Abstract
A molecular phylogenetic hypothesis is presented for the anoplocephaline cestodes of placental mammals based on sequence data from the mitochondrial cytochrome c oxidase I (COI) gene, the nuclear-encoded 28S rRNA gene and the internal transcribed spacer region I of rRNA (ITS1). The material consists of 35 species representing nine genera of cestodes, with emphasis on taxa parasitising rodents and lagomorphs in the Holarctic region. The resulting phylogenies show considerable disagreement with earlier systematic and phylogenetic hypotheses derived from morphology. Specifically, the results contradict the view of uterine morphology being the primary determinant of deeper phylogenetic splits within Anoplocephalinae. Also, the role of genital duplication as a means of generic divergence was not found to follow consistently the pattern suggested by earlier hypotheses. Colonisation of novel host lineages has evidently been the predominant mode of diversification in anoplocephaline cestodes of placental mammals; evidence for phyletic co-evolution was obscure. The phylogenies consistently distinguished a large monophyletic group including all species from arvicoline rodents (voles and lemmings), primarily representing the genera Anoplocephaloides Baer, 1923 and Paranoplocephala Lühe, 1910. Phylogenetic relationships within the “arvicoline clade” of cestodes were generally poorly resolved. Consistent support for nodes above and below the unresolved polytomy indicates a rapid radiation involving a nearly simultaneous diversification of many lineages, a scenario also proposed for the arvicoline hosts.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
J.G. Baer (1927) ArticleTitleMonographie des cestodes de la famille des Anoplocephalidae Bulletin Biologique de la France et de la Belgique (Supplement) 10 1–241
J.G. Baer (1955) ArticleTitleIncidence de la spécificité parasitaire sur la taxonomie. Problèmes d’évolution chez les cestodes cyclophyllidiens Bulletin de la Société Zoologique de France 30 275–287
D. Bensasson D.X. Zhang D.L. Hartl G. Hewitt (2001) ArticleTitleMitochondrial pseudogenes: evolution’s misplaced witnesses Trends in Ecology and Evolution 16 314–321 Occurrence Handle10.1016/S0169-5347(01)02151-6 Occurrence Handle11369110
I. Beveridge (1994) Family Anoplocephalidae Cholodkovsky, 1902 L.F. Khalil A. Jones R.A. Bray (Eds) Keys to the cestode parasites of vertebrates Cambridge CAB International 751
I. Beveridge N.B. Chilton (2001) ArticleTitleCo-evolutionary relationships between the nematode subfamily Cloacininae and its macropodid marsupial hosts International Journal for Parasitology 31 976–996 Occurrence Handle10.1016/S0020-7519(01)00200-4 Occurrence Handle11406145
I. Beveridge D.M. Spratt (1996) ArticleTitleThe helminth fauna of Ausralasian marsupials: origins and evolutionary biology Advances in Parasitology 37 135–254
S.V. Brant S.L. Gardner (2000) ArticleTitlePhylogeny of species of the genus Litomosoides (Nematoda: Onchocercidae): evidence of rampant host switching Journal of Parasitology 86 545–554 Occurrence Handle10864253
C.J. Conroy J.A. Cook (1999) ArticleTitleMtDNA evidence for repeated pulses of speciation within arvicoline and murid rodents Journal of Mammalian Evolution 6 221–245 Occurrence Handle10.1023/A:1020561623890
C.W. Cunningham (1997) ArticleTitleCan tree incongruence tests predict when data should be combined? Molecular Biology and Evolution 14 733–740 Occurrence Handle9214746
P. Foronda J.C. Casanova B. Valladares E. Martinez C. Feliu (2003) ArticleTitleMolecular systematics of several cyclophyllid families (Cestoda) based on the analysis of 18S ribosomal DNA gene sequences Parasitology Research 93 279–282
T. Genov B.B. Georgiev (1988) ArticleTitleReview of the species of the genus Anoplocephaloides Baer, 1923 emend Rausch, 1976 (Cestoda: Anoplocephalidae) parasitizing rodents in Bulgaria, with an analysis of the taxonomic structure of the genus Parasitologica Hungarica 21 31–52
T. Genov G.P. Vasileva B.B. Georgiev (1996) ArticleTitleParanoplocephala aquatica n. sp. (Cestoda, Anoplocephalidae) from Arvicola terrestris and Ondatra zibethica (Rodentia), with redescriptions and comments on related species Systematic Parasitology 34 135–152 Occurrence Handle10.1007/BF00009687
