• View in gallery

    Cytogenetic analyses of Psammolestes spp. Note the X and Y sex chromosomes forming the chromocenter of Psammolestes tertius (A, arrow), Psammolestes coreodes (B, arrow), and Psammolestes arthuri (C, arrow). Note that the autosomes and X chromosome are euchromatic and Y is heterochromatic in P. tertius (D), P. coreodes (E), and P. arthuri (F). Note that the X chromosome is rich in CG (G–I) and the Y chromosome is rich in AT (J–L) and the karyotype is 2n = 22 (20A + XY) (M–O) for P. tertius (G, J, and M), P. coreodes (H, K, and N), and P. arthuri (I, L, and O). X: X sex chromosome, Y: Y sex chromosome. Scale bar: 10 μm.

  • 1.

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

  • 2.

    Oliveira J, Alevi KCC, 2017. Taxonomic status of Panstrongylus herreri Wygodzinsky, 1948 and the number of Chagas disease vectors. Rev Soc Bras Med Trop 50: 434435.

    • Search Google Scholar
    • Export Citation
  • 3.

    Monteiro FA, Wesson DM, Dotson EM, Schofield CJ, Beard CB, 2000. Phylogeny and molecular taxonomy of the Rhodniini derived from mitochondrial and nuclear DNA sequences. Am J Trop Med Hyg 62: 460465.

    • Search Google Scholar
    • Export Citation
  • 4.

    Lent H, Wygodzinsky P, 1979. Revision of the Triatominae (Hemiptera: Reduviidae) and their significance as vector of Chagas’s disease. Bull Am Mus Nat Hist 163: 123520.

    • Search Google Scholar
    • Export Citation
  • 5.

    Justi S, Galvão C, 2017. The evolutionary origin of diversity in Chagas disease vectors. Trends Parasitol 33: 4252.

  • 6.

    Galvão C, Carcavallo R, Rocha DS, Jurberg J, 2003. A checklist of the current valid species of the subfamily Triatominae Jeannel, 1919 (Hemiptera, Reduviidae) and their geographical distribution, with nomenclatural and taxonomic notes. Zootaxa 202: 136.

    • Search Google Scholar
    • Export Citation
  • 7.

    Cabrera R, 2006. Notas breves sobre Psammolestes tertius Bergroth, 1911 (Reduviidae: Hemiptera): un triatomino silvestre. An Fac Med (Lima) 67: 345365.

    • Search Google Scholar
    • Export Citation
  • 8.

    Hypsa V, Tietz D, Zrzavy J, Rego RO, Galvão C, Jurberg J, 2002. Phylogeny and biogeography of Triatominae (Hemiptera, Reduviidae): molecular evidence of a New World origin of the Asiatic clade. Mol Phylogenet Evol 23: 447457.

    • Search Google Scholar
    • Export Citation
  • 9.

    Soares RPP, Barbosa SE, Borges EC, Melo Júnior TA, Romanha AJ, Dujardin JP, Schofield CJ, Diotaiuti L, 2001. Genetic studies of Psammolestes tertius (Hemíptera: Reduviidae: Triatominae) using male genital morphology, morphometry, isoenzymes, and random amplified polymorphic DNA. Biochem Genet 39: 113.

    • Search Google Scholar
    • Export Citation
  • 10.

    Schofield CJ, Dujardin JP, 1999. Theories on the evolution of Rhodnius. Actual Biol 21: 183197.

  • 11.

    Schreiber G, Pellegrino J, 1950. Eteropicnosi di autosomi come possibile meccanismo di speciazione; ricerche citologiche su alcuni Emitteri neotropici. Sci Genet 3: 215226.

    • Search Google Scholar
    • Export Citation
  • 12.

    Panzera F et al. 1998. Cytogenetics of triatomines. Carcavallo RU, Galíndez-Girón I, Jurberg J, Lent H, eds. Atlas of Chagas Disease Vectors in the Americas. Rio de Janeiro, Brazil: Editora Fiocruz, 621–664.

  • 13.

