#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Macrogeographic genetic structure of Lutzomyia longipalpis complex populations using Next Generation Sequencing


Autoři: Aline Etelvina Casaril aff001;  Diego Peres Alonso aff003;  Karina Garcia Franco aff002;  Marcus Vinicius Niz Alvarez aff003;  Suellem Petilim Gomes Barrios aff001;  Wagner de Souza Fernandes aff001;  Jucelei de Oliveira Moura Infran aff002;  Ana Caroline Moura Rodrigues aff004;  Paulo Eduardo Martins Ribolla aff003;  Alessandra Gutierrez de Oliveira aff001
Působiště autorů: Programa de Pós-Graduação em Doenças Infecciosas e Parasitárias, Universidade Federal de Mato Grosso do Sul, Campo Grande, Mato Grosso do Sul, Brasil aff001;  Laboratório de Parasitologia Humana, Universidade Federal de Mato Grosso do Sul, Campo Grande, Mato Grosso do Sul, Brasil aff002;  Laboratório de Pesquisas e Análises Genéticas, Departamento de Parasitologia, Universidade Estadual Paulista, Botucatu, São Paulo, Brasil aff003;  Laboratório de Doenças Parasitárias, Universidade Estadual do Ceará, Fortaleza, Ceará aff004
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pone.0223277

Souhrn

Lutzomyia longipalpis is the main vector of Leishmania infantum, the causative agent of visceral leishmaniasis in the Neotropical realm. Its taxonomic status has been widely discussed once it encompasses a complex of species. The knowledge about the genetic structure of insect vector populations helps the elucidation of components and interactions of the disease ecoepidemiology. Thus, the objective of this study was to genotypically analyze populations of the Lu. longipalpis complex from a macrogeographic perspective using Next Generation Sequencing. Polymorphism analysis of three molecular markers was used to access the levels of population genetic structure among nine different populations of sand flies. Illumina Amplicon Sequencing Protocol® was used to identify possible polymorphic sites. The library was sequenced on paired-end Illumina MiSeq platform. Significant macrogeographical population differentiation was observed among Lu. longipalpis populations via PCA and DAPC analyses. Our results revealed that populations of Lu. longipalpis from the nine municipalities were grouped into three clusters. In addition, it was observed that the levels of Lu. longipalpis population structure could be associated with distance isolation. This new sequencing method allowed us to study different molecular markers after a single sequencing run, and to evaluate population and inter-species differences on a macrogeographic scale.

Klíčová slova:

Principal component analysis – Sequence assembly tools – Population genetics – Polymerase chain reaction – Brazil – Next-generation sequencing – Sand flies – Insect vectors


Zdroje

1. Lutz A, Neiva A. Contribuição para o conhecimento das espécies do gênero Phlebotomus existente no Brasil. Memórias do Instituto Oswaldo Cruz. 1912; 4(1): 84–95. doi: 10.1590/S0074-02761912000100006

2. Deane LM, Deane MP. Encontro de leishmânias nas vísceras e na pele de uma raposa em zona endêmica de calazar, nos arredores de Sobral. Hospital. 1954a; 45: 419–421.

3. Deane MP, Deane LM. Infecção natural do Phlebotomus longipalpis por leptomonas, provavelmente de Leishmania donovani, em foco de calazar, no Ceará. Hospital. 1954b; 45: 697–702.

4. Deane LM. Leishmaniose Visceral no Brasil. Estudos sobre reservatórios e Transmissores realizados no estado do Ceará. Serviço Nacional de Educação Sanitária, Brasil.1956; viii: 82–84.

5. Lainson R, Ward RD, Shaw JJ. Experimental transmission of Leishmania chagasi causative agent of neotropical visceral leishmaniasis, by the sandfly Lutzomyia longipalpis. Nature. 1977; 266: 628–630. doi: 10.1038/266628a0 859627

6. Lainson R, Rangel EF. Lutzomyia longipalpis and the eco-epidemiology of American visceral leishmaniasis, with particular reference to Brazil–a review. Memórias do Instituto Oswaldo Cruz. 2005; 100: 811–827. doi: 10.1590/s0074-02762005000800001 16444411

7. WHO. World Health Organization. Leishmaniasis. Fact sheet. 2017. http://www.who.int/mediacentre/factsheets/fs375/en/

8. Aguiar GM, Medeiros WM. Distribuição regional e habitats das espécies de flebotomíneos do Brasil. In: RANGEL E.; LAINSON R. Flebotomíneos do Brasil. Rio de Janeiro: Fiocruz, cap.3, p.207–255, 2003.

