期刊论文详细信息
BMC Evolutionary Biology
Evidence for the occurrence of two sympatric sibling species within the Anopheles (Kerteszia) cruzii complex in southeast Brazil and the detection of asymmetric introgression between them using a multilocus analysis
Alexandre A Peixoto1  Carlos J Carvalho-Pinto1  Luísa DP Rona1 
[1] Instituto Nacional de Ciência e Tecnologia em Entomologia Molecular, Rio de Janeiro, RJ, Brazil
关键词: Mosquitoes;    Malaria;    Multilocus analysis;    Complex of cryptic species;    Speciation;    Anopheles;   
Others  :  1085949
DOI  :  10.1186/1471-2148-13-207
 received in 2012-12-07, accepted in 2013-08-21,  发布年份 2013
PDF
【 摘 要 】

Background

Anopheles (Kerteszia) cruzii (Diptera: Culicidae) is a primary vector of human and simian malaria parasites in southern and southeastern Brazil. Earlier studies using chromosome inversions, isoenzymes and a number of molecular markers have suggested that An. cruzii is a species complex.

Results

In this study, a multilocus approach using six loci, three circadian clock genes and three encoding ribosomal proteins, was carried out to investigate in more detail the genetic differentiation between the An. cruzii populations from Florianópolis–Santa Catarina (southern Brazil) and Itatiaia–Rio de Janeiro States (southeastern Brazil). The analyses were performed first comparing Florianópolis and Itatiaia, and then comparing the two putative sympatric incipient species from Itatiaia (Itatiaia A and Itatiaia B). The analysis revealed high FST values between Florianópolis and Itatiaia (considering Itatiaia A and B together) and also between the sympatric Itatiaia A and Itatiaia B, irrespective of their function. Also, using the IM program, no strong indication of migration was found between Florianópolis and Itatiaia (considering Itatiaia A and B together) using all loci together, but between Itatiaia A and Itatiaia B, the results show evidence of migration only in the direction of Itatiaia B.

Conclusions

The results of the multilocus analysis indicate that Florianópolis and Itatiaia represent different species of the An. cruzii complex that diverged around 0.6 Mya, and also that the Itatiaia sample is composed of two sympatric incipient species A and B, which diverged around 0.2 Mya. Asymmetric introgression was found between the latter two species despite strong divergence in some loci.

【 授权许可】

   
2013 Rona et al.; licensee BioMed Central Ltd.

【 预 览 】
附件列表
Files Size Format View
20150113181823893.pdf 1725KB PDF download
Figure 5. 69KB Image download
Figure 4. 33KB Image download
Figure 3. 56KB Image download
Figure 2. 56KB Image download
Figure 1. 49KB Image download
【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

