• View in gallery

    Metaphase I of Triatoma vitticeps stained by C-banding. Note the karyotype 2n = 24 (20A + X1X2X3Y) and heterochromatin restricted to only one of the X sex chromosomes and in the Y sex chromosome. X = X sex chromosome; Y = Y sex chromosome. Bar: 10 μm.

  • 1.

    Martins-Melo FR, Ramos AN, Alencar CH, Heukelbach J, 2014. Prevalence of Chagas disease in Brazil: a systematic review and meta-analysis. Acta Trop 130: 167174.

    • Search Google Scholar
    • Export Citation
  • 2.

    World Health Organization, 2015. Chagas disease (American trypanosomiasis). Wkly Epidemiol Rec 90: 3344.

  • 3.

    Silveira AC, Dias JC, 2011. The control of vectorial transmission. Rev Soc Bras Med Trop 44: 5263.

  • 4.

    Costa J, Lorenzo M, 2009. Biology, diversity and strategies for the monitoring and control of triatomines-Chagas disease vectors. Mem Inst Oswaldo Cruz 104: 4651.

    • Search Google Scholar
    • Export Citation
  • 5.

    Galvão C, 2014. Vetores da Doença de Chagas no Brasil. Curitiba, Brazil: Sociedade Brasileira de Zoologia, 289.

  • 6.

    Gonçalves TCM, Rocha DS, Cunha RA, 2000. Feeding patterns of Triatoma vitticeps in the state of Rio de Janeiro, Brazil. Rev Saude Publica 34: 348352.

    • Search Google Scholar
    • Export Citation
  • 7.

    Santos CB, Ferreira AL, Leite GR, Ferreira GEM, Rodrigues AAF, Falqueto A, 2005. Peridomiciliary colonies of Triatoma vitticeps (Stal, 1859) (Hemiptera, Reduviidae, Triatominae) infected with Trypanosoma cruzi in rural areas of the state of Espírito Santo, Brazil. Mem Inst Oswaldo Cruz 100: 471473.

    • Search Google Scholar
    • Export Citation
  • 8.

    Lorosa ES, Valente MVMP, Cunha V, Lent H, Jurberg J, 2003. Foco de doença de Chagas em Arcádia, estado do Rio de Janeiro, Brasil. Mem Inst Oswaldo Cruz 98: 885887.

    • Search Google Scholar
    • Export Citation
  • 9.

    Gonçalves TCM, Oliveira E, Dias LS, Almeida MD, Nogueira WO, Pires FDA, 1998. An investigation on the ecology of Triatoma vitticeps (Stål, 1859) and its possible role in the transmission of Trypanosoma cruzi in the locality of Triunfo, Santa Maria Madalena municipal district, state of Rio de Janeiro, Brazil. Mem Inst Oswaldo Cruz 93: 711717.

    • Search Google Scholar
    • Export Citation
  • 10.

    Gonçalves TCM, Victório VMN, Jurberg J, Cunha V, 1988. Biologia do Triatoma vitticeps (Stal, 1859) em condições de laboratório (Hemiptera: Reduviidae: Triatominae). I Ciclo evolutivo. Mem Inst Oswaldo Cruz 83: 519523.

    • Search Google Scholar
    • Export Citation
  • 11.

    Souza RCM, Barbosa SE, Sonoda IV, Azeredo BMV, Romanha AJ, Diotaiuti L, 2008. Population dynamics of Triatoma vitticeps (Stal, 1859) in Itanhomi, Minas Gerais, Brazil. Mem Inst Oswaldo Cruz 103: 1420.

    • Search Google Scholar
    • Export Citation
  • 12.

    Sumner AT, 1972. A simple technique for demonstrating centromeric heterochromatin. Exp Cell Res 75: 305306.

  • 13.

    Tamura K, Stecher G, Peterson D, Filipski A, Kumar S, 2013. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30: 27252729.

    • Search Google Scholar
    • Export Citation
  • 14.

    Ceretti-Junior W, Vendrami DP, Gil JM, Barata JMS, Marrelli MT, 2008. Análise das relações taxonômicas e sistemáticas entre espécies de triatomíneos (Hemiptera, Reduviidae) de colônias mantidas pelo Serviço Especial de Saúde de Araraquara, inferida de seqüências do 16S rDNA mitocondrial. Rev Bras Entomol 52: 455462.

