The influence of anthropogenic habitat fragmentation on the genetic structure and diversity of the malaria vector Anopheles cruzii (Diptera: Culicidae)

Carregando...
Imagem de Miniatura
Citações na Scopus
18
Tipo de produção
article
Data de publicação
2020
Título da Revista
ISSN da Revista
Título do Volume
Editora
NATURE RESEARCH
Autores
MULTINI, Laura Cristina
MARRELLI, Mauro Toledo
WILKE, Andre Barretto Bruno
Citação
SCIENTIFIC REPORTS, v.10, n.1, article ID 18018, 13p, 2020
Projetos de Pesquisa
Unidades Organizacionais
Fascículo
Resumo
Fragmentation of natural environments as a result of human interference has been associated with a decrease in species richness and increase in abundance of a few species that have adapted to these environments. The Brazilian Atlantic Forest, which has been undergoing an intense process of fragmentation and deforestation caused by human-made changes to the environment, is an important hotspot for malaria transmission. The main vector of simian and human malaria in this biome is the mosquito Anopheles cruzii. Anthropogenic processes reduce the availability of natural resources at the tree canopies, An. cruzii primary habitat. As a consequence, An. cruzii moves to the border of the Atlantic Forest nearing urban areas seeking resources, increasing their contact with humans in the process. We hypothesized that different levels of anthropogenic changes to the environment can be an important factor in driving the genetic structure and diversity in An. cruzii populations. Five different hypotheses using a cross-sectional and a longitudinal design were tested to assess genetic structure in sympatric An. cruzii populations and microevolutionary processes driving these populations. Single nucleotide polymorphisms were used to assess microgeographic genetic structure in An. cruzii populations in a low-endemicity area in the city of Sao Paulo, Brazil. Our results show an overall weak genetic structure among the populations, indicating a high gene flow system. However, our results also pointed to the presence of significant genetic structure between sympatric An. cruzii populations collected at ground and tree-canopy habitats in the urban environment and higher genetic variation in the ground-level population. This indicates that anthropogenic modifications leading to habitat fragmentation and a higher genetic diversity and structure in groundlevel populations could be driving the behavior of An. cruzii, ultimately increasing its contact with humans. Understanding how anthropogenic changes in natural areas affect An. cruzii is essential for the development of more effective mosquito control strategies and, on a broader scale, for malariaelimination efforts in the Brazilian Atlantic Forest.
Palavras-chave
Referências
  1. Alvarado-Serrano DF, 2019, HEREDITY, V122, P29, DOI 10.1038/s41437-018-0106-x
  2. Araujo RV, 2015, BRAZ J INFECT DIS, V19, P146, DOI 10.1016/j.bjid.2014.10.004
  3. Archer FI, 2017, MOL ECOL RESOUR, V17, P5, DOI 10.1111/1755-0998.12559
  4. Ayala D, 2011, INFECT GENET EVOL, V11, P940, DOI 10.1016/j.meegid.2011.03.003
  5. Benjamini Y., 1995, THE J, V57, P289
  6. Brasil P, 2017, LANCET GLOB HEALTH, V5, pE1038, DOI 10.1016/S2214-109X(17)30333-9
  7. Wilke ABB, 2017, PLOS ONE, V12, DOI 10.1371/journal.pone.0185150
  8. Campos M, 2019, PARASIT VECTORS, V12, P1
  9. Campos M, 2017, PARASITE VECTOR, V10, DOI 10.1186/s13071-017-2014-y
