Triatoma vitticeps subcomplex (Hemiptera, Reduviidae, Triatominae): a new grouping of Chagas disease vectors from South America
© The Author(s). 2017
Received: 3 December 2016
Accepted: 4 April 2017
Published: 13 April 2017
Triatomines have been grouped into complexes and subcomplexes based largely on morphological and geographical distribution. Although these groupings are not formally recognised as taxonomic ranks, they are likely monophyletic. However, recent studies have demonstrated that some subcomplexes from South America did not form monophyletic groups, and reorganisations have been suggested. One suggested reorganisation is to exclude Triatoma vitticeps, T. melanocephala, and T. tibiamaculata from the T. brasiliensis subcomplex. However, T. vitticeps and T. melanocephala exhibit several similar characteristics, including morphologic, cytogenetic, and phylogenetic features, a factor which supports the creation of a new subcomplex. Thus, this study aimed to describe the T. vitticeps subcomplex.
T. vitticeps and T. melanocephala are sister species and share a phylogenetic relationship, several similar morphological characteristics, the same composition of constitutive heterochromatin (Xs CG-rich and Y AT-rich), the same karyotype (2n = 20A + X1X2X3Y), and the same meiotic behaviour during spermatogenesis. Based on karyosystematics, for example, the T. vitticeps subcomplex may differ from all of the other subcomplexes from South America, as well as from the Rhodniini tribe and the genus Panstrongylus. We argue that the case of agmatoploidy involving the X chromosome was responsible for the karyotype divergence of this subcomplex in relation to the other South America subcomplexes.
Based on the phenotypic characteristics (morphology) and genotypes (cytogenetics and molecular features), we propose the creation of the monophyletic T. vitticeps subcomplex, which we believe is distinct from all other subcomplexes from South America.
KeywordsTriatoma vitticeps Triatoma melanocephala Triatomini tribe
Chagas disease is a potentially life-threatening illness caused by the protozoan Trypanosoma cruzi (Chagas, 1909), which is most commonly distributed in endemic areas of 21 Latin American countries. The disease is most frequently transmitted to humans through contact with faeces of triatomines. It is estimated that about 6 million to 7 million people are infected worldwide, most of whom reside in Latin America .
Chagas disease vectors belong to the order Hemiptera, the suborder Heteroptera, the family Reduviidae and, the subfamily Triatominae . This subfamily is composed of 151 species distributed across 18 genera and five tribes [2–5], and all species (nymphs and adults of both sexes) are considered to be potential vectors of T. cruzi.
Based mainly on morphological and geographical distribution, these vectors have been grouped into complexes and subcomplexes [6–11]. Although these groupings are not formally recognized as taxonomic ranks and, thus do not necessarily represent natural groups, Justi et al.  propose that they are likely to be monophyletic: once the relationships between vector species are known, information about a species may be reliably extrapolated to other closely related species .
The species of the Triatomini tribe have been grouped into three groups, eight complexes, and eight subcomplexes ; the main species groups are Triatoma rubrofasciata (present mainly in North America and the Old World) and T. infestans (present in South America). South American triatomines were initially grouped into the T. infestans complex and the T. brasiliensis, T. infestans, T. matogrossensis, T. maculata, T. rubrovaria, and T. sordida subcomplexes . However, several studies have demonstrated that the T. brasiliensis [12, 14–16], T. matogrossensis [17–19], T. rubrovaria [16, 17], and T. sordida subcomplexes [16, 19] do not form monophyletic groups, and reorganizations of the subcomplexes have been suggested [14–16, 20].
As part of these suggested reorganisations, Alevi et al.  and Gardim et al.  suggest that T. vitticeps (Stal, 1859), T. melanocephala Neiva and Pinto, 1923, and T. tibiamaculata (Pinto, 1926) should be excluded from the T. brasiliensis subcomplex. In some studies, it has been argued that these species lack a subcomplex [21, 22]. However, phylogenetic analyses detected a relationship between T. tibiamaculata and Panstrongyus megistus (Burmeister, 1835), which have been found to be sister species [12, 16, 23]. Recently, Justi et al.  argued that T. tibamaculata is a member of the clade megistus, along with other species of Panstrongylus [+ Nesotriatoma bruneri (Usinger 1944)].