    • Search Google Scholar
    • Export Citation
  • 15.

    Gardim S, Almeida CE, Takiya DM, Oliveira J, Araújo RF, Cicarelli RMB, Rosa JA, 2014. Multiple mitochondrial genes of some sylvatic Brazilian Triatoma: non-monophyly of the T. brasiliensis subcomplex and the need for a generic revision in the Triatomini. Infect Genet Evol 23: 7479.

    • Search Google Scholar
    • Export Citation
  • 16.

    Justi SA, Russo CAM, Mallet JRS, Obara MT, Galvão C, 2014. Molecular phylogeny of Triatomini (Hemiptera: Reduviidae: Triatominae). Parasit Vectors 7: 149.

    • Search Google Scholar
    • Export Citation
  • 17.

    Imperador CHL, Alevi KCC, Oliveira J, Rosa JA, Azeredo-Oliveira MTV, 2016. Cytogenetic analysis of Triatoma pseudomaculata Corrêa and Espínola, 1964 (Hemiptera, Triatominae) from different Brazilian states. Genet Mol Res 15, doi: 10.4238/gmr.15016937.

    • Search Google Scholar
    • Export Citation
  • 18.

    Pereira LHG, Hanner R, Foresti F, Oliveira C, 2013. Can DNA barcoding accurately discriminate megadiverse neotropical freshwater fish fauna? BMC Genet 14: 20.

    • Search Google Scholar
    • Export Citation
  • 19.

    Mendonça VJ, Alevi KCC, Pinotti H, Gurgel-Gongalves R, Pita S, Guerra AL, Panzera F, Araújo RF, Azeredo-Oliveira MTV, Rosa JA, 2016. Revalidation of Triatoma bahiensis Sherlock & Serafim, 1967 (Hemiptera: Reduviidae) and phylogeny of the T. brasiliensis species complex. Zootaxa 4107: 239254.

    • Search Google Scholar
    • Export Citation
  • 20.

    Alevi KCC, Guerra AL, Imperador CHL, Jurberg J, Moreira FF, Azeredo-Oliveira MTV, 2017. Mitochondrial gene confirms the specific status of Triatoma pintodiasi Jurberg, Cunha, and Rocha, 2013 (Hemiptera, Triatominae), an endemic species in Brazil. Am J Trop Med Hyg 96: 200201.

    • Search Google Scholar
    • Export Citation
  • 21.

    Alevi KCC, Reis YV, Guerra AL, Imperador CHL, Banho CA, Moreira FFF, Azeredo-Oliveira MTV, 2016. Would Nesotriatoma bruneri Usinger, 1944 be a valid species? Zootaxa 4103: 396400.

    • Search Google Scholar
    • Export Citation
  • 22.

    Monteiro FA, Donnelly MJ, Beard CB, Costa J, 2004. Nested clade and phylogeographic analyses of the Chagas disease vector Triatoma brasiliensis in northeast Brazil. Mol Phylogenet Evol 32: 4656.

    • Search Google Scholar
    • Export Citation
  • 23.

    Panzera F, Pita S, Nattero J, Panzera Y, Galvão C, Chavez T, Arias AR, Téllez LC, Noireau F, 2015. Cryptic speciation in the Triatoma sordida subcomplex (Hemiptera, Reduviidae) revealed by chromosomal markers. Parasit Vectors 8: 495.

    • Search Google Scholar
    • Export Citation
  • 24.

    Abad-Franch F, Pavan MG, Jaramillo N, Palomeque FS, Dale C, Chaverra D, Monteiro FA, 2013. Rhodnius barretti, a new species of Triatominae (Hemiptera: Reduviidae) from western Amazonia. Mem Inst Oswaldo Cruz 108: 9299.

    • Search Google Scholar
    • Export Citation
  • 25.

    Rua N, Stevens L, Dorn PL, 2011. High genetic diversity in a single population of Triatoma sanguisuga (LeConte, 1855) inferred from two mitochondrial markers: cytochrome b and 16 S ribosomal DNA. Infect Genet Evol 11: 671677.