V.D. Gulyaev (1996) ArticleTitleOn a taxonomic separation of Anoplocephaloides spp. (Cestoda: Anoplocephalidae) with serial alternation of the genital apertures Parazitologiya 30 263–269
V. Haukisalmi H. Henttonen (2001) ArticleTitleBiogeography of helminth parasitism in Lemmus Link (Arvicolinae), with the description of Paranoplocephala fellmani n. sp. (Cestoda: Anoplocephalidae) from the Norwegian lemming L. lemmus (Linnaeus) Systematic Parasitology 49 7–22 Occurrence Handle10.1023/A:1010778504559 Occurrence Handle11389326
V. Haukisalmi H. Henttonen (2003) ArticleTitleWhat is Paranoplocephala macrocephala (Douthitt, 1915) (Cestoda: Anoplocephalidae)? Systematic Parasitology 54 53–69 Occurrence Handle10.1023/A:1022141809571 Occurrence Handle12567010
V. Haukisalmi L.M. Wickström J. Hantula H. Henttonen (2001) ArticleTitleTaxonomy, genetic differentiation and Holarctic biogeography of Paranoplocephala spp. (Cestoda: Anoplocephalidae) in collared lemmings (Dicrostonyx; Arvicolinae) Biological Journal of the Linnean Society 74 171–196 Occurrence Handle10.1006/bijl.2001.0570
V. Haukisalmi L.M. Wickström H. Henttonen J. Hantula A. Gubányi (2004) ArticleTitleMolecular and morphological evidence for multiple species within Paranoplocephala omphalodes (Cestoda, Anoplocephalidae) in Microtus voles (Arvicolinae) Zoologica Scripta 33 277–290 Occurrence Handle10.1111/j.0300-3256.2004.00148.x
E.P. Hoberg (1995) ArticleTitleHistorical biogeography and modes of speciation across high latitude seas of the holarctic - concepts for host-parasite coevolution among the Phocini (Phocidae) and Tetrabothriidae (Eucestoda) Canadian Journal of Zoology 73 45–57
E.P. Hoberg A. Jones R.A. Bray (1999) ArticleTitlePhylogenetic analysis among the families of the Cyclophyllidea (Eucestoda) based on comparative morphology, with new hypotheses for co-evolution in vertebrates Systematic Parasitology 42 51–73 Occurrence Handle10.1023/A:1006100629059 Occurrence Handle10613546
E.P. Hoberg A. Jones R.L. Rausch K.S. Eom S.L. Gardner (2000) ArticleTitleA phylogenetic hypothesis for species of the genus Taenia (Eucestoda: Taeniidae) Journal of Parasitology 86 89–98 Occurrence Handle10.1007/s004360050016 Occurrence Handle10701570
E.P. Hoberg G.J. Klassen (2002) ArticleTitleRevealing the faunal tapestry: co-evolution and historical biogeography of hosts and parasites in marine systems Parasitology (Supplement) 124 S3–S22 Occurrence Handle10.1017/S0031182002001841
E.P. Hoberg S.J. Kutz K.E. Galbreath J.A. Cook (2003) ArticleTitleArctic biodiversity: from discovery to faunal baselines - revealing the history of a dynamic ecosystem Journal of Parasitology 89 IssueIDSuppl. S84–S95
E.P. Hoberg J.R. Lichtenfels (1994) ArticleTitlePhylogenetic systematic analysis of the Trichostrongylidae (Nematoda), with an initial assessment of coevolution and biogeography Journal of Parasitology 80 976–96 Occurrence Handle7799171
J.P. Huelsenbeck F. Ronquist R. Nielsen J.P. Bollback (2001) ArticleTitleBayesian inference of phylogeny and its impact on evolutionary biology Science 294 2310–2314 Occurrence Handle10.1126/science.1065889 Occurrence Handle11743192
M. Jaarola N. Martínková I. Gündüz C. Brunhoff J. Zima A. Nadachowski G. Amori N.S. Bulatova B. Chondropoulos S. Fraguedakis-Tsolis J. González-Esteban M.J. López-Fuster A.S. Kandaurov H. Kefelioglu M. daLuz Mathias I. Villate J.B. Searle (2005) ArticleTitleMolecular phylogeny of the speciose vole genus Microtus (Arvicolinae, Rodentia) inferred from mitochondrial DNA sequences Molecular Phylogenetics and Evolution 33 647–663 Occurrence Handle10.1016/j.ympev.2004.07.015
E.P. Lessa J.A. Cook (1998) ArticleTitleThe molecular phylogenetics of tuco-tucos (genus Ctenomys, Rodentia: Octodontidae) suggests an early burst of speciation Molecular Phylogenetics and Evolution 9 88–99 Occurrence Handle10.1006/mpev.1997.0445 Occurrence Handle9479698
Y.-H. Lin P.J. Waddell D. Penny (2002) ArticleTitlePika and vole mitochondrial genomes increase support for both rodent monophyly and glires Gene 294 119–129 Occurrence Handle10.1016/S0378-1119(02)00695-9 Occurrence Handle12234673
