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Molecular phylogeny of anoplocephalid tapeworms (Cestoda: Anoplocephalidae) infecting humans and non-human primates

Published online by Cambridge University Press:  05 June 2015

JANA DOLEŽALOVÁ*
Affiliation:
Department of Physiology, Faculty of Veterinary Medicine, University of Veterinary and Pharmaceutical Sciences, Palackého tř.1/3, 612 00 Brno, Czech Republic Department of Pathology and Parasitology, Faculty of Veterinary Medicine, University of Veterinary and Pharmaceutical Sciences, Palackého tř.1/3, 612 00 Brno, Czech Republic CEITEC – Central European Institute of Technology, University of Veterinary and Pharmaceutical Sciences, Palackého tř.1/3, 612 00 Brno, Czech Republic
PETER VALLO
Affiliation:
Department of Pathology and Parasitology, Faculty of Veterinary Medicine, University of Veterinary and Pharmaceutical Sciences, Palackého tř.1/3, 612 00 Brno, Czech Republic Institute of Vertebrate Biology, ASCR, v.v.i., Květná 8, 603 65 Brno, Czech Republic
KLÁRA J. PETRŽELKOVÁ
Affiliation:
Department of Pathology and Parasitology, Faculty of Veterinary Medicine, University of Veterinary and Pharmaceutical Sciences, Palackého tř.1/3, 612 00 Brno, Czech Republic Institute of Vertebrate Biology, ASCR, v.v.i., Květná 8, 603 65 Brno, Czech Republic Institute of Parasitology, Biology Centre, Czech Academy of Sciences, 370 05 České Budějovice, Czech Republic Liberec Zoo, Liberec, Masarykova 1347/31, 460 01 Liberec, Czech Republic
IVONA FOITOVÁ
Affiliation:
Department of Botany and Zoology, Faculty of Science, Masaryk University, Kotlářská 267/2, 611 37 Brno, Czech Republic
WISNU NURCAHYO
Affiliation:
Department of Parasitology, Faculty of Veterinary Medicine, Gadjah Mada University, Yogyakarta, Indonesia
ANTOINE MUDAKIKWA
Affiliation:
Rwanda Development Board, Gishushu, Nyarutarama Road, P.O. Box 6239 Kigali, Rwanda
CHIE HASHIMOTO
Affiliation:
Primate Research Institute, Kyoto University, Inuyama, Aichi 484-8506, Japan
MILAN JIRKŮ
Affiliation:
Institute of Parasitology, Biology Centre, Czech Academy of Sciences, 370 05 České Budějovice, Czech Republic
JULIUS LUKEŠ
Affiliation:
Institute of Parasitology, Biology Centre, Czech Academy of Sciences, 370 05 České Budějovice, Czech Republic Faculty of Science, University of South Bohemia, Branišovská 31, 370 05 České Budějovice, Czech Republic Canadian Institute for Advanced Research, Toronto, Ontario M5 G 1Z8, Canada
TOMÁŠ SCHOLZ
Affiliation:
Institute of Parasitology, Biology Centre, Czech Academy of Sciences, 370 05 České Budějovice, Czech Republic Faculty of Science, University of South Bohemia, Branišovská 31, 370 05 České Budějovice, Czech Republic
DAVID MODRÝ
Affiliation:
Department of Pathology and Parasitology, Faculty of Veterinary Medicine, University of Veterinary and Pharmaceutical Sciences, Palackého tř.1/3, 612 00 Brno, Czech Republic CEITEC – Central European Institute of Technology, University of Veterinary and Pharmaceutical Sciences, Palackého tř.1/3, 612 00 Brno, Czech Republic Institute of Parasitology, Biology Centre, Czech Academy of Sciences, 370 05 České Budějovice, Czech Republic
*
*Corresponding author. Department of Physiology, Faculty of Veterinary Medicine, University of Veterinary and Pharmaceutical Sciences, Palackého tř.1/3, 612 00 Brno, Czech Republic. E-mail: petrasovaj@atlas.cz

