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A novel phylogeny for the genus Echinococcus, based on nuclear data, challenges relationships based on mitochondrial evidence

Published online by Cambridge University Press:  21 January 2009

U. SAARMA ,
I. JÕGISALU ,
E. MOKS ,
A. VARCASIA ,
A. LAVIKAINEN ,
A. OKSANEN ,
S. SIMSEK ,
V. ANDRESIUK ,
G. DENEGRI  and
L. M. GONZÁLEZ
...Show all authors
U. SAARMA*
Affiliation:
Department of Zoology, Institute of Ecology and Earth Sciences, University of Tartu, Vanemuise 46, 51014, Tartu, Estonia
I. JÕGISALU
Affiliation:
Department of Zoology, Institute of Ecology and Earth Sciences, University of Tartu, Vanemuise 46, 51014, Tartu, Estonia Department of Game Monitoring, Centre of Forest Protection and Silviculture, Rõõmu tee 2, 51013, Tartu, Estonia
E. MOKS
Affiliation:
Department of Zoology, Institute of Ecology and Earth Sciences, University of Tartu, Vanemuise 46, 51014, Tartu, Estonia
A. VARCASIA
Affiliation:
Dipartimento di Biologia Animale Sezione di Parassitologia e Malattie Parassitarie, Università degli Studi di Sassari, Via Vienna 2, 07100, Sassari
A. LAVIKAINEN
Affiliation:
Department of Bacteriology and Immunology (FINPAR), Haartman Institute, P.O. Box 21, FI-00014University of Helsinki, Finland
A. OKSANEN
Affiliation:
Finnish Food Safety Authority Evira, Fish and Wildlife Health Research Unit (FINPAR), P.O. Box 517, FI-90101Oulu, Finland
S. SIMSEK
Affiliation:
Department of Parasitology, Faculty of Veterinary Medicine, University of Firat, 23119, Elazig, Turkey
V. ANDRESIUK
Affiliation:
Laboratory of Parasitic Zoonoses, Department of Biology, FCEyN, Mar del Plata National University, Funes 3350, CP 7600, Mar del Plata, Buenos Aires, Argentina (CONICET)
G. DENEGRI
Affiliation:
Laboratory of Parasitic Zoonoses, Department of Biology, FCEyN, Mar del Plata National University, Funes 3350, CP 7600, Mar del Plata, Buenos Aires, Argentina (CONICET)
L. M. GONZÁLEZ
Affiliation:
Instituto de Salud Carlos III, Centro Nacional de Microbiología, Ctra. Majadahonda Pozuelo Km 2,2, 28220Majadahonda, Madrid, Spain
E. FERRER
Affiliation:
Instituto de Salud Carlos III, Centro Nacional de Microbiología, Ctra. Majadahonda Pozuelo Km 2,2, 28220Majadahonda, Madrid, Spain Departamento de Parasitología and Instituto de Investigaciones Biomédicas (BIOMED), Universidad de Carabobo, Maracay, Venezuela
T. GÁRATE
Affiliation:
Instituto de Salud Carlos III, Centro Nacional de Microbiología, Ctra. Majadahonda Pozuelo Km 2,2, 28220Majadahonda, Madrid, Spain
L. RINALDI
Affiliation:
Department of Pathology and Animal Health, Faculty of Veterinary Medicine, University of Naples Federico II, Naples, Italy
P. MARAVILLA
Affiliation:
Direccion de Investigacion, Hospital General “Dr. Manuel Gea Gonzalez”, SSA, MexicoDF, Mexico
*
*Corresponding author: Department of Zoology, Institute of Ecology and Earth Sciences, University of Tartu, Vanemuise 46, 51014, Tartu, Estonia. Tel: +37 27375099. Fax: +37 27375830. E-mail: Urmas.Saarma@ut.ee
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Summary

