Hostname: page-component-8448b6f56d-42gr6 Total loading time: 0 Render date: 2024-04-18T21:22:23.716Z Has data issue: false hasContentIssue false
  • English
  • Français

Evolutionary history of trypanosomes from South American caiman (Caiman yacare) and African crocodiles inferred by phylogenetic analyses using SSU rDNA and gGAPDH genes

Published online by Cambridge University Press:  04 November 2008

L. B. VIOLA ,
R. S. ALMEIDA ,
R. C. FERREIRA ,
M. CAMPANER ,
C. S. A. TAKATA ,
A. C. RODRIGUES ,
F. PAIVA ,
E. P. CAMARGO  and
M. M. G. TEIXEIRA
L. B. VIOLA
Affiliation:
Departamento de Parasitologia, Instituto de Ciências Biomédicas, Universidade de São Paulo, São Paulo, SP, 05508-900, Brasil
R. S. ALMEIDA
Affiliation:
Departamento de Parasitologia Veterinária, Universidade Federal do Mato Grosso do Sul, Mato Grosso do Sul, MS, 7909-900, Brasil
R. C. FERREIRA
Affiliation:
Departamento de Parasitologia, Instituto de Ciências Biomédicas, Universidade de São Paulo, São Paulo, SP, 05508-900, Brasil
M. CAMPANER
Affiliation:
Departamento de Parasitologia, Instituto de Ciências Biomédicas, Universidade de São Paulo, São Paulo, SP, 05508-900, Brasil
C. S. A. TAKATA
Affiliation:
Departamento de Parasitologia, Instituto de Ciências Biomédicas, Universidade de São Paulo, São Paulo, SP, 05508-900, Brasil
A. C. RODRIGUES
Affiliation:
Departamento de Parasitologia, Instituto de Ciências Biomédicas, Universidade de São Paulo, São Paulo, SP, 05508-900, Brasil
F. PAIVA
Affiliation:
Departamento de Parasitologia Veterinária, Universidade Federal do Mato Grosso do Sul, Mato Grosso do Sul, MS, 7909-900, Brasil
E. P. CAMARGO
Affiliation:
Departamento de Parasitologia, Instituto de Ciências Biomédicas, Universidade de São Paulo, São Paulo, SP, 05508-900, Brasil
M. M. G. TEIXEIRA*
Affiliation:
Departamento de Parasitologia, Instituto de Ciências Biomédicas, Universidade de São Paulo, São Paulo, SP, 05508-900, Brasil
*
*Corresponding author: Departamento de Parasitologia, Instituto de Ciências Biomédicas, Universidade de São Paulo, São Paulo, SP, 05508-900, Brasil. Tel: +55 11 3091 7268. Fax: +55 11 3091 7417. E-mail: mmgteix@icb.usp.br
Get access Rights & Permissions [Opens in a new window]

Summary

In this study, using a combined data set of SSU rDNA and gGAPDH gene sequences, we provide phylogenetic evidence that supports clustering of crocodilian trypanosomes from the Brazilian Caiman yacare (Alligatoridae) and Trypanosoma grayi, a species that circulates between African crocodiles (Crocodilydae) and tsetse flies. In a survey of trypanosomes in Caiman yacare from the Brazilian Pantanal, the prevalence of trypanosome infection was 35% as determined by microhaematocrit and haemoculture, and 9 cultures were obtained. The morphology of trypomastigotes from caiman blood and tissue imprints was compared with those described for other crocodilian trypanosomes. Differences in morphology and growth behaviour of caiman trypanosomes were corroborated by molecular polymorphism that revealed 2 genotypes. Eight isolates were ascribed to genotype Cay01 and 1 to genotype Cay02. Phylogenetic inferences based on concatenated SSU rDNA and gGAPDH sequences showed that caiman isolates are closely related to T. grayi, constituting a well-supported monophyletic assemblage (clade T. grayi). Divergence time estimates based on clade composition, and biogeographical and geological events were used to discuss the relationships between the evolutionary histories of crocodilian trypanosomes and their hosts.