9. Salomón OD, Basmajdian Y, Fernández MS, Santini MS. Lutzomyia longipalpis in Uruguay: the first report and the potential of visceral leishmaniasis transmission. Memórias do Instituto Oswaldo Cruz. 2011; 106: 381–382. doi: 10.1590/s0074-02762011000300023 21655832

10. Souza GD, Santos E, Andrade-Filho JD. The first report of the main vector of visceral leishmaniasis in America, Lutzomyia longipalpis (Lutz & Neiva) (Diptera: Psychodidae: Phlebotominae), in the state of Rio Grande do Sul, Brazil. Memórias do Instituto Oswaldo Cruz. 2009; 104: 1181–1182. doi: 10.1590/s0074-02762009000800017 20140381

11. Mangabeira O. Sobre a sistemática e Biologia dos Phlebotomus do Ceará. Revista Brasileira de Malariologia e Doenças Tropicais. 1969; 21: 3–25.

12. Araki AS, Vigoder FM, Bauzer LGSR, Ferreira GEM, Souza NA, Araujo IB, et al. Molecular and Behavioral Differentiation among Brazilian Populations of Lutzomyia longipalpis (Diptera:Psychodidae:Phlebotominae). Plos Neglected Tropical Diseases. 2009; 3: (e365): 1–12. doi: 10.1371/journal.pntd.0000365.g001

13. Bauzer LGSR, Souza NA, Maingon RDC, Peixoto A. Lutzomyia longipalpis in Brazil: a complex or a single species? A mini-review. Memórias do Instituto Oswaldo Cruz. 2007; 102(1): 1–12. doi: 10.1590/s0074-02762007000100001 17293992

14. Gouveia C, Asensi MD, Zahner V, Rangel EF, Oliveira SMP. Study on the Bacterial Midgut Microbiota Associated to Different Brazilian Populations of Lutzomyia longipalpis (Lutz & Neiva) (Diptera: Psychodidae). Neotropical Entomology. 2008; 37: 597–601. doi: 10.1590/S1519-566X2008000500016 19061048

15. Hamilton JGC, Dougherty MJ, Ward RD. Sex pheromone activity in a single component of tergal gland extract of Lutzomyia Longipalpis (Diptera: Psychodidae) from Jacobina, Northeastern Brazil. Journal of Chemical Ecology. 1994; 2: 141–151.

16. Lane R, Phillips A, Procter G, Ward RD. Chemical analysis of the abdominal glands of two forms of Lutzomyia longipalpis: site of a possible sex pheromone. Annals of Tropical Medicine Parasitology. 1985; 79(2): 225–229. doi: 10.1080/00034983.1985.11811912 4096569

17. Aransay A, Scoulica E, Tselentis Y, Ready P. Phylogenetic relationships of phlebotomine sandflies inferred from small subunit nuclear ribosomal DNA. Insect Molecular Biology. 2000; 9: 157–168. doi: 10.1046/j.1365-2583.2000.00168.x 10762423

18. Bauzer L, Gesto J, Souza N, Ward R, Hamilton J, Kyriacou C, et al. Molecular divergence in the period gene between two putative sympatric species of the Lutzomyia longipalpis Complex. Molecular Biology and Evolution. 2002; 19: 1624–1627. doi: 10.1093/oxfordjournals.molbev.a004224 12200489

19. Bottechia M, Oliveira SG, Bauzer LGSR, Souza NA, Ward RD, Garner KJ, et al. Genetic divergence in the cacophony IVS6 intron among five Brazilian populations of Lutzomyia longipalpis. Journal of Molecular Evolution. 2004; 58: 754–761. doi: 10.1007/s00239-004-2586-y 15461432

20. Depaquit J, Perrotey S, Lecointre G, Tillier A, Tillier S, Ferté H, et al. Systématique moléculaire des phlebotominae: Étude pilote. Paraphylie du genre Phlebotomus. Comptes Rendus de l’Académie des Sciences. 1998; 321: 849–855.

21. Lins RM, Souza NA, Peixoto AA. Genetic divergence between two sympatric species of the Lutzomyia longipalpis complex in the paralytic gene, a locus associated with insecticide resistance and lovesong production. Memórias do Instituto Oswaldo Cruz. 2008; 103: 736–740. doi: 10.1590/s0074-02762008000700019 19057828

22. Ribolla PEM, Gushi LT, Cruz MSP, Costa CHN, Costa DL, Lima-Jr MSC, et al. Leishmania infantum Genetic Diversity and Lutzomyia longipalpis Mitochondrial Haplotypes in Brazil. BioMed Research International. 2016; Article ID 9249217: 1–11. doi: 10.1155/2016/9249217 27119085

23. Galati EAB. Classification Morphology and Terminology of Adults and Identification of American Taxa. In: Rangel EF, Lainson R, editors. Brazilian Sand Flies: Biology, Taxonomy, Medical Importance and Control. Springer; 2018. pp. 9–212.