    • Search Google Scholar
    • Export Citation
  • 26.

    Alevi KCC, Oliveira J, Azeredo-Oliveira MTV, Rosa JA, 2017. Triatoma vitticeps subcomplex (Hemiptera, Triatominae): a new grouping of Chagas disease vectors from South American. Parasit Vectors 10: 180.

    • Search Google Scholar
    • Export Citation
  • 27.

    Panzera F, Pérez R, Nicolini P, Hornos S, Costa J, Borges E, Diotaiuti L, Schofield CJ, 2000. Chromosome homogeneity in populations of Triatoma brasiliensis Neiva 1911 (Hemiptera-Reduviidae-Triatominae). Cad Saude Publica 16: 8388.

    • Search Google Scholar
    • Export Citation
  • 28.

    Alevi KCC, Nunes GM, Rosa JA, Azeredo-Oliveira MTV, 2015. Homogeneidade cromossômica em diferentes populações de Panstrongylus megistus do Brasil. Rev Cienc Farm Basica Apl 36: 307310.

    • Search Google Scholar
    • Export Citation

 

 

 

 

Triatoma vitticeps (Stal, 1859) (Hemiptera, Triatominae): A Chagas Disease Vector or a Complex of Vectors?

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  • 1 Laboratório de Biologia Celular, Departamento de Biologia, Instituto de Biociências, Letras e Ciências Exatas, Universidade Estadual Paulista “Júlio de Mesquita Filho”, São José do Rio Preto, São Paulo, Brazil;
  • 2 Laboratório de Biodiversidade Entomológica, Instituto Oswaldo Cruz, Manguinhos, Rio de Janeiro, Brazil;
  • 3 Laboratório de Parasitologia, Departamento de Ciências Biológicas, Faculdade de Ciências Farmacêuticas, Universidade Estadual Paulista “Júlio de Mesquita Filho”, Araraquara, São Paulo, Brazil

Triatoma vitticeps is a Chagas disease vector that was found infected with Trypanosoma cruzi in homes. As this species is endemic from Brazil (Bahia, Espírito Santo, Minas Gerais, and Rio de Janeiro) and no study comparing the specimens from different Brazilian states was conducted, we analyzed the genetic distance (16S rDNA, Cyt b, and COI mitochondrial genes) and the chromosomal characteristics for T. vitticeps from Minas Gerais, Rio de Janeiro, and Espírito Santo. All specimens showed the same cytogenetic characteristics. On the other hand, the different mitochondrial genes demonstrated high intraspecific variation between the genetic distances of T. vitticeps from different states ranging from 2.3% to 7.2%. Based on this, our results suggest that possibly what is characterized as T. vitticeps is a complex of cryptic species (or subspecies).

The Chagas disease is caused by the protozoan Trypanosoma cruzi (Chagas, 1909) and transmitted to humans mainly through contact with feces of insects from the Triatominae subfamily. This disease is among the main neglected diseases in Latin America and is estimated that approximately 6–7 million people are infected worldwide; in Brazil there are about 2–3 million people who are infected with T. cruzi.1,2

The vector control is the main way to minimize the incidence of new cases of Chagas disease. In Brazil, after significant reduction of vectors, the number of cases with the acute form of Chagas disease has been reduced dramatically.3,4 Characterizing the different species of the triatomines and the structure of the populations of these vectors can assist in the activities of vector control programs because there are species with greater or lesser degrees of importance in the transmission of T. cruzi.4,5

Triatoma vitticeps (Stål, 1859) is an endemic species from Brazil, distributed in the states of Bahia, Espírito Santo, Minas Gerais, and Rio de Janeiro.5 This triatomine was initially characterized as a sylvatic species,6 but adults of T. vitticeps often invade houses attracted by light and form small colonies in domiciliary regions.7 In addition, worrying rates of domiciliary capture occurred in Rio de Janeiro8,9 and high rates of T. cruzi infection were observed in T. vitticeps captured in homes of Espírito Santo,7 although it has been shown that this species does not have the habit of defecating during hematophagy.10

Souza et al.11 analyzed the population dynamics of T. vitticeps in the state of Minas Gerais, by means of morphometry, isoenzymes, and random amplification of polymorphic DNA. The authors observed migration between domestic, peridomiciliary, and sylvatic habitats and gene flow between the sylvatic and domestic habitats. However, as no study comparing the specimens from different Brazilian states was conducted, we analyzed the genetic (mitochondrial markers—16S rDNA, Cyt b, and COI genes) and cytogenetic aspects (karyotype and heterochromatin) of T. vitticeps from Minas Gerais, Rio de Janeiro, and Espírito Santo.