Summary

Anoplocephalid tapeworms of the genus Bertiella Stiles and Hassall, 1902 and Anoplocephala Blanchard, 1848, found in the Asian, African and American non-human primates are presumed to sporadic ape-to-man transmissions. Variable nuclear (5.8S-ITS2; 28S rRNA) and mitochondrial genes (cox1; nad1) of isolates of anoplocephalids originating from different primates (Callicebus oenanthe, Gorilla beringei, Gorilla gorilla, Pan troglodytes and Pongo abelii) and humans from various regions (South America, Africa, South-East Asia) were sequenced. In most analyses, Bertiella formed a monophyletic group within the subfamily Anoplocephalinae, however, the 28S rRNA sequence-based analysis indicated paraphyletic relationship between Bertiella from primates and Australian marsupials and rodents, which should thus be regarded as different taxa. Moreover, isolate determined as Anoplocephala cf. gorillae from mountain gorilla clustered within the Bertiella clade from primates. This either indicates that A. gorillae deserves to be included into the genus Bertiella, or, that an unknown Bertiella species infects also mountain gorillas. The analyses allowed the genetic differentiation of the isolates, albeit with no obvious geographical or host-related patterns. The unexpected genetic diversity of the isolates studied suggests the existence of several Bertiella species in primates and human and calls for revision of the whole group, based both on molecular and morphological data.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2015 

