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Genetic Divergence in the cacophony IVS6 Intron Among Five BrazilianPopulations of Lutzomyia longipalpis

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Abstract

Genes involved in the reproductive isolation are particularly useful as molecular markers in speciation studies. Lutzomyia longipalpis (Diptera: Psychodidae: Phlebotominae), a putative species complex, is a vector of visceral leishmaniasis in Latin America. We isolated from this species a fragment homologous to cacophony, a Drosophila gene that encodes features of the lovesong, an acoustic signal that is important in the sexual isolation of closely related species and known to vary considerably among L. longipalpis putative siblings species. Using an intron of the sandfly cacophony as a marker, we analyzed the molecular variation and sequence divergence among five populations of L. longipalpis from Brazil, three allopatric (Jacobina, Lapinha and Natal) and two putative sympatric sibling species from the locality of Sobral. A high level of polymorphism was found and analysis of the data indicates that very little gene flow is occurring among the populations of Jacobina, Lapinha, and Natal. A high level of differentiation was also observed between the two putative sympatric species of Sobral, one of which seems to be the same sibling species found in Natal, while the other is somewhat more related to Jacobina and Lapinha. However, the amount of estimated gene flow among the Sobral siblings is about seven times higher than the previously estimated for period, another lovesong gene, perhaps indicating that introgression might be affecting cacophony more than period. The results suggest that L. longipalpis is not a single species in Brazil, but it is yet not clear whether the different populations studied deserve species status rather than representing an incipient speciation process.

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References

  • S Alt J Ringo B Talyn W Bray H Dowse (1998) ArticleTitleThe period gene controls courtship song cycles in Drosophila melanogaster Anim Behav 56 87–97 Occurrence Handle10.1006/anbe.1998.0743 Occurrence Handle9710465

    Article  PubMed  Google Scholar 

  • JC Arrivillaga MD Feliciangeli (2001) ArticleTitle Lutzomyia pseudolongipalpis: The first new species within the longipalpis (Diptera: Psychodidae: Phlebotominae) complex from La Rinconada, Curarigua, Lara State, Venezuela J Med Entomol 38 783–790 Occurrence Handle1:STN:280:DC%2BD38%2FjtFOmtA%3D%3D Occurrence Handle11761375

    CAS  PubMed  Google Scholar 

  • JC Arrivillaga DE Norris MD Feliciangeli GC Lanzaro (2002) ArticleTitlePhylogeography of the neotropical sand fly Lutzomyia longipalpis inferred from mitochondrial DNA sequences Inf Gen Evol 2 83–95 Occurrence Handle10.1016/S1567-1348(02)00087-4 Occurrence Handle1:CAS:528:DC%2BD38XoslCjurs%3D

    Article  CAS  Google Scholar 

  • ACR Azevedo FA Monteiro PH Cabello NA Souza MG Rosa-Freitas EF Rangel (2000) ArticleTitleStudies on populations of Lutzomyia longipalpis (Lutz. & Neiva, 1912) (Diptera: Psychodidae: Phlebotominae) in Brazil Mem Inst Oswaldo Cruz 95 305–322 Occurrence Handle10.1590/S0074-02762000000300005 Occurrence Handle10800188

    Article  PubMed  Google Scholar 

  • LGSR Bauzer NA Souza RD Ward CP Kyriacou AA Peixoto (2002a) ArticleTitleThe period gene and genetic differentiation between three Brazilian populations of Lutzomyia longipalpis Insect Mol Biol 11 315–323 Occurrence Handle10.1046/j.1365-2583.2002.00340.x Occurrence Handle1:CAS:528:DC%2BD38Xmt1Chu7Y%3D

    Article  CAS  Google Scholar 

  • LGSR Bauzer JSM Gesto NA Souza RD Ward JGC Hamilton CP Kyriacou AA Peixoto (2002b) ArticleTitleMolecular divergence in the period gene between two putative sympatric species of the Lutzomyia longipalpis complex Mol Biol Evol 19 1624–1627 Occurrence Handle1:CAS:528:DC%2BD38XntVyhtb4%3D

