Abstract
The parasite-vector interaction of Chagas disease is still poorly understood and the understanding of this relationship can help in the development of new strategies to control Trypanosoma cruzi transmission, which is the etiological agent of this disease. Considering the need to know if T. cruzi can cause some pathology in the reproductive system of the Chagas disease vectors, we investigated the spermatogenesis of Triatoma infestans infected by T. cruzi through histological and cytogenetic analysis. Trypanosoma cruzi Bolivia strain infection was not pathogenic for the reproductive system of T. infestans, because all the analyzed males had normal spermatogenesis, with all phases (spermatocytogenesis, meiosis and spermiogenesis) happening without any change. Thus, we demonstrated that the presence of T. cruzi Bolivia strain does not have influence in the spermatogenesis of T. infestans and we suggest that the influences on reproductive system observed for other species were a result of the action of the parasite on gametogenesis of females.
References
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? Inf Gen Evol 12:1652–1653. https://doi.org/10.1016/j.meegid.2012.06.011
Alevi KCC, Rosa JA, Azeredo-Oliveira MTV (2014) Spermatogenesis in Triatoma melanica Neiva and Lent, 1941 (Hemiptera, Triatominae). J Vec Ecol 39:231–233. https://doi.org/10.1111/j.1948-7134.2014.12094.x
Alevi KCC, Castro NFC, Oliveira J, Rosa JA, Azeredo-Oliveira MTV (2015) Cystic spermatogenesis in three species of the prolixus complex (Hemiptera: Triatominae). Ital J Zool 82:1–7. https://doi.org/10.1080/11250003.2015.1020347
Alvarenga NJ, Bronfen E (1982) Incapacity of the evolution of Trypanosoma cruzi in the hemocele of triatomids. Mem Inst Oswaldo Cruz 77:431–436. https://doi.org/10.1590/S0074-02761982000400010
Atella GC, Gondim KC, Machado EA, Medeiros MN, Silva-Neto MA, Masuda H (2005) Oogenesis and egg development in triatomines: a biochemical approach. An Acad Bras Cienc 77:405–430. https://doi.org/10.1590/S0001-37652005000300005
Botto-Mahan C, Cattan PE, Medel R (2006) Chagas disease parasite induces behavioural changes in the kissing bug Mepraia spinolai. Acta Trop 98:219–223. https://doi.org/10.1016/j.actatropica.2006.05.005
Coppens I, Courtoy PJ (1995) Exogenous and endogenous sources of sterols in the culture-adapted procyclic trypomastigotes of Trypanosoma brucei. Mol Biochem Parasitol 73:179–188. https://doi.org/10.1016/0166-6851(95)00114-G
Coppens I, Levade T, Courtoy PJ (1995) Host plasma low density lipoprotein particles as an essential source of lipids for the bloodstream forms of Trypanosoma brucei. J Biol Chem 270:5736–5741. https://doi.org/10.1074/jbc.270.11.5736
De Vaio ES, Grucci B, Castagnino AM, Franca ME, Martinez ME (1985) Meiotic differences between three triatomine species (Hemiptera:Reduviidae). Genetica 67:185–191. https://doi.org/10.1007/BF02424489
Fellet MR, Lorenzo MG, Elliot SL, Carrasco D, Guarneri AA (2014) Effects of infection by Trypanosoma cruzi and Trypanosoma rangeli on the reproductive performance of the vector Rhodnius prolixus. PLoS One 9:26–32. https://doi.org/10.1371/journal.pone.0105255
Funayama GK, Prado Junior JC (1974) Estudo sobre os caracteres de una amostra boliviana do Trypanosoma cruzi. Rev Soc Bras Med Trop 8:75–81. https://doi.org/10.1590/S0037-86821974000200002
Galvão C (2014) Vetores da Doença de Chagas no Brasil. Sociedade Brasileira de Zoologia, Curitiba
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 202:1–36. https://doi.org/10.11646/zootaxa.202.1.1
Gondim KC, Oliveira PL, Masuda H (1989) Lipophorin and oogenesis in Rhodnius prolixus: transfer of phopholipids. J Insect Physiol 35:19–27. https://doi.org/10.1016/0022-1910(89)90032-2
Guarneri AA, Lorenzo MG (2017) Triatomine physiology in the context of trypanosome infection. J Insect Physiol 97:66–76. https://doi.org/10.1016/j.jinsphys.2016.07.005
Guarneri AA, Pereira MH, Diotaiuti L (2000) Influence of the blood meal source on the development of Triatoma infestans, Triatoma brasiliensis, Triatoma sordida, and Triatoma pseudomaculata (Heteroptera, Reduviidae). J Med Entomol 37:373–379. https://doi.org/10.1093/jmedent/37.3.373
Hurd H (2001) Host fecundity reduction: a strategy for damage limitation? Trends Parasitol 17:363–368. https://doi.org/10.1016/S1471-4922(01)01927-4
Kollien AH, Schmidt J, Schaub GA (1998) Modes of association of Trypanosoma cruzi with the intestinal tract of the vector Triatoma infestans. Acta Trop 70:127–141. https://doi.org/10.1016/S0001-706X(97)00117-4
