• View in gallery

    Composition of the heterochromatin base pairs in prophases of Rhodnius marabaensis (A and B) and Rhodnius domesticus (C and D). (A and C) Y sex chromosome rich in AT. (B) X sex chromosome rich in CG. (D) X sex chromosome and autosomes rich in GC. Bar: 10 μm. This figure appears in color at www.ajtmh.org.

  • 1.

    World Health Organization, 2020. Chagas disease (American trypanosomiasis). Geneva, Switzerland: WHO. Available at: http://www.who.int/chagas/en/. Accessed July 17, 2020.

    • Search Google Scholar
    • Export Citation
  • 2.

    Dias JCP 2016. II consenso Brasileiro em Doença de Chagas, 2015. Epidemiol Serv Saúde 25: 786.

  • 3.

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

  • 4.

    Justi SA, Russo CA, dos Santos Mallet JR, Obara MT, Galvão C, 2014. Molecular phylogeny of triatomini (Hemiptera: Reduviidae: Triatominae). Parasit Vectors 7: 149.

    • Search Google Scholar
    • Export Citation
  • 5.

    Justi SA, Galvao C, Schrago CG, 2016. Geological changes of the Americas and their influence on the diversification of the Neotropical kissing bugs (Hemiptera: Reduviidae: Triatominae). PLoS Negl Trop Dis 10: e0004527.

    • Search Google Scholar
    • Export Citation
  • 6.

    Hypša V, Tietz DF, Zrzavý J, Rego ROM, Galvão C, Jurberg J, 2002. Phylogeny and biogeography of Triatominae (Hemiptera: Reduvidae) molecular evidence of a new world origin of the Asiatic clade. Mol Phyl Evol 23: 447457.

    • Search Google Scholar
    • Export Citation
  • 7.

    Galvão C, Carcavallo RU, 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
  • 8.

    Pita S, Panzera F, Ferrandis I, Galvão C, Gómez-Palacio A, Panzera Y, 2013. Chromosomal divergence and evolutionary inferences in Rhodniini based on the chromosomal location of ribosomal genes. Mem Inst Oswaldo Cruz 108: 376382.

    • Search Google Scholar
    • Export Citation
  • 9.

    Morielle-Souza A, Azeredo-Oliveira MTV, 2007. Differential characterization of holocentric chromosomes in triatomines (Heteroptera, Triatominae) using different staining techniques and fluorescent in situ hybridization. Gen Mol Res 6: 713720.

    • Search Google Scholar
    • Export Citation
  • 10.

    Bardella VB, Pita S, Vanzela ALL, Galvão C, Panzera F, 2016. Heterochromatin base pair composition and diversification in holocentric chromosomes of kissing bugs. (Hemiptera, Reduviidae). Mem Inst Oswaldo Cruz 111: 614662.

    • Search Google Scholar
    • Export Citation
  • 11.

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

  • 12.

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

    • Search Google Scholar
    • Export Citation
  • 13.

    Alevi KCC, Ravazi A, Mendonça VJ, Rosa JA, Azeredo-Oliveira MTV, 2015. Karyotype of Rhodnius montenegrensis (Hemiptera, Triatominae). Gen Mol Res 14: 222226.

    • Search Google Scholar
    • Export Citation
  • 14.

    Panzera F, Pérez R, Panzera Y, Ferrandis I, Ferreiro MJ, Calleros L, 2010. Cytogenetics and genome evolution in the subfamily Triatominae (Hemiptera, Reduviidae). Cytogenet Genome Res 128: 7787.

    • Search Google Scholar
    • Export Citation
  • 15.

    Pérez R, Panzera Y, Scafiezzo S, Mazzella MC, Panzera F, Dujardin JP, Scvortzoff E, 1992. Cytogenetic as a tool for Triatominae species distinction (Hemiptera, Reduviidae). Mem Inst Oswaldo Cruz 87: 353361.

    • Search Google Scholar
    • Export Citation
  • 16.

    Panzera F 1998. Cytogenetics of triatomines. Carcavallo RU, ed. Atlas of Chagas Disease Vectors in the Americas. Rio de Janeiro, Brazil: Fiocruz, 621664.

    • Search Google Scholar
    • Export Citation
  • 17.

    Barth R, 1956. Estudos anatômicos e histológicos sôbre a subfamília Triatominae (Hemiptera, Reduviidae). VI. Estudo comparativo sôbre a espermiocitogênese das espécies mais importantes. Mem Inst Oswaldo Cruz 54: 599623.