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References

REFERENCES

Baer, J. G. (1953). Notes de faunistique éburnéenne. IV. Bertiella douceti n. sp. Cestode nouveau de l'anomalure de Pel. Acta Tropica 10, 7982.Google Scholar
Beveridge, I. (1985). The genus Bertiella (Cestoda: Anoplocephalidae) from Australasian mammals: new species, new records and redescriptions. Systematic Parasitology 7, 241289.Google Scholar
Beveridge, I. (1989). Species of Bertiella (Cestoda: Anoplocephalidae) in dermopterans and squirrels from South-East Asia. Systematic Parasitology 14, 115.CrossRefGoogle Scholar
Beveridge, I. (1994). Family anoplocephalidae cholodkovsky, 1902. In Keys to the Cestode Parasites of Vertebrates (ed. Khalil, L. F., Jones, A. and Bray, R. A.), pp. 315366. Commonwealth Agricultural Bureaux International, Wallingford.Google Scholar
Bhagwant, S. (2004). Human Bertiella studeri (family Anoplocephalidae) infection of probable Southeast Asian origin in Mauritian children and an adult. American Journal of Tropical Medicine and Hygiene 70, 225228.Google Scholar
Blanchard, R. (1891). Sur les helminthes des primates antropoides. Memoires de la Société de Zoologique de France 4, 186196.Google Scholar
Bouzid, W., Štefka, J., Hypša, V., Lek, S., Scholz, T., Legal, L., Ben Hassine, O. K. and Loot, G. (2008). Geography and host specificity: two forces behind the genetic structure of the freshwater fish parasite Ligula intestinalis (Cestoda: Diphyllobothriidae). International Journal for Parasitology 38, 14651479.Google Scholar
Caira, J. N., Jensen, K. and Barbeau, E. (2012). Global Cestode Database. World Wide Web electronic publication. http://tapewormdb.uconn.edu/.Google Scholar
Cameron, T. W. M. (1929). A new record of the occurrence of a tapeworm of the genus Bertiella in man. Journal of Helminthology 7, 231234.Google Scholar
Chandler, A. C. (1925). New records of Bertiella satyri (Cestoda) in man and apes. Parasitology 17, 421425.Google Scholar
Denegri, G. M. and Perez-Serrano, J. (1997). Bertiellosis in man: a review of cases. Revista do Instituto de Medicina Tropical de São Paulo 39, 123127.CrossRefGoogle Scholar
Dunn, F. L. (1963). Acanthocephalans and cestodes of South American monkeys and marmosets. Journal of Parasitology 49, 717722.Google Scholar
Eilenberger, U. (1998). Der Einfluß von individuellen, gruppenspezifischen und ökologischen Faktoren auf den Endoparasitenstatus von wildlebenden östlichen Flachlandgorillas (Gorilla gorilla graueri) im Kahuzi-Biega Nationalpark von Zaire. Ein multidisziplinärer Ansatz. Doctoral thesis. Freie Universität Berlin, Berlin, Germany. http://www.diss.fu-berlin.de/diss/receive/FUDISS_thesis_000000000016.Google Scholar
El-Dib, N. A., Al-Rufaii, A., El-Badry, A. A., Al-Zoheiry, A. A. and El-Aall, A. A. (2004). Human infection with Bertiella species in Saudi Arabia. Saudi Pharmaceutical Journal 12, 168169.Google Scholar
El-Sherry, S., Ogedengbe, M. E., Hafeez, M. A. and Barta, J. R. (2013). Divergent nuclear 18S rDNA paralogs in a turkey coccidium, Eimeria meleagrimitis, complicate molecular systematics and identification. International Journal for Parasitology 43, 679685.CrossRefGoogle Scholar
Fiennes, R. (1967). Zoonoses of Primates: The Epidemiology and Ecology of Simian Diseases in Relation to Man. Weidenfeld and Nicolson, London.Google Scholar
Foitová, I., Mašová, S., Tenora, F., Koubková, B., Hodová, I., Vyskočilová, M., Baruš, V. and Nurcahyo, W. (2011). Redescription and resurrection of Bertiella satyri (Cestoda, Anoplocephalidae) parasitizing the orangutan (Pongo abelii) in Indonesia. Parasitology Research 109, 689697.Google Scholar
Furtado, A. P., Batista Ede, J., Gonçalves, E. C., Silva, A. M., Melo, F. T., Giese, E. G. and Santos, J. N. (2012). Human bertielliasis in Amazonia: case report and challenging diagnosis. PLoS Neglected Tropical Diseases 6, e1580.Google Scholar
Galán-Puchades, M. T., Fuentes, M. V. and Mas-Coma, S. (2000). Morphology of Bertiella studeri (Blanchard, 1891) sensu Stunkard (1940) (Cestoda: Anoplocephalidae) of human origin and a proposal of criteria for the specific diagnosis of bertiellosis. Folia Parasitologica 47, 2328.CrossRefGoogle Scholar
Gómez-Puerta, L. A., López-Urbina, M. T. and González, A. E. (2009). Occurrence of tapeworm Bertiella mucronata (Cestoda: Anoplocephalidae) in the Titi monkey Callicebus oenanthe from Peru: a new definitive host and geographical record. Veterinary Parasitology 163, 161163.Google Scholar
Griffin, P. C., Robin, C. and Hoffmann, A. A. (2011). A next-generation sequencing method for overcoming the multiple gene copy problem in polyploid phylogenetics, applied to Poa grasses. BMC Biology 9, 19.Google Scholar
Hall, T. A. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 9598.Google Scholar
Hardman, L. M., Haukisalmi, V. and Beveridge, I. (2012). Phylogenetic relationships of the anoplocephaline cestodes of Australasian marsupials and resurrection of the genus Wallabicestus Schmidt, 1975. Systematic Parasitology 82, 4963.Google Scholar