  10. Ceretti W, 2016, J ARTHROPOD-BORNE DI, V10, P102
  11. Chadee DD, 2016, ACTA TROP, V156, P137, DOI 10.1016/j.actatropica.2015.12.022
  12. Danecek P, 2011, BIOINFORMATICS, V27, P2156, DOI 10.1093/bioinformatics/btr330
  13. de Pina-Costa A, 2014, MEM I OSWALDO CRUZ, V109, P618, DOI 10.1590/0074-0276140228
  14. Deane L.M., 1984, Memorias do Instituto Oswaldo Cruz, V79, P461, DOI 10.1590/S0074-02761984000400011
  15. DEANE L M, 1971, Revista do Instituto de Medicina Tropical de Sao Paulo, V13, P311
  16. DEANE LM, 1992, MEM I OSWALDO CRUZ, V87, P1, DOI 10.1590/S0074-02761992000700001
  17. DEANE LM, 1988, AM J TROP MED HYG, V38, P223, DOI 10.4269/ajtmh.1988.38.223
  18. Dias GD, 2018, PARASITE VECTOR, V11, DOI 10.1186/s13071-018-2615-0
  19. Dorville LFM, 1996, STUD NEOTROP FAUNA E, V31, P68, DOI 10.1076/snfe.31.2.68.13331
  20. Dray S, 2007, J STAT SOFTW, V22, P1, DOI 10.18637/jss.v022.i04
  21. Duarte AMRC, 2013, PARASITE VECTOR, V6, DOI 10.1186/1756-3305-6-58
  22. Earl DA, 2012, CONSERV GENET RESOUR, V4, P359, DOI 10.1007/s12686-011-9548-7
  23. Emerson KJ, 2015, PLOS ONE, V10, DOI 10.1371/journal.pone.0130773
  24. Evanno G, 2005, MOL ECOL, V14, P2611, DOI 10.1111/j.1365-294X.2005.02553.x
  25. Excoffier L, 2005, EVOL BIOINFORM, V1, P47, DOI 10.1177/117693430500100003
  26. Fadista J, 2016, EUR J HUM GENET, V24, P1202, DOI 10.1038/ejhg.2015.269
  27. Falush D, 2007, MOL ECOL NOTES, V7, P574, DOI 10.1111/j.1471-8286.2007.01758.x
  28. Fernandez ME, 2013, GENET MOL BIOL, V36, P185, DOI 10.1590/S1415-47572013000200008
  29. Ferreira MU, 2016, MALARIA J, V15, DOI 10.1186/s12936-016-1335-1
  30. Flanagan SP, 2017, J HERED, V108, P561, DOI 10.1093/jhered/esx048
  31. Forattini O P, 1968, Rev Saude Publica, V2, P111
  32. Forattini O.P., 2002, CULICIDOLOGIA MED
  33. FORATTINI OP, 1993, REV SAUDE PUBL, V27, P398, DOI 10.1590/S0034-89101993000600002
  34. Forattini OP, 1996, REV SAUDE PUBL, V30, P107, DOI 10.1590/S0034-89101996000200001
  35. Forattini OP, 2000, REV SAUDE PUBL, V34, P565, DOI 10.1590/S0034-89102000000600001
  36. Gadelha P., 1994, Parassitologia (Rome), V36, P175
  37. Gardner TA, 2009, ECOL LETT, V12, P561, DOI 10.1111/j.1461-0248.2009.01294.x
  38. GOMES AD, 1985, REV SAUDE PUBL, V19, P190, DOI 10.1590/S0034-89101985000200009
  39. Gould E, 2017, ONE HEALTH-AMSTERDAM, V4, P1, DOI 10.1016/j.onehlt.2017.06.001
  40. Griffing SM, 2015, MEM I OSWALDO CRUZ, V110, P701, DOI 10.1590/0074-02760150041
  41. Guimaraes AE, 2000, MEM I OSWALDO CRUZ, V95, P17, DOI 10.1590/S0074-02762000000100002
  42. Hale ML, 2012, PLOS ONE, V7, DOI 10.1371/journal.pone.0045170
  43. Helyar SJ, 2011, MOL ECOL RESOUR, V11, P123, DOI 10.1111/j.1755-0998.2010.02943.x
  44. Johnson MTJ, 2017, SCIENCE, V358, DOI 10.1126/science.aam8327
  45. Joly CA, 2014, NEW PHYTOL, V204, P459, DOI 10.1111/nph.12989
  46. Jombart T, 2008, BIOINFORMATICS, V24, P1403, DOI 10.1093/bioinformatics/btn129
  47. Jost L, 2008, MOL ECOL, V17, P4015, DOI 10.1111/j.1365-294X.2008.03887.x
  48. Kirchgatter K, 2014, REV INST MED TROP SP, V56, P403, DOI 10.1590/S0036-46652014000500006
  49. Knop E, 2016, GLOBAL CHANGE BIOL, V22, P228, DOI 10.1111/gcb.13091
  50. LaDeau SL, 2015, FUNCT ECOL, V29, P889, DOI 10.1111/1365-2435.12487
  51. Lanes EC, 2018, FRONT PLANT SCI, V9, DOI 10.3389/fpls.2018.00532
  52. Laporta GZ, 2015, MALARIA J, V14, DOI 10.1186/s12936-015-0680-9
  53. Laporta GZ, 2013, PLOS NEGLECT TROP D, V7, DOI 10.1371/journal.pntd.0002139