    • Search Google Scholar
    • Export Citation
  • 18.

    Koshy TK, 1979. Chromosomes of Triatominae I: haploid karyotypes of three species in the genus Rhodnius (Hemiptera: Reduviidae). Acta Cient Venezolana 30: 183190.

    • Search Google Scholar
    • Export Citation
  • 19.

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

    • Search Google Scholar
    • Export Citation
  • 20.

    Koshy TK, 1979. Chromosomes of triatominae II: karyotypes studies of five species in the genus Rhodnius (Hemiptera: Reduviidae). Acta Cient Venezolana 30: 191195.

    • Search Google Scholar
    • Export Citation
  • 21.

    Panzera Y, Pita S, Ferreiro MJ, Ferrandis I, Lages C, Pérez 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
  • 22.

    Panzera F, Pérez R, Hornos S, Panzera Y, Cestau R, Delgado V, Nicolini P, 1996. Chromosome numbers in the Triatominae (Hemiptera-Reduviidade): a review. Mem Inst Oswaldo Cruz 91: 515518.

    • Search Google Scholar
    • Export Citation
  • 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.

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

  • 25.

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

    • Search Google Scholar
    • Export Citation
  • 26.

    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
  • 27.

    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: 0125.

    • Search Google Scholar
    • Export Citation
  • 28.

    Nascimento JD 2019. Taxonomical over splitting in the Rhodnius prolixus (Insecta: Hemiptera: Reduviidae) clade: are R. taquarussuensis (da Rosa et al., 2017) and R. neglectus (Lent, 1954) the same species? PLoS One 14: 0211285.

    • Search Google Scholar
    • Export Citation
  • 29.

    Alevi KCC, Imperador CHL, Moreira FFF, Jurberg J, Azeredo-Oliveira MTV, 2016. Differentiation between Triatoma arthurneivai and Triatoma wygodzinskyi (Hemiptera: Reduviidae: Triatominae) using cytotaxonomy. Gen Mol Res 15: gmr.15027869.

    • Search Google Scholar
    • Export Citation
  • 30.

    Alevi KCC, Borsatto KC, Moreira FFF, Jurberg J, Azeredo-Oliveira MTV, 2015. Karyosystematics of Triatoma rubrofasciata (De Geer, 1773) (Hemiptera: Reduviidae: Triatominae). Zootaxa 3994: 433438.

    • Search Google Scholar
    • Export Citation
  • 31.

    Ravazi A, Oliveira J, Alevi KCC, 2020. Taxonomia e sistemática da tribo Rhodniini (Hemiptera, Triatominae): uma mini-revisão. Oliveira J, Alevi KCC, Camargo LMA, Meneguetti DUO, eds. Atualidades em Medicina Tropical no Brasil: Vetores. Rio Branco, Brazil: Stricto Sensu Editora, 3848.

    • Search Google Scholar
    • Export Citation

 

 

 

 

 

Revisiting the Chromosomal Diversification of the Genus Rhodnius (Stål, 1859) (Hemiptera, Triatominae)

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  • 1 Instituto de Biociências, Universidade Estadual Paulista “Júlio de Mesquita Filho” (IBB/UNESP), Botucatu, Brazil;
  • 2 Departamento de Ciências Biológicas, Laboratório de Parasitologia, Faculdade de Ciências Farmacêuticas, Universidade Estadual Paulista “Júlio de Mesquita Filho” (FCFAR/UNESP), Araraquara, Brazil;
  • 3 Departamento de Biologia, Laboratório de Biologia Celular, Instituto de Biociências, Letras e Ciências Exatas, Universidade Estadual Paulista “Júlio de Mesquita Filho” (IBILCE/UNESP), São José do Rio Preto, Brazil

ABSTRACT

Although all triatomines are considered as potential vectors of the Chagas disease, the Triatoma, Panstrongylus, and Rhodnius genera are the most important from the epidemiological point of view. Based on cytogenetic analyzes carried out so far (C banding and FISH), the species of the genus Rhodnius show little interspecific chromosomal variation. Thus, we analyzed the distribution of AT- and CG-rich DNA in the chromatin and chromosomes of the genus Rhodnius and discuss the chromosome evolution of these vectors. Except for Rhodnius domesticus, Rhodnius nasutus, Rhodnius pictipes, Rhodnius colombiensis, and Rhodnius pallescens, all Rhodnius species have euchromatic autosomes with the absence of AT- and CG-rich blocks. Curiously, the same species that have heterochromatin blocks in the autosomes also have chromomycin A3 (CMA3+) blocks dispersed in the prophasic nucleus (demonstrating that the heterochromatin of these species is rich in CG). Thus, we characterize the AT- and CG-rich DNA pattern for the genus Rhodnius, and we suggest that the pattern of CG-rich heterochromatin in the autosomes of these vectors evolved independently in pallescens, pictipes, and prolixus groups.

