A Phylogenetic Hypothesis for Species of the Genus Taenia (Eucestoda: Taeniidae)
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University of Nebraska - Lincoln DigitalCommons@University of Nebraska - Lincoln Faculty Publications from the Harold W. Manter Laboratory of Parasitology Parasitology, Harold W. Manter Laboratory of 2-2000 A Phylogenetic Hypothesis for Species of the Genus Taenia (Eucestoda: Taeniidae) Eric P. Hoberg United States Department of Agriculture, [email protected] Arlene Jones Natural History Museum (London) Robert L. Rausch University of Washington, [email protected] Keeseon S. Eom Chungbuk National University Scott Lyell Gardner University of Nebraska - Lincoln, [email protected] Follow this and additional works at: https://digitalcommons.unl.edu/parasitologyfacpubs Part of the Biodiversity Commons, Ecology and Evolutionary Biology Commons, and the Parasitology Commons Hoberg, Eric P.; Jones, Arlene; Rausch, Robert L.; Eom, Keeseon S.; and Gardner, Scott Lyell, "A Phylogenetic Hypothesis for Species of the Genus Taenia (Eucestoda: Taeniidae)" (2000). Faculty Publications from the Harold W. Manter Laboratory of Parasitology. 333. https://digitalcommons.unl.edu/parasitologyfacpubs/333 This Article is brought to you for free and open access by the Parasitology, Harold W. Manter Laboratory of at DigitalCommons@University of Nebraska - Lincoln. It has been accepted for inclusion in Faculty Publications from the Harold W. Manter Laboratory of Parasitology by an authorized administrator of DigitalCommons@University of Nebraska - Lincoln. J. Parasitol., 86(1), 2(XX)p. 89-98 ? American Society of Parasitologists 2(XX) A PHYLOGENETICHYPOTHESIS FOR SPECIES OF THE GENUS TAENIA (EUCESTODA:TAENIIDAE) Eric P. Hoberg, Arlene Jones*, Robert L. Rauscht, Keeseon S. Eomf, and S. L. Gardner? United States Departmentof Agriculture,Agricultural Research Service, Biosystematics and NationalParasite CollectionUnit, BARCEast No. 1180, 10300 BaltimoreAvenue, Beltsville,Maryland 20705 ABSTRACT: Cladistic analysis of a numericaldata matrix describing 27 charactersfor species of Taenia resulted in 4 most parsimoniousphylogenetic trees (174 steps; consistencyindex = 0.28; homoplasyindex = 0.72; retentionindex = 0.48). Mono- phyly for Taenia is diagnosed by the metacestodethat is either a cysticercus or a form derived from a bladder-likelarva; no other unequivocalsynapomorphies are evident. Tree structureprovides no supportfor recognition of a diversity of tribes or genera within the Taeniinae:Fimbriotaeniini and Taeniinihave no phylogeneticbasis. Hydatigera,Fimbriotaenia, Fossor, Mon- ordotaenia, Multiceps, Taeniarhynchus,Tetratirotaenia must be subsumed within Taenia as synonyms. Taenia saginata and Taenia asiatica are sister species and distantlyrelated to Taeniasolium. Cospeciationwith respectto carnivorousdefinitive hosts and Taenia appearsto be limited. Althoughfelids are putativeancestral hosts, contemporaryassociations appear to have resulted from extensive host-switchingamong felids, canids, hyaenids,and others.In contrast,relationships with herbivorousintermediate hosts are indicativeof more pervasive coevolution;rodents as intermediatehosts are postulatedas ancestralfor the Taeniidae, Taenia + Echinococcus.Patterns appear consistent with rapid shifts between phylogeneticallyunrelated carnivores but among those that historicallyexploited a common prey resourcewithin communitiesin specific biogeographicregions. Cestodes of the genus Taenia Linnaeus, 1758 are of consid- niarhynchus; whereas a solid-bodied larva or armathyridium erable medical and veterinary significance and, as a conse- was regarded as typical of metacestodes in Cladotaenia and quence studies at the species-level, have been focused and in- Tetratirotaenia. Subsequently, Fimbriotaenia Korniushin and tensive (e.g., Abuladze, 1964; Verster, 1969; Rausch, 1994, Sharpilo, 1986 was established for a unique, fimbriocercus lar- 1997). There have been in excess of 70 nominal species de- val form characteristic of a limited number of species formerly scribed in the genus (Verster, 1969), but morphological limits referred to Taenia (Korniushin and Sharpilo, 1986). among species are often problematic. Currently, approximately In a further modification of this taxonomic framework, Spas- 35-40 species are recognized based on adult specimens, in- skii (1998) recognized Taeniinae, Echinococcinae, and Anoplo- cluding those validated by Verster (1969) and additional species taeniinae Spasskii, 1990. In Taeniinae, he diagnosed 2 tribes: that were subsequently described (e.g., Jones and Khalil, 1984; (1) Taeniini Rosmassler, 1832, for forms with a reticulate vi- Jones et al., 1988; Eom and Rim, 1993); many species continue tellarium, including Taenia, Hydatigera, Multiceps, and Tae- to be established for metacestodes (e.g., Murai