    CAS  Google Scholar 

  • WC Black GC Lanzaro (2001) ArticleTitleDistribution of genetic variation among chromosomal forms of Anopheles gambiae s.s: Introgressive hybridization, adaptive inversions, or recent reproductive isolation? Insect Mol Biol 10 3–7 Occurrence Handle10.1046/j.1365-2583.2001.00234.x Occurrence Handle1:CAS:528:DC%2BD3MXhslGqtrg%3D Occurrence Handle11240631

    Article  CAS  PubMed  Google Scholar 

  • JP Dujardin EM Torrez F Le Pont D Hervas D Sossa (1997) ArticleTitleIsozymic and metric variation in the Lutzomyia longipalpis complex Med Vet Entomol 11 394–400 Occurrence Handle1:STN:280:DyaK1c%2FptF2mtA%3D%3D Occurrence Handle9430121

    CAS  PubMed  Google Scholar 

  • L Excoffier PE Smouse JM Quattro (1992) ArticleTitleAnalysis of molecular variance inferred from metric distances among DNA haplotypes: Application to human mitochondrial DNA restriction data Genetics 131 479–491 Occurrence Handle1:CAS:528:DyaK38XlsVCntro%3D Occurrence Handle1644282

    CAS  PubMed  Google Scholar 

  • DA Filatov D Charlesworth (1999) ArticleTitleDNA polymorphism, haplotype structure and balancing selection in the Leavenworthia PgiC locus Genetics 155 1423–1434

    Google Scholar 

  • YX Fu WH Li (1993) ArticleTitleStatistical tests of neutrality of mutations Genetics 133 693–709 Occurrence Handle1:STN:280:ByyB3c3kvVU%3D Occurrence Handle8454210

    CAS  PubMed  Google Scholar 

  • JGC Hamilton AM Hooper K Mori JA Pickett S Sano (1999a) ArticleTitle3-Methyl-α-himachalene confirmed, and the relative stereochemistry defined, by synthesis as the sex pheromone of the sandfly Lutzomyia longipalpis from Jacobina, Brazil Chem Comm pp 355–356 Occurrence Handle10.1039/a900242a

    Article  Google Scholar 

  • JGC Hamilton HC Ibbotson AM Hooper K Mori JA Pickett S Sano (1999b) ArticleTitle9-Methylgermacrene-B confirmed by synthesis as the sex pheromone of the sandfly Lutzomyia longipalpis from Lapinha, Brazil, and the absolute stereochemistry defined as 9S Chem Comm . 2335–2336 Occurrence Handle10.1039/a907910f

    Article  Google Scholar 

  • J Hey J Wakeley (1997) ArticleTitleA coalescent estimator of the population recombination rate Genetics 145 833–846 Occurrence Handle1:CAS:528:DyaK2sXmsVaktb4%3D Occurrence Handle9055092

    CAS  PubMed  Google Scholar 

  • RR Hudson M Kreitman M Aguade (1987) ArticleTitleA test of neutral molecular evolution based on nucleotide data Genetics 116 153–159 Occurrence Handle1:CAS:528:DyaL2sXktlCgsLk%3D Occurrence Handle3110004

    CAS  PubMed  Google Scholar 

  • RR Hudson M Slatkin WP Maddison (1992) ArticleTitleEstimation of levels of gene flow from DNA sequence data Genetics 132 583–589 Occurrence Handle1:CAS:528:DyaK3sXhsVSku7o%3D Occurrence Handle1427045

    CAS  PubMed  Google Scholar 

  • J Krzywinski NJ Besansky (2003) ArticleTitleMolecular systematics of Anopheles: From subgenera to subpopulations Annu Rev Entomol 48 111–139 Occurrence Handle10.1146/annurev.ento.48.091801.112647 Occurrence Handle1:CAS:528:DC%2BD3sXnvVymtQ%3D%3D Occurrence Handle12208816

    Article  CAS  PubMed  Google Scholar 

  • S Kumar K Tamura IB Jakobsen M Nei (2001) ArticleTitleMEGA2: Molecular Evolutionary Genetics Analysis software Bioinformatics 17 1244–1245 Occurrence Handle10.1093/bioinformatics/17.12.1244 Occurrence Handle1:CAS:528:DC%2BD38XmtVCktQ%3D%3D Occurrence Handle11751241