Ten adult males of each Brazilian state were used for cytogenetic analysis. The specimens were provided by the insectariums of FCFAR/UNESP, Araraquara, São Paulo, Brazil, and of the IOC/FIOCRUZ, Rio de Janeiro, Brazil. The seminiferous tubules were torn apart, crushed, and fixed on slides in liquid nitrogen. The cytogenetic technique of C-banding12 was then applied for the characterization of chromosome number and heterochromatin pattern and the analysis was performed using a Jenaval light microscope (Zeiss) attached to a digital camera and an Axio Vision LE 4.8 image analyzer (Copyright 2006–2009 Carl Zeiss Imaging Solutions Gmb H). For the analysis of the genetic distance between T. vitticeps coming from different states of the southeastern region of Brazil were used sequences deposited in the GenBank (Table 1), and the Tamura 3-parameter model was used to calculate genetic distances pairwise in the MEGA 6.0 software.13 The specimens used in cytogenetic studies were from the same populations of the material used for the molecular analysis.1416

Table 1

Sequences of Triatoma vitticeps coming from different Brazilian states deposited in the GenBank

T. vitticepsCOICyt b16S
Espírito SantoAF021219KF826896EU827202
Rio de JaneiroKC249397KC249304KC249088
Minas GeraisKC249395KC249301KC249085

All specimens analyzed showed the same cytogenetic characteristics: karyotype 2n = 24 (20A + X1X2X3Y) and heterochromatin restricted to only one of the X sex chromosomes and in the Y sex chromosome (Figure 1). These results demonstrate that T. vitticeps does not present intraspecific chromosome variation as already observed for other triatomines.17

Figure 1.
Figure 1.

Metaphase I of Triatoma vitticeps stained by C-banding. Note the karyotype 2n = 24 (20A + X1X2X3Y) and heterochromatin restricted to only one of the X sex chromosomes and in the Y sex chromosome. X = X sex chromosome; Y = Y sex chromosome. Bar: 10 μm.

Citation: The American Journal of Tropical Medicine and Hygiene 99, 4; 10.4269/ajtmh.17-0512

On the other hand, the different mitochondrial genes analyzed demonstrated high intraspecific variation between the genetic distances of T. vitticeps from different states ranging from 2.3% to 7.5% (Tables 24). Pereira et al.18 consider that taxa with a genetic distance greater than 2% represent new species that are possibly cryptic. For Triatominae, a genetic distance of 2.48%, associated with other tools, already supports specific status (as recently observed for Triatoma bahiensis Sherlock & Serafim, 1967).19

Table 2

Genetic distances for different populations of Triatoma vitticeps with the mitochondrial genes: COI

T. vitticeps(1)(2)(3)
(1) Espírito Santo0.000
(2) Rio de Janeiro0.0680.000
(3) Minas Gerais0.0720.0750.000
Table 3

Genetic distances for different populations of Triatoma vitticeps with the mitochondrial genes: Cyt b

T. vitticeps(1)(2)(3)
(1) Espírito Santo0.000
(2) Rio de Janeiro0.0500.000
(3) Minas Gerais0.0670.0630.000
Table 4

Genetic distances for different populations of Triatoma vitticeps with the mitochondrial genes: 16S rDNA