24. Beati L, Cáceres A, Lee J, Munstermann L. Systematic relationships among Lutzomyia sand flies (Diptera: Psychodidae) of Peru and Colombia based on the analysis of 12S and 28S ribosomal DNA sequences. International Journal for Parasitology. 2004; 34: 225–234. doi: 10.1016/j.ijpara.2003.10.012 15037108

25. Lins RMMA, Oliveira SG, Souza NA, Queiroz RG, Justiniano SCB, Ward RD, et al. Molecular evolution of the cacophony IVS6 region in sandflies. Insect Molecular Biology. 2002; 11: 117–122. doi: 10.1046/j.1365-2583.2002.00315.x 11966876

26. Langmead B, Trapnell C, Pop M, Salzberg SL. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biology. 2009; 10: R25.1–R25. doi: 10.1186/gb-2009-10-3-r25 19261174

27. Weir BS, Cockerham CC. Estimating F-statistics for the analysis of population structure. Evolution. 1984; 38:1358–1370. doi: 10.1111/j.1558-5646.1984.tb05657.x 28563791

28. Coutinho-Abreu IV, Sonoda IV, Fonseca JA, Melo MA, Balbino VQ, Ramalho-Ortigão M. Lutzomyia longipalpis s.l. in Brazil and the impact of the Sao Francisco River in the speciation of this sand fly vector. Parasites & Vectors. 2008; 1: 1–11. doi: 10.1186/1756-3305-1-16 18549496

29. Ebrahimi S, Bordbar A, Parvizi P. Genetic dynamics in the sand fly (Diptera: Psychodidae) nuclear and mitochondrial genotypes: evidence for vector adaptation at the border of Iran with Iraq. Parasites & Vectors. 2016; 9: 1–13. doi: 10.1186/s13071-016-1603-5 27260204

30. Mantel N. The detection of disease clustering and a generalized regression approach. Cancer Research. 1967; 27: 209–220. 6018555

31. Soto SIU, Lehmann T, Rowton ED, Vélez ID, Porter CH. Speciation and Population Structure in the Morphospecies Lutzomyia longipalpis (Lutz & Neiva) as Derived from the Mitochondrial ND4 Gene. Molecular Phylogenetics and Evolution. 2001; 18: 84–93. doi: 10.1006/mpev.2000.0863 11161745

32. Zhang L, Ma Y, Xu J. Genetic differentiation between sandfly populations of Phlebotomus chinensis and Phlebotomus sichuanensis (Diptera: Psychodidae) in China inferred by microsatellites. Parasites & Vectors. 2013; 6: 1–10. doi: 10.1186/1756-3305-6-115 23607337

33. Hongyu K, Sandanielo VLM, Oliveira GJ Jr. Análise de Componentes Principais: resumo teórico, aplicação e interpretação.—Engineering and Science. 2015; 5: 83–90.

34. Ogawa LM, Vallender EJ. Genetic substructure in cynomolgus macaques (Macaca fascicularis) on the island of Mauritius. BMC Genomics. 2014; 15:1–14.

35. Meirmans PG, Hedrick PW. Assessing population structure: FST and related measures. Molecular Ecology Resources. 2011; 11: 5–18. doi: 10.1111/j.1755-0998.2010.02927.x 21429096

36. Golczer G, Arrivillaga J. Use and trends of molecular markers in sandflies (Diptera: Psychodidae). Boletin de Malariologia y Salud Ambiental. 2015; 55:19–40.