The taxonomic status of Echinococcus, an important zoonotic cestode genus, has remained controversial, despite numerous attempts to revise it. Although mitochondrial DNA (mtDNA) has been the source of markers of choice for reconstructing the phylogeny of the genus, results derived from mtDNA have led to significant inconsistencies with earlier species classifications based on phenotypic analysis. Here, we used nuclear DNA markers to test the phylogenic relationships of members of the genus Echinococcus. The analysis of sequence data for 5 nuclear genes revealed a significantly different phylogeny for Echinococcus from that proposed on the basis of mitochondrial DNA sequence data, but was in agreement with earlier species classifications. The most notable results from the nuclear phylogeny were (1) E. multilocularis was placed as basal taxon, (2) all genotypes of Echinococcus granulosus grouped as a monophyletic entity, and (3) genotypes G8 and G10 clustered together. We conclude that the analysis of nuclear DNA data provides a more reliable means of inferring phylogenetic relationships within Echinococcus than mtDNA and suggest that mtDNA should not be used as the sole source of markers in future studies where the goal is to reconstruct a phylogeny that does not only reflect a maternal lineage, but aims to describe the evolutionary history at species level or higher.

Keywords

Echinococcusnuclear genesmitochondrial genesphylogeny

Information

Type
Research Article
Information
Parasitology , Volume 136 , Issue 3 , March 2009 , pp. 317 - 328
Copyright
Copyright © 2009 Cambridge University Press