Keywords

TrypanosomaevolutionphylogenyCaiman yacarephylogeographyribosomal genegGAPDH geneT. grayiavian trypanosomes
Type
Research Article
Information
Parasitology , Volume 136 , Issue 1 , January 2009 , pp. 55 - 65
Copyright
Copyright © 2008 Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Barbosa, J. A., Kellner, A. W. A. and Viana, M. S. S. (2008). New dyrosaurid crocodylomorph and evidences for faunal turnover at the K-P transition in Brazil. Proceedings of the Royal Society of London, B 275, 1385–1391. doi:10.1098/rspb.2008.0110.Google Scholar
Cortez, A. P., Ventura, R. M., Rodrigues, A. C., Batista, J. S., Paiva, F., Añez, N., Machado, R. Z., Gibson, W. C. and Teixeira, M. M. G. (2006). The taxonomic and phylogenetic relationships of Trypanosoma vivax from South America and Africa. Parasitology 133, 159–169. doi:10.1017/S0031182006000254.CrossRefGoogle ScholarPubMed
Dessauer, H. C., Glenn, T. C. and Densmore, L. D. (2002). Studies on the molecular evolution of the Crocodylia: Footprints in the sands of time. Journal of Experimental Zoology 294, 302–311. doi:10.1002/jez.10208.Google Scholar
Dirie, M. F., Wallbanks, K. R., Molyneux, D. H. and McNamara, J. (1991). Comparison of Trypanosoma grayi-like isolates from west and east Africa. Annals of Tropical Medicine and Parasitology 85, 49–52.CrossRefGoogle ScholarPubMed
Dutton, J. E., Todd, J. L. and Tobey, E. N. (1907). Concerning certain parasitic Protozoa observed in Africa. Annals of Tropical Medicine and Parasitology 1, 287–371.CrossRefGoogle Scholar
Ferreira, R. C., De Souza, A. A., Freitas, R. A., Campaner, M., Takata, C. S. A., Barrett, T. B., Shaw, J. J. and Teixeira, M. M. G. (2008). A phylogenetic lineage of closely related trypanosomes (Trypanosomatidae, Kinetoplastida) of anurans and sandy flies (Psychodidae, Diptera) sharing the same ecotopes in Brazilian Amazonia. Journal of Eukaryotic Microbiology 55, 427–435. doi: 10.1111/j.1550-7408.2008.00342.x.Google Scholar
Ferreira, R. C., Campaner, M., Viola, L. B., Takata, C. S. A., Takeda, G. F. and Teixeira, M. M. G. (2007). Morphological and molecular diversity and phylogenetic relationships among anuran trypanosomes from the Amazonia, Atlantic Forest and Pantanal biomes in Brazil. Parasitology 134, 1623–1638. doi:10.1017/S0031182007003058.Google Scholar
Haag, J., O'hUigin, C. and Overath, P. (1998). The molecular phylogeny of trypanosomes: evidence for an early divergence of the Salivaria. Molecular and Biochemical Parasitology 1, 37–49.Google Scholar
Hamilton, P. B., Gibson, W. C. and Stevens, J. R. (2007). Patterns of co-evolution between trypanosomes and their hosts deduced from ribosomal RNA and protein-coding gene phylogenies. Molecular and Phylogenetics Evolution 44, 15–25. doi:10.1016/j.ympev.2007.03.023.Google Scholar
Hamilton, P. B., Stevens, J. R., Gidley, J., Holz, P. and Gibson, W. C. (2005). A new lineage of trypanosomes from Australian vertebrates and terrestrial bloodsucking leeches (Haemadipsidae). International Journal for Parasitology 35, 431–443. doi:10.1016/j.ijpara.2004.12.005.CrossRefGoogle ScholarPubMed
Hamilton, P. B., Stevens, J. R., Gaunt, M. W., Gidley, J. and Gibson, W. C. (2004). Trypanosomes are monophyletic: evidence from genes for glyceraldehyde phosphate dehydrogenase and small subunit ribosomal RNA. International Journal for Parasitology 34, 1393–1404. doi:10.1016/j.ijpara.2004.08.011.Google Scholar
Hoare, C. A. (1972). The Trypanosomes of Mammals: a Zoological Monograph. Blackwell Scientific Publications, Oxford, UK.Google Scholar
Hoare, C. A. (1931). Studies on Trypanosoma grayi. III. Life cycle in tsetse-fly and in the crocodile. Parasitology 23, 449–484.Google Scholar
Hoare, C. A. (1929). Studies on Trypanosoma grayi. II. Experimental transmission to the crocodile. Transactions of Royal Society of Tropical Medicine and Hygiene 23, 39–56.CrossRefGoogle Scholar
Huelsenbeck, J. P. and Ronquist, F. (2001). MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17, 754–755. doi:10.1126/science.1065889.Google Scholar