T. vitticeps(1)(2)(3)
(1) Espírito Santo0.000
(2) Rio de Janeiro0.0310.000
(3) Minas Gerais0.0230.0230.000

Based on this, different authors evaluated the specific status of triatomines by means of genetic distance using mitochondrial genes: Alevi et al.20 through the 16S gene corroborates the specific status of Triatoma pintodiasi Jurberg et al. (2013); Alevi et al.21 through the 16S gene also have proposed the synonimization between Nesotriatoma bruneri Usinger (1944) and Nesotriatoma flavida (Neiva, 1911); Ceretti-Junior et al.14 based on the 16S gene reported low intraspecific variation between genetic distances of triatomines (0–0.6%), except for relationships between Triatoma brasiliensis Neiva (1911) specimens (1.3%) and Triatoma sordida (Stål, 1859) specimens (1%) from different geographic populations (specimens that possibly suffered cryptic speciation)22,23; Panzera et al.23 using the COI gene observed a genetic distance of 5.3% between T. sordida from Brazil and from Argentina and suggest that T. sordida from Argentina is possibly a new cryptic species of T. sordida; Abad-Franch et al.24 used the genetic distance of cyt b (8.7%) between Rhodnius robustus Larrousse (1927) and Rhodnius barretti to characterize that R. barretti represents a distinct entity within the “robustus lineage”; and Rua et al.25 suggested that populations of Triatoma sanguisuga (Leconte, 1855) are divided into two subspecies because they have genetic distances close to five for cyt b.

Recently, T. vitticeps and Triatoma melanocephala were grouped in the monophyletic subcomplex T. vitticeps because they presented karyotypic differences when compared with the other triatomines in South America.26 As observed for T. vitticeps, other populations of triatomines (e.g., T. brasiliensis) also did not present intraspecific chromosomal variations27 and presented genetic distances22 that supported the description of new species. Alevi et al.28 highlighted that gene evolution and chromosomal evolution are events mediated by different factors, being that the events that may lead to variations in DNA sequences are more common than those events that lead to chromosomal changes.

Thus, our results suggest that possibly what is characterized as T. vitticeps is a complex of cryptic species (or subspecies). We suggest that an extensive phylogeographic study (possibly with tools that characterize the presence of gene flow) be performed in T. vitticeps and be associated with taxonomic tools, such as experimental crosses between different populations of T. vitticeps, to evaluate the specific status of this vector of Chagas’ disease endemic to Brazil.

REFERENCES

  • 1.

    Martins-Melo FR, Ramos AN, Alencar CH, Heukelbach J, 2014. Prevalence of Chagas disease in Brazil: a systematic review and meta-analysis. Acta Trop 130: 167174.

    • Search Google Scholar
    • Export Citation
  • 2.

    World Health Organization, 2015. Chagas disease (American trypanosomiasis). Wkly Epidemiol Rec 90: 3344.

  • 3.

    Silveira AC, Dias JC, 2011. The control of vectorial transmission. Rev Soc Bras Med Trop 44: 5263.

  • 4.

    Costa J, Lorenzo M, 2009. Biology, diversity and strategies for the monitoring and control of triatomines-Chagas disease vectors. Mem Inst Oswaldo Cruz 104: 4651.

    • Search Google Scholar
    • Export Citation
  • 5.

    Galvão C, 2014. Vetores da Doença de Chagas no Brasil. Curitiba, Brazil: Sociedade Brasileira de Zoologia, 289.

  • 6.

    Gonçalves TCM, Rocha DS, Cunha RA, 2000. Feeding patterns of Triatoma vitticeps in the state of Rio de Janeiro, Brazil. Rev Saude Publica 34: 348352.

    • Search Google Scholar
    • Export Citation
  • 7.

    Santos CB, Ferreira AL, Leite GR, Ferreira GEM, Rodrigues AAF, Falqueto A, 2005. Peridomiciliary colonies of Triatoma vitticeps (Stal, 1859) (Hemiptera, Reduviidae, Triatominae) infected with Trypanosoma cruzi in rural areas of the state of Espírito Santo, Brazil. Mem Inst Oswaldo Cruz 100: 471473.

    • Search Google Scholar
    • Export Citation
  • 8.

    Lorosa ES, Valente MVMP, Cunha V, Lent H, Jurberg J, 2003. Foco de doença de Chagas em Arcádia, estado do Rio de Janeiro, Brasil. Mem Inst Oswaldo Cruz 98: 885887.

    • Search Google Scholar
    • Export Citation
  • 9.

    Gonçalves TCM, Oliveira E, Dias LS, Almeida MD, Nogueira WO, Pires FDA, 1998. An investigation on the ecology of Triatoma vitticeps (Stål, 1859) and its possible role in the transmission of Trypanosoma cruzi in the locality of Triunfo, Santa Maria Madalena municipal district, state of Rio de Janeiro, Brazil. Mem Inst Oswaldo Cruz 93: 711717.

