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Coloration of the testicular peritoneal sheath as a synapomorphy of triatomines (Hemiptera, Reduviidae)

Coloração da bainha peritoneal testicular como uma sinapomorfia dos triatomíneos (Hemiptera, Reduviidae)

Abstracts

Recently, were described some morphological characteristics of 18 species of terrestrial hemipteran grouped in the Alydidae, Coreidae, Corimelaenidae, Lygaeidae, Rhopalidae, Scutelleridae, Tingidae and Reduviidae family that presented found variation in coloration of testicular peritoneal sheath (Reddish, Orange, Yellowish or Transparent). Thus, this study aims to analyzed the coloration of the peritoneal sheath in 44 species of triatomines grouped in nine different genera, with the aim of analyze whether the insects of the Triatominae subfamily also show variations in coloration. By means of analysis of the sheath was possible to observe that members of this subfamily have no interspecific differences, because all species have a transparent sheath. Thus, this paper describes the coloring of the peritoneal sheath in 44 species of the subfamily Triatominae and mainly suggests that the transparent color is one synapomorphy of this important group of insect vectors.

testicle; Heteroptera; Triatominae subfamily


Recentemente, foram descritas algumas características morfológicas de 18 espécies de hemípteros terrestres agrupados nas famílias Alydidae, Coreidae, Corimelaenidae, Lygaeidae, Rhopalidae, Scutelleridae, Tingidae e Reduviidae que apresentaram grandes variações na coloração da bainha peritonial testicular (avermelhada, alaranjada, amarelada ou transparente). Assim, este estudo teve como objetivo analisar a coloração da bainha peritoneal em 44 espécies de triatomíneos agrupadas em nove gêneros diferentes, com o intuito de analisar se os insetos da subfamília Triatominae também apresentam variações na coloração da bainha. Por meio da análise da bainha, foi possível observar que os membros desta subfamília não apresentaram diferenças interespecíficas, pois todas as espécies analisadas possuem bainha transparente. Assim, o presente trabalho descreve a coloração da bainha peritoneal em 44 espécies da subfamília Triatominae e, principalmente, sugere que a cor transparente é uma sinapomorfia deste importante grupo de insetos vetores.

testículo; Heteroptera; subfamília Triatominae


Introduction

Triatomines are hematophagous insects of medico-sanitary importance because they are considered as the main vector of Chagas disease in the human population. These vectors are included in the Hemiptera order, Heteroptera suborder, Reduviidae family and Triatominae subfamily (Lent & Wygodzinsky 1979LENT, H. & WYGODZINSKY, P. 1979. Revision of the Triatominae (Hemiptera: Reduviidae) and their significance as vector of Chagas’s disease. Bull. Am. Mus. Nat. Hist. 163:123-520.).