【 参考文献 】
  • [1]Harbach RE: The culicidae (Diptera): a review of taxonomy, classification and phylogeny. Zootaxa 2007, 1668:591-638.
  • [2]Krzywinski J, Besansky NJ: Molecular systematics of Anopheles: from sub- genera to subpopulations. Annu Rev Entomol 2003, 48:111-139.
  • [3]Loaiza JR, Bermingham E, Sanjur OI, Scott ME, Bickersmith SA, Conn JE: Review of genetic diversity in malaria vectors (Culicidae: anophelinae). Infect Genet Evol 2012, 12:1-12.
  • [4]Consoli RAGB, Lourenço-de-Oliveira R: Principais mosquitos de importância sanitária no Brasil. Rio de Janeiro: Ed. Fiocruz; 1994.
  • [5]Marques GRAM, Forattini OP: Aedes albopictus em bromélias de solo em Ilhabela, litoral do estado de São Paulo. Rev Saude Publica 2005, 39:548-552.
  • [6]Marrelli MT, Malafronte RS, Sallum MA, Natal D: Kerteszia subgenus of Anopheles associated with the Brazilian Atlantic rainforest: current knowledge and future challenges. Malar J 2007, 6:127. BioMed Central Full Text
  • [7]Rachou RG: Anofelinos do Brasil: comportamento das espécies vetoras de malária. Rev Bras Malariol Doencas Trop 1958, 10:145-181.
  • [8]Deane LM, Ferreira-Neto JA, Deane SP, Silveira IP: Anopheles (Kerteszia) cruzii, a natural vector of the monkey malaria parasites, Plasmodium simium and Plamodium brasilianum. Trans R Soc Trop Med Hyg 1970, 64:647.
  • [9]Forattini OP, Kakitani I, Marques GRAM, Brito M: Formas imaturas de anofelíneos em recipientes artificiais. Rev Saude Publica 1998, 32:189-191.
  • [10]Rezende HR, Cerutti C Jr, Santos CB: Aspectos atuais da distribuição geográfica de Anopheles (Kerteszia) cruzii DYAR & KNAB, 1908 no Estado do Espírito Santo, Brasil. Entomol Vectores 2005, 12:123-126.
  • [11]Laporta GZ, Ramos DG, Ribeiro MC, Sallum MA: Habitat suitability of Anopheles vector species and association with human malaria in the Atlantic forest in south-eastern Brazil. Mem Inst Oswaldo Cruz 2011, 1:239-245.
  • [12]Marrelli MT, Honorio NA, Flores-Mendoza C, Lourenco-de-Oliveira R, Marinotti O, Kloetzel JK: Comparative susceptibility of two members of the Anopheles oswaldoi complex, An. oswaldoi and An. konderi to infection by Plasmodium vivax. Trans R Soc Trop Med Hyg 1999, 93:381-384.
  • [13]Della Torre A, Costantini C, Besansky NJ, Caccone A, Petrarca V, Powell JR, Coluzzi M: Speciation within Anopheles gambiae–the glass is half full. Science 2002, 298:115-117.
  • [14]Riehle MM, Guelbeogo WM, Gneme A, Eiglmeier K, Holm I, Bischoff E, Garnier T, Snyder GM, Li X, Markianos K, Sagnon N, Vernick KD: A cryptic subgroup of Anopheles gambiae is highly susceptible to human malaria parasites. Science 2011, 331:596-598.
  • [15]Norris DE: Genetic markers for study of the anopheline vectors of human malaria. Int J Parasitol 2002, 32:1607-1615.
  • [16]Djadid ND, Gholizadeh S, Aghajari M, Zehi AH, Raeisi A, Zakeri S: Genetic analysis of rDNA-ITS2 and RAPD loci in field populations of the malaria vector, Anopheles stephensi (Diptera: Culicidae): implications for the control program in Iran. Acta Trop 2006, 97:65-74.
  • [17]Bass C, Williamson MS, Field LM: Development of a multiplex real-time PCR assay for identification of members of the Anopheles gambiae species complex. Acta Trop 2008, 107:50-53.
  • [18]Paredes-Esquivel C, Donnelly MJ, Harbach RE, Townson H: A molecular phylogeny of mosquitoes in the Anopheles barbirostris Subgroup reveals cryptic species: implications for identification of disease vectors. Mol Phylogenet Evol 2009, 50:141-151.
  • [19]Chandra G, Bhattacharjee I, Chatterjee S: A review on Anopheles subpictus Grassi--a biological vector. Acta Trop 2010, 115:142-154.
