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    Constitutive heterochromatin pattern and composition of AT-rich and CG-rich DNA observed in Triatoma sordida Brazilians. (A) Early meiotic prophase prepared with C-banding. Note the several heterochromatic bodies dispersed in the nucleus, being one of them formed by the associated sex chromosomes surrounded by some autosomal heterochromatic regions (*). (B) Meiotic metaphase prepared with C-banding. Note that the most autosomal pairs present a C-heterochromatic block in one chromosomal end, Y sex chromosome is fully heterochromatin and X chromosome may present a small C-block. (C and D) Early meiotic prophase prepared with CMA3/DAPI banding. (C) Note the several bodies CG-rich dispersed in the nucleus, being one of them formed by the associated X sex chromosome surrounded by some autosomal (*). (D) Note that only the Y sex chromosome is AT-rich. X: X sex chromosome Y: Y sex chromosome. Bar = 10 μm.

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Genetic Structure of Brazilian Populations of Triatoma sordida (Stål, 1859) (Hemiptera, Triatominae) by Means of Chromosomal Markers

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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” (IBILCE/UNESP), São José do Rio Preto, Brazil;
  • | 2 Laboratório de Parasitologia, Departamento de Ciências Biológicas, Faculdade de Ciências Farmacêuticas, Universidade Estadual Paulista “Júlio de Mesquita Filho” (FCFAR/UNESP), Araraquara, Brazil;
  • | 3 Departamento de Parasitologia e Microbiologia, Centro de Ciências da Saúde, Universidade Federal do Piauí (UFPI), Teresina, Brazil;
  • | 4 Laboratório de Biodiversidade Entomológica, Instituto Oswaldo Cruz, Rio de Janeiro, Brazil

Triatoma sordida is among the main Brazilian species considered as Chagas disease vectors. The genetic studies are directed mainly to phylogenetic questions because this species possibly have suffered cryptic speciation. Furthermore, there are few studies that analyzed the structure and genetic variability of specimens from Brazil and that showed low genetic diversity and strong genetic structuring of the population samples. Therefore, because of great epidemiological importance of T. sordida and mainly the restriction of genetic characterization of this vector only for populations of Minas Gerais state, this article performs a genetic analysis of the T. sordida from seven different Brazilian states (representing different biomes), by means of cytogenetic markers. All analyzed specimens presents the same cytogenetic characteristics: early meiotic prophase with several heterochromatic bodies dispersed in the nucleus (CG-rich), being one of them formed by the associated sex chromosomes surrounded by some autosomal heterochromatic regions, meiotic metaphase with most autosomal pairs exhibiting a C-heterochromatic block in one chromosomal end (CG-rich), Y sex chromosome fully heterochromatin (AT-rich), and X chromosome may present a small C-block (CG-rich). These results are important because the chromosomal markers enable to confirm and expand the low genetic diversity for all Brazilian states occupied by T. sordida, suggesting that all Brazilian populations were originated from a small ancestral population and possibly dispersed to other biomes by founder effect. In addition, we suggest that T. sordida from Brazil are not suffering cryptic speciation and we confirm the classification of all Brazilian examples as T. sordida sensu stricto.

INTRODUCTION

Chagas disease is a neglected disease considered as a potentially life-threatening illness caused by the protozoan Trypanosoma cruzi (Chagas, 1909), distributed mainly in endemic areas of 21 Latin American countries, where it is mostly vector-borne transmitted to humans by contact with feces of triatomines.1 It is estimated that about eight million people are infected worldwide, mostly in Latin America where Chagas disease is endemic.1

Presently, there are 154 species of triatomines, distributed in 18 genera and five tribes, being all species considered as potential vector of Chagas disease.24 In Brazil, there are 68 species distributed throughout the country’s 27 states, and 64% of them are endemic species.58 Triatoma infestans (Klug, 1834), Triatoma brasiliensis (Neiva, 1911), Triatoma pseudomaculata (Corrêa and Espínola, 1964), Triatoma sordida (Stål, 1859), and Panstrongylus megistus (Burmeister, 1835) are the main species of triatomines related to the domestic transmission of Chagas disease.5,9