Meanwhile, T. vitticeps and T. melanocephala were not grouped into any new subcomplexes, since these species do not share phenotypic and genotypic characteristics with the triatomine subcomplexes from South America [14, 15, 24–26]. However, these species exhibit several similar characteristics, including morphological , cytogenetic , and phylogenetic  features, similarities which support the creation of a new subcomplex. Thus, this study aimed to describe, for the first time, the T. vitticeps subcomplex, highlighting the main phenotypic and genotypic characteristics that support the grouping of these species and how this subcomplex is distinct from the others present in South America.
Ten adult males of each species of the new subcomplex were used for cytogenomic analysis. The species considered herein were T. vitticeps [geographic origin: Guarapari, Espírito Santo, Brazil (Coordinates: 20°39'01.41478"S, 40°30'25.29000"W)] and T. melanocephala [geographic origin: Bom Jesus da Serra, Bahia, Brazil (Coordinates: 14°22'04.46160"S, 40°30'52.55281"W), Jequié, Bahia, Brazil (Coordinates: 13°51'03.75834"S, 40°04'52.22281"W), and Poções, Bahia, Brazil (Coordinates: 14°31'01.94880"S, 40°22'43.37040"W)]. The specimens were provided 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 were torn apart, crushed, and fixed on slides in liquid nitrogen. The cytogenomic technique of CMA3/DAPI banding was then applied , with the modifications offered by Severi-Aguiar et al.  for differentiating the regions of heterochromatin rich in AT and CG. The biological material was analysed using an Olympus BX-FLA fluorescence microscope.
Results and discussion
Cytotaxonomy and karyosystematics are important tools for determining the taxonomy of triatomines [14, 15, 31, 32]. For example, the karyotype analysis of the species within this T. vitticeps subcomplex is what distinguishes these species from all of the other South American subcomplexes, which have 2n = 22 (20A + XY) chromosomes [33, 34], from all of the species of the Rhodniini tribe (2n = 22) , and from the species of the genus Panstrongylus (2n = 21 or 23) .
Based on the phenotypic characteristics (morphology) and genotypes (cytogenetics and molecular features) that define these species, we propose the creation of the monophyletic T. vitticeps subcomplex, one which believe is distinct from all other subcomplexes from South America.
We appreciate the Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) (process number 2013/19764-0), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, Brazil) and Programa de Apoio ao Desenvolvimento Científico da Faculdade de Ciências Farmacêuticas da UNESP (PADC) for financial support.
The study was supported by Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) (process number 2013/19764-0), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, Brazil) and Programa de Apoio ao Desenvolvimento Científico da Faculdade de Ciências Farmacêuticas da UNESP (PADC).
Availability of data and materials
The data supporting the conclusions of this article are included within the article.
KCCA, JO, MTVAO and JAR contributed to the study design. JAR contributed to specimens analysed. KCCA and JO performed the experimental work and analysed the data. KCCA wrote the manuscript. All authors read and approved the final manuscript.
The authors declare that they have no competing interests.
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- World Health Organization. Chagas disease (American trypanosomiasis). Week Epidemiol Rec. 2015;90:33–44.Google Scholar
- Galvão C. Vetores da doença de chagas no Brasil. Curitiba: Sociedade Brasileira de Zoologia; 2014. p. 289p.View ArticleGoogle Scholar