  • [20]Seah IM, Ambrose L, Cooper RD, Beebe NW: Multilocus population genetic analysis of the Southwest Pacific malaria vector Anopheles punctulatus. Int J Parasitol 2013, 43:825-835.
  • [21]Coetzee M, Koekemoer LL: Molecular systematics and insecticide resistance in the major African malaria vector Anopheles funestus. Annu Rev Entomol 2013, 58:393-412.
  • [22]Ramirez CC, Dessen EM: Chromosomal evidence for sibling species of the malaria vector Anopheles cruzii. Genome 2000, 43:143-151.
  • [23]Ramirez CC, Dessen EM: Chromosome differentiated populations of Anopheles cruzii: evidence for a third sibling species. Genetica 2000, 108:73-80.
  • [24]Carvalho-Pinto CJ, Lourenço-de-Oliveira R: Isoenzymatic analysis of four Anopheles (Kerteszia) cruzii (Diptera: Culicidae) populations of Brazil. Mem Inst Oswaldo Cruz 2004, 99:471-475.
  • [25]Rona LD, Carvalho-Pinto CJ, Gentile C, Grisard EC, Peixoto AA: Assessing the molecular divergence between Anopheles (Kerteszia) cruzii populations from Brazil using the timeless gene: further evidence of a species complex. Malar J 2009, 8:60. BioMed Central Full Text
  • [26]Rona LD, Carvalho-Pinto CJ, Mazzoni CJ, Peixoto AA: Estimation of divergence time between two sibling species of the Anopheles (Kerteszia) cruzii complex using a multilocus approach. BMC Evol Biol 2010, 10:91. BioMed Central Full Text
  • [27]Rona LD, Carvalho-Pinto CJ, Peixoto AA: Molecular evidence for the occurrence of a new sibling species within the Anopheles (Kerteszia) cruzii complex in south-east Brazil. Malar J 2010, 9:33. BioMed Central Full Text
  • [28]Tajima F: Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 1989, 123:585-595.
  • [29]Fu YX, Li WH: Statistical tests of neutrality of mutations. Genetics 1993, 133:693-709.
  • [30]Nei M, Kumar S: Molecular evolution and phylogenetics. New York: Oxford University Press; 2000.
  • [31]Hey J, Nielsen R: Multilocus methods for estimating population sizes, migration rates and divergence time, with applications to the divergence of Drosophila pseudoobscura and D. persimilis. Genetics 2004, 167:747-760.
  • [32]Guindon S, Gascuel O: A simple, fast and accurate method to estimate large phylogenies by maximum-likelihood. Syst Biol 2003, 52:696-704.
  • [33]Posada D: jModelTest: phylogenetic model averaging. Mol Biol Evol 2008, 25:1253-1256.
  • [34]Kimura M: A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 1980, 16:111-120.
  • [35]Li WH: Molecular evolution. Sunderland: Sinauer Associates; 1997.
  • [36]Hey J, Pinho C: Population genetics and objectivity in species diagnosis. Evolution 2012, 66:1413-1429.
  • [37]Ayala FJ, Coluzzi M: Chromosome speciation: humans, drosophila, and mosquitoes. Proc Natl Acad Sci U S A 2005, 102:6535-6542.
  • [38]Hoffmann AA, Rieseberg L: Revisiting the impact of inversions in evolution: from population genetic markers to drivers of adaptive shifts and speciation? Annu Rev Ecol Evol Syst 2008, 39:21-42.
  • [39]Feder JL, Nosil P: Chromosomal inversions and species differences: when are genes affecting adaptive divergence and reproductive isolation expected to reside within inversions? Evolution 2009, 63:3061-3075.
  • [40]Turner TL, Hahn MW, Nuzhdin SV: Genomic islands of speciation in Anopheles gambiae. PLoS Biol 2005, 3:e285.
  • [41]Wang-Sattler R, Blandin S, Ning Y, Blass C, Dolo G, Touré YT, Delle Torre A, Lanzaro GC, Steinmetz LM, Kafatos FC, Zheng L: Mosaic genome architecture of the Anopheles gambiae species complex. PLoS One 2007, 2:e1249.