The knowledge of the biology of these vectors is of great importance to public health, because the main way to minimize the incidence of Chagas disease is by controlling populations (Dias & Schofield 1998DIAS, J.C.P & SCHOFIELD, C.J. 1998. Controle da transmissão transfusional da doença de Chagas na Iniciativa do Cone Sul. Rev. Soc. Bras. Med. Trop. 31:373-383., Alevi et al. 2012aALEVI, K.C.C., MENDONÇA, P.P., PEREIRA, N.P., ROSA, J.A. & AZEREDO-OLIVEIRA, M.T.V. 2012a. Karyotype of Triatoma melanocephala Neiva and Pinto (1923). Does this species fit in the Brasiliensis subcomplex? Infect. Gen. Evol. 12:1652-1653, 10.1016/j.meegid.2012.06.011.
https://doi.org/10.1016/j.meegid.2012.06...
). The reproductive biology of hemipterans was extensively studied by many aspects, such as anatomical (Barth 1956BARTH, R. 1956. Estudos anatômicos e histológicos sôbre a subfamília Triatominae (Heteroptera, Reduviidae). VI parte: Estudo comparativo sôbre a espermiocitogênese das espécies mais importantes. Mem. Inst. Oswaldo Cruz 54:599-616, 10.1590/S0074-02761956000300009.
https://doi.org/10.1590/S0074-0276195600...
, Freitas et al. 2008FREITAS, S.P.C., SANTOS-MALLET, J.E., COSTA, J., SOUZA, A.L.B., SERRÃO J.E. & GONÇALVES, T.C.M. 2008. A comparative study of testis follicles in species of Triatoma (Hemiptera, Triatominae). An. Biol. 58:227-233, 10.1163/157075608X328062.
https://doi.org/10.1163/157075608X328062...
), morphological (Gomes et al. 2013GOMES M.O., CASTANHOLE, M.M.U., SOUZA, H.V., MURAKAMI, A.S., FIRMINO, T.S.S., SARAN, P.S., BANHO, C.A., MONTEIRO, L.S., SILVA, J.C.P. & ITOYAMA, M.M. 2013. Morphological aspects of the testes of 18 species of terrestrial of Heteroptera from Northwestern São Paulo (Brazil). Biota Neotrop. 13:132-135., Rosa et al. 2014ROSA, J.A., MENDONÇA, V.J., GARDIM, S., DE CARVALHO DB, DE OLIVEIRA J., NASCIMENTO, JD, PINOTTI, H, PINTO, MC, CILENSE, M, GLAVÃO, C & BARATA, J.M. 2014. Study of the external female genitalia of 14 Rhodnius species (Hemiptera, Reduviidae, Triatominae) using scanning electron microscopy. Paras. Vect. 7:17, 10.1186/1756-3305-7-17.
https://doi.org/10.1186/1756-3305-7-17...
), structural (Freitas et al. 2010FREITAS, S.P.C., GONÇALVES, T.C.M., SERRÃO, J.E., COSTA, J. & SANTOS-MALLET, J.R. 2010. Male reproductive system structure and accessory glands ultrastructure of two species of Triatoma (Hemiptera, Reduviidae, Triatominae). Micron 41:518-525, 10.1016/j.micron.2010.01.008.
https://doi.org/10.1016/j.micron.2010.01...
, Silistino-Souza et al. 2012SILISTINO-SOUZA, R., PERUQUETTI, R.L., TABOGA, S.R. & AZEREDO-OLIVEIRA, M.T.V. 2012. Chromatoid body: Remnants of nucleolar proteins during spermatogenesis in triatomine (Heteroptera, Triatominae). Micron 43:954-960, 10.1016/j.micron.2012.03.017.
https://doi.org/10.1016/j.micron.2012.03...
), ultrastructural (Morielle-Souza et al. 2010MORIELLE-SOUZA A., TABOGA, S.R. & AZEREDO-OLIVEIRA, M.T.V. 2010. Ultrastructural analysis of the nucleolar aspects at spermiogenesis in triatomines (Heteroptera, Triatominae). Micron 41:791-796, 10.1016/j.micron.2010.05.009.
https://doi.org/10.1016/j.micron.2010.05...
, Freitas et al. 2010FREITAS, S.P.C., GONÇALVES, T.C.M., SERRÃO, J.E., COSTA, J. & SANTOS-MALLET, J.R. 2010. Male reproductive system structure and accessory glands ultrastructure of two species of Triatoma (Hemiptera, Reduviidae, Triatominae). Micron 41:518-525, 10.1016/j.micron.2010.01.008.
https://doi.org/10.1016/j.micron.2010.01...
, Silistino-Souza et al. 2012SILISTINO-SOUZA, R., PERUQUETTI, R.L., TABOGA, S.R. & AZEREDO-OLIVEIRA, M.T.V. 2012. Chromatoid body: Remnants of nucleolar proteins during spermatogenesis in triatomine (Heteroptera, Triatominae). Micron 43:954-960, 10.1016/j.micron.2012.03.017.
https://doi.org/10.1016/j.micron.2012.03...
) and cytogenetic (Alevi et al. 2012aALEVI, K.C.C., MENDONÇA, P.P., PEREIRA, N.P., ROSA, J.A. & AZEREDO-OLIVEIRA, M.T.V. 2012a. Karyotype of Triatoma melanocephala Neiva and Pinto (1923). Does this species fit in the Brasiliensis subcomplex? Infect. Gen. Evol. 12:1652-1653, 10.1016/j.meegid.2012.06.011.
https://doi.org/10.1016/j.meegid.2012.06...
, bALEVI, K.C.C., MENDONÇA, P.P., SUCCI, M., PEREIRA, N.P., ROSA, J.A. & AZEREDO-OLIVEIRA, M.T.V. 2012b. Karyotype and spermatogenesis in Triatoma lenti (Hemiptera, Triatominae), a potentical Chagas vector. Gen. Mol. Res. 11:4278-4284, 10.4238/2012.December.17.3.
https://doi.org/10.4238/2012.December.17...
, 2013aALEVI, K.C.C., MENDONÇA, P.P., PEREIRA, N.P, GUERRA, A.L, FACINA, C.H,ROSA, J.A. & AZEREDO-OLIVEIRA, M.T.V. 2013a. Distribution of constitutive heterochromatin in two species of triatomines: Triatoma lenti Sherlock and Serafim (1967) and Triatoma sherlocki Papa, Jurberg, Carcavallo, Cerqueira & Barata (2002). Infect. Gen. Evol. 13:301-303, 10.1016/j.meegid.2012.11.011.
https://doi.org/10.1016/j.meegid.2012.11...
, bALEVI, K.C.C., MENDONÇA, P.P., PEREIRA, N.P., FERNANDES, A.L.V.Z., ROSA, J.A., AZEREDO-OLIVEIRA, M.T.V. 2013b. Analysis of spermiogenesis like a tool in the study of the triatomines of the Brasiliensis subcomplex. C. R. Biologies. 336:46-50, 10.1016/j.crvi.2013.01.005.
https://doi.org/10.1016/j.crvi.2013.01.0...
, cALEVI, K.C.C., MENDONÇA, P.P., PEREIRA, N.P., ROSA, J.A & AZEREDO-OLIVEIRA, M.T.V. 2013c. Heteropyknotic filament in spermatids of Triatoma melanocephala and T. vitticeps (Hemiptera, Triatominae). Inv. Rep. Dev. 58:9-12, 10.1080/07924259.2013.793623.
https://doi.org/10.1080/07924259.2013.79...
, dALEVI, K.C.C., MENDONÇA, P.P., PEREIRA, N.P., ROSA, J.A & AZEREDO-OLIVEIRA, M.T.V. 2013d. Spermatogenesis in Triatoma melanocephala (Hemiptera, Triatominae). Gen. Mol.Res. 12:4944-4947, 10.4238/2013.October.24.5.
https://doi.org/10.4238/2013.October.24....
, 2014aALEVI, K.C.C., ROSA, J.A & AZEREDO-OLIVEIRA, M.T.V. 2014a. Spermatogenesis in Triatoma melanica Neiva and Lent, 1941 (Hemiptera, Triatominae) J. Vec. Ecol. 39:231-233, 10.1111/j.1948-7134.2014.12094.x.
https://doi.org/10.1111/j.1948-7134.2014...
, bALEVI, K.C.C., MENDONÇA, P.P., PEREIRA, N.P., ROSA, J.A & AZEREDO-OLIVEIRA, M.T.V. 2014b. Is there post-meiotic transcriptional activity during hemiperan spermiogenesis? Inv. Rep. Dev. 58:193-198, 10.1080/07924259.2014.889767.
https://doi.org/10.1080/07924259.2014.88...
).