    Panzera Y, Pita S, Ferreiro MJ, Ferrandis I, Lages C, Perez R, Silva AE, Guerra M, Panzera F, 2012. High dynamics of rDNA cluster location in kissing bug holocentric chromosomes (Triatominae, Heteroptera). Cytogenet Genome Res 138: 5667.

    • Search Google Scholar
    • Export Citation
  • 14.

    Oliveira J, Alevi KCC, Fonseca EO, Souza OM, Santos CG, Azeredo-Oliveira MTV, Rosa JA, 2016. New record and cytogenetic analysis of Psammolestes tertius Lent & Jurberg, 1965 (Hemiptera, Reduviidae, Triatominae) from Bahia state, Brazil. Genet Mol Res 15: 16.

    • Search Google Scholar
    • Export Citation
  • 15.

    De Vaio ES, Grucci B, Castagnino AM, Franca ME, Martinez ME, 1985. Meiotic differences between three triatomine species (Hemiptera:Reduviidae). Genetica 67: 185191.

    • Search Google Scholar
    • Export Citation
  • 16.

    Alevi KCC, Mendonça PP, Pereira NP, Rosa JA, Azeredo-Oliveira MTV, 2012. Karyotype of Triatoma melanocephala Neiva and Pinto (1923). Does this species fit in the Brasiliensis subcomplex? Infect Genet Evol 12: 16521653.

    • Search Google Scholar
    • Export Citation
  • 17.

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

  • 18.

    Schimid M, 1980. Chromosoma banding an amphibia IV. Differentiation of GC and AT rich regions in Anura. Chromosoma 77: 83103.

  • 19.

    Severi-Aguiar GD, Lourenço LB, Bicudo HE, Azeredo-Oliveira MTV, 2006. Meiosis aspects and nucleolar activity in Triatoma vitticeps (Triatominae, Heteroptera). Genetica 126: 141151.

    • Search Google Scholar
    • Export Citation
  • 20.

    Alevi KCC, Ravazi A, Mendonça VJ, Rosa JA, Azeredo-Oliveira MTV, 2015. Karyotype of Rhodnius montenegrensis (Hemiptera, Triatominae). Genet Mol Res 12: 222226.

    • Search Google Scholar
    • Export Citation
  • 21.

    Rosa JA, Justino HHG, Nascimento JD, Mendonça VJ, Rocha CS, Carvalho DB, Falcone R, Azeredo-Oliveira MTV, Alevi KCC, Oliveira J, 2017. A new species of Rhodnius from Brazil (Hemiptera, Reduviidae, Triatominae). ZooKeys 675: 125.

    • Search Google Scholar
    • Export Citation
  • 22.

    Ueshima N, 1966. Cytotaxonomy of the Triatominae (Reduviidae, Hemiptera). Chromosoma 18: 97122.

  • 23.

    Alevi KCC, Oliveira J, Rosa JA, Azeredo-Oliveira MTV, 2018. Karyotype evolution of Chagas disease vectors (Hemiptera, Triatominae). Am J Trop Med Hyg 99: 8789.

    • Search Google Scholar
    • Export Citation
  • 24.

    Perez R, Panzera Y, Scafiezzo S, Mazzella M, Panzera P, Dujardin JP, Scvortzoff E, 1992. Cytogenetics as a tool for triatominae species distinction. Mem Inst Oswaldo Cruz 87: 353361.

    • Search Google Scholar
    • Export Citation
  • 25.

    Alevi KCC, Nascimento JGO, Moreira FFF, Jurberg J, Azeredo-Oliveira MTV, 2016. Cytogenetic characterisation of Triatoma rubrofasciata (De Geer) (Hemiptera, Triatominae) spermatocytes and its cytotaxonomic application. Afr Entomol 24: 257260.

    • Search Google Scholar
    • Export Citation
  • 26.

    Alevi KCC, Oliveira J, Moreira FFF, Jurberg J, Rosa JA, Azeredo-Oliveira MTV, 2015. Chromosomal characteristics and distribution of constitutive heterochromatin in the Matogrossensis and Rubrovaria subcomplexes. Infect Genet Evol 33: 158162.

    • Search Google Scholar
    • Export Citation
  • 27.