Jakes, K. A., O'Donogue, P. J. and Adlard, R. D. (2001). Phylogenetic relationships of Trypanosoma chelodina and Trypanosoma binneyi from Australian tortoises and platypuses inferred from small subunit rRNA analyses. Parasitology 123, 483–487. doi:10.1017/s0031182001008721.Google Scholar
Janke, A., Gullberg, A., Hughes, S., Aggarwal, R. K. and Arnason, U. (2005). Mitogenomic analysis place the gavial (Gavialis gangeticus) on the crocodile tree and provide pre-K/T divergence times for most crocodilians. Journal of Molecular Evolution 61, 620–626. doi:10.1007/s00239-004-0336-9.CrossRefGoogle Scholar
Jordan, A. M. (1993). Tsetse-flies (Glossinidae). In Medical Insects and Arachnids (ed.Lane, R. P. and Crosskey, R. W.), pp. 333–388. Chapman and Hall, London, UK.CrossRefGoogle Scholar
Jouve, S., Bouya, B. and Amaghzaz, M. (2008). A long-snouted dyrosaurid (Crocodyliformes, mesoeucrocodylia) from the Paleocene of Morocco: Phylogenetic and palaeobiogeographic implications. Paleontology 51, 281–294. doi:10.1111/j.1475-4983.2007.00747.x.CrossRefGoogle Scholar
Kirkpatrick, C. E., Terway-Thompson, C. A. and Iyengar, M. R. (1986). Biochemical characterization of some raptor trypanosomes. II. Enzyme studies, with a description of Trypanosoma bennetti n. sp. Canadian Journal of Zoology 64, 195–203. doi:10.1139/z86-031.CrossRefGoogle Scholar
Lainson, R. (1977). Trypanosoma cecili n. sp., a parasite of the South American cayman, Caiman crocodilus crocodilus (Linnaeus, 1758) (Crocodilia: Alligatoridae). Protozoology 3, 87–93.Google Scholar
Lukes, J., Jirku, M., Dolezel, D., Kral'ová, I., Hollar, L. and Maslov, D. A. (1997). Analysis of ribosomal RNA genes suggests that trypanosomes are monophyletic. Journal of Molecular Evolution 44, 521–527.Google Scholar
MacNamara, J. J. and Snow, W. F. (1991). Improved identification of Nannomonas infections in tsetse flies from The Gambia. Acta Tropica 48, 127–136.Google Scholar
Maia da Silva, F., Junqueira, A. C., Campaner, M., Rodrigues, A. C., Crisante, G., Ramirez, L. E., Monteiro, F., Coura, J. R., Añez, N. and Teixeira, M. M. G. (2007). Comparative phylogeography of Trypanosoma rangeli and Rhodnius (Hemiptera:Reduviidae) supports a long coexistence of parasite lineages and their sympatric vectors. Molecular Ecology 16, 3361–3373. doi:10.1111/j.1365-294x.2007.03371.x.CrossRefGoogle ScholarPubMed
Maia da Silva, F., Noyes, H., Campaner, M., Junqueira, A. C., Coura, J. R., Añez, N., Shaw, J. J., Stevens, J. R. and Teixeira, M. M. G. (2004). Phylogeny, taxonomy and grouping of Trypanosoma rangeli isolates from man, triatomines and sylvatic mammals from widespread geographical origin based on SSU and ITS ribosomal sequences. Parasitology 129, 549–561. doi:10.1017/S0031182004005931.Google Scholar
Minter-Goedbloed, E., Leak, C. J., Minter, D. M., McNamara, J., Kimber, C., Bastien, P., Evans, D. A. and Le Ray, D. (1993). Trypanosoma varani and T. grayi-like trypanosomes: development in vitro and in insect hosts. Parasitology Research 79, 329–333.Google Scholar
Minter-Goedbloed, E., Pudney, M., Kilgour, V. and Evans, D. A. (1983). First record of a reptile trypanosome isolated from Glossina pallidipes in Kenya. Zeitschrift für Parasitenkunde 69, 17–26.Google Scholar
Molyneux, D. H. (1973). Experimental infections of avian trypanosomes in Glossina. Annals of Tropical Medicine and Parasitology 67, 223–228.CrossRefGoogle ScholarPubMed
Nieberding, C. M. and Olivieri, I. (2006). Parasites: proxies for host genealogy and ecology? Trends in Ecology and Evolution 22, 156–165. doi:10.1016/j.tree.2006.11.012.Google Scholar
Nunes, V. L. B. and Oshiro, E. T. (1990). Trypanosoma sp. em jacaré, Caiman crocodilus yacare (Daudin, 1802) (Crocodilia: Alligatoridae). Semina 11, 62–65.Google Scholar
Paterson, A. M. and Banks, J. (2001). Analytical approaches to measuring cospeciation of host and parasites: through a glass, darkly. International Journal for Parasitology 31, 1012–1022.CrossRefGoogle ScholarPubMed