Recently, Gomes et al. (2013)GOMES M.O., CASTANHOLE, M.M.U., SOUZA, H.V., MURAKAMI, A.S., FIRMINO, T.S.S., SARAN, P.S., BANHO, C.A., MONTEIRO, L.S., SILVA, J.C.P. & ITOYAMA, M.M. 2013. Morphological aspects of the testes of 18 species of terrestrial of Heteroptera from Northwestern São Paulo (Brazil). Biota Neotrop. 13:132-135. described some morphological traits of 18 species of terrestrial hemipteran grouped in the Alydidae, Coreidae, Corimelaenidae, Lygaeidae, Rhopalidae, Scutelleridae, Tingidae and Reduviidae family. Among the characteristics, the color of the peritoneal sheath covering the seminiferous tubules was analyzed. The authors found variation in coloration of sheath (Reddish, Orange, Yellowish or Transparent). Thus, this study aims to analyze the peritoneal sheath in 44 species of triatomines grouped in nine different genera (Table 1), with the aim of analyze whether the insects of the Triatominae subfamily also show variations in coloration.

Table 1
Genus and species of Triatominae who had the peritoneal sheath analyzed.

Material and Methods

Exemplars males of 44 species (Table 1) were provided by “Triatominae Insectarium” within the Department of Biological Sciences, in the College of Pharmaceutical Sciences, at Sao Paulo State University’s Araraquara campus, Brazil (FCFAR/UNESP). The testicles were removed and photographed according to the methodology of Gomes et al. (2013)GOMES M.O., CASTANHOLE, M.M.U., SOUZA, H.V., MURAKAMI, A.S., FIRMINO, T.S.S., SARAN, P.S., BANHO, C.A., MONTEIRO, L.S., SILVA, J.C.P. & ITOYAMA, M.M. 2013. Morphological aspects of the testes of 18 species of terrestrial of Heteroptera from Northwestern São Paulo (Brazil). Biota Neotrop. 13:132-135..

