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Molecular Phylogeny of Anoplocephalid Tapeworms (Cestoda: Anoplocephalidae) Infecting Humans and Non-Human Primates

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Molecular Phylogeny of Anoplocephalid Tapeworms (Cestoda: Anoplocephalidae) Infecting Humans and Non-Human Primates 1278 Molecular phylogeny of anoplocephalid tapeworms (Cestoda: Anoplocephalidae) infecting humans and non-human primates JANA DOLEŽALOVÁ1,2,3*, PETER VALLO2,4, KLÁRA J. PETRŽELKOVÁ2,4,5,6,IVONAFOITOVÁ7, WISNU NURCAHYO8, ANTOINE MUDAKIKWA9, CHIE HASHIMOTO10, MILAN JIRKŮ5, JULIUS LUKEŠ5,11,12, TOMÁŠ SCHOLZ5,11 and DAVID MODRÝ2,3,5 1 Department of Physiology, Faculty of Veterinary Medicine, University of Veterinary and Pharmaceutical Sciences, Palackého tř.1/3, 612 00 Brno, Czech Republic 2 Department of Pathology and Parasitology, Faculty of Veterinary Medicine, University of Veterinary and Pharmaceutical Sciences, Palackého tř.1/3, 612 00 Brno, Czech Republic 3 CEITEC – Central European Institute of Technology, University of Veterinary and Pharmaceutical Sciences, Palackého tř.1/3, 612 00 Brno, Czech Republic 4 Institute of Vertebrate Biology, ASCR, v.v.i., Květná 8, 603 65 Brno, Czech Republic 5 Institute of Parasitology, Biology Centre, Czech Academy of Sciences, 370 05 České Budějovice, Czech Republic 6 Liberec Zoo, Liberec, Masarykova 1347/31, 460 01 Liberec, Czech Republic 7 Department of Botany and Zoology, Faculty of Science, Masaryk University, Kotlářská 267/2, 611 37 Brno, Czech Republic 8 Department of Parasitology, Faculty of Veterinary Medicine, Gadjah Mada University, Yogyakarta, Indonesia 9 Rwanda Development Board, Gishushu, Nyarutarama Road, P.O. Box 6239 Kigali, Rwanda 10 Primate Research Institute, Kyoto University, Inuyama, Aichi 484-8506, Japan 11 Faculty of Science, University of South Bohemia, Branišovská 31, 370 05 České Budějovice, Czech Republic 12 Canadian Institute for Advanced Research, Toronto, Ontario M5 G 1Z8, Canada (Received 24 October 2014; revised 26 March 2015; accepted 21 April 2015; first published online 5 June 2015) 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 differentia- tion 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. Key words: Bertiella, Anoplocephala, phylogeny, primates, zoonotic potential. INTRODUCTION components of parasite communities. However, oc- casional infections by representatives of the subfam- The adult stages of tapeworms of the cyclophylli- ilies Linstowiinae (Mathevotaenia Akhumian, 1946) dean family Anoplocephalidae Cholodkovsky, and Inermicapsiferinae (Thysanotaenia Beddard, 1902, are intestinal parasites of mammals, birds 1911) have also been reported (Beveridge, 1994). and reptiles (Beveridge, 1994). In primates, several Although the genus Anoplocephala mostly includes species of the subfamily Anoplocephalinae mostly species from hyraxes, odd-toed ungulates and ele- from the genera Anoplocephala, Bertiella and phants, Anoplocephala gorillae Nybelin, 1927, was Moniezia Blanchard, 1891, represent typical described from eastern gorillas (Gorilla beringei) and is considered to be a common parasite in the * Corresponding author. Department of Physiology, Rwandan and Ugandan mountain gorilla popula- Faculty of Veterinary Medicine, University of Veterinary and Pharmaceutical Sciences, Palackého tions (Sleeman et al. 2000; Rothman et al. 2008). tř.1/3, 612 00 Brno, Czech Republic. E-mail: petrasovaj@ In contrast, almost no cestodes have been found in atlas.cz western gorillas (Gorilla gorilla) of Gabon Parasitology (2015), 142, 1278–1289. © Cambridge University Press 2015 doi:10.1017/S003118201500058X Diversity of anoplocephalid tapeworms in primates 1279 Fig. 1. The phylogenetic trees of anoplocephaline cestodes: (A) position of Bertiella based on morphological-characters (Beveridge, 1994); (B) position of Bertiella based on analysis of the 28S rRNA gene (Hardman et al. 2012). (Landsoud-Soukate et al. 1995) and in G. gorilla America and South-East Asia, respectively from various localities in the Congo basin (author’s (Gómez-Puerta et al. 2009; Foitová et al. 2011). unpublished data); only Lilly et al. (2002) reported Diagnostics of the anoplocephaline infections are anoplocephalid eggs in two fecal samples of G. based mostly on the