37. Santos MFC, Ribolla PEM, Alonso DP, Andrade-Filho JD, Casaril AE, Ferreira AMT, et al. Genetic structure of Lutzomyia longipalpis populations in Mato Grosso do Sul, Brazil, based on microsatellite markers. Plos One. 2013; 8:1–7. doi: 10.1371/journal.pone.0074268 24066129

38. Souza NA, Brazil RP, Araki AS. The current status of the Lutzomyia longipalpis (Diptera: Psychodidae: Phlebotominae) species complex. Memórias do Instituto Oswaldo Cruz. 2017; 112: 161–174. doi: 10.1590/0074-02760160463 28225906

39. Spiegel CN, Dias DBS, Araki AS, Hamilton JGC, Brazil RP. Jones TM. The Lutzomyia longipalpis complex: a brief natural history of aggregation-sex pheromone communication. Parasites & Vectors. 2016; 9. doi: 10.1186/s13071-016-1866-x 27842601

40. Vigoder FM, Souza NA, Brazil RP, Bruno RV, Costa PL, Ritchie MG, et al. Phenotypic differentiation in love song traits among sibling species of the Lutzomyia longipalpis complex in Brazil. Parasites & Vectors. 2015; 8. doi: 10.1186/s13071-015-0900-8 26017472

41. Adamson RE, Ward RD, Feliciangeli MD. Maingon R. The application of random amplified polymorphic DNA for sandfly species identification. Medical and Veterinary Entomology. 1993; 7: 203–207. doi: 10.1111/j.1365-2915.1993.tb00677.x 8369553

42. Arrivillaga J, Mutebi J, Piñango H, Norris D, Alexander B, Feliciangeli M, et al. The taxonomic status of genetically divergent populations of Lutzomyia longipalpis (diptera: Psychodidae) based on the distribution of mitochondrial and isozyme variation. Journal of Medical Entomology. 2003; 40: 615–627. doi: 10.1603/0022-2585-40.5.615 14596274

43. Maingon R, Feliciangeli MD, Ward R, Chance M, Adamson R, Rodriguez N, et al. Molecular approaches applied to the epidemiology of leishmaniasis in Venezuela. Archives De l’Institut Pasteur De Tunis. 1993; 70: 309–324. 7802485

44. Maingon R, Ward R, Hamilton J, Noyes H, Souza N, Kemp S, et al. Genetic identification of two sibling species of Lutzomyia longipalpis (Diptera: Psychodidae) that produce distinct male sex pheromones in Sobral, Ceará state, Brazil. Molecular Ecology. 2003; 12: 1879–1894. doi: 10.1046/j.1365-294x.2003.01871.x 12803639

45. Vivero R, Contreras-Gutierrez M, Bejarano E. Análisis de la estrutura primaria y secundaria del ARN de transferência mitocondrial para serina em siete especies de Lutzomyia. Biomédica. 2007; 27: 429–438.

46. Lozier JD. Revisiting comparisons of genetic diversity in stable and declining species: assessing genome-wide polymorphism in North American bumble bees using RAD sequencing. Molecular Ecology. 2014; 23: 788–801. doi: 10.1111/mec.12636 24351120

47. Novembre J, Stephens M. Interpreting principal component analyses of spatial population genetic variation. Nature Genetics. 2008; 40: 646–649. doi: 10.1038/ng.139 18425127

48. Ekblom R, Galindo J. Applications of next generation sequencing in molecular ecology of non-model organisms. Heredity. 2011; 107:1–15. doi: 10.1038/hdy.2010.152 21139633

49. Harismendy O, Ng PC, Strausberg RL, Wang X, Stockwell TB, Beeson KY, et al. Evaluation of next generation sequencing platforms for population targeted sequencing studies. Genome biology.2009; 10: R32.1–32.13. doi: 10.1186/gb-2009-10-3-r32 19327155

50. Shokralla S, Porter TM, Gibson JF, Dobosz R, Janzen DH, Hallwachs W, et al. Massively parallel multiplex DNA sequencing for specimen identification using an Illumina MiSeq platform. Scientific Reports. 2015; 5: 1–7. doi: 10.1038/srep09687 25884109

51. Willing EM, Dreyer C, Oosterhout C. Estimates of Genetic Differentiation Measured by FST Do Not Necessarily Require Large Sample Sizes When Using Many SNP Markers. Plos One. 2012; 7: e42649–e42649. doi: 10.1371/journal.pone.0042649 22905157

52. Wright S. Evolution and Genetics of Populations: Variability within and among Natural Populations. University of Chicago Press; 1978.

53. Hart DL, Clark AG. Princípios de Genética de Populações. 4st ed. Editora Artmed; 2010.

54. Darwin C. On the origin of species. The Eletronic Classic Series Hazleton; 1859.

55. Polato NR, Gray MM, Gill BA, Becker CG, Casner KL, Flecker AS, et al. Genetic diversity and gene flow decline with elevation in montane mayflies. Heredity. 2017; 119: 107–116. doi: 10.1038/hdy.2017.23 28489073

56. Star B, Spencer HG. Effects of Genetic Drift and Gene Flow on the Selective Maintenance of Genetic Variation. Genetics. 2013; 194: 235–244. doi: 10.1534/genetics.113.149781 23457235

57. Mayr E. Systematics and the Origin of Species, from the Viewpoint of a Zoologist. Columbia University Press; 1942.

58. Martins AB. Especiação por distância e a evolução de espécies em anel. PhD Thesis—Instituto de Biociências da Universidade de São Paulo. Departamento de Ecologia, 2014. http://www.teses.usp.br/teses/disponiveis/41/41134/tde-09122014-152748/pt-br.php.