Triatomines (Hemiptera, Triatominae) are hematophagous insects of great epidemiological importance because they are vectors of the protozoan Trypanosoma cruzi (Chagas, 1909) (Kinetoplastida, Trypanosomatidae), the etiological agent of Chagas disease—a neglected disease that affects about eight million people, resulting in approximately 10,000 deaths per year from clinical manifestations (such as terminal heart failure, thromboembolic complications, refractory ventricular arrhythmias, and sudden death).1,2 Although all of triatomine species, of both sexes, are considered as potential vectors of Chagas disease, the Triatoma (Laporte, 1832), Panstrongylus (Berg, 1879), and Rhodnius (Stål, 1859) genera are the most important from the epidemiological point of view.3

The genus Rhodnius is a paraphyletic group composed of 23 species grouped into three large groups (pallescens, pictipes, and prolixus) (Table 1). The genus paraphilia is related to the fact that the species of the prolixus group present greater phylogenetic proximity with the Psammolestes (Bergroth, 1911 genus) than with other groups of Rhodnius spp.4,5 In an attempt to solve this issue, Hypsa et al.6 suggested changing the generic status from Psammolestes to Rhodnius. However, because of morphological and habitat divergences, the genus Psammolestes was maintained by the scientific community.7

Table 1

Cytogenetic characteristics of Rhodnius spp.

C-bandingCMA3/DAPI
Rhodnius genusKaryotypeAXYAXY
prolixus group
Rhodnius barretti
Rhodnius dalessandroi
Rhodnius domesticus2n = 22 (20A + XY)*YesNoYesCMA3+CMA3+DAPI+
Rhodnius milesi2n = 22 (20A + XY)NoNoYesCMA3+DAPI+
Rhodnius marabaensis2n = 22 (20A + XY)NoNoYesCMA3+DAPI+
Rhodnius montenegrensis2n = 22 (20A + XY)NoNoYesCMA3+DAPI+
Rhodnius nasutus2n = 22 (20A + XY)§YesNoYesCMA3+CMA3+DAPI+
Rhodnius neglectus2n = 22 (20A + XY)NoNoYesCMA3+DAPI+
Rhodnius neivai2n = 22 (20A + XY)#NoNoYesCMA3+DAPI+
Rhodnius prolixus2n = 22 (20A + XY)**NoNoYesCMA3+DAPI+
Rhodnius robustus2n = 22 (20A + XY)††NoNoYesCMA3+DAPI+
pictipes group
Rhodnius amazonicus
Rhodnius brethesi2n = 22 (20A + XY)NoNoYesCMA3+DAPI+
Rhodnius paraensis
Rhodnius pictipes2n = 22 (20A + XY)††Yes§No§Yes§CMA3+CMA3+DAPI+
Rhodnius stali2n = 22 (20A + XY)*NoNoYesCMA3+DAPI+
Rhodnius zeledoni
pallescens group
Rhodnius colombiensis2n = 22 (20A + XY)*Yes‡‡No‡‡Yes‡‡CMA3+CMA3+DAPI+
Rhodnius ecuadoriensis2n = 22 (20A + XY)NoNoYesCMA3+DAPI+
Rhodnius pallescens2n = 22 (20A + XY)§§YesNoYesCMA3+CMA3+DAPI+

A: autosome, X: X sex chromosome, Y: Y sex chromosome.