Lima MM, Pereira JB, Santos JAA, Pinto ZT, Braga MV (1992) Development and reproduction of Panstrongylus megistus (Hemiptera: Reduviidae) infected with Trypanosoma cruzi, under laboratory conditions. Ann Entomol Soc Am 85:458–461. https://doi.org/10.1093/aesa/85.4.458
Madeira FF, Borsatto KC, Lima ACC, Ravazi A, Oliveira J, Rosa JA, Azeredo-Oliveira MTV, Alevi KCC (2016) Nucleolar persistence: peculiar characteristic of spermatogenesis of the vectors of Chagas disease (Hemiptera, Triatominae). Am J Trop Med Hyg 95:1118–1120. https://doi.org/10.4269/ajtmh.16-0149
Martínez-Díaz RA, Escario JA, Nogal-Ruiz JJ, Gómez-Barrio A (2001) Biological characterization of Trypanosoma cruzi strains. Mem Inst Oswaldo Cruz 96:53–59. https://doi.org/10.1590/S0074-02762001000100006
Martins R, Ruiz N, Fonseca RND, Vaz Junior IDS, Logullo C (2018) The dynamics of energy metabolism in the tick embryo. Rev Bras Parasitol Vet 27:259–266. https://doi.org/10.1590/s1984-296120180051
Nouvellet P, Ramirez-Sierra MJ, Dumonteil E, Gourbiere S (2011) Effects of genetic factors and infection status on wing morphology of Triatoma dimidiata species complex in the Yucatán peninsula, Mexico. Infect Genet Evol 11:1243–1249. https://doi.org/10.1016/j.meegid.2011.04.008
Oliveira ABB, Alevi KCC, Imperador CHL, Madeira FF, Azeredo-Oliveira MTV (2018) Parasite-vector interaction of Chagas disease: a mini-review. Am J Trop Med Hyg 98:653–655. https://doi.org/10.4269/ajtmh.17-0657
Panzera F, Alvarez F, Sanchez-Rufas J, Pérez R, Suja J, Scvortzoff E, Estramil E, Dujardin J, Salvatella R (1992) C-heterochromatin polymorphism in holocentric chromosomes of T. infestans (Hemiptera-Reduviidae). Genome 35:1068–1074. https://doi.org/10.1139/g92-164
Panzera F, Pérez R, Panzera Y, Alvarez F, Scvortzoff E, Salvatella R (1995) Karyotype evolution in holocentric chromosomes of three related species of triatomines (Hemiptera-Reduviidae). Chromosom Res 3:143–150. https://doi.org/10.1007/BF00710707
Penin P, Gamallo C, Diego JA (1996) Biological comparison between three clones of Trypanosoma cruzi and the strain of origin (Bolivia) with reference to clonal evolution studies. Mem Inst Oswaldo Cruz 91:285–291. https://doi.org/10.1590/S0074-02761996000300006
Pérez R, Panzera F, Page J, Suja J, Rufas J (1997) Meiotic behaviour of holocentric chromosomes: orientation and segregation of autosomes in Triatoma infestans (Heteroptera). Chromosom Res 5:47–56. https://doi.org/10.1023/A:1018493419208
Pérez R, Rufas J, Suja J, Paje J, Panzera F (2000) Meiosis in holocentric chromosomes: orientation and segregation of an autosome and sex chromosomes in Triatoma infestans (Heteroptera). Chromosom Res 8:17–25. https://doi.org/10.1023/A:1009266801160
Reis YV, Alevi KCC, Moreira FF, Azeredo-Oliveira MTV (2016) Spermatogenesis in Nesotriatoma bruneri (Usinger 1944) (Hemiptera, Triatominae). Gen Mol Res 15:1–5. https://doi.org/10.4238/gmr.15038286
Ribeiro AR (2014) Caracterização biológica e molecular de cepas de Trypanosoma cruzi Chagas, 1909 (Kinetoplastida, Trypanosomatidae) isoladas de triatomíneos da Bahia, Rio Grande do Sul, Santa Catarina e São Paulo. Dissertação. Universidade de Campinas
Schaub GA (1988) Developmental time and mortality of larvae of Triatoma infestans infected with Trypanosoma cruzi. Trans R Soc Med Hyg 82:94–96. https://doi.org/10.1016/0035-9203(88)90273-8
Webb TJ, Hurd H (1999) Direct manipulation of insect reproduction by agents of parasite origin. Proc Biol Sci 266:1537–1541. https://doi.org/10.1098/rspb.1999.0812
WHO (World Health Organization) (2019) Chagas disease (American trypanosomiasis). http://wwwwhoint/news-room/fact-sheets/detail/chagas-disease-(american-trypanosomiasis) Acessed 10 June 2019
Funding
This work was supported by the Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) (Process number 2017/05015-7), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) and by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior – Brasil (CAPES) – Finance Code 001.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Section Editor: David Bruce Conn
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
de Oliveira, A.B.B., Tedeschi, B.B.B., de Oliveira, J. et al. Parasite × vector relationship in Chagas disease: does Trypanosoma cruzi (Chagas, 1909) infection affect the spermatogenesis of Triatoma infestans (Klug, 1834)?. Parasitol Res 119, 3517–3522 (2020). https://doi.org/10.1007/s00436-020-06788-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00436-020-06788-z