Triatoma sordida is distributed in 14 Brazilian states (Acre, Bahia, Goiás, Mato Grosso, Mato Grosso do Sul, Maranhão, Minas Gerais, Paraná, Pernambuco, Piauí, Rio Grande do Sul, Santa Catarina, São Paulo, and Tocantins)5,10,11 and is considered the species with the highest frequency of domiciliary captures in Brazil.5 Although T. sordida exhibits endemism centered in the Cerrado, this species is also prevalent in Bahia and the states of the Southeast and Midwest regions of Brazil, including transition areas to the Amazon,5,11 occupying thus other biomes besides the Cerrado: Pantanal, Atlantic forest, and Caatinga.10

The epidemiological importance of T. sordida is increasing because of its tendency to invade houses, particularly in areas where T. infestans has been controlled,1214 being thus considered as “semi-domestic.”15 The anthropic activities have influence in the richness of this species because the areas of higher occurrence of T. sordida are the ones related to the agricultural activities in the past, which could explain its presence in areas that suffered ecologic impact due to significant loss of vegetation.16 Furthermore, T. sordida also is associated with the reinfestation of dwellings treated with insecticides.17

Although T. sordida exhibits wide geographic distribution in Brazil,5,10,11 genetic studies are directed mainly to phylogenetic questions1822 because this species is also found in Argentina, Bolivia, Paraguay, and Uruguay5 and possibly has suffered cryptic speciation.1921 Furthermore, there are few studies that analyzed the genetic structure and genetic variability of specimens from Minas Gerais, Brazil, that showed low genetic diversity and strong genetic structuring of the population samples.22,23

Recently, Pessoa et al.23 related low genetic diversity and strong genetic structuring of the population samples of T. sordida with five possible factors: possible geographical isolation due to an obstacle to Triatominae flow between neighboring localities; focal distribution of insects in small colonies usually comprised a few individuals, thereby limiting gene flow between them; the low dispersal capacity of T. sordida; the long Triatominae life cycle, which ensures that contributions from young adults able to reproduce (and consequently exchange genetic material) occurs over long intervals that differ among triatomine species; and continuous pressure from insecticides used since the 1950s to triatomines control.

As Chagas disease has no cure and treatment with benznidazole and nifurtimox are more effective in the acute phase of the disease (which is often asymptomatic),1 vector control is the most effective method of preventing this neglected disease1 and all knowledge about these hematophagous insects is important and can generate subsidies to assist the vector control programs. Thus, because of great epidemiological importance of T. sordida in Brazil and mainly the restriction of genetic characterization of this vector only for populations of Minas Gerais state, this article performs a genetic analysis of the T. sordida from seven different Brazilian states representing different biomes, by means of cytogenetic markers.

MATERIAL AND METHODS

Material.

One hundred adult males coming from the municipalities described in Table 1 (at a minimum three copies of each locality) were used in the study (males were used because spermatogenesis is continued in adulthood, allowing the visualization of chromatin and chromosomes). The triatomines were provided by the insectariums of Faculdade de Ciências Farmacêuticas, Universidade Estadual Paulista “Júlio de Mesquita Filho”, Araraquara, São Paulo, Brazil, of Instituto Oswaldo Cruz (IOC/FIOCRUZ), Rio de Janeiro, Rio de Janeiro, Brazil, and of Centro de Pesquisas René Rachou (CPqRR/FIOCRUZ), Belo Horizonte, Minas Gerais, Brazil. The characterization of biomes was performed according to the Brazilian Institute of Geography and Statistics.24

Table 1

Geographical origin of the specimens used in the study and their corresponding biomes

Triatoma sordida collection sites
Brazilian statesMunicipalitiesBrazilian biomes
Mato GrossoRondonópolisCerrado
GoiásPosseCerrado
São Luiz dos Montes BelosCerrado
Minas GeraisMatias Cardoso and Monte AzulCerrado and Caatinga
ItingaMata Atlântica
BahiaSeabra and MacaúbasCaatinga
Rio Grande do SulSão Francisco de AssisPampa and Mata Atlântica
São PauloMirassol and GuaíraMata Atlântica and Cerrado
São PauloMata Atlântica
Mato Grosso do SulRio Verde de Mato GrossoCerrado and Pantanal
CorumbáPantanal
BrasilândiaMata Atlântica and Cerrado

Chromosome preparation.