    Article  CAS  PubMed  Google Scholar 

  • CP Kyriacou JC Hall (1989) ArticleTitleSpectral-analysis of Drosophila courtship song rhythms Anim Behav 37 850–859 Occurrence Handle10.1016/0003-3472(89)90069-9

    Article  Google Scholar 

  • M Lampo D Torgerson LM Márquez M Rinaldi CZ Garcia A Arab (1999) ArticleTitleOccurrence of sibling species of Lutzomyia longipalpis (Diptera: Psychodidae) in Venezuela: First evidence from reproductively isolated sympatric populations Am J Trop Med Hyg 61 1004–1009 Occurrence Handle1:STN:280:DC%2BD3c7jslWmsw%3D%3D Occurrence Handle10674686

    CAS  PubMed  Google Scholar 

  • GC Lanzaro K Ostrovska MV Herrero PG Lawyer A Warburg (1993) ArticleTitle Lutzomyia longipalpis is a species complex: Genetic divergence and interspecific hybrid sterility among three populations Am J Trop Med Hyg 48 839–847 Occurrence Handle1:STN:280:ByyA38rnslQ%3D Occurrence Handle8333579

    CAS  PubMed  Google Scholar 

  • RMMA Lins SG Oliveira NA Souza RG Queiroz Particlede SCB Justiniano RD Ward CP Kyriacou AA Peixoto (2002) ArticleTitleMolecular evolution of the cacophony IVS6 region in sandflies Insect Mol Biol 11 117–122 Occurrence Handle10.1046/j.1365-2583.2002.00315.x Occurrence Handle1:CAS:528:DC%2BD38XjvFSiurY%3D Occurrence Handle11966876

    Article  CAS  PubMed  Google Scholar 

  • CA Machado RM Kliman J Market J Hey (2002) ArticleTitleInferring the history of speciation from multilocus DNA sequence data: The case of Drosophila pseudoobscura and close relatives Mol Biol Evol 19 472–488 Occurrence Handle1:CAS:528:DC%2BD38XivV2gtb8%3D Occurrence Handle11919289

    CAS  PubMed  Google Scholar 

  • RDC Maingon RD Ward JGC Hamilton HA Noyes N Souza SJ Kemp PC Watts (2003) ArticleTitleGenetic identification of two sibling species of Lutzomyia longipalpis (Diptera: Psychodidae) that produce distinct male sex pheromones in Sobral, Ceará State, Brazil Mol Ecol 12 1879–1894 Occurrence Handle10.1046/j.1365-294X.2003.01871.x Occurrence Handle1:STN:280:DC%2BD3szjsF2isg%3D%3D Occurrence Handle12803639

    Article  CAS  PubMed  Google Scholar 

  • J Mukhopadhyay K Ghosh EF Rangel LE Munstermann (1998a) ArticleTitleGenetic variability in biochemical characters of Brazilian field populations of the Leishmania vector, Lutzomyia longipalpis (Diptera: Psychodidae) Am J Trop Med Hyg 59 893–901 Occurrence Handle1:STN:280:DyaK1M7gtFartQ%3D%3D

    CAS  Google Scholar 

  • J Mukhopadhyay K Ghosh AC Azevedo EF Rangel LE Munstermann (1998b) ArticleTitleGenetic polymorphism of morphological and biochemical characters in a Natal, Brazil, population of Lutzomyia longipalpis (Diptera: Psychodidae) J Am Mosq Control Assoc 14 277–282 Occurrence Handle1:CAS:528:DyaK1cXnsVKksbs%3D

    CAS  Google Scholar 

  • JP Mutebi B Alexander I Sherlock J Wellington AA Souza J Shaw EF Rangel GC Lanzaro (1999) ArticleTitleBreeding structure of the sand fly Lutzomyia longipalpis (Lutz & Neiva) in Brazil Am J Trop Med Hyg 61 149–157 Occurrence Handle1:STN:280:DyaK1MzlvFSiuw%3D%3D

    CAS  Google Scholar 

  • SG Oliveira M Bottecchia LGSR Bauzer NA Souza RD Ward CP Kyriacou AA Peixoto (2001) ArticleTitleCourtship song genes and speciation in sandflies Mem Inst Oswaldo Cruz 96 403–405 Occurrence Handle1:CAS:528:DC%2BD3MXivVGktLg%3D Occurrence Handle11313653