    Dujardin JP, Schofield CJ, Panzera F, 2002. Los Vectores de la Enfermedad de Chagas. Bruxelles, Belgium: Académie Royale des Sciences D’Outre-Mer.

  • 28.

    Alevi KCC, Ravazi A, Franco-Bernardes MF, Rosa JA, Azeredo-Oliveira MTV, 2015. Chromosomal evolution in the pallescens group (Hemiptera, Triatominae). Genet Mol Res 14: 1265412659.

    • Search Google Scholar
    • Export Citation
 
 
 
 

 

 
 
 

 

 

 

 

 

 

New Evidence of the Monophyletic Relationship of the Genus Psammolestes Bergroth, 1911 (Hemiptera, Reduviidae, Triatominae)

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  • 1 Departamento de Ciências Biológicas, Faculdade de Ciências Farmacêuticas, Universidade Estadual Paulista “Júlio de Mesquita Filho”, Araraquara, Brazil;
  • | 2 Departamento de Biologia, Instituto de Biociências, Letras e Ciências Exatas, Universidade Estadual Paulista “Júlio de Mesquita Filho”, São José do Rio Preto, Brazil;
  • | 3 Universidade Católica Dom Bosco, Campo Grande, Brazil

The genus Psammolestes within the subfamily Triatominae and tribe Rhodniini comprises the species Psammolestes arthuri, Psammolestes coreodes, and Psammolestes tertius, all potential vectors of Chagas disease. A feature of Psammolestes is their close association with birds, which makes them an interesting model for evolutionary studies. We analyzed cytogenetically Psammolestes spp., with the aim of contributing to the genetic and evolutionary knowledge of these vectors. All species of the Psammolestes showed the same chromosomal characteristics: chromocenter formed only by sex chromosomes X and Y, karyotype 2n = 22 and constitutive heterochromatin, and AT base pairs restricted to the sex chromosome Y. These results corroborate the monophyly of the genus and lead to the hypothesis that during the derivation of P. tertius, P. coreodes, and P. arthuri from their common ancestor, there was no reorganization in the number or structure of chromosomes.

Chagas disease is caused by the protozoan Trypanosoma cruzi (Chagas, 1909) and transmitted mainly by triatomines.1 Presently, the subfamily Triatominae (Hemiptera, Reduviidae) consists of 152 species (150 living species and two fossil ones) distributed in 18 genera and five tribes (Alberproseniini, Bolboderini, Cavernicolini, Rhodniini, and Triatomini),2 all the species being potential vectors of T. cruzi.

The tribe Rhodniini is a monophyletic group3 consisting of two genera with different phenotypes: one with long thin legs and a long head, living mainly in palm trees (genus Rhodnius Stål, 1859), and the other having a short head, strong legs, wide femora, and a very wide rostrum (the widest in all the subfamily), living in nests of birds of the family Furnariidae (genus Psammolestes Bergroth, 1911).4 The genera include 21 species of Rhodnius (divided into the groups pallescens, pictipes, and prolixus) and three species of Psammolestes.2,5

Psammolestes coreodes Bergroth, 1911 is distributed in Argentina (Catamarca, Corrientes, Chaco, Entre Rios, Formosa, Santa Fe, Santiago del Estero, Salta, Jujuy, and Tucumán), Bolivia (Santa Cruz), Brazil (Mato Grosso), and Paraguay (Central); Psammolestes tertius Lent and Jurberg, 1965 is distributed in Brazil (Bahia, Ceará, Goiás, Mato Grosso, Maranhão, Minas Gerais, Para, Paraíba, Pernambuco, and São Paulo) and Peru (San Martin); and Psammolestes arthuri (Pinto, 1926) is distributed in Colombia (Meta) and Venezuela (Aragua, Cojedes, Miranda, Guárico, Portuguesa, Yaracuy, Anzoátegui, Apure, Lara, Táchira, Barinas, and Monagas).6,7