et al., 1993). niarhynchus; and (2) Fimbriotaeniini Spasskii, 1996 in which Although considerable taxonomic revision has been con- the vitellarium was compact or lobed, including Fimbriotaenia, ducted, disagreements continue over both the number of genera Insinuarotaenia, Monordotaenia Little, 1967 and Paraclado- in the family (2-13) and the number of species that are valid taenia. In Anoplotaeniinae, the tribes Dasyurotaeniini Spasskii, within Taenia, e.g., compare Abuladze (1964), Movsessian 1998 (for the rostellate and armed, Dasyurotaenia) and Ano- (1989), Bessonov et al. (1994), and Spasskii (1998) with Verster plotaeniini Spasskii, 1998 (for the arostellate and unarmed An- (1969), Schmidt (1986), and Rausch (1994). At 1 extreme of oplotaenia) were established. Thus, a primary character of adult this continuum, the taxonomy proposed by Abuladze (1964) strobilate worms was used to justify the tribes, whereas a com- and adopted with some modifications by Bessonov et al. (1994) bination of morphological characters for adults or larvae or the recognized 2 subfamilies with 12 or 13 genera: (1) Taeniinae range of intermediate and definitive hosts were employed to Stiles, 1896 for Taenia, Taeniarhynchus Weinland, 1758, Mul- diagnose each of the genera. This proposal embodied much of ticeps Goeze, 1782, Hydatigera Lamarck, 1816, Fossor Honess, the taxonomy outlined previously in the Russian literature 1937, Anoplotaenia Beddard, 1912, Insinuarotaenia Spasskii, where a number of genera, proposed for putative inclusive 1948, Tetratirotaenia Abuladze, 1964, Cladotaenia Cohn, 1901 groups within Taenia, were based primarily on characteristics and Paracladotaenia Yamaguti, 1935; and (2) Echinococcinae of larvae (e.g., Abuladze, 1964; Korniushin and Sharpilo, 1986; Abuladze, 1960 for Echinococcus Rudolphi, 1801 and Alveo- Movsessian, 1989; Bessonov et al., 1994). coccus Abuladze, 1960. Taeniinae was partitioned into genera A contrasting view was outlined by Verster (1969) who di- along 2 major ontogenetic paths; possession of fluid-filled meta- agnosed 2 major groups within Taenia based on the relative cestodes characterized Taenia, Hydatigera, Multiceps, and Tae- positions of the genital ducts and osmoregulatory canals in stro- bilate adults. In Taenia, Group I, the genital ducts pass between Received 29 March 1999; revised 30 July 1999; accepted 30 July the osmoregulatory canals; in Taenia, Group II, they are ventral 1999. to the canals. referred to II were to * of The Natural Cromwell Species Group postulated Department Zoology, History Museum, be older or in carnivoran hosts. Road, London, SW7 5BD, U.K. relatively relatively primitive t Department of Comparative Medicine, School of Medicine, Univer- Verster (1969) relegated to synonymy with Taenia most of the sity of Washington, Box 357190, Seattle, Washington, 98195. genera of the Taeniinae regarded as valid in the taxonomy pro- t Department of Parasitology, College of Medicine, Chungbuk National posed by Abuladze (1964); she did not comment on Anoplo- Korea. University, Chongju 360-763, taenia, Cladotaenia, or Paracladotaenia. ? Harold W. Manter Laboratory of Parasitology, Nebraska State Mu- Dasyurotaenia, seum, University of Nebraska-Lincoln, Lincoln, Nebraska 68588- This concept for a reduced number of genera within the Tae- 0514. niidae was supported by Rausch (1994, 1997), in part consistent 89 90 THE JOURNAL OF PARASITOLOGY,VOL. 86, NO. 1, FEBRUARY2000 with Verster (1969) and Schmidt (1986), who recognized 2 In the current study, we present the first comprehensive hy- monotypic subfamilies: (1) Taeniinae for Taenia and (2) Echin- pothesis for phylogeny of Taenia based on analysis of structural ococcinae for Echinococcus (with Alveococcus as a synonym). characters of adults and metacestodes within a comparative Such genera as Hydatigera, Multiceps, Fossor, Monordotaenia, morphological context; this represents an extension of studies Taeniarhynchus, Tetratirotaenia, and Fimbriotaenia were sub- at the family level within the Cyclophyllidea (Hoberg et al., sumed as synonyms of Taenia. Additionally, Cladotaenia, Par- 1999). We do not examine here the larger issue of the placement acladotaenia (earlier referred to Dilepididae by Freeman [1959] of such genera as Anoplotaenia, Dasyurotaenia, or Cladotaenia and Schmidt [1986]), Anoplotaenia (to Dilepididae by Schmidt but focus on phylogeny for species within the Taeniinae sensu [1986]), Dasyurotaenia (to Davaineidae by Schmidt [1986]), stricto. Results of this analysis are applied to: (1) an examina- and Insinuarotaenia were excluded from the Taeniidae based tion of the taxonomic structure for the subfamily and genus; on the contention that they were morphologically and ontoge- and (2) a discussion of putative relationships and coevolution- netically incompatible (Rausch, 1994, 1997).