    • Search Google Scholar
    • Export Citation
  • 10.

    Gonçalves TCM, Victório VMN, Jurberg J, Cunha V, 1988. Biologia do Triatoma vitticeps (Stal, 1859) em condições de laboratório (Hemiptera: Reduviidae: Triatominae). I Ciclo evolutivo. Mem Inst Oswaldo Cruz 83: 519523.

    • Search Google Scholar
    • Export Citation
  • 11.

    Souza RCM, Barbosa SE, Sonoda IV, Azeredo BMV, Romanha AJ, Diotaiuti L, 2008. Population dynamics of Triatoma vitticeps (Stal, 1859) in Itanhomi, Minas Gerais, Brazil. Mem Inst Oswaldo Cruz 103: 1420.

    • Search Google Scholar
    • Export Citation
  • 12.

    Sumner AT, 1972. A simple technique for demonstrating centromeric heterochromatin. Exp Cell Res 75: 305306.

  • 13.

    Tamura K, Stecher G, Peterson D, Filipski A, Kumar S, 2013. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30: 27252729.

    • Search Google Scholar
    • Export Citation
  • 14.

    Ceretti-Junior W, Vendrami DP, Gil JM, Barata JMS, Marrelli MT, 2008. Análise das relações taxonômicas e sistemáticas entre espécies de triatomíneos (Hemiptera, Reduviidae) de colônias mantidas pelo Serviço Especial de Saúde de Araraquara, inferida de seqüências do 16S rDNA mitocondrial. Rev Bras Entomol 52: 455462.

    • Search Google Scholar
    • Export Citation
  • 15.

    Gardim S, Almeida CE, Takiya DM, Oliveira J, Araújo RF, Cicarelli RMB, Rosa JA, 2014. Multiple mitochondrial genes of some sylvatic Brazilian Triatoma: non-monophyly of the T. brasiliensis subcomplex and the need for a generic revision in the Triatomini. Infect Genet Evol 23: 7479.

    • Search Google Scholar
    • Export Citation
  • 16.

    Justi SA, Russo CAM, Mallet JRS, Obara MT, Galvão C, 2014. Molecular phylogeny of Triatomini (Hemiptera: Reduviidae: Triatominae). Parasit Vectors 7: 149.

    • Search Google Scholar
    • Export Citation
  • 17.

    Imperador CHL, Alevi KCC, Oliveira J, Rosa JA, Azeredo-Oliveira MTV, 2016. Cytogenetic analysis of Triatoma pseudomaculata Corrêa and Espínola, 1964 (Hemiptera, Triatominae) from different Brazilian states. Genet Mol Res 15, doi: 10.4238/gmr.15016937.

    • Search Google Scholar
    • Export Citation
  • 18.

    Pereira LHG, Hanner R, Foresti F, Oliveira C, 2013. Can DNA barcoding accurately discriminate megadiverse neotropical freshwater fish fauna? BMC Genet 14: 20.

    • Search Google Scholar
    • Export Citation
  • 19.

    Mendonça VJ, Alevi KCC, Pinotti H, Gurgel-Gongalves R, Pita S, Guerra AL, Panzera F, Araújo RF, Azeredo-Oliveira MTV, Rosa JA, 2016. Revalidation of Triatoma bahiensis Sherlock & Serafim, 1967 (Hemiptera: Reduviidae) and phylogeny of the T. brasiliensis species complex. Zootaxa 4107: 239254.

    • Search Google Scholar
    • Export Citation
  • 20.

    Alevi KCC, Guerra AL, Imperador CHL, Jurberg J, Moreira FF, Azeredo-Oliveira MTV, 2017. Mitochondrial gene confirms the specific status of Triatoma pintodiasi Jurberg, Cunha, and Rocha, 2013 (Hemiptera, Triatominae), an endemic species in Brazil. Am J Trop Med Hyg 96: 200201.

    • Search Google Scholar
    • Export Citation
  • 21.