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References

REFERENCES

Abascal, F., Zardoya, R. and Posada, D. (2005). ProtTest: Selection of best-fit models of protein evolution. Bioinformatics 21, 2104–2105.CrossRefGoogle ScholarPubMed
Anderson, S., Bankier, A. T., Barrell, B. G., Debruijn, M. H. L., Coulson, A. R., Drouin, J., Eperon, I. C., Nierlich, D. P., Roe, B. A., Sanger, F., Schreier, P. H., Smith, A. J. H., Staden, R. and Young, I. G. (1981). Sequence and organization of the human mitochondrial genome. Nature, London 290, 457–465.CrossRefGoogle ScholarPubMed
Arendt, J. and Reznick, D. (2008). Convergence and parallelism reconsidered: what have we learned about the genetics of adaptation? Trends in Ecology and Evolution 23, 26–32.Google Scholar
Avise, J. C., Arnold, R. M., Ball, R. M., Bermingham, E., Lamb, T., Neigel, J. E., Reeb, C. A. and Saunders, N. C. (1987). Intraspecific phylogeography: the mitochondrial DNA bridge between population genetics and systematics. Annual Review of Ecology and Systematics 18, 489–522.CrossRefGoogle Scholar
Ballard, J. W. O. and Rand, D. M. (2005). The population biology of mitochondrial DNA and its phylogenetic implications. Annual Review of Ecology, Evolution and Systematics 36, 621–642.CrossRefGoogle Scholar
Bowles, J., Blair, D. and McManus, D. P. (1992). Genetic variants within the genus Echinococcus identified by mitochondrial DNA sequencing. Molecular and Biochemical Parasitology 54, 165–173.CrossRefGoogle ScholarPubMed
Bowles, J., Blair, D. and McManus, D. P. (1994). Molecular genetic characterization of the cervid strain (‘northern form’) of Echinococcus granulosus. Parasitology 109, 215–221.CrossRefGoogle ScholarPubMed
Bowles, J., Blair, D. and McManus, D. P. (1995). A molecular phylogeny of the genus Echinococcus. Parasitology 110, 317–328.Google Scholar
Brehm, K., Jensen, K., Frosch, P. and Frosch, M. (1999). Characterization of the genomic locus expressing the ERM-like protein of Echinococcus multilocularis. Molecular and Biochemical Parasitology 100, 147–152.CrossRefGoogle ScholarPubMed
Brown, W. M. (1983). Evolution of animal mitochondrial DNA. In Evolution of Genes and Proteins (ed. Nei, M. and Koehn, R. K.), pp. 62–88. Sinauer, Sunderland, Mass, USA.Google Scholar
Brown, W. M., George, M. Jr. and Wilson, A. C. (1979). Rapid evolution of animal mitochondrial DNA. Proceedings of the National Academy of Sciences, USA 76, 1967–1971.Google Scholar
Busi, M., Snabel, V., Varcasia, A., Garippa, G., Perrone, V., De Liberato, C. and Amelio, S. D. (2007). Genetic variation within and beween G1 and G3 genotypes of Echinococcus granulosus in Italy revealed by multilocus DNA sequencing. Veterinary Parasitology 150, 75–83.CrossRefGoogle Scholar
Drummond, A. J. and Rambaut, A. (2007). BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology 7, 214.Google Scholar
Engstrom, T. N., Shaffer, H. B. and McCord, W. P. (2004). Multiple data sets, high homoplasy, and the phylogeny of softshell turtles (Testudines: Trionychidae). Systematic Biology 53, 693–710.CrossRefGoogle ScholarPubMed
Farris, J. S., Källersjö, M., Kluge, A. G. and Bult, C. (1995). Testing significance of incongruence. Cladistics 10, 315–319.CrossRefGoogle Scholar
Funk, D. J. and Omland, K. E. (2003). Species-level paraphyly and polyphyly: Frequency, causes, and consequences, with insights from animal mitochondrial DNA. Annual Review of Ecology, Evolution and Systematics 34, 397–423.CrossRefGoogle Scholar
Giles, R. E., Blanc, H., Cann, M. and Wallace, D. C. (1980). Maternal inheritance of human mitochondrial DNA. Proceedings of the National Academy of Sciences, USA 77, 6715–6719.CrossRefGoogle ScholarPubMed
Gordon, D., Abajian, C. and Green, P. (1998). Consed: A graphical tool for sequence finishing. Genome Research 8, 195–202.CrossRefGoogle ScholarPubMed
Hall, T. A. (1999). BioEdit: a user friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acid Symposium Series 41, 95–98.Google Scholar
Hurst, G. D. D. and Jiggins, F. M. (2005). Problems with mitochondrial DNA as a marker in population, phylogeographic and phylogenetic studies: the effects of inherited symbionts. Proceedings of the Royal Society, B 272, 1525–1534.CrossRefGoogle ScholarPubMed
Hüttner, M., Nakao, M., Torsten, W., Siefert, L., Boomker, J. D. F., Dinkel, A., Sako, Y., Mackenstedt, U., Romig, T. and Ito, A. (2008). Genetic characterization and phylogenetic position of Echinococcus felidis (Cestoda: Taeniidae) from the African lion. International Journal for Parasitology 38, 861–868.CrossRefGoogle ScholarPubMed
