Hostname: page-component-586b7cd67f-2plfb Total loading time: 0 Render date: 2024-11-30T15:47:11.990Z Has data issue: false hasContentIssue false
  • English
  • Français

Phylogeny of hymenolepidids (Cestoda: Cyclophyllidea) from mammals: sequences of 18S rRNA and COI genes confirm major clades revealed by the 28S rRNA analyses

Published online by Cambridge University Press:  21 April 2021

B. Neov ,
G.P. Vasileva ,
G. Radoslavov ,
P. Hristov ,
D.T.J. Littlewood  and
B.B. Georgiev Open the ORCID record for B.B. Georgiev [Opens in a new window]
B. Neov
Affiliation:
Institute of Biodiversity and Ecosystem Research, Bulgarian Academy of Sciences, 2 Gagarin Street, 1113Sofia, Bulgaria
G.P. Vasileva
Affiliation:
Institute of Biodiversity and Ecosystem Research, Bulgarian Academy of Sciences, 2 Gagarin Street, 1113Sofia, Bulgaria
G. Radoslavov
Affiliation:
Institute of Biodiversity and Ecosystem Research, Bulgarian Academy of Sciences, 2 Gagarin Street, 1113Sofia, Bulgaria
P. Hristov
Affiliation:
Institute of Biodiversity and Ecosystem Research, Bulgarian Academy of Sciences, 2 Gagarin Street, 1113Sofia, Bulgaria
D.T.J. Littlewood
Affiliation:
Department of Life Sciences, The Natural History Museum, Cromwell Road, London, SW7 5BD, UK
B.B. Georgiev*
Affiliation:
Institute of Biodiversity and Ecosystem Research, Bulgarian Academy of Sciences, 2 Gagarin Street, 1113Sofia, Bulgaria
*
Author for correspondence: B.B. Georgiev, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

The aim of the study is to test a hypothesis for the phylogenetic relationships among mammalian hymenolepidid tapeworms, based on partial (D1–D3) nuclear 28S ribosomal RNA (rRNA) genes, by estimating new molecular phylogenies for the group based on partial mitochondrial cytochrome c oxidase I (COI) and nuclear 18S rRNA genes, as well as a combined analysis using all three genes. New sequences of COI and 18S rRNA genes were obtained for Coronacanthus integrus, C. magnihamatus, C. omissus, C. vassilevi, Ditestolepis diaphana, Lineolepis scutigera, Spasskylepis ovaluteri, Staphylocystis tiara, S. furcata, S. uncinata, Vaucherilepis trichophorus and Neoskrjabinolepis sp. The phylogenetic analyses confirmed the major clades identified by Haukisalmi et al. (Zoologica Scripta 39: 631–641, 2010): Ditestolepis clade, Hymenolepis clade, Rodentolepis clade and Arostrilepis clade. While the Ditestolepis clade is associated with soricids, the structure of the other three clades suggests multiple evolutionary events of host switching between shrews and rodents. Two of the present analyses (18S rRNA and COI genes) show that the basal relationships of the four mammalian clades are branching at the same polytomy with several hymenolepidids from birds (both terrestrial and aquatic). This may indicate a rapid radiation of the group, with multiple events of colonizations of mammalian hosts by avian parasites.