  • [42]Marsden CD, Lee Y, Nieman CC, Sanford MR, Dinis J, Martins C, Rodrigues A, Cornel AJ, Lanzaro GC: Asymmetric introgression between the M and S forms of the malaria vector, Anopheles gambiae, maintains divergence despite extensive hybridization. Mol Ecol 2011, 20:4983-4994.
  • [43]Donnelly MJ, Pinto J, Girod R, Besansky NJ, Lehmann T: Revisiting the role of introgression vs shared ancestral polymorphisms as key processes shaping genetic diversity in the recently separated sibling species of the Anopheles gambiae complex. Heredity 2004, 92:61-68.
  • [44]Nevado B, Fazalova V, Backeljau T, Hanssens M, Verheyen E: Repeated unidirectional introgression of nuclear and mitochondrial DNA between four congeneric Tanganyikan cichlids. Mol Biol Evol 2011, 28:2253-2267.
  • [45]Khimoun A, Burrus M, Andalo C, Liu ZL, Vicédo-Cazettes C, Thébaud C, Pujol B: Locally asymmetric introgressions between subspecies suggest circular range expansion at the Antirrhinum majus global scale. J Evol Biol 2011, 24:1433-1441.
  • [46]Jacquemyn H, Brys R, Honnay O, Roldan-Ruiz I: Asymmetric gene introgression in two closely related Orchis species: evidence from morphometric and genetic analyses. BMC Evol Biol 2012, 12:178. BioMed Central Full Text
  • [47]Godbout J, Yeh FC, Bousquet J: Large-scale asymmetric introgression of cytoplasmic DNA reveals Holocene range displacement in a North American boreal pine complex. Ecol Evol 2012, 2:1853-1866.
  • [48]Beysard M, Perrin N, Jaarola M, Heckel G, Vogel P: Asymmetric and differential gene introgression at a contact zone between two highly divergent lineages of field voles (Microtus agrestis). J Evol Biol 2012, 25:400-408.
  • [49]Gomes B, Sousa CA, Novo MT, Freitas FB, Alves R, Côrte-Real AR, Salgueiro P, Donnelly MJ, Almeida AP, Pinto J: Asymmetric introgression between sympatric molestus and pipiens forms of Culex pipiens (Diptera: Culicidae) in the Comporta region. Portugal. BMC Evol Biol 2009, 9:262. BioMed Central Full Text
  • [50]Cantolla AU: Earth’s climate history: servicio central de publicaciones del gobierno vasco. 2003.
  • [51]Mirabello L, Conn JE: Population analysis using the nuclear white gene detects Pliocene/Pleistocene lineage divergence within Anopheles nuneztovari in South America. Med Vet Entomol 2008, 22:109-119.
  • [52]O’Loughlin SM, Okabayashi T, Honda M, Kitazoe Y, Kishino H, Somboon P, Sochantha T, Nambanya S, Saikia PK, Dev V, Walton C: Complex population history of two Anopheles dirus mosquito species in South Asia suggests the influence of Pleistocene climate change rather than human- mediated effects. J Evol Biol 2008, 21:1555-1569.
  • [53]Loaiza JR, Scott ME, Bermingham E, Rovira J, Conn JE: Evidence for Pleistocene population divergence and expansion of Anopheles albimanus in southern Central America. Am J Trop Med Hyg 2010, 82:156-164.
  • [54]Loaiza JR, Scott ME, Bermingham E, Sanjur OI, Wilkerson R, Rovira J, Gutiérrez LA, Correa MM, Grijalva MJ, Birnberg L, Bickersmith S, Conn JE: Late Pleistocene environmental changes lead to unstable demography and population divergence of Anopheles albimanus in the northern Neotropics. Mol Phylogenet Evol 2010, 57:1341-1346.
  • [55]Morgan K, Linton YM, Somboon P, Saikia P, Dev V, Socheat D, Walton C: Inter-specific gene flow dynamics during the Pleistocene-dated speciation of forest-dependent mosquitoes in Southeast Asia. Mol Ecol 2010, 19:2269-2285.
  • [56]Haffer J: Speciation in Amazonian forest birds. Science 1969, 165:131-137.