Jannotti-Passos, L. K., Souza, C. P., Parra, J. C. and Simpson, A. J. G. (2001). Biparental mitochondrial DNA inheritance in the parasitic trematode Schistosoma mansoni. Journal of Parasitology 87, 79–82.Google Scholar
Jenkins, D. J., Romig, T. and Thompson, R. C. A. (2005). Emergence/re-emergence of Echinococcus spp., a global update. International Journal for Parasitology 35, 1205–1219.CrossRefGoogle ScholarPubMed
Kedra, A. H., Swiderski, Z., Tkach, V. V., Dubinsky, P., Pawlowski, Z., Stefaniak, J. and Pawlowski, J. (1999). Genetic analysis of Echinococcus granulosus from humans and pigs in Poland, Slovakia and Ukraine. A multicenter study. Acta Parasitologica 44, 248–254.Google Scholar
Lavikainen, A., Lehtinen, M. J., Laaksonen, S., Ågren, E., Oksanen, A. and Meri, S. (2006). Molecular characterization of Echinococcus isolates of cervid origin from Finland and Sweden. Parasitology 133, 565–570.CrossRefGoogle ScholarPubMed
Lavikainen, A., Lehtinen, M. J., Meri, T., Hirvelä-Koski, V. and Meri, S. (2003). Molecular genetic characterization of the Fennoscandian cervid strain, a new genotype group (G10) of Echinococcus granulosus. Parasitology 127, 207–215.Google Scholar
Le, T. H., Blair, D., Agatsuma, T., Humair, P. F., Campbell, N. J., Iwagami, M., Littlewood, D. T., Peacock, B., Johnston, D. A., Bartley, J., Rollinson, D., Herniou, E. A., Zarlenga, D. S. and McManus, D. P. (2000). Phylogenies inferred from mitochondrial gene orders – a cautionary tale from the parasitic flatworms. Molecular Biology and Evolution 17, 1123–1125.Google Scholar
Le, T. H., Pearson, M. S., Blair, D., Dai, N., Zhang, L. H. and McManus, D. P. (2002). Complete mitochondrial genomes confirm the distinctiveness of the horse-dog and sheep-dog strains of Echinococcus granulosus. Parasitology 124, 97–112.Google Scholar
Leister, D. (2005). Origin, evolution and genetic effects of nuclear insertions of organelle DNA. Trends in Genetics 21, 655–663.CrossRefGoogle ScholarPubMed
López-Neyra, C. R. and Soler Planas, M. A. (1943). Revision del genero Echinococcus Rud y descripción de una especie nueva parárita intestinal del perro en Almería. Revista Ibérica de Parasitología 3, 169–194 (in Spanish).Google Scholar
Maravilla, P., Thompson, R. C. A., Palacios-Ruiz, J. A., Estcourt, A., Ramirez-Solis, E., Mondragon-de-la-Peña, C., Moreno-Moller, M., Cardenas-Mejia, A., Mata-Miranda, P., Aguirre-Alcantara, M. T., Bonilla-Rodriguez, C. and Flisser, A. (2004). Echinococcus granulosus cattle strain identification in an autochthonous case of cystic echinococcosis in central Mexico. Acta Tropica 92, 231–236.CrossRefGoogle Scholar
McManus, D. P. and Thompson, R. C. A. (2003). Molecular epidemiology of cystic echinococcosis. Parasitology 127, S37–S51.Google Scholar
Moks, E., Jõgisalu, I., Saarma, U., Talvik, H., Järvis, T. and Valdmann, H. (2006). Helminthologic survey of the wolf (Canis lupus) in Estonia, with an emphasis on Echinococcus granulosus. Journal of Wildlife Diseases 42, 359–365.CrossRefGoogle ScholarPubMed
Moks, E., Jõgisalu, I., Valdmann, H. and Saarma, U. (2008). First report of Echinococcus granulosus G8 in Eurasia and a reappraisal of the phylogenetic relationships of ‘genotypes’ G5–G10. Parasitology 135, 647–654.CrossRefGoogle Scholar
Moks, E., Saarma, U. and Valdmann, H. (2005). Echinococcus multilocularis in Estonia. Emerging Infectious Diseases 11, 1973–1974.Google Scholar
Nakao, M., McManus, D. P., Schantz, P. M., Craig, P. S. and Ito, A. (2007). A molecular phylogeny of the genus Echinococcus inferred from complete mitochondrial genomes. Parasitology 134, 713–722.Google Scholar
Naylor, G. J. P. and Brown, W. M. (1998). Amphioxus mitochondrial DNA, chordate phylogeny, and the limits of inference based on comparisons of sequences. Systematic Biology 47, 61–76.Google Scholar
Obwaller, A., Schneider, R., Walochnik, J., Gollackner, B., Deutz, A., Janitschke, K., Aspöck, H. and Auer, H. (2004). Echinococcus granulosus strain differentiation based on sequence heterogeneity in mitochondrial genes of cytochrome c oxidase-1 and NADH dehydrogenase-1. Parasitology 128, 569–575.CrossRefGoogle ScholarPubMed
Page, R. D. (1996). TreeView: an application to display phylogenetic trees on personal computers. Computer Applications in the Biosciences 12, 357–358.Google ScholarPubMed
