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Morphological and molecular diversity and phylogenetic relationships among anuran trypanosomes from the Amazonia, Atlantic Forest and Pantanal biomes in Brazil

  • R. C. FERREIRA (a1), M. CAMPANER (a1), L. B. VIOLA (a1), C. S. A. TAKATA (a1), G. F. TAKEDA (a1) and M. M. G. TEIXEIRA (a1)...

Summary

We examined for the presence of trypanosomes in blood samples from 259 anurans (47 species from 8 families), the majority of which were from the Brazilian Amazonia, Atlantic Forest and Pantanal biomes. Trypanosomes were detected by a combination of microhaematocrit and haemoculture methods in 45% of the anurans, and 87 cultures were obtained: 44 from Hylidae, 22 from Leptodactylidae, 15 from Bufonidae, 5 from Leiuperidae and 1 from an unidentified anuran. High morphological diversity (11 morphotypes) was observed among blood trypanosomes from anurans of different species and of the same species as well as among trypanosomes from the same individual. Conversely, morphologically similar trypanosomes were found in anurans from distinct species and biomes. ITS and SSU rDNA polymorphisms revealed high diversity among the 82 isolates examined. Twenty-nine genotypes could be distinguished, the majority distributed in 11 groups. Phylogenetic relationships based on rDNA sequences indicated that isolates from more phylogenetically related anurans are more closely related. Comparison of anuran trypanosomes from Brazil and other countries revealed several new species among the isolates examined in this study. Phylogenetic relationships suggest that host restriction, host switching and overall ecogeographical structure may have played a role in the evolution of the anuran trypanosomes.

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*Corresponding author. Fax: +55 11 3818 7417. E-mail: mmgteix@icb.usp.br