Poinar, G. Jr. (2007). Early Cretaceous trypanosomatids associated with fossil sand fly larvae in Burmese amber. Memórias do Instituto Oswaldo Cruz 102, 635–637.Google Scholar
Poinar, G. Jr. and Poinar, R. (2004). Paleoleishmania proterus n. gen., n. sp., (Trypanosomatidae: Kinetoplastida) from Cretaceous Burmese amber. Protist 155, 305–310.CrossRefGoogle Scholar
Poulin, R. and Keeney, D. B. (2007). Host specificity under molecular and experimental scrutiny. Trends in Parasitology 24, 24–28. doi:10.1016/j.pt.2007.10.002.Google Scholar
Rodrigues, A. C., Paiva, F., Campaner, M., Stevens, J. R., Noyes, H. A. and Teixeira, M. M. G. (2006). Phylogeny of Trypanosoma (Megatrypanum) theileri and related trypanosomes reveals lineages of isolates associated with artiodactyl hosts diverging on SSU and ITS ribosomal sequences. Parasitology 132, 215–224. doi:10.1017/s0031182005008929.CrossRefGoogle ScholarPubMed
Rodrigues, A. C., Neves, L., Garcia, H. A., Viola, L. B., Marcili, A., Maia da Silva, F., Sigauque, I., Batista, J. S., Paiva, F. and Teixeira, M. M. G. (2008). Phylogenetic analysis of Trypanosoma vivax supports the separation of South American/West African from East African isolates and a new T. vivax-like genotype infecting a nyala antelope from Mozambique. Parasitology 135, 1317–1335. doi:10.1017/S0031182008004848.Google Scholar
Roos, J., Aggarwal, R. K. and Janke, A. (2007). Extended mitogenomic phylogenetic analyses yield new insight into crocodilian evolution and their survival of the Cretaceous-Tertiary boundary. Molecular Phylogenetics and Evolution 45, 663–673. doi:10.1016/j.ympev.2007.06.018.CrossRefGoogle ScholarPubMed
Roos, J. P. (1998). Crocodiles. Status Survey and Conservation Action Plan, 2nd Edn, VIII 96 pp., IUCN/SSC, Crocodile Specialist Group, IUCN, Gland, Switzerland and Cambridge, UK.Google Scholar
Sehgal, R. N., Jones, H. I. and Smith, T. B. (2001). Host specificity and incidence of Trypanosoma in some African rainforest birds: a molecular approach. Molecular Ecology 10, 2319–2327.Google Scholar
Simpson, A. G. B., Stevens, J. R. and Lukes, J. (2006). The evolution and diversity of kinetoplastid flagellates. Trends in Parasitology 22, 168–174. doi:10.1016/j.pt.2006.02.006.Google Scholar
Stamatakis, A. (2006). RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22, 2688–2690. doi:10.1093/bioinformatics/btl446.CrossRefGoogle ScholarPubMed
Stevens, J. R., Noyes, H. A., Schofield, C. J. and Gibson, W. C. (2001). The molecular evolution of Trypanosomatidae. Advances in Parasitology 48, 1–56. doi:10.1016/s0065-308.(01)48003-1.CrossRefGoogle ScholarPubMed
Swofford, D. L. (2002). PAUP*: Phylogenetic Analysis using Parsimony (*and Other Methods), Beta Version 4.0b10. Sinauer and Associates, Sunderland, Massachusetts, USA.Google Scholar
Telford, R. S. (1995). The kinetoplastid hemoflagellates of reptiles. In Parasitic Protozoa, Vol. 10 (ed. Kreier, J. P.), pp. 161–223. Academic Press, New York, USA.CrossRefGoogle Scholar
Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F. and Higgins, D. G. (1997). The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research, 25, 4876–4882. doi: 10.1093/nar/25.24.4876.Google Scholar
Viola, L. B., Campaner, M., Takata, C. S. A., Ferreira, R. C., Rodrigues, A. C., Freitas, R. A., Duarte, M. R., Greco, K. F., Barrett, T. V., Camargo, E. P. and Teixeira, M. M. G. (2008). Phylogeny of snake trypanosomes inferred by SSU rDNA sequences, their possible transmission by phlebotomines, and taxonomic appraisal by molecular, cross-infection and morphological analysis. Parasitology 135, 595–605. doi:10.1017/s0031182008004253.Google Scholar
Votýpka, J., Lukes, J. and Oborník, M. (2004). Phylogenetic relationship of Trypanosoma corvi with other avian trypanosomes. Acta Protozoologica 43, 225–231.Google Scholar
Votýpka, J., Oborník, M., Volf, P., Svobodová, M. and Lukes, J. (2002). Trypanosoma avium of raptors (Falconiformes): phylogeny and identification of vectors. Parasitology 125, 253–263. doi:10.1017/s0031182002002093.Google Scholar