Phylogenetic characterisation of Taenia tapeworms in spotted hyenas and reconsideration of the ‘‘Out of Africa’’ hypothesis of Taenia in humans q Yitagele Terefe a,1 , Zerihun Hailemariam a,1 , Sissay Menkir b,1 , Minoru Nakao c,⇑ , Antti Lavikainen d , Voitto Haukisalmi e , Takashi Iwaki f , Munehiro Okamoto g , Akira Ito c a College of Veterinary Medicine, Haramaya University, P.O. Box 281, Dire Dawa, Ethiopia b Department of Biology, Haramaya University, P.O. Box 138, Dire Dawa, Ethiopia c Department of Parasitology, Asahikawa Medical University, Asahikawa, Hokkaido 078-8510, Japan d Immunobiology Program/Department of Bacteriology and Immunology, Haartman Institute, P.O. Box 21, FI-00014 University of Helsinki, Finland e Finnish Museum of Natural History, P.O. Box 17, FI-00014 University of Helsinki, Finland f 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 article info Article history: Received 3 February 2014 Received in revised form 25 March 2014 Accepted 27 March 2014 Available online xxxx Keywords: Taenia Spotted hyena Crocuta crocuta Ethiopia Molecular systematics 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 sam- ples into four mitochondrial lineages designated as I–IV. DNA profiles of nuclear genes for DNA polymer- ase 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 lin- eages 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 recon- structed by the maximum likelihood method using all protein-coding genes of their mitochondrial gen- omes. 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. Ó 2014 Australian Society for Parasitology Inc. Published by Elsevier Ltd. All rights reserved. 1. Introduction Sub-Saharan Africa is a key region when considering the origin of modern humans (Homo sapiens Linnaeus, 1758) and their dispersal into new areas of the world, which are referred to as the ‘‘Out of Africa’’ hypothesis (Cann et al., 1987; Stringer and Andrews, 1988). During the evolution of hominins in Africa, their change from herbivory to carnivory could have been a driver to promote the host-switching of intestinal parasites from carnivores to early humans (extinct members of the genus Homo), particularly in tapeworms of the genus Taenia (Hoberg et al., 2001). Predator–prey relationships of mammals maintain the life cycle of Taenia. The adult tapeworms inhabit the small intestine of definitive hosts, and their proglottids with eggs are released into http://dx.doi.org/10.1016/j.ijpara.2014.03.013 0020-7519/Ó 2014 Australian Society for Parasitology Inc. Published by Elsevier Ltd. All rights reserved. q Nucleotide sequence data reported in this paper are available in DDBJ/EMBL/ GenBank databases under the accession numbers AB905198–AB905203 and AB905332–AB905359. ⇑ Corresponding author. Tel.: +81 166682422; fax: +81 166682429. E-mail address: nakao@asahikawa-med.ac.jp (M. Nakao). 1 These authors contributed equally to this work. International Journal for Parasitology xxx (2014) xxx–xxx Contents lists available at ScienceDirect International Journal for Parasitology journal homepage: www.elsevier.com/locate/ijpara Please cite this article in press as: Terefe, Y., et al. Phylogenetic characterisation of Taenia tapeworms in spotted hyenas and reconsideration of the ‘‘Out of Africa’’ hypothesis of Taenia in humans. Int. J. Parasitol. (2014), http://dx.doi.org/10.1016/j.ijpara.2014.03.013