References

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Anderson, J. R. and Ayala, S. C. (1968). Trypanosome transmitted by Phlebotomus: first report from the Americas. Science 161, 10231025. doi: 10.1126/science.161.3845.1023.
Ayala, S. C. (1970). Two new trypanosomes from California toads and lizards. Journal of Protozoology 17, 370373.
Bardsley, J. E. and Harmsen, R. (1973). The trypanosomes of Anura. Advances in Parasitology 11, 173.
Barta, J. R., Boulard, Y. and Desser, S. S. (1989). Blood parasites of Rana esculenta from Corsica: Comparison of its parasites with those of eastern North American ranids in the context of host phylogeny. Transactions of the American Microscopical Society 108, 620. doi: 10.2307/3226201.
Barta, J. R. and Desser, S. S. (1984). Blood parasites of amphibians from Algonquin Park, Ontario. Journal of Wildlife Diseases 20, 180189.
Bentz, S., Sinnappaah-Kang, N. D., Lim, L.-HS., Lebedev, B., Combes, C. and Verneau, O. (2006). Historical biogeography of amphibian parasites, genus Polystoma (Monogenea: Polystomidadee). Journal of Biogeography 33, 742749. doi: 10.1111/j.1365-2699.2005.01402.x.
Clark, C. G., Martin, D. S. and Diamond, L. S. (1995). Phylogenetic relationships among anuran trypanosomes as revealed by riboprinting. Journal of Eukaryotic Microbiology 42, 9296.
Cortez, A. P., Ventura, R. M., Rodrigues, A. C., Batista, J. S., Paiva, F., Anez, 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, 159169. doi: 10.1017/50031182006000254.
Desser, S. S. (2001). The blood parasites of anurans from Costa Rica with reflections on the taxonomy of their trypanosomes. Journal of Parasitology 87, 152160. doi: 10.1645/0022-3395(2001)087[0152:TBPOAF]2.0.CO;2.
Desser, S. S., McIver, S. B. and Jez, D. (1975). Observations on the role of simuliids and culicids in the transmission of avian and anuran trypanosomes. International Journal for Parasitology 5, 507509.
Desser, S. S., McIver, S. B. and Ryckman, A. (1973). Culex territans as a potential vector of Trypanosoma rotatorium. I. Development of the flagellate in the mosquito. Journal of Parasitology 59, 353358.
Diamond, L. S. (1965). A study of the morphology, biology and taxonomy of the trypanosomes of anura. Wildlife Diseases 44, 185.
Frost, D. R. (2006). Amphibian Species of the World: an Online Reference. Version 4 (17 August 2006), http://research.amnh.org/herpetology/amphibia/index.php.
Gibson, W. C., Lom, J., Peckova, H., Ferris, V. R. and Hamilton, P. B. (2005). Phylogenetic analysis of freshwater fish trypanosomes from Europe using SSUrRNA gene sequences and random amplification of polymorphic DNA. Parasitology 130, 405412. doi: 10.1017/S0031182004006778.
Gruby, M. (1843). Recherches et observations sur une nouvelle espèce d'hématozoaire, Trypanosoma sanguinis. Comptes Rendus Hebdomadaire des Séances de l'Académie des Sciences, Paris 55, 11341136.
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, 13931404. doi: 10.1016/j.ijpara.2004.08.011.
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, 431443. doi: 10.1016/j.ijpara.2004.12.005.
Jakes, K. A., O'Donoghue, P. J. and Adlard, R. D. (2001). Phylogenetic relationships of Trypanosoma chelodina and Trypanosoma binneyi from Australian turtles and platypuses inferred from small subunit rRNA analyses. Parasitology 123, 483487. doi: 10.1017/S0031182001008721.
Levine, N. D. and Nye, R. R. (1977). A survey of blood and other tissue parasites of leopard frogs Rana pipiens in the United States. Journal of Wildlife Diseases 13, 1723.
Lun, Z. R. and Desser, S. S. (1995). Karyotype analysis of anuran trypanosomes by pulsed-field gradient gel electrophoresis. Journal of Parasitology 81, 10181020.
Lun, Z. R. and Desser, S. S. (1996). Analysis of isolates within species of anuran trypanosomes using random amplified polymorphic DNA. Parasitology Research 82, 2227. doi: 10.1007/s004360050062.
Maia da Silva, F., Rodrigues, A. C., Campaner, M., Takata, C. S., Brigido, M. C., Junqueira, A. C., Coura, J. R., Takeda, G. F., Shaw, J. J. and Teixeira, M. M. G. (2004). Randomly amplified polymorphic DNA analysis of Trypanosoma rangeli and allied species from human, monkeys and other sylvatic mammals of the Brazilian Amazon disclosed a new group and a species-specific marker. Parasitology 128, 283294. doi: 10.1017/S0031182003004554.
Martin, D. S. and Desser, S. S. (1990). A light and electron microscopic study of Trypanosoma fallisi n. sp. in toads (Bufo americanus) from Algonquin Park, Ontario. Journal of Protozoology 37, 199206.
Martin, D. S. and Desser, S. S. (1991 a). Development of Trypanosoma fallisi in the leech, Desserobdella picta, in toads (Bufo americanus), and in vitro. A light and electron microscopic study. Parasitology Research 77, 1826. doi: 10.1007/BF00934379.
Martin, D. S. and Desser, S. S. (1991 b). Infectivity of cultured Trypanosoma fallisi (Kinetoplastida) to various anuran species and its evolutionary implications. Journal of Parasitology 77, 498500.
Martin, D. S., Desser, S. S. and Hong, H. (1992 a). Allozyme comparison of three Trypanosoma species (Kinetoplastida: Trypanosomatidae) of toads and frogs by starch-gel electrophoresis. Journal of Parasitology 78, 317322.
Martin, D. S., Desser, S. S. and Werner, J. K. (1992 b). Allozyme comparison and infectivity of cultured stages of Trypanosoma fallisi from southern Ontario and a trypanosome of toads from northern Michigan. Journal of Parasitology 78, 10831086.
Martin, D. S., Wright, A. D., Barta, J. R. and Desser, S. S. (2002). Phylogenetic position of the giant anuran trypanosomes Trypanosoma chattoni, Trypanosoma fallisi, Trypanosoma mega, Trypanosoma neveulemairei, and Trypanosoma ranarum inferred from 18S rRNA gene sequences. Journal of Parasitology 88, 566571. doi: 10.1645/0022-3395(2002)088[0566:PPOTGA]2.0.CO;2.
Miyata, A. (1978). Anuran trypanosomes in Kyushu and Ryukyu islands, with descriptions of six new species. Tropical Medicine 20, 5180.
Reilly, B. O. and Woo, P. T. K. (1982). The in vivo and in vitro development of Trypanosoma andersoni Reilly and Woo, 1982 and Trypanosoma grylli Nigrelli, 1944 (Kinetoplastida). Canadian Journal of Zoology 60, 124133.
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, 215224. doi: 10.1017150031182005008929.
Ronquist, F. and Huelsenbeck, J. P. (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 15721574. doi: 10.1093/bioinformatics/btg180.
Siddall, M. E. and Desser, S. S. (1992). Alternative leech vectors of frog and turtle trypanosomes. Journal of Parasitology 78, 562563.
Simpson, A. G. B., Stevens, J. R. and Lukes, J. (2006). The evolution and diversity of kinetoplastid flagellates. Trends in Parasitology 22, 168174. doi: 10.1016/j.pt.2006.02.006.
Sinnappah, N. D., Lim, L.-HS., Rohde, K., Tinsley, R., Combes, C. and Verneau, O. (2001). A paedomorphic parasite associated with a neotenic amphibian host: phylogenetic evidence suggests a revised systematic position for Sphyranuridae within anuran and turtle polystomatoineans. Molecular Phylogenetics and Evolution 18, 189201. doi: 10.1006/mpev.2000.0877.
Stevens, J. R., Noyes, H. A., Schofield, C. J. and Gibson, W. (2001). The molecular evolution of Trypanosomatidae. Advances in Parasitology 48, 156. doi: 10.1016/S0065-308X(01)48003-1.
Werner, J. K. (1993). Blood parasites of amphibians from Sichuan Province, People's Republic of China. Journal of Parasitology 79, 356363.
Werner, J. K. and Walewski, K. (1976). Amphibian trypanosomes from the McCormick forest, Michigan. Journal of Parasitology 62, 2025.
Woo, P. T. and Bogart, J. P. (1984). Trypanosoma spp. (Protozoa: Kinetoplastida) in Hylidae (Anura) from eastern North America, with notes on their distribution and prevalences. Canadian Journal of Zoology 62, 820824.
Zickus, T. (2002). The first data on the fauna and distribution of blood parasites of amphibians in Lithuania. Acta Zoologica Lituanica 12, 197202.

Keywords

Morphological and molecular diversity and phylogenetic relationships among anuran trypanosomes from the Amazonia, Atlantic Forest and Pantanal biomes in Brazil

  • R. C. FERREIRA (a1), M. CAMPANER (a1), L. B. VIOLA (a1), C. S. A. TAKATA (a1), G. F. TAKEDA (a1) and M. M. G. TEIXEIRA (a1)...

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