Results and Discussion

The analysis of the peritoneal sheath of 44 species possible to observe that members of Triatominae subfamily have no interspecific differences, as described by Gomes et al (2013)GOMES M.O., CASTANHOLE, M.M.U., SOUZA, H.V., MURAKAMI, A.S., FIRMINO, T.S.S., SARAN, P.S., BANHO, C.A., MONTEIRO, L.S., SILVA, J.C.P. & ITOYAMA, M.M. 2013. Morphological aspects of the testes of 18 species of terrestrial of Heteroptera from Northwestern São Paulo (Brazil). Biota Neotrop. 13:132-135. for phytophagous hemipterans, because all species have a transparent sheath. Like all species of nine genera analyzed show the same coloring, we represent with image the testicle of one species of each genus (Figures 1 and 2).

Figure 1
Peritoneal sheath of different genus of the subfamily Triatominae analyzed. Note that in all genus the sheath is transparent. (a) T. infestans. (b) M. pallidipennis. (c) P. megistus. (d) D. maximus. Bar: 10 mm.
Figure 2
Peritoneal sheath of different genus of the subfamily Triatominae analyzed. Note that in all genus the sheath is transparent. (a) M. spinolai. (b) E. cuspidatus. (c) P. tertius. (d) R. montenegrensis. (e) C. pilosa. Bar: 10 mm.

The insects of the subfamily Triatominae share synapomorphies related to reproductive biology, such as the presence of chromosomes holocentric (Panzera et al. 1996PANZERA, 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 91:515-518, 10.1590/S0074-02761996000400021.
https://doi.org/10.1590/S0074-0276199600...
), inverted meiosis for sex chromosomes (Gómez-Palacio et al. 2008G=MEZ-PALACIO, A., JARAMILLO-OCAMPO, N., TRIANA-CHÁVEZ, O., SALDAÑA, A., CALZADA, J., PÉREZ, R. & PANZERA, F. 2008. Chromosome variability in the Chagas disease vector Rhodnius pallescens (Hemiptera, Reduviidae, Rhodniini). Mem. Inst. Oswaldo Cruz 103:160-164, 10.1590/S0074-02762008000200006.
https://doi.org/10.1590/S0074-0276200800...
), the phenomenon of nucleolar persistence during meiosis (Tartarotti & Azeredo-Oliveira 1999TARTAROTTI, E. & AZEREDO-OLIVEIRA, M.T.V. 1999. Patterns of nucleolar activity during spermatogenesis of two triatomines, Panstrongylus megistus and P. herreri. Caryologia 52:177-184, 10.1080/00087114.1998.10589171.
https://doi.org/10.1080/00087114.1998.10...
, Alevi et al. 2014cALEVI, K.C.C., CASTRO, N.F.C., LIMA, A.N.C., RAVAZI, A., MORIELLE-SOUZA, A., OLIVEIRA, J., ROSA, J.A. & AZEREDO-OLIVEIRA, M.T.V. 2014c. Nucleolar persistence during spermatogenesis of the Rhodnius (Hemiptera, Triatominae). Cell Biol. Int. 38:977-980, 10.1002/cbin.10297.
https://doi.org/10.1002/cbin.10297...
), nucleolar inactivation during spermiogenesis (Alevi et al. 2014bALEVI, K.C.C., MENDONÇA, P.P., PEREIRA, N.P., ROSA, J.A & AZEREDO-OLIVEIRA, M.T.V. 2014b. Is there post-meiotic transcriptional activity during hemiperan spermiogenesis? Inv. Rep. Dev. 58:193-198, 10.1080/07924259.2014.889767.
https://doi.org/10.1080/07924259.2014.88...
), presence seven testicular follicles (Schreiber et al. 1968SCHREIBER, G., PENALVA, F. & CARVALHO HC. 1968. Morfologia comparada dos folículos testiculares e sistemática dos Triatominae (Hemiptera, Reduviidae). Cien. Cult. 20:640-641.) and testicular peritoneal sheath transparent (this paper), demonstrating that during the evolution and speciation of the triatomines, the reproductive aspects undergone few modifications.