For cytological preparations, testes were removed from adult insects alive, fixed in an ethanol–acetic acid (3:1), and stored at −20°C. Squashes were made in a 50% acetic acid drop, coverslips were removed after freezing in liquid nitrogen, and the slides were air-dried and then stored at 4°C.

Chromomycin A3 (CMA3)/4,6-diamidino-2-phenylindole (DAPI) banding.

C-banding was performed according to Sumner 25 for the characterization of constitutive heterochromatin and CMA3/DAPI banding was performed according to Schimid,26 with modifications according to Severi-Aguiar et al.,27 for differentiating the regions of heterochromatin rich in AT (DAPI+) and CG (CMA3+).

Analysis of biological material.

At least 50 cells in prophase (for analysis of the chromatin) and 50 in metaphase (for analysis of the chromosomes) of T. sordida from each location were analyzed. The analysis of C-banding preparations was made 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 GmbH) and of CMA3/DAPI banding preparation was analyzed using a fluorescence microscopy Zeiss-Axioskop and Olympus BX-FLA.

RESULTS

All analyzed specimens, regardless the locality (Table 1), present the same cytogenetic characteristic: C-banding: during early meiotic prophase, several heterochromatic bodies are observed, being one of them formed by the associated sex chromosomes surrounded by some autosomal heterochromatic regions (Figure 1A, *); Furthermore, during the meiotic metaphase, the most autosomal pairs present a C-heterochromatic block in one chromosomal end and X chromosome may present a small C-block (Figure 1B) (Y sex chromosome is heterochromatin in all species of triatomine); CMA3/DAPI banding: several bodies CG-rich dispersed in the nucleus of early meiotic prophase, being one of them formed by the association of the X sex chromosome surrounded by some autosomal (Figure 1C, *) and Y sex chromosome AT-rich DNA (Figure 1D).

Figure 1.
Figure 1.

Constitutive heterochromatin pattern and composition of AT-rich and CG-rich DNA observed in Triatoma sordida Brazilians. (A) Early meiotic prophase prepared with C-banding. Note the several heterochromatic bodies dispersed in the nucleus, being one of them formed by the associated sex chromosomes surrounded by some autosomal heterochromatic regions (*). (B) Meiotic metaphase prepared with C-banding. Note that the most autosomal pairs present a C-heterochromatic block in one chromosomal end, Y sex chromosome is fully heterochromatin and X chromosome may present a small C-block. (C and D) Early meiotic prophase prepared with CMA3/DAPI banding. (C) Note the several bodies CG-rich dispersed in the nucleus, being one of them formed by the associated X sex chromosome surrounded by some autosomal (*). (D) Note that only the Y sex chromosome is AT-rich. X: X sex chromosome Y: Y sex chromosome. Bar = 10 μm.

Citation: The American Journal of Tropical Medicine and Hygiene 100, 4; 10.4269/ajtmh.18-0336

DISCUSSION

Cytogenetic markers have been used because initially Panzera et al.19 differentiated T. sordida from Brazil and Argentina by the pattern of heterochromatin. Recently, Panzera et al.21 and Bardella et al.28 recognized three chromosomal taxa for T. sordida (T. sordida sensu stricto, T. sordida Argentina and T. sordida La Paz). Panzera et al.21 analyzed Brazilian representatives from Minas Gerais, Piauí, and Mato Grosso with C-banding and observed the same results that we observed for all analyzed specimens. Beyond that, we characterized the composition of DNA rich in AT and CG in chromatin of these vectors, and all the specimens of T. sordida analyzed showed the same disposition in chromatin and chromosomes.

These results are important because the chromosomal markers enable confirming and expanding the results described by Pessoa et al.23 and Monteiro et al.22 for all Brazilian states occupied by T. sordida. In addition, the low genetic diversity can also be confirmed by the low genetic distance observed between T. sordida from different Brazilian states [e.g., 0.011 among populations of Mato Grosso (Pocotó) and Mato Grosso do Sul (Pantanal) with the cytochrome oxidase I gene; 0.007 among populations of Mato Grosso (Rondonópolis) and Mato Grosso do Sul (Pantanal) with cytochrome oxidase II gene; and 0.006 among populations from municipalities in the state of Mato Grosso (Rondonópolis and Pocotó), and 0.004 and 0.002 distance observed between Rondonópolis and Pantanal and Pocotó and Pantanal, respectively, both with the 16S r DNA gene]29 and by the low variability of the wing geometry of T. sordida observed recently among populations from Brazil.30