Dujardin et al.12

Alevi et al.13

Panzera et al.14

Pérez et al.15

Panzera et al.16

Barth.17

Koshy.18

Schreiber and Pellegrino.19

Koshy.20

Panzera et al.21

Panzera et al.22

The species of the genus Rhodnius show little interspecific chromosomal variation because all species analyzed so far have karyotype 2n = 22 (20A + XY) (Table 1) and 45S rDNA clusters restricted to sex chromosomes.8 Besides, most species have heterochromatin restricted to the Y sex chromosome (Table 1). However, the knowledge of the genomic composition of heterochromatin base pairs (AT and CG) is limited to Rhodnius pallescens (Barber, 1932),9 and Rhodnius prolixus (Stål, 1859),10 highlighting the necessity for further studies on the molecular cytogenetics of these vectors. Based on the data presented earlier, we analyzed the distribution of AT- and CG-rich DNA in the chromatin and chromosomes of the genus Rhodnius, and discuss the chromosome evolution of these vectors.

At least five adult males from each species (10 R. prolixus, 10 Rhodnius robustus (Larrousse, 1927), 10 Rhodnius neglectus (Lent, 1954), five Rhodnius nasutus (Stål, 1859), five Rhodnius domesticus (Neiva and Pinto, 1923), 10 Rhodnius montenegrensis (Rosa et al. [2012]), and five Rhodnius marabaensis (Souza et al. [2016])) were used. They had been assigned by the Triatominae Insectarium within the Department of Biological Sciences, in the College of Pharmaceutical Sciences, at Sao Paulo State University’s Araraquara campus (FCFAR/UNESP), São Paulo, Brazil. The seminiferous tubules of the specimens were squashed and fixed to a coverslip. Then, they underwent the cytogenetic technique of CMA3/4′,6-diamidino-2-phenylindole (DAPI)9 and C banding.11 The biological material was analyzed using a Jenaval light microscope (Zeiss) attached to a digital camera, with the AxioVision LE 4.8 image analyzer (Copyright 2006–2009 Carl Zeiss Imaging Solutions GmbH), and using a fluorescence microscope Zeiss-Axioskop and Olympus BX-FLA.

All species had the same number of chromosomes, 2n = 22 (20A + XY) (Table 1), confirming the hypothesis that all species of the Rhodniini tribe have 22 chromosomes.23 Taking into account that the ancestral karyotype is 2n = 22,23,24 Alevi et al.23 highlight that during the diversification of the pallescens, pictipes, and prolixus groups, there were no evolutionary events (as agmatoploidy and simploidy) that resulted in changes in the number of chromosomes.

Except for R. domesticus, R. nasutus, Rhodnius pictipes (Stål, 1872), Rhodnius colombiensis (Mejia, Galvão and Jurberg, 1999), and R. pallescens, all Rhodnius species have euchromatic autosomes with the absence of AT- and CG-rich blocks (Figure 1A and B) (Table 1). Curiously, the same species that have heterochromatin blocks in the autosomes also have CMA3+ blocks dispersed in the prophasic nucleus (Figure 1D) (Table 1), emphasizing that the heterochromatin present in the chromosomes of R. domesticus, R. nasutus, R. pictipes, R. colombiensis, and R. pallescens is rich in CG regions. Besides, all species had the euchromatic X sex chromosome and CMA3+ (Figure 1B and D), and the heterochromatic Y chromosome and DAPI+ (Figure 1A and C) (Table 1).

Figure 1.
Figure 1.

Composition of the heterochromatin base pairs in prophases of Rhodnius marabaensis (A and B) and Rhodnius domesticus (C and D). (A and C) Y sex chromosome rich in AT. (B) X sex chromosome rich in CG. (D) X sex chromosome and autosomes rich in GC. Bar: 10 μm. This figure appears in color at www.ajtmh.org.

Citation: The American Journal of Tropical Medicine and Hygiene 104, 2; 10.4269/ajtmh.20-0875

Taking into account that Rhodnius species whose autosomes present heterochromatic blocks and CMA3+ belong to different groups (prolixus group: R. domesticus and R. nasutus; pictipes group: R. pictipes; and pallescens group: R. colombiensis and R. pallescens), we suggest that the gain/loss of CG-rich heterochromatin was an event that took place independently in the three groups of Rhodnius and can be related to different evolutionary factors. Alevi et al.,25 for example, suggest that the different patterns of heterochromatin losses observed in the pallescens group can be associated with adaptation to different environments occupied by species.