Phylogenetic analyses of P. tertius and P. coreodes suggest that this genus is monophyletic3 (there are no phylogenetic studies of P. arthuri in the literature) and presents a phylogenetic relationship with the species of the prolixus group,3 which led to suggest the inclusion of the genus Psammolestes in the genus Rhodnius.8 Monteiro et al.3 suggest that perhaps Psammolestes should be regarded as a specialized lineage from the prolixus group of Rhodnius because the genus Psammolestes and species of the prolixus group share a common ancestral origin, which highlights the paraphyly of the genus Rhodnius.5

Based on mitochondrial DNA data presented by Monteiro et al.,3 Soares et al.9 suggest that Psammolestes has derived from a form similar to Rhodnius robustus Larrousse, 1927. In addition, the authors suggest that these triatomines spread from the Amazon region northward into the llanos of Venezuela, where P. arthuri is now abundant in furnariidae nests, and southeastward into the caatinga–cerrado path of Central Brazil. Furthermore, as predicted by Schofield and Dujardin,10 the authors suggest subsequent differentiation of P. tertius along a north–south cline, from the larger specimens of the northeastern caatinga region to the smaller individuals of the central cerrado. According to them, the third species of the genus, P. coreodes, from the Chaco region of Argentina and Paraguay, may represent the southernmost differentiation of these descending populations.

Cytogenetic studies on the genus Psammolestes started in 1950 with the description of the karyotype of P. coreodes.11 After 48 years, the karyotype of P. tertius was described,12 and in 2012, the constitutive heterochromatin pattern of the species was characterized by Panzera et al.13 (Table 1). In addition, a more recent cytogenetic study comparing P. tertius of different Brazilian states (Bahia and Ceará) was performed and showed the absence of intraspecific chromosome variation.14 The present work seeks to characterize the karyotype evolution and the chromatin composition of the species of the genus Psammolestes, with the aim of contributing to the genetic and evolutionary knowledge of these potential vectors.

Table 1

Cytogenetic characteristics of species of the genus Psammolestes

SpeciesKaryotypeMeiosisC-bandingCMA3/DAPI
ChromocenterAXYAXY
Psammolestes arthuri2n = 22 (20A + XY)XY+CMA+DAPI
Psammolestes coreodes2n = 22 (20A + XY)11XY+CMA+DAPI
Psammolestes tertius2n = 22 (20A + XY)12,14XY13+13,14CMA+DAPI

Five adult males of each species were used for cytogenetic analysis. The wild species considered herein were P. tertius (Castro Alves, Bahia, Brazil), P. coreodes (Corumbá, Mato Grosso do Sul, Brazil), and P. arthuri (Maracay, Aragua, Venezuela), all of them being from the field. The seminiferous tubules were torn apart, crushed, and fixed on slides in liquid nitrogen. The cytogenetic techniques Lacto-Aceto Orcein15,16 and C-banding17 were applied for the description of karyotype, characterization of meiosis, and description of heterochromatin pattern, respectively. Then the cytogenomic technique of CMA3/DAPI banding was applied according to Schimid18 with the modifications provided by Severi-Aguiar et al.19 to differentiate the heterochromatin regions rich in AT and CG. The biological material was analyzed using a Jenaval light microscope (Zeiss, Jena, Germany) and Olympus BX-FLA fluorescence microscope.

All species of the genus Psammolestes presented the same chromosomal characteristics, namely, chromocenter formed only by sex chromosomes X and Y during the prophase (Figure 1A–C), euchromatic autosomes and sex chromosome X and heterochromatic sex chromosome Y (Figure 1D–F), sex chromosomes X rich in CG (Figure 1G–I) and Y rich in CG (Figure 1J–L), and karyotype 2n = 22 (Figure 1M–O). These characteristics confirm the data already described in the literature (Table 1) and corroborate the monophyly of this genus.

Figure 1.
Figure 1.

Cytogenetic analyses of Psammolestes spp. Note the X and Y sex chromosomes forming the chromocenter of Psammolestes tertius (A, arrow), Psammolestes coreodes (B, arrow), and Psammolestes arthuri (C, arrow). Note that the autosomes and X chromosome are euchromatic and Y is heterochromatic in P. tertius (D), P. coreodes (E), and P. arthuri (F). Note that the X chromosome is rich in CG (G–I) and the Y chromosome is rich in AT (J–L) and the karyotype is 2n = 22 (20A + XY) (M–O) for P. tertius (G, J, and M), P. coreodes (H, K, and N), and P. arthuri (I, L, and O). X: X sex chromosome, Y: Y sex chromosome. Scale bar: 10 μm.

