Phlebotomus papatasi<\/italic> (Diptera: Psychodidae) in the laboratory. J Med Entomol 20: 568\u2013569. Available: http:\/\/www.ncbi.nlm.nih.gov\/pubmed\/6644754<\/ext-link>. Accessed 2013 Aug 16."},{"key":"ref27","unstructured":"Jones TM, Balmford A, Quinnell RJ (2000) Adaptive female choice for middle-aged mates in a lekking sandfy. Proc R Soc Lond B 267: 681\u2013686. Available: http:\/\/www.ncbi.nlm.nih.gov\/pubmed\/10821613<\/ext-link>. Accessed 2013 Aug 16."},{"key":"ref28","unstructured":"Ottoni EB (2000) EthoLog 2.2: a tool for the transcription and timing of behavior observation sessions. Behav Res Meth Ins C 32: 446\u2013449. Available: http:\/\/www.ncbi.nlm.nih.gov\/pubmed\/11029818<\/ext-link>. Accessed 2013 Aug 16."},{"key":"ref29","unstructured":"Lazareva AA, Roman G, Mattox W, Hardin PE, Dauwalder B (2007) A role for the adult fat body in Drosophila<\/italic> male courtship behavior. PLoS Genet 3: e16. Available: http:\/\/www.pubmedcentral.nih.gov\/articlerender.fcgi?artid=1781494&tool=pmcentrez&rendertype=abstract<\/ext-link>. Accessed 2013 Aug 16."},{"key":"ref30","doi-asserted-by":"crossref","unstructured":"Jones TM, Quinnell RJ, Balmford A (1998) Fisherian flies: Benefits of female choice in a lekking sandfly. Proc R Soc Lond 265: 1651\u20131657. Available: http:\/\/www.jstor.org\/discover\/10.2307\/51137?uid=24156&uid=3737664&uid=5909624&uid=2&uid=3&uid=67&uid=24155&uid=62&sid=21101378063307<\/ext-link>. Accessed 2013 Aug 16.","DOI":"10.1098\/rspb.1998.0484"},{"key":"ref31","unstructured":"Ilango K (2005) Structure and function of the spermathecal complex in the phlebotomine sandfly Phlebotomus papatasi<\/italic> Scopoli (Diptera: Psychodidae): I. ultrastructure and histology. J Bioscience 30: 711\u2013731. Available: http:\/\/www.ncbi.nlm.nih.gov\/pubmed\/16388145<\/ext-link>. Accessed 2013 Aug 16."},{"key":"ref32","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/0020-7322(84)90027-8","article-title":"The spermatozoon of three species of Phlebotomus<\/italic> (Phlebotominae) and the acrosomal evolution in nematoceran dipterans","volume":"13","author":"R Dallai","year":"1984","journal-title":"Int J Insect Morphol & Embryol"},{"key":"ref33","unstructured":"Forattini OP (1973) Entomologia M\u00e9dica. Vol. 4, Psychodidae, Phlebotominae, Leishmanioses, Bartonelose. S\u00e3o Paulo: Edgar Bl\u00fccher & Editora da Universidade de S\u00e3o Paulo. 658 p."},{"key":"ref34","doi-asserted-by":"crossref","unstructured":"Riemann JG (1973) Ultrastructure of the ejaculatory duct region producing the male housefly accessory material. J Insect Physiol 19: 213\u2013223. Available: http:\/\/www.sciencedirect.com\/science\/article\/pii\/0022191073902345<\/ext-link>. Accessed 2013 Aug 16.","DOI":"10.1016\/0022-1910(73)90234-5"},{"key":"ref35","unstructured":"Meikle DB, Sheehan KB, Phillis DM, Richmond RC (1990) Localization and longevity of seminal-fluid esterase 6 in mated female Drosophila melanogaster<\/italic>. J Insect Physiol 36: 93\u2013101. Available: http:\/\/linkinghub.elsevier.com\/retrieve\/pii\/002219109090179J<\/ext-link>. Accessed 2013 Aug 16."},{"key":"ref36","unstructured":"Lee JJ, Klowden MJ (1999) A male accessory gland protein that modulates female mosquito (Diptera: Culicidae) host-seeking behavior. J Am Mosquito Control 15: 4\u20137. Available: http:\/\/www.ncbi.nlm.nih.gov\/pubmed\/10342262<\/ext-link>. Accessed 2013 Aug 16."