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A Molecular Phylogeny of the Genus Echinococcus Inferred from Complete Mitochondrial Genomes

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A Molecular Phylogeny of the Genus Echinococcus Inferred from Complete Mitochondrial Genomes 713 A molecular phylogeny of the genus Echinococcus inferred from complete mitochondrial genomes M. NAKAO1*, D. P. MCMANUS2,P.M.SCHANTZ3,P.S.CRAIG4 and A. ITO1 1 Department of Parasitology, Asahikawa Medical College, Asahikawa, Hokkaido 078-8510, Japan 2 Molecular Parasitology Laboratory, The Queensland Institute of Medical Research and the University of Queensland, Brisbane, Queensland 4029, Australia 3 Division of Parasitic Diseases, National Centers for Infectious Diseases, Centers for Disease Control and Prevention, Atlanta, GA 30341, USA 4 Cestode Zoonoses Research Group, Bioscience Research Institute and School of Environment and Life Sciences, University of Salford, Great Manchester M5 4WT, UK (Received 21 August 2006; revised 2 October 2006; accepted 3 October 2006; first published online 11 December 2006) SUMMARY Taxonomic revision by molecular phylogeny is needed to categorize members of the genus Echinococcus (Cestoda: Taeniidae). We have reconstructed the phylogenetic relationships of E. oligarthrus, E. vogeli, E. multilocularis, E. shiquicus, E. equinus, E. ortleppi, E. granulosus sensu stricto and 3 genotypes of E. granulosus sensu lato (G6, G7 and G8) from their complete mitochondrial genomes. Maximum likelihood and partitioned Bayesian analyses using concatenated data sets of nucleotide and amino acid sequences depicted phylogenetic trees with the same topology. The 3 E. granulosus genotypes corresponding to the camel, pig, and cervid strains were monophyletic, and their high level of genetic similarity supported taxonomic species unification of these genotypes into E. canadensis. Sister species relationships were confirmed between E. ortleppi and E. canadensis, and between E. multilocularis and E. shiquicus, regardless of the analytical approach employed. The basal positions of the phylogenetic tree were occupied by the neotropical endemic species, E. oligarthrus and E. vogeli, whose definitive hosts are derived from carnivores that immigrated from North America after the formation of the Panamanian land bridge. Host-parasite co-evolution comparisons suggest that the ancestral homeland of Echinococcus was North America or Asia, depending on whether the ancestral definitive hosts were canids or felids. Key words: Echinococcus, mitochondrial genome, phylogeny, taxonomic revision. INTRODUCTION stage. The self-fertilization of the adults and the clonal amplification of the larvae are responsible for Cestodes of the family Taeniidae are parasitic in genetic monomorphism within isolated Echinococcus mammals and are placed within either of 2 genera, populations (Lymbery and Thompson, 1996; Haag Taenia and Echinococcus (Hoberg et al. 2000; Kum- et al. 1999), and may lead, eventually, to the specia- aratilake and Thompson, 1982). The adult tape- tion of Echinococcus (Smyth and Smyth, 1964). worms live in the digestive tract of their definitive The classification of Echinococcus has been con- hosts, while the bladder-like larvae occur in the troversial because of the paucity of phenotypic internal organs of intermediate hosts. The predator- characters and inadequate taxonomic descriptions. prey relationships of the mammalian hosts perpetu- In taxonomic terms, many species and subspecies ate the life-cycle of the taeniid cestodes. The tiny of Echinococcus were originally described, based adult tapeworms of the genus Echinococcus utilize mainly on host-parasite specificity characteristics canids and/or felids as definitive hosts, and their (Ortlepp, 1937; Lopez-Neyra and Soler Planas, larvae develop into hydatid cysts in intermediate 1943; Williams and Sweatman, 1963; Verster, 1965). hosts including ungulates, rodents and humans. The However, most of these taxa were regarded as 2 main species, E. granulosus and E. multilocularis, synonyms for E. granulosus (Rausch, 1967), and the cause cystic and alveolar echinococcosis in humans, subsequent reclassification permitted only 4 mor- respectively. The organisms of Echinococcus have a phospecies, namely E. granulosus, E. multilocularis, biphasic propagation manner comprising a sexual E. oligarthrus and E. vogeli (Rausch and Bernstein, reproductive phase in the hermaphroditic adults and 1972). The biological variants of E. granulosus, an asexual proliferation of protoscoleces in the larval which utilize particular ungulates as intermediate hosts, have been designated as strains (Thompson et al. 1995). Molecular genetic studies, using mainly * Corresponding author: Department of Parasitology, Asahikawa Medical College, Asahikawa, Hokkaido 078- mitochondrial DNA (mtDNA) sequences, supported 8510, Japan. Tel: +81 166 68 2422. Fax: +81 166 68 2429. the