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Phylogenetic characterisation of Taenia tapeworms in spotted hyenas and reconsideration of the “Out of Africa” hypothesis of Taenia in humans
Authors:Yitagele Terefe  Zerihun Hailemariam  Sissay Menkir  Minoru Nakao  Antti Lavikainen  Voitto Haukisalmi  Takashi Iwaki  Munehiro Okamoto  Akira Ito
Institution:1. College of Veterinary Medicine, Haramaya University, P.O. Box 281, Dire Dawa, Ethiopia;2. Department of Biology, Haramaya University, P.O. Box 138, Dire Dawa, Ethiopia;3. Department of Parasitology, Asahikawa Medical University, Asahikawa, Hokkaido 078-8510, Japan;4. Immunobiology Program/Department of Bacteriology and Immunology, Haartman Institute, P.O. Box 21, FI-00014 University of Helsinki, Finland;5. Finnish Museum of Natural History, P.O. Box 17, FI-00014 University of Helsinki, Finland;6. Meguro Parasitological Museum, Shimomeguro, Meguro-ku, Tokyo 153-0064, Japan;g Section of Wildlife Diversity, Center for Human Evolution Modeling Research, Primate Research Institute, Kyoto University, Inuyama, Aichi 484-8506, Japan
Abstract:The African origin of hominins suggests that Taenia spp. in African carnivores are evolutionarily related to the human-infecting tapeworms Taenia solium, Taenia saginata and Taenia asiatica. Nevertheless, the hypothesis has not been verified through molecular phylogenetics of Taenia. This study aimed to perform phylogenetic comparisons between Taenia spp. from African hyenas and the congeneric human parasites. During 2010–2013, 233 adult specimens of Taenia spp. were collected from 11 spotted hyenas in Ethiopia. A screening based on short DNA sequences of the cytochrome c oxidase subunit 1 gene classified the samples into four mitochondrial lineages designated as I–IV. DNA profiles of nuclear genes for DNA polymerase delta (pold) and phosphoenolpyruvate carboxykinase (pepck) showed that lineages II and III can be assigned as two independent species. Common haplotypes of pold and pepck were frequently found in lineages I and IV, suggesting that they constitute a single species. Morphological observations suggested that lineage II is Taenia crocutae, but the other lineages were morphologically inconsistent with known species, suggesting the involvement of two new species. A phylogenetic tree of Taenia spp. was reconstructed by the maximum likelihood method using all protein-coding genes of their mitochondrial genomes. The tree clearly demonstrated that T. crocutae is sister to T. saginata and T. asiatica, whereas T. solium was confirmed to be sister to the brown bear tapeworm, Taenia arctos. The tree also suggested that T. solium and T. arctos are related to two species of Taenia in hyenas, corresponding to lineages I + IV and III. These results may partially support the African origin of human-infecting Taenia spp., but there remains a possibility that host switching of Taenia to hominins was not confined to Africa. Additional taxa from African carnivores are needed for further testing of the “Out of Africa” hypothesis of Taenia in humans.
Keywords:Taenia  Spotted hyena  Crocuta crocuta  Ethiopia  Molecular systematics
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