    Alevi KCC, Reis YV, Guerra AL, Imperador CHL, Banho CA, Moreira FFF, Azeredo-Oliveira MTV, 2016. Would Nesotriatoma bruneri Usinger, 1944 be a valid species? Zootaxa 4103: 396400.

    • Search Google Scholar
    • Export Citation
  • 22.

    Monteiro FA, Donnelly MJ, Beard CB, Costa J, 2004. Nested clade and phylogeographic analyses of the Chagas disease vector Triatoma brasiliensis in northeast Brazil. Mol Phylogenet Evol 32: 4656.

    • Search Google Scholar
    • Export Citation
  • 23.

    Panzera F, Pita S, Nattero J, Panzera Y, Galvão C, Chavez T, Arias AR, Téllez LC, Noireau F, 2015. Cryptic speciation in the Triatoma sordida subcomplex (Hemiptera, Reduviidae) revealed by chromosomal markers. Parasit Vectors 8: 495.

    • Search Google Scholar
    • Export Citation
  • 24.

    Abad-Franch F, Pavan MG, Jaramillo N, Palomeque FS, Dale C, Chaverra D, Monteiro FA, 2013. Rhodnius barretti, a new species of Triatominae (Hemiptera: Reduviidae) from western Amazonia. Mem Inst Oswaldo Cruz 108: 9299.

    • Search Google Scholar
    • Export Citation
  • 25.

    Rua N, Stevens L, Dorn PL, 2011. High genetic diversity in a single population of Triatoma sanguisuga (LeConte, 1855) inferred from two mitochondrial markers: cytochrome b and 16 S ribosomal DNA. Infect Genet Evol 11: 671677.

    • Search Google Scholar
    • Export Citation
  • 26.

    Alevi KCC, Oliveira J, Azeredo-Oliveira MTV, Rosa JA, 2017. Triatoma vitticeps subcomplex (Hemiptera, Triatominae): a new grouping of Chagas disease vectors from South American. Parasit Vectors 10: 180.

    • Search Google Scholar
    • Export Citation
  • 27.

    Panzera F, Pérez R, Nicolini P, Hornos S, Costa J, Borges E, Diotaiuti L, Schofield CJ, 2000. Chromosome homogeneity in populations of Triatoma brasiliensis Neiva 1911 (Hemiptera-Reduviidae-Triatominae). Cad Saude Publica 16: 8388.

    • Search Google Scholar
    • Export Citation
  • 28.

    Alevi KCC, Nunes GM, Rosa JA, Azeredo-Oliveira MTV, 2015. Homogeneidade cromossômica em diferentes populações de Panstrongylus megistus do Brasil. Rev Cienc Farm Basica Apl 36: 307310.

    • Search Google Scholar
    • Export Citation

Author Notes

Address correspondence to Kaio Cesar Chaboli Alevi, Instituto de Biociências, Letras e Ciências Exatas, IBILCE/UNESP, Rua Cristóvão Colombo, 2265, Jardim Nazareth, CEP 15054-000, São José do Rio Preto, São Paulo, Brazil. E-mail: kaiochaboli@hotmail.com

Financial support: This work was supported by the Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) (Process number 2013/19764-0) and the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq).

Authors’ addresses: Kaio Cesar Chaboli Alevi, Ariane Cristina Caris Garcia, Ana Letícia Guerra, and Maria Tercília Vilela de Azeredo Oliveira, Departamento de Biologia, Instituto de Biociências, Letras e Ciências Exatas, Universidade Estadual Paulista “Júlio de Mesquita Filho”, São José do Rio Preto, São Paulo, Brazil, E-mails: kaiochaboli@hotmail.com, ariane.garcia@outlook.com, analebio@yahoo.com.br, and tercilia@ibilce.unesp.br. Felipe Ferraz Figueiredo Moreira, Laboratório de Biodiversidade Entomológica, Fundação Oswaldo Cruz, Rio de Janeiro, Brazil, E-mail: felipento@hotmail.com. Jader de Oliveira and João Aristeu da Rosa, Departamento de Ciências Biológicas, Faculdade de Ciências Farmacêuticas, Universidade Estadual Paulista “Júlio de Mesquita Filho”, Araraquara, São Paulo, Brazil, E-mails: jdr.oliveira@hotmail.com and joaoaristeu@gmail.com.

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