identification of gravid proglot- gorilla in the southern Dzanga-Ndoki National tids or eggs that possess a typical pyriform apparatus Park, Central African Republic, yet without (Schmidt, 1986; Denegri and Perez-Serrano, 1997); specific identification. Other anoplocephalids, such yet identifying these parasites to the species level in as Moniezia rugosa Lühe, 1895, were encountered clinical material from primates remains rather rather exceptionally in New World primates from difficult. the families Atelidae and Cebidae (Dunn, 1963; In the last decade, molecular approaches helped to Fiennes, 1967), with no recent records being resolve the phylogenetic relationships of several available. genera of the Anoplocephalinae, including Bertiella More common tapeworms in primates are (see e.g. Haukisalmi et al. 2010; Hardman et al. members of the genus Bertiella, although other 2012; Taleb-Hossenkhan and Bhagwant, 2012). members of this genus parasitize a broad spectrum Not surprisingly, molecular analyses showed that of mammalian hosts including marsupials, flying previous morphology-based classification may not lemurs and rodents in Africa, Asia, Australia and reflect the actual relationships within the subfamily. South America (Denegri and Perez-Serrano, 1997). In morphology-based phylogeny by Beveridge The type species, Bertiella studeri, was described (1994), Bertiella and Triplotaenia Boas, 1902, were from a common chimpanzee Pan troglodytes by sister genera, whereas the genus Anoplocephala was Blanchard (1891). Thereafter, more than 40 species basal taxon of the subfamily (Fig. 1A). Molecular- have been assigned to the genus (Schmidt, 1986; based phylogeny by Hardman et al. (2012), Caira et al. 2012), ten of them being known to however, showed a sister relationship between infect primates (Schmidt, 1986; Denegri and Bertiella and Anoplocephala, with the genera Perez-Serrano, 1997; Galán-Puchades et al. 2000). Schizorchis Hansen, 1948, and Mosgovoyia Infections by three of the typical primate tape- Spasskii, 1951, emerging as basal taxa (Fig. 1B). worms, B. studeri (Blanchard, 1891), Bertiella The genus Bertiella deserves special attention, as mucronata (Meyner, 1895) and Bertiella satyri previous studies did not include any isolates from (Blanchard, 1891), are sporadically reported also primates (Hardman et al. 2012), or the used molecu- from humans (Chandler, 1925; Cameron, 1929; lar marker was not sufficient for the establishment of Denegri and Perez-Serrano, 1997; Bhagwant, 2004; intra-generic relationships within the cestodes Foitová et al. 2011). Human infections with B. (Taleb-Hossenkhan and Bhagwant, 2012). studeri were reported mostly from India, the The present study provides the first molecular Russian Far-East and Africa (Bhagwant, 2004; El- insight into the diversity of Bertiella and Dib et al. 2004), or from non-residents that visited Anoplocephala from humans and non-human pri- these regions (Cameron, 1929; Galán-Puchades mates from Africa, Asia, Europe and South America, et al. 2000), while B. mucronata and B. satyri were and describes their host specificity and phylogenetic confined to men and primates living in South relationships. Jana Petrášová-Doležalová and others 1280 Table 1. The locality, source of DNA and GenBank accession numbers of particular genes of cestodes from non-human primates and humans. The extended dataset includes an isolate from horse Host species/ Source of 5.8S- Cestode isolate locality Habitat DNA cox1 nad1 ITS2 28S Bertiella sp. H.s. BR c/s Proglottid – JQ771110 JQ771093 Bertiella studeria H.s. ES c/s Proglottid JQ771102 JQ771111 JQ771094 Bertiella satyrib P.a. ID c/s Proglottid JQ771103 JQ771112 JQ771195 Bertiella mucronatac C.o. PE c/s Proglottid JQ771104 JQ771113 JQ771096 Bertiella sp. P.t. UG w Proglottid JQ771105 JQ771114 JQ771097 KJ888951 Bertiella sp. P.t. KE c/s Proglottid JQ771106 JQ771115 JQ771098 Bertiella sp. P.t. GW w Eggs ––– Bertiella sp. G.g. CF w Proglottid – JQ771116 JQ771099 KJ888952 Anoplocephala cf. G.b. RW w Eggs – JQ771117 JQ771100 gorillae Anoplocephala E.c. CZ c/s Eggs JQ771109 JQ771118 – perfoliata H.s., Homo sapiens; P.a., Pongo abelii; C.o., Callicebus oenanthe; P.t., Pan troglodytes; G.g., Gorilla gorilla; G.b., Gorilla beringei;
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