  • [57]Vasconcelos PM, Becker TA, Renne PR, Brimhall GH: Age and duration of weathering by 40K-40Ar and 40Ar/39Ar analysis of potassium-manganese oxides. Science 1992, 258:451-455.
  • [58]Ravelo AC, Andreasen DH, Lyle M, Olivarez Lyle A, Wara MW: Regional climate shifts caused by gradual global cooling in the Pliocene epoch. Nature 2004, 429:263-267.
  • [59]Carnaval AC, Hickerson MJ, Haddad CF, Rodrigues MT, Moritz C: Stability predicts genetic diversity in the Brazilian Atlantic forest hotspot. Science 2009, 323:785-789.
  • [60]Thomé MT, Zamudio KR, Giovanelli JG, Haddad CF, Baldissera FA Jr, Alexandrino J: Phylogeography of endemic toads and post-Pliocene persistence of the Brazilian Atlantic forest. Mol Phylogenet Evol 2010, 55:1018-1031.
  • [61]Marroig G, Cropp S, Cheverud JM: Systematics and evolution of the Jacchus group of marmosets (Platyrrhini). Am J Phys Anthropol 2004, 123:11-22.
  • [62]Grazziotin FG, Monzel M, Echeverrigaray S, Bonatto SL: Phylogeography of the Bothrops jararaca complex (Serpentes: Viperidae): past fragmentation and island colonization in the Brazilian Atlantic forest. Mol Ecol 2006, 15:3969-3982.
  • [63]Conn JE, Mirabello L: The biogeography and population genetics of neotropical vector species. Heredity 2007, 99:245-256.
  • [64]Mata H, Fontana CS, Maurício GN, Bornschein MR, de Vasconcelos MF, Bonatto SL: Molecular phylogeny and biogeography of the eastern Tapaculos (Aves: Rhinocryptidae: Scytalopus, Eleoscytalopus): cryptic diversification in Brazilian Atlantic Forest. Mol Phylogenet Evol 2009, 53:450-462.
  • [65]Turchetto-Zolet AC, Cruz F, Vendramin GG, Simon MF, Salgueiro F, Margis-Pinheiro M, Margis R: Large-scale phylogeography of the disjunct Neotropical tree species Schizolobium parahyba (Fabaceae-Caesalpinioideae). Mol Phylogenet Evol 2012, 65:174-182.
  • [66]Lorenz-Lemke AP, Muschner VC, Bonatto SL, Cervi AC, Salzano FM, Freitas LB: Phylogeographic inferences concerning evolution of Brazilian Passiflora actinia and P. elegans (Passifloraceae) based on ITS (nrDNA) variation. Ann Bot 2005, 95:799-806.
  • [67]Palma-Silva C, Lexer C, Paggi GM, Barbará T, Bered F, Bodanese-Zanettini MH: Range-wide patterns of nuclear and chloroplast DNA diversity in Vriesea gigantea (Bromeliaceae), a neotropical forest species. Heredity (Edinb) 2009, 103:503-512.
  • [68]Jowett T: Preparation of nucleic acids. In Drosophila, a practical approach. Edited by Roberts DB. Oxford: IRL press; 1998:347-371.
  • [69]GenBank databasehttp://www.ncbi.nlm.nih.gov/BLAST/ webcite
  • [70]Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG: The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 1997, 25:4876-4882.
  • [71]Rozas J, Sánchez-DelBarrio JC, Messeguer X, Rozas R: DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 2003, 19:2496-2497.
  • [72]Filatov DA, Charlesworth D: DNA polimorphism, haplotype structure and balancing selection in the Leavenworthia PgiC locus. Genetics 1999, 153:1423-1434.
  • [73]Tamura K, Dudley J, Nei M, Kumar S: MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 2007, 24:1596-1599.
  • [74]Hey lab distributed software: evolutionary genetics; IM 2009. http://lifesci.rutgers.edu/~heylab/HeylabSoftware.htm#IM webcite
  • [75]Kimura M: The number of heterozygous nucleotide sites maintained in a finite population due to steady flux of mutations. Genetics 1969, 61:893-903.
  • [76]Woerner AE, Cox MP, Hammer MF: Recombination-filtered genomic datasets by information maximization. Bioinformatics 2007, 23:1851-1853.
  • [77]Hammer lab, IMGC Online. http://hammerlab.biosci.arizona.edu/imgc_online.html webcite
  文献评价指标  
  下载次数:31次 浏览次数:19次