The divergences in the composition of the autosomes can also be used as taxonomic tools to differentiate some species of Rhodnius because events of phenotypic plasticity and cryptic speciation have been reported for this genus of medical importance.26 Within the prolixus group, for example, R. domesticus and R. nasutus can be distinguished from all other species with euchromatic autosomes; within the pictipes group, R. pictipes can be distinguished from all other species by cytotaxonomy; besides, R. colombiensis and R. pallescens can be differentiated from R. ecuadoriensis (Lent and León, 1958) (euchromatic autosomes). Still, R. colombiensis and R. pallescens can also be differentiated from each other by the amount of heterochromatin in the autosomes.25

Recently, the heterochromatin pattern and the composition of AT and CG was one of the tools used to describe R. taquarussuensis Rosa et al.27 However, molecular analyzes and experimental crosses showed that R. taquarussuensis was R. neglectus with chromosomal polymorphisms.28 Based on this, it is evident that although cytogenetic analyses are of great taxonomic importance,29,30 the confirmation that different cytotypes represent valid taxa must be performed through integrative taxonomy.31

Thus, we characterize the AT- and CG-rich DNA pattern for the genus Rhodnius, and we suggest that the pattern of CG-rich heterochromatin in the autosomes of these vectors evolved independently in pallescens, pictipes, and prolixus groups.

REFERENCES

  • 1.

    World Health Organization, 2020. Chagas disease (American trypanosomiasis). Geneva, Switzerland: WHO. Available at: http://www.who.int/chagas/en/. Accessed July 17, 2020.

    • Search Google Scholar
    • Export Citation
  • 2.

    Dias JCP 2016. II consenso Brasileiro em Doença de Chagas, 2015. Epidemiol Serv Saúde 25: 786.

  • 3.

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

  • 4.

    Justi SA, Russo CA, dos Santos Mallet JR, Obara MT, Galvão C, 2014. Molecular phylogeny of triatomini (Hemiptera: Reduviidae: Triatominae). Parasit Vectors 7: 149.

    • Search Google Scholar
    • Export Citation
  • 5.

    Justi SA, Galvao C, Schrago CG, 2016. Geological changes of the Americas and their influence on the diversification of the Neotropical kissing bugs (Hemiptera: Reduviidae: Triatominae). PLoS Negl Trop Dis 10: e0004527.

    • Search Google Scholar
    • Export Citation
  • 6.

    Hypša V, Tietz DF, Zrzavý J, Rego ROM, Galvão C, Jurberg J, 2002. Phylogeny and biogeography of Triatominae (Hemiptera: Reduvidae) molecular evidence of a new world origin of the Asiatic clade. Mol Phyl Evol 23: 447457.

    • Search Google Scholar
    • Export Citation
  • 7.

    Galvão C, Carcavallo RU, 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
  • 8.

    Pita S, Panzera F, Ferrandis I, Galvão C, Gómez-Palacio A, Panzera Y, 2013. Chromosomal divergence and evolutionary inferences in Rhodniini based on the chromosomal location of ribosomal genes. Mem Inst Oswaldo Cruz 108: 376382.

    • Search Google Scholar
    • Export Citation
  • 9.

    Morielle-Souza A, Azeredo-Oliveira MTV, 2007. Differential characterization of holocentric chromosomes in triatomines (Heteroptera, Triatominae) using different staining techniques and fluorescent in situ hybridization. Gen Mol Res 6: 713720.

    • Search Google Scholar
    • Export Citation
  • 10.

    Bardella VB, Pita S, Vanzela ALL, Galvão C, Panzera F, 2016. Heterochromatin base pair composition and diversification in holocentric chromosomes of kissing bugs. (Hemiptera, Reduviidae). Mem Inst Oswaldo Cruz 111: 614662.

    • Search Google Scholar
    • Export Citation
  • 11.

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

  • 12.

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

    • Search Google Scholar
    • Export Citation
  • 13.

    Alevi KCC, Ravazi A, Mendonça VJ, Rosa JA, Azeredo-Oliveira MTV, 2015. Karyotype of Rhodnius montenegrensis (Hemiptera, Triatominae). Gen Mol Res 14: 222226.

    • Search Google Scholar
    • Export Citation
  • 14.

    Panzera F, Pérez R, Panzera Y, Ferrandis I, Ferreiro MJ, Calleros L, 2010. Cytogenetics and genome evolution in the subfamily Triatominae (Hemiptera, Reduviidae). Cytogenet Genome Res 128: 7787.

    • Search Google Scholar
    • Export Citation
  • 15.