Citation: The American Journal of Tropical Medicine and Hygiene 99, 6; 10.4269/ajtmh.18-0109

The karyotype 2n = 22 is present in all species of the tribe Rhodniini.20,21 This karyotype is the same number of chromosomes as the ancestor of Triatominae,17 which indicates that the genomic reorganization events that occurred during the evolution of the tribe Rhodniini did not lead to numerical alterations in the chromosomes, unlike what happened to the tribe Triatomini, which presents karyotypes ranging from 2n = 21 to 25.22,23

The chromocenter formed only by sex chromosomes X and Y is also shared with the species of Rhodnius,13,24 which demonstrates that this meiotic behavior is present in all species of the tribe Rhodniini. In the tribe Triatomini, there are species with the pattern described for Psammolestes and species that present union of autosomes with sexual chromosomes in the formation of the chromocenter.25 This meiotic behavior can be used as a taxonomic tool to group related species. For example, all species of the Triatoma brasiliensis complex present a chromocenter formed by the sex chromosomes plus a pair of autosomes (characteristics that make it possible to differentiate seven species in this complex from all other triatomine complexes).26

With the exception of Rhodnius colombiensis Mejia, Galvão and Jurberg, 1999; Rhodnius nasutus Stål, 1859; Rhodnius pallescens Barber, 1932; R. pictipes Stål, 1872; and R. taquarussuensis Rosa et al. 2017, 21,27 all Rhodnius species also have constitutive heterochromatin restricted to the sex chromosome Y, as well as observed in Psammolestes spp. The distribution pattern of constitutive heterochromatin is extremely important for the taxonomy of Triatominae, being one of the main tools used in the description of the last species of the tribe Rhodniini, namely, R. taquarussuensis.21 In addition, the three species of the genus Psammolestes showed the same DNA composition rich in AT and CG.

Heterochromatin loss/reorganization in AT and CG composition could have occurred during the speciation of Psammolestes spp, as observed for the species of the group pallescens.28 However, considering that the ancestor of P. tertius, P. coreodes, and P. arthuri was similar to R. robustus (which does not present heterochromatin in the autosomes either, only in the sexual chromosome Y27) and especially the degree of specialization of these species during their evolution (they inhabit only bird nests), it can be stated that the species maintained the genetic material without chromosomal changes.

The cytogenetic characteristics analyzed indicate chromosomal homogeneity in the genus Psammolestes, which corroborates the monophyletic feature of the genus and suggests that during the derivation of P. tertius, P. coreodes, and P. arthuri from the common ancestor, there was no reorganization in the number or structure of chromosomes.

Acknowledgments:

We appreciate Wilma Savini and Jose Manuel Ayala for their support in the Venezuela and Central Laboratory of Public Health and Professor Gonçalo Moniz (LACEN - BA) for field support in Bahia.

REFERENCES

  • 1.

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

  • 2.

    Oliveira J, Alevi KCC, 2017. Taxonomic status of Panstrongylus herreri Wygodzinsky, 1948 and the number of Chagas disease vectors. Rev Soc Bras Med Trop 50: 434435.

    • Search Google Scholar
    • Export Citation
  • 3.

    Monteiro FA, Wesson DM, Dotson EM, Schofield CJ, Beard CB, 2000. Phylogeny and molecular taxonomy of the Rhodniini derived from mitochondrial and nuclear DNA sequences. Am J Trop Med Hyg 62: 460465.

    • Search Google Scholar
    • Export Citation
  • 4.

    Lent H, Wygodzinsky P, 1979. Revision of the Triatominae (Hemiptera: Reduviidae) and their significance as vector of Chagas’s disease. Bull Am Mus Nat Hist 163: 123520.

    • Search Google Scholar
    • Export Citation
  • 5.

    Justi S, Galvão C, 2017. The evolutionary origin of diversity in Chagas disease vectors. Trends Parasitol 33: 4252.