  54. Lee Y, 2014, MOL ECOL RESOUR, V14, P297, DOI 10.1111/1755-0998.12181
  55. Lee Y, 2012, J MED ENTOMOL, V49, P307, DOI 10.1603/ME11113
  56. Li H, 2009, BIOINFORMATICS, V25, P2078, DOI 10.1093/bioinformatics/btp352
  57. Lima JMT, 2017, PHILOS T R SOC B, V372, DOI 10.1098/rstb.2016.0125
  58. Lorenz C, 2017, INFECT GENET EVOL, V54, P205, DOI 10.1016/j.meegid.2017.06.029
  59. Lorenz C, 2014, PARASITE VECTOR, V7, DOI 10.1186/s13071-014-0581-8
  60. Louise C, 2015, PLOS ONE, V10, DOI 10.1371/journal.pone.0137851
  61. Marques GRAM, 2009, REV SAUDE PUBL, V43, P369, DOI 10.1590/s0034-89102009005000006
  62. Marrelli MT, 2007, MALARIA J, V6, DOI 10.1186/1475-2875-6-127
  63. McKinney ML, 2006, BIOL CONSERV, V127, P247, DOI 10.1016/j.biocon.2005.09.005
  64. Medeiros-Sousa AR, 2019, MALARIA J, V18, DOI 10.1186/s12936-019-2744-8
  65. Medeiros-Sousa AR, 2017, SCI REP-UK, V7, DOI 10.1038/s41598-017-18208-x
  66. Meirmans PG, 2011, MOL ECOL RESOUR, V11, P5, DOI 10.1111/j.1755-0998.2010.02927.x
  67. Meneguzzi VC, 2009, MEM I OSWALDO CRUZ, V104, P570, DOI 10.1590/S0074-02762009000400006
  68. Miles A, 2017, NATURE, V552, P96, DOI 10.1038/nature24995
  69. Ministerio da Saude, 2018, SIST INF AGR NOT SIN
  70. Morellato LPC, 2000, BIOTROPICA, V32, P786, DOI 10.1646/0006-3606(2000)032[0786:ITBAF]2.0.CO;2
  71. Morin PA, 2004, TRENDS ECOL EVOL, V19, P208, DOI 10.1016/j.tree.2004.01.009
  72. Multini LC, 2019, TRENDS PARASITOL, V35, P383, DOI 10.1016/j.pt.2019.03.009
  73. Multini LC, 2019, PLOS ONE, V14, DOI 10.1371/journal.pone.0220773
  74. Multini LC, 2019, ACTA TROP, V190, P30, DOI 10.1016/j.actatropica.2018.10.009
  75. Multini LC, 2016, PLOS ONE, V11, DOI 10.1371/journal.pone.0162328
  76. Sallum MAM, 2014, MALARIA J, V13, DOI 10.1186/1475-2875-13-337
  77. Myers N, 2000, NATURE, V403, P853, DOI 10.1038/35002501
  78. Narasimhan V, 2016, BIOINFORMATICS, V32, P1749, DOI 10.1093/bioinformatics/btw044
  79. Pelletier F, 2018, BMC BIOL, V16, DOI 10.1186/s12915-017-0476-1
  80. Prussing C, 2018, MALARIA J, V17, DOI 10.1186/s12936-018-2234-4
  81. R Core Team, 2017, R LANGUAGE ENV STAT, V2, P1
  82. Rezende CL, 2018, PERSPECT ECOL CONSER, V16, P208, DOI 10.1016/j.pecon.2018.10.002
  83. Ribeiro AF, 2012, J VECTOR ECOL, V37, P316, DOI 10.1111/j.1948-7134.2012.00233.x
  84. Ribeiro MC, 2009, BIOL CONSERV, V142, P1141, DOI 10.1016/j.biocon.2009.02.021
  85. Rochlin I, 2016, NAT COMMUN, V7, DOI 10.1038/ncomms13604
  86. Rona LDP, 2013, BMC EVOL BIOL, V13, DOI 10.1186/1471-2148-13-207
  87. Rona LDP, 2010, BMC EVOL BIOL, V10, DOI 10.1186/1471-2148-10-91
  88. Russello MA, 2015, PEERJ, V3, DOI 10.7717/peerj.1106
  89. Schmidt TL, 2017, PLOS NEGLECT TROP D, V11, DOI 10.1371/journal.pntd.0006009
  90. Sobota RS, 2015, ANN HUM GENET, V79, P136, DOI 10.1111/ahg.12095
  91. Ueno HM, 2007, REV SAUDE PUBL, V41, P269, DOI 10.1590/S0034-89102007000200014
  92. Vignal A, 2002, GENET SEL EVOL, V34, P275, DOI [10.1186/1297-9686-34-3-275, 10.1051/gse:2002009]
  93. Weaver SC, 2013, TRENDS MICROBIOL, V21, P360, DOI 10.1016/j.tim.2013.03.003
  94. Wilke ABB, 2019, CURR OPIN INSECT SCI, V35, P1, DOI 10.1016/j.cois.2019.06.002
  95. Wilke ABB, 2019, SCI REP-UK, V9, DOI 10.1038/s41598-019-45337-2
  96. Wilke ABB, 2018, INFECT GENET EVOL, V65, P333, DOI 10.1016/j.meegid.2018.08.017
  97. Yamasaki T, 2011, J MED PRIMATOL, V40, P392, DOI 10.1111/j.1600-0684.2011.00498.x