Posada, D. and Crandall, K. A. (1998). MODELTEST: testing the model of DNA substitution. Bioinformatics 14, 817–818.CrossRefGoogle ScholarPubMed
Rambaut, A. and Drummond, A. J. (2007). Tracer v1.4, Available from http://beast.bio.ed.ac.uk/TracerGoogle Scholar
Rausch, R. L. (1967). A consideration of infraspecific categories in the genus Echinococcus Rudolphi, 1801 (Cestoda: Taeniidae). The Journal of Parasitology 53, 484–491.CrossRefGoogle ScholarPubMed
Rinaldi, L., Maurelli, M. P., Capuano, F., Perugini, A. G., Veneziano, V. and Cringoli, S. (2008). Molecular update on cystic echinococcosis in cattle and water buffaloes of southern Italy. Zoonoses and Public Health 55, 119–123.CrossRefGoogle ScholarPubMed
Romig, T., Dinkel, A. and Mackenstedt, U. (2006). The present situation of echinococcosis in Europe. Parasitology International 55, S187–S191.CrossRefGoogle ScholarPubMed
Ronquist, F. and Huelsenbeck, J. P. (2003). MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574.CrossRefGoogle ScholarPubMed
Scott, J. C., Stefaniak, J., Pawlowski, Z. S. and McManus, D. P. (1997). Molecular genetic analysis of human cystic hydatid cases from Poland: identification of a new genotypic group (G9) of Echinococcus granulosus. Parasitology 114, 37–43.CrossRefGoogle ScholarPubMed
Swofford, D. L. (1998). PAUP*: Phylogenetic Analysis Using Parsimony (*and Other Methods), Version 4.0g10. Sinauer Associates, Massachusetts, USA.Google Scholar
Thompson, J. D., Higgins, D. G. and Gibson, T. J. (1994). Clustal W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position specific gap penalties and weight matrix choice. Nucleic Acids Research 22, 4673–4680.CrossRefGoogle ScholarPubMed
Thompson, R. C. A. (2008). The taxonomy, phylogeny and transmission of Echinococcus. Experimental Parasitology 119, 439–446.Google Scholar
Thompson, R. C. A., Boxell, A. C., Ralston, B. J., Constantine, C. C., Hobbs, R. P., Shury, T. and Olson, M. E. (2006). Molecular and morphological characterization of Echinococcus in cervids from North America. Parasitology 132, 439–447.CrossRefGoogle ScholarPubMed
Thompson, R. C. A., Kumaratilake, L. M. and Eckert, J. (1984). Observations on Echinococcus granulosus of cattle origin in Switzerland. International Journal for Parasitology 14, 283–291.CrossRefGoogle ScholarPubMed
Thompson, R. C. A., Lymbery, A. J. and Constantine, C. C. (1995). Variation in Echinococcus: towards a taxonomic revision of the genus. Advances in Parasitology 35, 145–176.CrossRefGoogle ScholarPubMed
Thompson, R. C. A. and McManus, D. P. (2001). Aetiology: parasites and life cycles. In Manual on Echinococcus in Humans and Animals a Public Health Problem of Global Concern (ed. Eckert, J., Gemmell, M. A., Meslin, F.-X. and Pawlowski, Z. S.), pp. 1–19. WHO/OIE, Paris. World Health Organization, Geneva, Switzerland.Google Scholar
Thompson, R. C. A. and McManus, D. P. (2002). Towards a taxonomic revision of the genus Echinococcus. Trends in Parasitology 18, 452–457.CrossRefGoogle ScholarPubMed
Utuk, A. E., Simsek, S., Koroglu, E. and McManus, D. P. (2008). Molecular genetic characterization of different isolates of Echinococcus granulosus in East and Southeast regions of Turkey. Acta Tropica 107, 192–194.CrossRefGoogle Scholar
Varcasia, A., Canu, S., Kogkos, A., Pipia, A. P., Scala, A., Garippa, G. and Seimenis, A. (2007). Molecular characterization of Echinococcus granulosus in sheep and goats of Peloponnesus, Greece. Parasitology Research 101, 1135–1139.CrossRefGoogle ScholarPubMed
Varcasia, A., Canu, S., Lightowlers, M. W., Scala, A. and Garippa, G. (2006). Molecular characterization of Echinococcus granulosus strains in Sardinia. Parasitology Research 98, 273–277.CrossRefGoogle ScholarPubMed
Varcasia, A., Garippa, G., Pipia, A. P., Scala, A., Brianti, E., Giannetto, S., Battelli, G., Poglayen, G. and Micagni, G. (2008). Cystic echinococcosis in equids in Italy. Parasitology Research 102, 815–818.CrossRefGoogle ScholarPubMed
Williams, R. J. and Sweatman, G. K. (1963). On the transmission, biology and morphology of Echinococcus granulosus equinus, a new subspecies of hydatid tapeworm in horses in Great Britain. Parasitology 53, 391–407.Google Scholar
Xiao, N., Qiu, J., Nakao, M., Li, T., Yang, W., Chen, X., Schantz, P. M., Craig, P. S. and Ito, A. (2005). Echinococcus shiquicus n. sp., a taeniid cestode from Tibetan fox and plateau pika in China. International Journal for Parasitology 35, 693–701.CrossRefGoogle Scholar