Thus, this paper describes the coloring of the peritoneal sheath in 44 species of the subfamily Triatominae and mainly suggests that the transparent color is one synapomorphy of this important group of insect vectors.

Acknowledgments

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

References

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    » https://doi.org/10.1016/j.meegid.2012.06.011
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    » https://doi.org/10.4238/2012.December.17.3
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    » https://doi.org/10.1080/07924259.2013.793623
  • ALEVI, K.C.C., MENDONÇA, P.P., PEREIRA, N.P., ROSA, J.A & AZEREDO-OLIVEIRA, M.T.V. 2013d. Spermatogenesis in Triatoma melanocephala (Hemiptera, Triatominae). Gen. Mol.Res. 12:4944-4947, 10.4238/2013.October.24.5.
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  • ALEVI, K.C.C., ROSA, J.A & AZEREDO-OLIVEIRA, M.T.V. 2014a. Spermatogenesis in Triatoma melanica Neiva and Lent, 1941 (Hemiptera, Triatominae) J. Vec. Ecol. 39:231-233, 10.1111/j.1948-7134.2014.12094.x.
    » https://doi.org/10.1111/j.1948-7134.2014.12094.x
  • ALEVI, K.C.C., MENDONÇA, P.P., PEREIRA, N.P., ROSA, J.A & AZEREDO-OLIVEIRA, M.T.V. 2014b. Is there post-meiotic transcriptional activity during hemiperan spermiogenesis? Inv. Rep. Dev. 58:193-198, 10.1080/07924259.2014.889767.
    » https://doi.org/10.1080/07924259.2014.889767
  • ALEVI, K.C.C., CASTRO, N.F.C., LIMA, A.N.C., RAVAZI, A., MORIELLE-SOUZA, A., OLIVEIRA, J., ROSA, J.A. & AZEREDO-OLIVEIRA, M.T.V. 2014c. Nucleolar persistence during spermatogenesis of the Rhodnius (Hemiptera, Triatominae). Cell Biol. Int. 38:977-980, 10.1002/cbin.10297.
    » https://doi.org/10.1002/cbin.10297
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    » https://doi.org/10.1590/S0074-02761956000300009
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    » https://doi.org/10.1163/157075608X328062
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    » https://doi.org/10.1016/j.micron.2010.01.008
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    » https://doi.org/10.1590/S0074-02762008000200006
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  • MORIELLE-SOUZA A., TABOGA, S.R. & AZEREDO-OLIVEIRA, M.T.V. 2010. Ultrastructural analysis of the nucleolar aspects at spermiogenesis in triatomines (Heteroptera, Triatominae). Micron 41:791-796, 10.1016/j.micron.2010.05.009.
    » https://doi.org/10.1016/j.micron.2010.05.009
  • 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 91:515-518, 10.1590/S0074-02761996000400021.
    » https://doi.org/10.1590/S0074-02761996000400021
  • ROSA, J.A., MENDONÇA, V.J., GARDIM, S., DE CARVALHO DB, DE OLIVEIRA J., NASCIMENTO, JD, PINOTTI, H, PINTO, MC, CILENSE, M, GLAVÃO, C & BARATA, J.M. 2014. Study of the external female genitalia of 14 Rhodnius species (Hemiptera, Reduviidae, Triatominae) using scanning electron microscopy. Paras. Vect. 7:17, 10.1186/1756-3305-7-17.
    » https://doi.org/10.1186/1756-3305-7-17
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  • SILISTINO-SOUZA, R., PERUQUETTI, R.L., TABOGA, S.R. & AZEREDO-OLIVEIRA, M.T.V. 2012. Chromatoid body: Remnants of nucleolar proteins during spermatogenesis in triatomine (Heteroptera, Triatominae). Micron 43:954-960, 10.1016/j.micron.2012.03.017.
    » https://doi.org/10.1016/j.micron.2012.03.017
  • TARTAROTTI, E. & AZEREDO-OLIVEIRA, M.T.V. 1999. Patterns of nucleolar activity during spermatogenesis of two triatomines, Panstrongylus megistus and P. herreri Caryologia 52:177-184, 10.1080/00087114.1998.10589171.
    » https://doi.org/10.1080/00087114.1998.10589171

Publication Dates

  • Publication in this collection
    Dec 2014

History

  • Received
    07 July 2014
  • Reviewed
    25 Aug 2014
  • Accepted
    21 Oct 2014
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