    CAS  PubMed  Google Scholar 

  • AA Peixoto JC Hall (1998) ArticleTitleAnalysis of temperature-sensitive mutants reveals new genes involved in the courtship song of Drosophila Genetics 148 827–838 Occurrence Handle1:STN:280:DyaK1c7os1aksA%3D%3D Occurrence Handle9504928

    CAS  PubMed  Google Scholar 

  • AA Peixoto LA Smith JC Hall (1997) ArticleTitleGenomic organization and evolution of alternative exons in a Drosophila calcium channel gene Genetics 145 1003–1013 Occurrence Handle1:CAS:528:DyaK2sXmsVakur0%3D Occurrence Handle9093853

    CAS  PubMed  Google Scholar 

  • AA Peixoto CA Gomes PR Amoretty RMMA Lins ACA Meireles-Filho NA Souza CP Kyriacou (2001) ArticleTitleNew molecular markers for Phlebotomine sand flies Int J Parasitol 31 635–639 Occurrence Handle1:CAS:528:DC%2BD3MXjtFCmsbk%3D Occurrence Handle11334955

    CAS  PubMed  Google Scholar 

  • J Rozas R Rozas (1999) ArticleTitleDnaSP version 3: An integrated program for population genetics and molecular evolution analysis Bioinformatics 15 174–175 Occurrence Handle10.1093/bioinformatics/15.2.174 Occurrence Handle1:CAS:528:DyaK1MXisVOksrY%3D Occurrence Handle10089204

    Article  CAS  PubMed  Google Scholar 

  • N Saitou M Nei (1987) ArticleTitleThe neighbor-joining method: A new method for reconstructing phylogenetic trees Mol Biol Evol 4 406–425 Occurrence Handle1:STN:280:BieC1cbgtVY%3D Occurrence Handle3447015

    CAS  PubMed  Google Scholar 

  • S Schneider D Roessli L Excoffier (2000) Arlequin ver. 2.000: A software for population genetics data analysis Genetics and Biometry Laboratory, University of Geneva Geneva, Switzerland

    Google Scholar 

  • FM Sene HL Carson (1977) ArticleTitleGenetic variation in Hawaiian Drosophila. IV. Allozymic similarity between D. silvestris and D. heteroneura from the island of Hawaii Genetics 86 187–198 Occurrence Handle1:CAS:528:DyaE2sXlvFOksbw%3D Occurrence Handle885341

    CAS  PubMed  Google Scholar 

  • LA Smith AA Peixoto EM Kramer A Villella JC Hall (1998) ArticleTitleCourtship and visual defects of cacophony mutants reveal functional complexity of a calcium-channel α-1 subunit in Drosophila Genetics 149 1407–1426 Occurrence Handle1:CAS:528:DyaK1cXkslOnurs%3D Occurrence Handle9649530

    CAS  PubMed  Google Scholar 

  • SI Soto T Lehmann ED Rowton BID Velez CH Porter (2001) ArticleTitleSpeciation and population structure in the morphospecies Lutzomyia longipalpis (Lutz & Neiva) as derived from the mitochondrial ND4 gene Mol Phylogenet Evol 18 84–93 Occurrence Handle1:CAS:528:DC%2BD3MXmt1Wrtw%3D%3D Occurrence Handle11161745

    CAS  PubMed  Google Scholar 

  • NA Souza RD Ward JGC Hamilton CP Kyriacou AA Peixoto (2002) ArticleTitleCopulation songs in three siblings of Lutzomyia longipalpis (Diptera:Psychodidae) Trans RR Soc Trop Med Hyg 96 102–103

    Google Scholar 

  • F Tajima (1989) ArticleTitleStatistical method for testing the neutral mutation hypothesis by DNA polymorphism Genetics 123 585–595 Occurrence Handle1:CAS:528:DyaK3cXhslentA%3D%3D Occurrence Handle2513255

    CAS  PubMed  Google Scholar 

  • JD Thompson TJ Gibson F Plewniak F Jeanmougin DG Higgins (1997) ArticleTitleThe ClustalX windows interface: Flexible strategies for multiple sequence alignment aided by quality analysis tools Nucleic Acids Res 24 4876–4882 Occurrence Handle10.1093/nar/25.24.4876