},{"key":"ref37","unstructured":"Bray DP, Hamilton JGC (2007) Courtship behaviour in the sandfly Lutzomyia longipalpis<\/italic>, the New World vector of visceral leishmaniasis. Med Vet Entomol 21: 332\u2013338. Available: http:\/\/www.ncbi.nlm.nih.gov\/pubmed\/18092971<\/ext-link>. Accessed 2013 Aug 16."},{"key":"ref38","unstructured":"Souza NA, Andrade-Coelho CA, Vigoder FM, Ward RD, Peixoto AA (2008) Reproductive isolation between sympatric and allopatric Brazilian populations of Lutzomyia longipalpis<\/italic> s.l. (Diptera: Psychodidae). Mem Inst Oswaldo Cruz 103: 2016\u20132019. Available: http:\/\/www.scielo.br\/scielo.php?script=sci_arttext&pid=S0074-02762008000200017<\/ext-link>. Accessed 2013 Aug 16."},{"key":"ref39","unstructured":"Jones M (2001) A Potential Cost of Monandry in the Lekking. J Insect Behavior 14: 385\u2013399. Available: http:\/\/link.springer.com\/article\/10.1023%2FA%3A1011127514317#page-1<\/ext-link>. Accessed 2013 Aug 16."},{"key":"ref40","unstructured":"Vitta ACR, Lorenzo MG (2009) Copulation and mate guarding behavior in Triatoma brasiliensis (Hemiptera: Reduviidae). J Med Entomol 46: 789\u2013795. Available: http:\/\/www.ncbi.nlm.nih.gov\/pubmed\/19645281<\/ext-link>. Accessed 2013 Aug 16."},{"key":"ref41","unstructured":"Nattero J, Leonhard G, Rodr\u00edguez CS, Crocco L (2011) Influence of the quality and quantity of blood ingested on reproductive parameters and life-span in Triatoma infestans<\/italic> (Klug). Acta tropica 119: 183\u2013187. Available: http:\/\/www.ncbi.nlm.nih.gov\/pubmed\/21672510<\/ext-link>. Accessed 2013 Aug 16."},{"key":"ref42","doi-asserted-by":"crossref","unstructured":"Yuval B (2006) Mating systems of blood-feeding flies. Ann Rev Entomol 51: 413\u2013440. Available: http:\/\/www.ncbi.nlm.nih.gov\/pubmed\/16332218<\/ext-link>. 2013. Accessed 2013 Aug 16.","DOI":"10.1146\/annurev.ento.51.110104.151058"},{"key":"ref43","unstructured":"Souza NA, Andrade-Coelho CA, Silva VC, Ward RD, Peixoto AA (2009) Life cycle differences among Brazilian sandflies of the Lutzomyia longipalpis<\/italic> sibling species complex. Med Vet Entomol 23: 287\u2013292. Available: http:\/\/www.ncbi.nlm.nih.gov\/pubmed\/19712160<\/ext-link>. Accessed 2013 Aug 16."},{"key":"ref44","unstructured":"Valenta D, Killick-Kendrick R, Killick-Kendrick M (2000) Courtship and mating by the sandfly Phlebotomus duboscqi<\/italic>, a vector of zoonotic cutaneous leishmaniasis in the Afrotropical region. Med Vet Entomol 14: 207\u2013212. Available: http:\/\/www.ncbi.nlm.nih.gov\/pubmed\/10872866<\/ext-link>. Accessed 2013 Aug 16."},{"key":"ref45","unstructured":"Bray DP, Hamilton JGC (2007) Courtship behaviour in the sandfly Lutzomyia longipalpis<\/italic>, the New World vector of visceral leishmaniasis. Medical and veterinary entomology 21: 332\u2013338. Available: http:\/\/www.ncbi.nlm.nih.gov\/pubmed\/18092971<\/ext-link>. Accessed 2013 Aug 16."},{"key":"ref46","doi-asserted-by":"crossref","unstructured":"Bretman A, Westmancoat JD, Chapman T (2013) Male control of mating duration following exposure to rivals in fruitflies. J Insect Physiol 59: 824\u2013827. Available: http:\/\/www.ncbi.nlm.nih.gov\/pubmed\/23727302<\/ext-link>. 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