  • 6.

    Galvão C, Carcavallo R, Rocha DS, Jurberg J, 2003. A checklist of the current valid species of the subfamily Triatominae Jeannel, 1919 (Hemiptera, Reduviidae) and their geographical distribution, with nomenclatural and taxonomic notes. Zootaxa 202: 136.

    • Search Google Scholar
    • Export Citation
  • 7.

    Cabrera R, 2006. Notas breves sobre Psammolestes tertius Bergroth, 1911 (Reduviidae: Hemiptera): un triatomino silvestre. An Fac Med (Lima) 67: 345365.

    • Search Google Scholar
    • Export Citation
  • 8.

    Hypsa V, Tietz D, Zrzavy J, Rego RO, Galvão C, Jurberg J, 2002. Phylogeny and biogeography of Triatominae (Hemiptera, Reduviidae): molecular evidence of a New World origin of the Asiatic clade. Mol Phylogenet Evol 23: 447457.

    • Search Google Scholar
    • Export Citation
  • 9.

    Soares RPP, Barbosa SE, Borges EC, Melo Júnior TA, Romanha AJ, Dujardin JP, Schofield CJ, Diotaiuti L, 2001. Genetic studies of Psammolestes tertius (Hemíptera: Reduviidae: Triatominae) using male genital morphology, morphometry, isoenzymes, and random amplified polymorphic DNA. Biochem Genet 39: 113.

    • Search Google Scholar
    • Export Citation
  • 10.

    Schofield CJ, Dujardin JP, 1999. Theories on the evolution of Rhodnius. Actual Biol 21: 183197.

  • 11.

    Schreiber G, Pellegrino J, 1950. Eteropicnosi di autosomi come possibile meccanismo di speciazione; ricerche citologiche su alcuni Emitteri neotropici. Sci Genet 3: 215226.

    • Search Google Scholar
    • Export Citation
  • 12.

    Panzera F et al. 1998. Cytogenetics of triatomines. Carcavallo RU, Galíndez-Girón I, Jurberg J, Lent H, eds. Atlas of Chagas Disease Vectors in the Americas. Rio de Janeiro, Brazil: Editora Fiocruz, 621–664.

  • 13.

    Panzera Y, Pita S, Ferreiro MJ, Ferrandis I, Lages C, Perez R, Silva AE, Guerra M, Panzera F, 2012. High dynamics of rDNA cluster location in kissing bug holocentric chromosomes (Triatominae, Heteroptera). Cytogenet Genome Res 138: 5667.

    • Search Google Scholar
    • Export Citation
  • 14.

    Oliveira J, Alevi KCC, Fonseca EO, Souza OM, Santos CG, Azeredo-Oliveira MTV, Rosa JA, 2016. New record and cytogenetic analysis of Psammolestes tertius Lent & Jurberg, 1965 (Hemiptera, Reduviidae, Triatominae) from Bahia state, Brazil. Genet Mol Res 15: 16.

    • Search Google Scholar
    • Export Citation
  • 15.

    De Vaio ES, Grucci B, Castagnino AM, Franca ME, Martinez ME, 1985. Meiotic differences between three triatomine species (Hemiptera:Reduviidae). Genetica 67: 185191.

    • Search Google Scholar
    • Export Citation
  • 16.

    Alevi KCC, Mendonça PP, Pereira NP, Rosa JA, Azeredo-Oliveira MTV, 2012. Karyotype of Triatoma melanocephala Neiva and Pinto (1923). Does this species fit in the Brasiliensis subcomplex? Infect Genet Evol 12: 16521653.

    • Search Google Scholar
    • Export Citation
  • 17.

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

  • 18.

    Schimid M, 1980. Chromosoma banding an amphibia IV. Differentiation of GC and AT rich regions in Anura. Chromosoma 77: 83103.

  • 19.

    Severi-Aguiar GD, Lourenço LB, Bicudo HE, Azeredo-Oliveira MTV, 2006. Meiosis aspects and nucleolar activity in Triatoma vitticeps (Triatominae, Heteroptera). Genetica 126: 141151.

    • Search Google Scholar
    • Export Citation
  • 20.