- Mendonça VJ, Alevi KCC, Pinotti H, Gurgel-Gonçalves R, Pita S, Guerra AL, et al. Revalidation of Triatoma bahiensis Sherlock & Serafim, 1967 (Hemiptera: Reduviidae) and phylogeny of the T. brasiliensis species complex. Zootaxa. 2016;4107:239–54.View ArticlePubMedGoogle Scholar
- Alevi KCC, Reis YV, Guerra AL, Imperador CHL, Banho CA, Moreira FFF, et al. Would Nesotriatoma bruneri Usinger, 1944 be a valid species? Zootaxa. 2016;4103:396–400.View ArticlePubMedGoogle Scholar
- Souza ES, Atzinger NCBV, Furtado MB, Oliveira J, Damieli JN, Vendramini DP, et al. Description of Rhodnius marabaensis sp. n. (Hemiptera: Reduviidae: Triatominae) from Pará State, Brazil. ZooKeys. 2016;621:45–62.View ArticleGoogle Scholar
- Usinger RL, Wygodzinsky P, Ryckman RE. The biosystematics of Triatominae. Annu Rev Entomol. 1966;11:309–30.View ArticlePubMedGoogle Scholar
- Lucena DT. Estudos sobre a doença de Chagas no Brasil. Rev Bras Malariol Doenças Trop. 1970;22:3–173.PubMedGoogle Scholar
- Lent H, Wygodzinsky P. Revision of the Triatominae (Hemiptera, Reduviidae), and their significance as vectors of Chagas’s disease. Bull Am Mus Nat Hist. 1979;163:123–520.Google Scholar
- Carcavallo RU, Jurberg J, Lent H, Noireau F, Galvão C. Phylogeny of the Triatominae (Hemiptera: Reduviidae). Proposals for taxonomic arrangements. Entomol Vect. 2000;7:01–99.Google Scholar
- Dujardin JP, Schofield CJ, Panzera F. Los vectores de la enfermedad de Chagas. Bruxelles: Académie Royale des Sciences D’Outre-Mer; 2002. p. 189p.Google Scholar
- Schofield CJ, Galvão C. Classification, evolution, and species groups within the Triatominae. Acta Trop. 2009;110:88–100.View ArticlePubMedGoogle Scholar
- Justi SA, Russo CAM, Mallet JRS, Obara MT, Galvão C. Molecular phylogeny of Triatomini (Hemiptera: Reduviidae: Triatominae). Parasit Vectors. 2014;7:149.View ArticlePubMedPubMed CentralGoogle Scholar
- Schaefer CW. Triatominae (Hemiptera: Reduviidae): systematic questions and some others. Neotrop Entomol. 2003;32:1–10.View ArticleGoogle Scholar
- Alevi KCC, Mendonça PP, Pereira NP, Rosa JA, Azeredo-Oliveira MTV. Karyotype of Triatoma melanocephala Neiva & Pinto (1923). Does this species fit in the Brasiliensis subcomplex? Infect Genet Evol. 2012;12:1652–3.View ArticlePubMedGoogle Scholar
- Alevi KCC, Rosa JA, Azeredo-Oliveira MTV. Cytotaxonomy of the Brasiliensis subcomplex and the Triatoma brasiliensis complex (Hemiptera: Reduviidae: Triatominae). Zootaxa. 2014;3838:583–9.View ArticlePubMedGoogle Scholar
- Gardim S, Almeida CE, Takiya DM, Oliveira J, Araújo RF, Cicarelli RMB, et al. 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. 2014;23:74–9.View ArticlePubMedGoogle Scholar
- Alevi KCC, Oliveira J, Moreira FF, Jurberg J, Rosa J, Azeredo-Oliveira MTV. Chromosomal characteristics and distribution of constitutive heterochromatin in the Matogrossensis and Rubrovaria subcomplexes. Infect Genet Evol. 2015;33:158–62.View ArticlePubMedGoogle Scholar
- Gardim S, Rocha CS, Almeida CE, Takiya DM, Silva MTA, Ambrósio DL, et al. Evolutionary relationships of the Triatoma matogrossensis subcomplex, the endemic Triatoma in central-western Brazil, based on mitochondrial DNA sequences. Am J Trop Med Hyg. 2013;89:766–74.View ArticlePubMedPubMed CentralGoogle Scholar
- Justi SA, Galvão C, Schrago CG. Geological changes of the Americas and their Influence on the diversification of the Neotropical kissing bugs (Hemiptera: Reduviidae: Triatominae). PLoS Negl Trop Dis. 2016;10:e0004527.View ArticlePubMedPubMed CentralGoogle Scholar
- Pita S, Lorite P, Nattero J, Galvão C, Alevi KCC, Teves SC, et al. New arrangements on several species subcomplexes of Triatoma genus based on the chromosomal position of ribosomal genes (Hemiptera: Triatominae). Infect Genet Evol. 2016;43:225–31.View ArticlePubMedGoogle Scholar