59. Ridley M. Evolução. 3 st ed. Editora Artmed; 2006.

60. Slatkin M. Gene Flow and the Geographic Structure of Natural Populations. Science. 1987; 236: 787–792. doi: 10.1126/science.3576198 3576198

61. Jombart T, Devillard S, Balloux F. Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genetics. 2010; 11: 1–15.

62. Andrade-Filho JD, Brazil RP. Relationships of New World Phlebotomine Sand Flies (Diptera: Psychodidae) Based on Fossil Evidence. Memórias do Instituto Oswaldo Cruz. 2003; 98: 145–149. doi: 10.1590/S0074-02762003000900022 12687775

63. Watts PC, Hamilton J G, Ward RD, Noyes HA, Souza NA, Kemp SJ, et al. Male sex pheromones and the phylogeographic structure of the Lutzomyia longipalpis species complex (Diptera: Psychodidae) from Brazil and Venezuela. The American Journal of Tropical Medicine and Hygiene. 2005; 73: 734–743. 16222018

64. Arrivillaga JC, Feliciangeli MD. Lutzomyia pseudolongipalpis: The First New Species Within the longipalpis (Diptera: Psychodidae: Phlebotominae) Complex from La Rinconada, Curarigua, Lara State, Venezuela. Entomological Society of America. 2001; 38: 783–790. doi: 10.1603/0022-2585-38.6.783 11761375

65. Souza NA, Ward RD, Hamilton JGC, Kyriacou CP, Peixoto AA. Copulation songs in three siblings of Lutzomyia longipalpis (Diptera: Psychodidae). Transactions of the Royal Society of Tropical Medicine and Hygiene. 2002; 96: 102–103. doi: 10.1016/s0035-9203(02)90258-0 11925981

66. Souza NA, Vigoder FM, Araki AS, Ward RD, Kyriacou CP, Peixoto AA. Analysis of the copulatory courtship songs of Lutzomyia longipalpis in six populations from Brazil. Journal of Medical Entomology. 2004; 41: 906–913. doi: 10.1603/0022-2585-41.5.906 15535620

67. Ward R, Phillips A, Burnet B, Marcondes C. The Lutzomyia longipalpis complex: reproduction and distribution. In Biosystematics of Haematophagous Insects. Oxford: Oxford University Press. 1988; 258–69.

68. Hamilton JGC, Maingon RDC, Alexander B, Ward RD, Brazil RP. Analysis of the sex pheromone extract of individual male Lutzomyia longipalpis sandflies from six regions In Brazil. Medical and Veterinary Entomology. 2005; 19: 480–488. doi: 10.1111/j.1365-2915.2005.00594.x 16336313

69. Hamilton JGC, Dawson GW, Pickett JA. 9-Methylgermacrene-B; proposed structure for the novel homosesquiterpene sex pheromone of Lutzomyia longipalpis (Diptera: Psychodidae) from Lapinha, Brazil. Journal of Chemical Ecology. 1996; 22: 1477–1492. doi: 10.1007/BF02027726 24226250

70. Vigoder FM, Araki AS, Bauzer LGSR, Souza NA, Brazil RP, Peixoto AA. Lovesongs and period gene polymorphisms indicate Lutzomyia cruzi (Mangabeira, 1938) as a sibling species of the Lutzomyia longipalpis (Lutz and Neiva, 1912) complex. Infection, Genetics and Evolution. 2010; 10: 734–739. doi: 10.1016/j.meegid.2010.05.004 20478408

71. Aransay A, Scoulica E, Chaniotis B, Tselentis Y. Typing of sandflies from Greece and Cyprus by DNA polymorphism of 18S rRNA gene. Insect Molecular Biology. 1999; 8: 179–184. doi: 10.1046/j.1365-2583.1999.820179.x 10380101


Článok vyšiel v časopise

PLOS One


2019 Číslo 10
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Aktuální možnosti diagnostiky a léčby litiáz
nový kurz
Autori: MUDr. Tomáš Ürge, PhD.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#