    Article  Google Scholar 

  • CT Ting SC Tsaur CI Wu (2000) ArticleTitleThe phylogeny of closely related species as revealed by the genealogy of a speciation gene, Odysseus Proc. Natl. Acad. Sci. USA 97 5313–5316 Occurrence Handle1:CAS:528:DC%2BD3cXjsVWntbc%3D Occurrence Handle10779562

    CAS  PubMed  Google Scholar 

  • S Uribe (1999) ArticleTitleThe status of the Lutzomyia longipalpis species complex and possible implications for Leishmania transmission Mem Inst Oswaldo Cruz 94 729–734 Occurrence Handle1:STN:280:DC%2BD3c7jvVektw%3D%3D Occurrence Handle10585647

    CAS  PubMed  Google Scholar 

  • J Wakeley J Hey (1997) ArticleTitleEstimating ancestral population parameters Genetics 145 847–855 Occurrence Handle1:CAS:528:DyaK2sXmsVaktb8%3D Occurrence Handle9055093

    CAS  PubMed  Google Scholar 

  • RL Wang J Wakeley J Hey (1997) ArticleTitleGene flow and natural selection in the origin of Drosophila pseudoobscura and close relatives Genetics 147 1091–1106 Occurrence Handle1:CAS:528:DyaK2sXntlKrt7k%3D Occurrence Handle9383055

    CAS  PubMed  Google Scholar 

  • RD Ward AL Ribeiro PR Ready A Murtagh (1983) ArticleTitleReproductive 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 78 269–280

    Google Scholar 

  • RD Ward A Phillips B Burnet CB Marcondes (1988) The Lutzomyia longipalpis complex: Reproduction and distribution MW Service (Eds) Biosystematics of hematophagous insects Oxford University Press Oxford 258–269

    Google Scholar 

  • H Yin JP Mutebi S Marriott GC Lanzaro (1999) ArticleTitleMetaphase karyotypes and G-banding in sandflies of the Lutzomyia longipalpis complex Med Vet Entomol 13 72–77 Occurrence Handle1:STN:280:DyaK1M3htVKmtA%3D%3D Occurrence Handle10194752

    CAS  PubMed  Google Scholar 

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Acknowledgments

This work was supported by The Wellcome Trust and the Howard Hughes Medical Institute, with additional support from Faperj, Fiocruz, CAPES, and CNPq. The sandflies used in this work were obtained thanks to the help of Reginaldo Brazil (CPqRR), Iraci Duarte (FUNASA), Italo Sherlock (CPqGM), Mauricio Vilela (IOC), Gordon Hamilton (University of Keele, UK), José Wellington Oliveira-Lima (FUNASA), and Lindembergh C. Souza (FUNASA). We would like to thank Paulo de Amoretty and Caroline da Fonseca for their technical assistance, Jane Yardley and Robson da Silva for their help with the DNA sequencing, and Camila Mazzoni for her help with the data analysis.

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Authors and Affiliations

  1. Departamento de Bioquímica e Biologia Molecular, Fundacão Oswaldo Cruz, Av. Brasil 4365, Manguinhos, CEP 21045-900, Rio de Janeiro, Brazil

    M. Bottecchia, S. G. Oliveira, L. G. S. R. Bauzer & A. A. Peixoto

  2. Departamento de Entomologia, Fundação Oswaldo Cruz, Rio de Janeiro, Brazil

    N. A. Souza

  3. The Centre for Applied Entomology and Parasitology, School of Life Sciences, University of Keele, Keele, UK

    R. D. Ward

  4. Department of Genetics, University of Leicester, Leicester, UK

    K. J. Garner & C. P. Kyriacou

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  1. M. Bottecchia
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  2. S. G. Oliveira
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  3. L. G. S. R. Bauzer
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  4. N. A. Souza
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  5. R. D. Ward
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  7. C. P. Kyriacou
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  8. A. A. Peixoto
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Correspondence to A. A. Peixoto.

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Bottecchia, M., Oliveira, S.G., Bauzer, L.G.S.R. et al. Genetic Divergence in the cacophony IVS6 Intron Among Five BrazilianPopulations of Lutzomyia longipalpis . J Mol Evol 58, 754–761 (2004). https://doi.org/10.1007/s00239-004-2586-y

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