Haukisalmi, V., Wickström, L. M., Henttonen, H., Hantula, J. and Gubányi, A. (2004). Molecular and morphological evidence for multiple species within Paranoplocephala omphalodes (Cestoda, Anoplocephalidae) in Microtus voles (Arvicolinae). Zoologica Scripta 33, 277290.Google Scholar
Haukisalmi, V., Hardman, L. M., Hardman, M., Laakkonen, J., Niemimaa, J. and Henttonen, H. (2007). Morphological and molecular characterisation of Paranoplocephala buryatiensis n. sp. and P. longivaginata Chechulin & Gulyaev, 1998 (Cestoda: Anoplocephalidae) in voles of the genus Clethrionomys . Systematic Parasitology 66, 5571.Google Scholar
Haukisalmi, V., Hardman, L. M., Foronda, P., Feliu, C. and Henttonen, H. (2010). Systematic relationships of Mosgovoyia Spasskii, 1951 (Cestoda: Anoplocephalidae) and related genera inferred from mitochondrial and nuclear sequence data. Systematic Parasitology 77, 7179.Google Scholar
Králová-Hromadová, I., Štefka, J., Špakulová, M., Orosová, M., Bombarová, M., Hanzelová, V., Bazsalovicsová, E. and Scholz, T. (2010). Intra-individual internal transcribed spacer 1 (ITS1) and ITS2 ribosomal sequence variation linked with multiple rDNA loci: a case of triploid Atractolytocestus huronensis, the monozoic cestode of common carp. International Journal for Parasitology 40, 175181.Google Scholar
Landsoud-Soukate, J., Tutin, C. E. and Fernandez, M. (1995). Intestinal parasites of sympatric gorillas and chimpanzees in the Lopé Reserve, Gabon. Annals of Tropical Medicine and Parasitology 89, 7379.Google Scholar
Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P. A., McWilliam, H., Valentin, F., Wallace, I. M., Wilm, A., Lopez, R., Thompson, J. D., Gibson, T. J. and Higgins, D. G. (2007). Clustal W and Clustal X version 2.0. Bioinformatics 23, 29472948.Google Scholar
Lilly, A. A., Mehlman, P. T. and Doran, D. (2002). Intestinal parasites in gorillas, chimpanzees, and humans at Mondika Research Site, Dzanga-Ndoki National Park, Central African Republic. International Journal of Primatology 23, 555573.Google Scholar
Littlewood, D. T. J., Waeschenbach, A. and Nikolov, P. N. (2008). In search of mitochondrial markers for resolving the phylogeny of cyclophyllidean tapeworms (Platyhelminthes, Cestoda) – a test study with Davaineidae. Acta Parasitologica 53, 133144.CrossRefGoogle Scholar
Lockyer, A. E., Olson, P. D. and Littlewood, D. T. J. (2003). Utility of complete large and small subunit rRNA genes in resolving the phylogeny of the Neodermata (Platyhelminthes): implications and a review of the cercomer theory. Biological Journal of the Linnean Society 78, 155171.Google Scholar
Meyner, R. (1895). Anatomie und Histologie zweier neuer Taenien. Arten des subgenus Bertia; Taenia (Bertia) mucronata n. sp. und Taenia (Bertia) conferta n. sp. Ein Beitrag zur Kenntniss der Cestoden. Doctoral thesis. Leipzig.Google Scholar
Nybelin, O. (1927). Anoplocephala gorillae n. sp. Arkiv Zoologie 19B, 13.Google Scholar
Nylander, J. A. A. (2004). MrModeltest v2. Program distributed by the author. Evolutionary Biology Centre, Uppsala University.Google Scholar
Ronquist, F. and Huelsenbeck, J. P. (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 15721574.Google Scholar
Rothman, J. M., Pell, A. N. and Bowman, D. D. (2008). Host-parasite ecology of the helminths in mountain gorillas. Journal of Parasitology 94, 834840.Google Scholar
, R. M., Petrášová, J., Pomajbíková, K., Profousová, I., Petrželková, K. J., Sousa, C., Cable, J., Bruford, M. W. and Modrý, D. (2013). Gastrointestinal symbionts of chimpanzees in Cantanhez National Park, Guinea-Bissau with respect to habitat fragmentation. American Journal of Primatology 75, 10321041.Google Scholar
Schmidt, G. D. (1986). CRC Handbook of Tapeworm Identification. CRC Press, Boca Raton, FL.Google Scholar
Sheather, A. L. (1923). The detection of intestinal protozoa and mange parasites by a flotation technique. Journal of Comparative Pathology 36, 266275.Google Scholar
Škeříková, A., Hypša, V. and Scholz, T. (2004). A paraphyly of the genus Bothriocephalus Rudolphi, 1808 (Cestoda: Pseudophyllidea) inferred from internal transcribed spacer-2 and 18S ribosomal DNA sequences. Journal of Parasitology 90, 612617.Google Scholar
Sleeman, J. M., Meader, L. L., Mudakikwa, A. B., Foster, J. W. and Patton, S. (2000). Gastrointestinal parasites of mountain gorillas (Gorilla gorilla beringei) in the Parc National des Volcans, Rwanda. Journal of Zoo and Wildlife Medicine 31, 322328.Google Scholar
Sun, X., Fang, Q., Chen, X. Z., Hu, S. F., Xia, H. and Wang, X. M. (2006). Bertiella studeri infection, China. Emerging Infectious Diseases 12, 176177.CrossRefGoogle ScholarPubMed
Taleb-Hossenkhan, N. and Bhagwant, S. (2012). Molecular characterization of the parasitic tapeworm Bertiella studeri from the island of Mauritius. Parasitology Research 110, 759768.CrossRefGoogle ScholarPubMed
Waeschenbach, A., Webster, B. L., Bray, R. A. and Littlewood, D. T. J. (2007). Added resolution among ordinal level relationships of tapeworms (Platyhelminthes: Cestoda) with complete small and large subunit nuclear ribosomal RNA genes. Molecular Phylogenetics and Evolution 45, 311325.Google Scholar
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