    Pérez R, Panzera Y, Scafiezzo S, Mazzella MC, Panzera F, Dujardin JP, Scvortzoff E, 1992. Cytogenetic as a tool for Triatominae species distinction (Hemiptera, Reduviidae). Mem Inst Oswaldo Cruz 87: 353361.

    • Search Google Scholar
    • Export Citation
  • 16.

    Panzera F 1998. Cytogenetics of triatomines. Carcavallo RU, ed. Atlas of Chagas Disease Vectors in the Americas. Rio de Janeiro, Brazil: Fiocruz, 621664.

    • Search Google Scholar
    • Export Citation
  • 17.

    Barth R, 1956. Estudos anatômicos e histológicos sôbre a subfamília Triatominae (Hemiptera, Reduviidae). VI. Estudo comparativo sôbre a espermiocitogênese das espécies mais importantes. Mem Inst Oswaldo Cruz 54: 599623.

    • Search Google Scholar
    • Export Citation
  • 18.

    Koshy TK, 1979. Chromosomes of Triatominae I: haploid karyotypes of three species in the genus Rhodnius (Hemiptera: Reduviidae). Acta Cient Venezolana 30: 183190.

    • Search Google Scholar
    • Export Citation
  • 19.

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

    • Search Google Scholar
    • Export Citation
  • 20.

    Koshy TK, 1979. Chromosomes of triatominae II: karyotypes studies of five species in the genus Rhodnius (Hemiptera: Reduviidae). Acta Cient Venezolana 30: 191195.

    • Search Google Scholar
    • Export Citation
  • 21.

    Panzera Y, Pita S, Ferreiro MJ, Ferrandis I, Lages C, Pérez 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
  • 22.

    Panzera F, Pérez R, Hornos S, Panzera Y, Cestau R, Delgado V, Nicolini P, 1996. Chromosome numbers in the Triatominae (Hemiptera-Reduviidade): a review. Mem Inst Oswaldo Cruz 91: 515518.

    • Search Google Scholar
    • Export Citation
  • 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.

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

  • 25.

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

    • Search Google Scholar
    • Export Citation
  • 26.

    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
  • 27.

    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: 0125.

    • Search Google Scholar
    • Export Citation
  • 28.

    Nascimento JD 2019. Taxonomical over splitting in the Rhodnius prolixus (Insecta: Hemiptera: Reduviidae) clade: are R. taquarussuensis (da Rosa et al., 2017) and R. neglectus (Lent, 1954) the same species? PLoS One 14: 0211285.

    • Search Google Scholar
    • Export Citation
  • 29.

    Alevi KCC, Imperador CHL, Moreira FFF, Jurberg J, Azeredo-Oliveira MTV, 2016. Differentiation between Triatoma arthurneivai and Triatoma wygodzinskyi (Hemiptera: Reduviidae: Triatominae) using cytotaxonomy. Gen Mol Res 15: gmr.15027869.

    • Search Google Scholar
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  • 30.

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Author Notes

Address correspondence to Kaio Cesar Chaboli Alevi, FCFAR/UNESP, Rodovia Araraquara-Jaú km 1, Araraquara, SP 14801-902, Brazil. E-mail: kaiochaboli@hotmail.com

Disclosure: The experiments comply with the current laws of the country in which they were performed.

Financial support: This work was financed by the Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) (Number processes 2015/11372-1 and 2018/23846-6), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), and the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior-Brasil (CAPES), Finance Code 001.

Authors' addresses: Amanda Ravazi, Instituto de Biociências, Universidade Estadual Paulista “Júlio de Mesquita Filho”, Botucatu, Brazil, E-mail: amandaravazi95@gmail.com. Nicoly Olaia, Jader de Oliveira, Eder dos Santos Souza, João Aristeu da Rosa, and Kaio Cesar Chaboli Alevi, Laboratório de Parasitologia, Faculdade de Ciências Farmacêuticas, Universidade Estadual Paulista Júlio de Mesquita Filho (FCFAR/UNESP), Araraquara, Brazil, E-mails: olaia.nicoly1@gmail.com, jdr.oliveira@hotmail.com, ederss1@hotmail.com, joaoaristeu@gmail.com, and kaiochaboli@hotmail.com. Maria Tercília Vilela de Azeredo-Oliveira, Departamento de Biologia, Instituto de Biociências, Letras e Ciências Exatas, São José do Rio Preto, Brazil, E-mail: tercilia.vilela@unesp.br.

These authors contributed equally to this work.

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