strain definition and identified 10 genotypes (G1 E-mail: [email protected] to G10) within E. granulosus (Bowles et al. 1994, Parasitology (2007), 134, 713–722. f 2006 Cambridge University Press doi:10.1017/S0031182006001934 Printed in the United Kingdom Downloaded from https:/www.cambridge.org/core. Open University Library, on 08 Feb 2017 at 12:45:16, subject to the Cambridge Core terms of use, available at https:/www.cambridge.org/core/terms. https://doi.org/10.1017/S0031182006001934 M. Nakao and others 714 Table 1. Mitochondrial genomes of Echinococcus and Taenia tapeworms analysed in this study Nucleotide compositions of sense strand Database Species bp in total accession (genotype) length %A %G %T %C no. References E. oligarthrus 13,791 20.823.348.57.4 AB208545 This study E. vogeli 13,750 18.925.348.27.6 AB208546 This study E. granulosus (G1) 13,588 19.225.047.98.0 AF297617 Le et al. (2002) E. equinus (G4) 13,598 19.924.348.07.7 AF346403 Le et al. (2002) E. ortleppi (G5) 13,717 19.623.948.28.3 AB235846 This study E. sp. (G6) 13,721 19.524.148.18.3 AB208063 This study E. sp. (G7) 13,719 19.524.148.28.2 AB235847 This study E. sp. (G8) 13,717 19.524.248.28.2 AB235848 This study E. multilocularis 13,738 20.623.448.57.6 AB018440 Nakao et al. (2002b) E. shiquicus 13,807 20.124.148.37.5 AB208064 This study T. solium 13,709 25.419.746.78.3 AB086256 Nakao et al. (2003) 1995; Scott et al. 1997; Lavikainen et al. 2003). The published sequences were available for mitochon- taxonomic revision of Echinococcus is now required to drial genomes of E. granulosus sensu stricto, E. determine the status of sibling or cryptic species. To equinus, E. multilocularis and T. solium (Le et al. 2002; date, reviving the names of synonyms, the over- Nakao et al. 2002b, 2003). In addition, complete simplified E. granulosus has been split into E. gran- mtDNA sequences were obtained for larval isolates ulosus sensu stricto (genotypes G1 to G3), E. equinus of E. oligarthrus (Panama), E. vogeli (Colombia), (G4) and E. ortleppi (G5), but the species status of E. shiquicus (Tibet), E. ortleppi (Argentina), E. granu- genotypes G6 to G10 is still ambiguous (Thompson losus genotype G6 (Kazakhstan), E. granulosus geno- and McManus, 2003). Most recently, a new sibling type G7 (Poland) and E. granulosus genotype G8 species, E. shiquicus, whose adult is morphologically (USA). Previous studies (Bowles et al. 1995; Lavi- similar to E. multilocularis, has been found in Tibet kainen et al. 2003) indicate that the taxa of Echino- (Xiao et al. 2005). coccus examined in this study cover a range of major Mitochondrial DNA (mtDNA) has more power sequence variation in mtDNA within the genus. than nuclear DNA in reconstructing phylogenetic relationships among closely related species because of the rapid sequence evolution (Brown et al. 1979), DNA sequencing and large data sets derived from mitochondrial Genomic DNA purified from each of the Echino- genomes have the potential for resolving problem- coccus isolates was used as a template for the poly- atic issues in taxonomy (Mueller et al. 2004). In this merase chain reaction (PCR). As reported previously study, the phylogeny of the genus Echinococcus was (Nakao et al. 2003), DNA fragments (0.7–2.5 kb) clarified by using the complete mitochondrial geno- covering complete mitochondrial genomes were mes of representative taxa in order to improve the amplified by PCR, and their DNA sequences were consistency between species status and traditional compiled into a total sequence. In brief, the initial nomenclatures. The concatenated data sets of nu- amplification of mtDNA was carried out using pri- cleotide and amino acid sequences derived from all mers designed from the conserved regions of mitochondrial genes were analysed with an array of E. multilocularis mtDNA (Nakao et al. 2002b). The phylogenetic methods including maximum likeli- sequences of these amplicons allowed us to design hood and partitioned Bayesian analyses. In particu- additional primers, whereby the remaining unknown lar, the latter is the only method that can be used to regions were amplified. The cycle sequencing kits, analyse a large data set by incorporating complex DYEnamic ET terminator (Amersham Biosciences) substitution models into the statistical process and BigDye terminator (Applied Biosystems), were (Ronquist and Huelsenbeck, 2003; Nylander et al. used for the direct sequencing of PCR products. 2004). Also, the ancestral origin of Echinococcus was After each sequencing reaction, synthesized ladders inferred, based on the phylogeny of Echinococcus and were run on an ABI PRISM 377 genetic analyser the evolutionary history of mammalian host animals. (Applied Biosystems). Large DNA templates were sequenced by primer walking. MATERIALS AND METHODS Taxon sampling Data processing Ten taxa of Echinococcus and 1 outgroup (Taenia Mitochondrial genomes were annotated as
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