A.E. Lockyer P.D. Olson D.T.J. Littlewood (2003) ArticleTitleUtility of complete large and small subunit rRNA genes in resolving the phylogeny of the Neodermata (Platyhelminthes): implications and a review of the cercomer theory Biological Journal of the Linnean Society 78 155–171 Occurrence Handle10.1046/j.1095-8312.2003.00141.x
D.R. Maddison W.P. Maddison (2000) MacClade 4: Analysis of phylogeny and character evolution Sinauer Associates Sunderland, MA
W.J. Murphy E. Eizirik S.J. O’Brien O. Madsen M. Scally C.J. Douady E. Teeling O.A. Ryder M.J. Stanhope W.W. Jong Particlede M.S. Springer (2001) ArticleTitleResolution of the early placental mammal radiation using Bayesian phylogenetics Science 294 2348–2351 Occurrence Handle10.1126/science.1067179 Occurrence Handle11743200
D. Posada K.A. Crandall (1998) ArticleTitleModeltest: testing the model of DNA substitution Bioinformatics 14 817–818 Occurrence Handle10.1093/bioinformatics/14.9.817 Occurrence Handle9918953
R.L. Rausch (1976) ArticleTitleThe genera Paranoplocephala Lühe, 1910 and Anoplocephaloides Baer, 1923 (Cestoda: Anoplocephalidae), with particular reference to species in rodents Annales de Parasitologie Humaine et Comparée 51 513–562 Occurrence Handle1020889
R.L. Rausch (1980) ArticleTitleRedescription of Diandrya composita Darrah, 1930 (Cestoda, Anoplocephalidae) from Nearctic marmots (Rodentia: Sciuridae) and the relationships of the genus Diandrya emend Proceedings of the Helminthological Society of Washington 47 157–164
F. Ronquist J.P. Huelsenbeck (2003) ArticleTitleMRBAYES 3: Bayesian phylogenetic inference under mixed models Bioinformatics 19 1572–1574 Occurrence Handle10.1093/bioinformatics/btg180 Occurrence Handle12912839
G.D. Schmidt (1986) CRC handbook of tapeworm identification CRC Press Inc. Boca Raton 675
A.A. Spasskii (1951) [Anoplocephalate tapeworms of domestic and wild animals] Izdatel’tsvo Nauka Moscow 783
D.L. Swofford (2002) PAUP*. Phylogenetic analysis using parsimony (*and other methods) Sinauer Associates Sunderland, Massachusetts
F. Tenora (1976) ArticleTitleTapeworms of the family Anoplocephalidae Cholodkowsky, 1902. Evolutionary implications Acta Scientiarum Naturalium Brno 10 1–37
F. Tenora (1998) ArticleTitleSeveral comments to the systematic status of certain genera from Anoplocephalinae (Cestoda), parasites of Rodentia and Lagomorpha Acta Universitatis Agriculturae et Silviculturae Mendelianae Brunensis 46 57–72
F. Tenora É. Murai C. Vaucher (1986) ArticleTitleOn Andrya Railliet, 1893 and Paranoplocephala Lühe, 1910 (Cestoda, Monieziinae) Parasitologica Hungarica 19 43–75
J.D. Thompson D.G. Higgins T.J. Gibson (1994) ArticleTitleCLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice Nucleic Acids Research 22 4673–4680 Occurrence Handle7984417
Wickström L.M. (2004) Phylogeny, phyletic coevolution and phylogeography of anoplocephaline cestodes in mammals. PhD. Thesis, University of Helsinki, pp 22.
L.M. Wickström V. Haukisalmi S. Varis J. Hantula V.B. Fedorov H. Henttonen (2003) ArticleTitlePhylogeography of the circumpolar Paranoplocephala arctica species complex (Cestoda: Anoplocephalidae) parasitizing collared lemmings (Dicrostonyx spp.) Molecular Ecology 12 3359–3371 Occurrence Handle10.1046/j.1365-294X.2003.01985.x Occurrence Handle14629352
S. Yamaguti (1959) Systema helminthum The cestodes of vertebrates NumberInSeriesVol. II. Interscience Publishers Inc. New York 860
A.D. Yoder J.A. Irwin B.A. Payseur (2001) ArticleTitleFailure of the ILD to determine data compatability for slow loris phylogeny Systematic Biology 50 408–424 Occurrence Handle10.1080/106351501300318003 Occurrence Handle12116583
D.-X. Zhang G.M. Hewitt (1996) ArticleTitleNuclear integrations: challenges for mitochondrial DNA markers Trends in Ecology and Evolution 11 247–251 Occurrence Handle10.1016/0169-5347(96)10031-8
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Wickström, L.M., Haukisalmi, V., Varis, S. et al. Molecular Phylogeny and Systematics of Anoplocephaline Cestodes in Rodents and Lagomorphs. Syst Parasitol 62, 83–99 (2005). https://doi.org/10.1007/s11230-005-5488-5
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/s11230-005-5488-5