Some authors suggest that T. sordida probably have originated in the Brazilian Cerrado16,18,31 and as a consequence of deforestation and T. infestans control strategies, it has dispersed toward the south.13,14,32 Our results also suggest that all Brazilian populations originated from a small ancestral population (possibly in the Cerrado, as suggested previously) and dispersed to other biomes by the founder effect (possibly by active dispersal by flight33 or passive dispersion by nymphs associated with bird feathers34). However, because there are evidences that genetic diversity of T. infestans is reduced in areas treated with insecticides because of bottleneck events,35,36 we cannot also dismiss this hypothesis for T. sordida.

Noireau et al.20 reported for the first time the presence of cryptic speciation to T. sordida specimens from Bolivia. Monteiro et al.22 analyzed this phenomenon for four populations from Minas Gerais, Brazil, and found no cryptic speciation. Our results demonstrate that T. sordida Brazilians are not suffering cryptic speciation, because if this evolutionary event was taking place, the results with chromosomal markers would demonstrate differences, and were recently observed for specimens of Bolivia.21

Besides its importance for the genetic and evolutionary characterization of Brazilian T. sordida, cytogenetic analysis confirms that all triatomine present in Brazilian insectariums, initially classified as T. sordida by morphology, exhibit the same chromosome pattern characterized by Panzera et al.21 as T. sordida sensu stricto, assisting directly in the taxonomy of these vectors. In addition, for the first time, T. sordida specimens from several Brazilian biomes and mainly representing areas of peridomicile (Rondonópolis and Guaira chicken coops), intradomicile (Mirassol and Miranda’s houses), and wild (Corumbá, associated with bird nests) had their genetic diversity analyzed. The low genetic variability observed for T. sordida can be an important tool for the control of this species by the vector programs.

Thus, by means of the cytogenetic study of Brazilian T. sordida, it was observed that this vector species, although widely distributed in Brazil, has extremely low genetic diversity. Moreover, we confirm the classification of all Brazilian examples as T. sordida sensu stricto. Our results are important to direct further studies (such as phylogeography) and, especially, to assist in developing tools for the control of this vector species by vector control programs.

Acknowledgments:

This work was supported by the Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) (Processes number 2013/19764-0, 2014/07706-9, 2017/05015-7, agreement with CAPES and 2018/12039-2), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) - Finance Code 001.

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Author Notes

Address correspondence to Kaio Cesar Chaboli Alevi, Faculdade de Ciências Farmacêuticas, Universidade Estadual Paulista “Júlio de Mesquita Filho” (FCFAR/UNESP), Rod. Araraquara-Jaú km 1, Araraquara 14801-902, Brazil. E-mail: kaiochaboli@hotmail.com

Authors’ addresses: Fernanda Fernandez Madeira, Yago Visinho dos Reis, Isadora de Freitas Bittinelli, Luiza Maria Grzyb Delgado, and Maria Tercília Vilela de Azeredo-Oliveira, 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, Brazil, E-mails: fernanda.bio56@hotmail.com, yagoreis@outlook.com.br, Isadora_bittinelli@hotmail.com, luiza_grzyb.1998@hotmail.com, and tercilia@ibilce.unesp.br. Jader de Oliveira, João Aristeu da Rosa, and Kaio Cesar Chaboli Alevi, Laboratório de Parasitologia, Departamento de Ciências Biológicas, Faculdade de Ciências Farmacêuticas, Universidade Estadual Paulista “Júlio de Mesquita Filho”, Araraquara, Brazil, E-mails: jdr.oliveira@hotmail.com, joaoaristeu@gmail.com, and kaiochaboli@hotmail.com. Vagner José Mendonça, Departamento de Parasitologia e Microbiologia, Centro de Ciências da Saúde, Universidade Federal do Piauí, Teresina, Brazil, E-mail: vagjose@hotmail.com. Felipe Ferraz Figueiredo Moreira, Laboratório de Biodiversidade Entomológica, Instituto Oswaldo Cruz, Rio de Janeiro, Brazil, E-mail: felipento@hotmail.com.

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