    Alevi KCC, Ravazi A, Mendonça VJ, Rosa JA, Azeredo-Oliveira MTV, 2015. Karyotype of Rhodnius montenegrensis (Hemiptera, Triatominae). Genet Mol Res 12: 222226.

    • Search Google Scholar
    • Export Citation
  • 21.

    Rosa JA, Justino HHG, Nascimento JD, Mendonça VJ, Rocha CS, Carvalho DB, Falcone R, Azeredo-Oliveira MTV, Alevi KCC, Oliveira J, 2017. A new species of Rhodnius from Brazil (Hemiptera, Reduviidae, Triatominae). ZooKeys 675: 125.

    • Search Google Scholar
    • Export Citation
  • 22.

    Ueshima N, 1966. Cytotaxonomy of the Triatominae (Reduviidae, Hemiptera). Chromosoma 18: 97122.

  • 23.

    Alevi KCC, Oliveira J, Rosa JA, Azeredo-Oliveira MTV, 2018. Karyotype evolution of Chagas disease vectors (Hemiptera, Triatominae). Am J Trop Med Hyg 99: 8789.

    • Search Google Scholar
    • Export Citation
  • 24.

    Perez R, Panzera Y, Scafiezzo S, Mazzella M, Panzera P, Dujardin JP, Scvortzoff E, 1992. Cytogenetics as a tool for triatominae species distinction. Mem Inst Oswaldo Cruz 87: 353361.

    • Search Google Scholar
    • Export Citation
  • 25.

    Alevi KCC, Nascimento JGO, Moreira FFF, Jurberg J, Azeredo-Oliveira MTV, 2016. Cytogenetic characterisation of Triatoma rubrofasciata (De Geer) (Hemiptera, Triatominae) spermatocytes and its cytotaxonomic application. Afr Entomol 24: 257260.

    • Search Google Scholar
    • Export Citation
  • 26.

    Alevi KCC, Oliveira J, Moreira FFF, Jurberg J, Rosa JA, Azeredo-Oliveira MTV, 2015. Chromosomal characteristics and distribution of constitutive heterochromatin in the Matogrossensis and Rubrovaria subcomplexes. Infect Genet Evol 33: 158162.

    • Search Google Scholar
    • Export Citation
  • 27.

    Dujardin JP, Schofield CJ, Panzera F, 2002. Los Vectores de la Enfermedad de Chagas. Bruxelles, Belgium: Académie Royale des Sciences D’Outre-Mer.

  • 28.

    Alevi KCC, Ravazi A, Franco-Bernardes MF, Rosa JA, Azeredo-Oliveira MTV, 2015. Chromosomal evolution in the pallescens group (Hemiptera, Triatominae). Genet Mol Res 14: 1265412659.

    • Search Google Scholar
    • Export Citation

Author Notes

Address correspondence to Jader Oliveira, Departamento de Ciências Biológicas, Faculdade de Ciências Farmacêuticas, Universidade Estadual Paulista “Júlio de Mesquita Filho”, Câmpus de Araraquara, Rod. Araraquara-Jaú km 1, Araraquara 14801-902, Brazil. E-mail: jdr.oliveira@hotmail.com

Financial support: The study was supported by Fundação de Amparo à Pesquisa do Estado de São Paulo (process numbers 2013/19764-0 and 2015/11372-1) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, Brazil).

Authors’ addresses: Jader Oliveira and João Aristeu da Rosa, Departamento de Ciências Biológicas, Faculdade de Ciências Farmacêuticas, Universidade Estadual Paulista “Júlio de Mesquita Filho”, Araraquara, Brazil, E-mails: jdr.oliveira@hotmail.com and rosaja@fcfar.unesp.br. Kaio Cesar Chaboli Alevi, Amanda Ravazi, 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, Brazil, E-mails: kaiochaboli@hotmail.com, amandaravazi95@gmail.com, and tercilia@ibilce.unesp.br. Heitor Miraglia Herrera and Filipe Martins Santos, Universidade Católica Dom Bosco, Campo Grande, Brazil, E-mails: herrera@ucdb.br and filipemsantos@outlook.com.

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