- Panzera Y, Pita S, Ferreiro MJ, Ferrandis I, Lages C, Pérez R, et al. High dynamics of rDNA cluster location in kissing bug holocentric chromosomes (Triatominae, Heteroptera). Cytogenet Genome Res. 2012;138:56–67.View ArticlePubMedGoogle Scholar
- Bardella VB, Pita S, Vanzela ALL, Galvão C, Panzera F. Heterochromatin base pair composition and diversification in holocentric chromosomes of kissing bugs (Hemiptera, Reduviidae). Mem Inst Oswaldo Cruz. 2016;111:614–24.View ArticlePubMedPubMed CentralGoogle Scholar
- Hypsa V, Tietz D, Zrzavy J, Rego RO, Galvão C, Jurberg J. Phylogeny and biogeography of Triatominae (Hemiptera, Reduviidae): molecular evidence of a New World origin of the asiatic clade. Mol Phylogenet Evol. 2002;23:447–57.View ArticlePubMedGoogle Scholar
- Schreiber G, Pellegrino J. Eteropicnosi di autosomi come possible meccanismo di speciazione. Sci Genet. 1950;3:215–26.PubMedGoogle Scholar
- Rosa JA, Mendonça VJ, Rocha CS, Gardim S, Cilense N. Characterization of the external female genitalia of six species of Triatominae (Hemiptera: Reduviidade) by scanning electron microscopy. Mem Inst Oswaldo Cruz. 2010;105:286–92.View ArticlePubMedGoogle Scholar
- Oliveira J, Mendonça VJ, Araújo RF, Nascimento EG, Rosa JA. Biological, morphological and morphometric studies of Triatoma melanocephala Neiva & Pinto, 1923 (Hemiptera: Reduviidae: Triatominae). Zootaxa. 2015;4012:514–24.View ArticlePubMedGoogle Scholar
- Sherlock ÍA, Guitton N. Fauna triatominae do estado da Bahia [Triatominae fauna of the State of Bahia], Brasil: IV. Triatoma melanocephala Neiva & Pinto, 1923. Mem Inst Oswaldo Cruz. 1980;75:23–31.View ArticlePubMedGoogle Scholar
- Schimid M. Chromosoma banding an amphibia IV. Differentiation of GC and AT rich regions in Anura. Chromosoma. 1980;77:83–103.View ArticleGoogle Scholar
- Severi-Aguiar GD, Lourenço LB, Bicudo HE, Azeredo-Oliveira MTV. Meiosis aspects and nucleolar activity in Triatoma vitticeps (Triatominae, Heteroptera). Genetica. 2006;126:141–51.View ArticlePubMedGoogle Scholar
- Alevi KCC, Mendonça PP, Pereira NP, Rosa JA, Azeredo-Oliveira MTV. Spermatogenesis in Triatoma melanocephala (Hemiptera: Triatominae). Gen Mol Res. 2013;12:4955.View ArticleGoogle Scholar
- Alevi KCC, Borsatto KC, Moreira FFF, Jurberg J, Azeredo-Oliveira MTV. Karyosystematics of Triatoma rubrofasciata (De Geer, 1773) (Hemiptera: Reduviidae: Triatominae). Zootaxa. 2015;3994:433–8.View ArticlePubMedGoogle Scholar
- Alevi KCC, Nascimento JGO, Moreira FFF, Jurberg J, Azeredo-Oliveira MTV. Cytogenetic Characterisation of Triatoma rubrofasciata (De Geer) (Hemiptera, Triatominae) spermatocytes and its cytotaxonomic application. Afr Entomol. 2016;24:257–60.View ArticleGoogle Scholar
- Alevi KCC, Rosa JA, Azeredo-Oliveira MTV. Mini review: karyotypic survey in Triatominae subfamily (Hemiptera, Heteroptera). Entomol Ornithol Herpetol. 2013;2:106.View ArticleGoogle Scholar
- Alevi KCC, Moreira FFF, Jurberg J, Azeredo-Oliveira MTV. Description of the diploid chromosome set of Triatoma pintodiasi (Hemiptera, Triatominae). Gen Mol Res. 2016;25:15.Google Scholar
- Alevi KCC, Ravazi A, Mendonça VJ, Rosa JA, Azeredo-Oliveira MTV. Karyotype of Rhodnius montenegrensis (Hemiptera, Triatominae). Gen Mol Res. 2015;14:222–6.View ArticleGoogle Scholar
- Ueshima N. Cytotaxonomy of the Triatominae (Reduviidae, Hemiptera). Chromosoma. 1966;18:97–122.View ArticleGoogle Scholar
- Ueshima N. Hemiptera II: Heteroptera. In: John B, editor. Animal Cytogenetics. Berlim: Gebrüder Borntraeger; 1979. 117 pp.Google Scholar
- Panzera F, Scvortzoff E, Pérez R, Panzera Y, Hornos S, Cestau R, et al. Cytogenetics of Triatomines. In: Carcavallo RU, Galíndez-Girón I, Jurberg J, Lent H, editors. Atlas of Chagas disease vectors in the Americas. Rio de Janeiro: Editora Fiocruz; 1998. p. 621–64.Google Scholar