Keywords

PhylogenyshrewsrodentsHymenolepididae
Type
Research Paper
Information
Journal of Helminthology , Volume 95 , 2021 , e23
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Binkienė, R, Kornienko, SA and Tkach, VV (2015) Soricinia genovi n. sp. from Neomys fodiens in Bulgaria, with redescription of Soricinia globosa (Baer, 1931) (Cyclophyllidea: Hymenolepididae). Parasitology Research 114, 209–218.CrossRefGoogle Scholar
Binkienė, R, Miliūtė, A and Stunžėnas, V (2019) Molecular data confirm the taxonomic position of Hymenolepis erinacei (Cyclophyllidea: Hymenolepididae) and host switching, with notes on cestodes of Palaearctic hedgehogs (Erinaceidae). Journal of Helminthology 93, 195–202.CrossRefGoogle Scholar
Cunningham, LJ and Olson, PD (2010) Description of Hymenolepis microstoma (Nottingham strain): a classical tapeworm model for research in the genomic era. Parasites and Vectors 3, 123.CrossRefGoogle ScholarPubMed
Czaplinski, B and Vaucher, C (1994) Family Hymenolepididae Ariola, 1899. pp. 595–663 in Khalil, LF, Jones, A and Bray, RA (Eds) Keys to the cestode parasites of vertebrates. Wallingford, UK, CAB International.Google Scholar
Dimitrova, YD, Georgiev, BB, Mariaux, J and Vasileva, GP (2019) Two new cestode species of the family Hymenolepididae Perrier, 1897 (Cyclophyllidea) from passerine birds in Ethiopia, with the erection of Citrilolepis n. g. Systematic Parasitology 96, 279–297.CrossRefGoogle ScholarPubMed
Gao, JF, Hou, MR, Cui, YC, Wang, LK and Wang, CR (2017) The complete mitochondrial genome sequence of Drepanidotaenia lanceolata (Cyclophyllidea: Hymenolepididae). Mitochondrial DNA Part A 28, 317–318.CrossRefGoogle Scholar
Gardner, SL, Dursahinhan, AT, Campbell, M and Rácz, SE (2020) A new genus and two new species of unarmed hymenolepidid cestodes (Cestoda: Hymenolepididae) from geomyid rodents in Mexico and Costa Rica. Zootaxa 4766, 358–376.CrossRefGoogle ScholarPubMed
Genov, T (1980) Morphology and taxonomy of the species of genus Coronacanthus Spassky, 1954 (Cestoda: Hymenolepididae) in Bulgaria. Helminthologia 17, 245–255.Google Scholar
Georgiev, B, Biserkov, V and Genov, T (1986) In toto staining method for cestodes with iron acetocarmine. Helminthologia 23, 279–281.Google Scholar
Georgiev, BB, Bray, RA, Littlewood, DTJ, Morand, S, Krasnov, BR and Poulin, R (2006) Cestodes of small mammals: taxonomy and life cycles. pp. 23–62 in Morand, S, Krasnov, BR and Poulin, R (Eds) Micromammals and macroparasites. From evolutionary ecology to management. Tokyo, Springer.Google Scholar
Greiman, SE and Tkach, VV (2012) Description and phylogenetic relationships of Rodentolepis gnoskei n. sp. (Cyclophyllidea: Hymenolepididae) from a shrew Suncus varilla minor in Malawi. Parasitology International 61, 343–350.CrossRefGoogle ScholarPubMed
Greiman, SE, Tkach, VV and Cook, JA (2013) Description and molecular differentiation of a new Staphylocystoides (Cyclophyllidea: Hymenolepididae) from the dusky shrew Sorex monticolus in Southeast Alaska. Journal of Parasitology 99, 1045–1049.CrossRefGoogle ScholarPubMed
Guo, A (2016) Characterization of the complete mitochondrial genome of the cloacal tapeworm Cloacotaenia megalops (Cestoda: Hymenolepididae). Parasites and Vectors 9, 490.CrossRefGoogle Scholar
Haukisalmi, V, Hardman, LM, Foronda, P, Feliu, C, Laakkonen, J, Niemimaa, J, Lehtonen, JT and Henttonen, H (2010) Systematic relationships of hymenolepidid cestodes of rodents and shrews inferred from sequences of 28S ribosomal RNA. Zoologica Scripta 39, 631–641.CrossRefGoogle Scholar
Hillis, DM and Dixon, MT (1991) Ribosomal DNA: molecular evolution and phylogenetic inference. Quarterly Review of Biology 66, 411–453.CrossRefGoogle ScholarPubMed
Kikuchi, T, Holroyd, N and Berriman, M (2019) Hymenolepis nana mitochondrial DNA, complete genome. GenBank: AP017666.1. Available at https://www.ncbi.nlm.nih.gov/nuccore/AP017666.Google Scholar
Kornienko, SA, Binkienė, R, Dokuchaev, NE and Tkach, VV (2019) Molecular phylogeny and systematics of cestodes with rudimentary rostellum (Cestoda: Hymenolepididae) from Holarctic Sorex shews (Eulipotyphla: Soricidae). Zoological Journal of the Linnean Society 187, 965–986.CrossRefGoogle Scholar
Kumar, S, Stecher, G and Tamura, K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33, 1870–1874.CrossRefGoogle ScholarPubMed
Kumar, S, Stecher, G, Li, M, Knyaz, C and Tamura, K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution 35, 1547–1549.CrossRefGoogle ScholarPubMed
Littlewood, DTJ and Olson, PD (2001) Small subunit rDNA and the Platyhelminthes: signal, noise, conflict and compromise. pp. 262–278 in Littlewood, DTJ, Bray, RA (Eds) Interrelationships of the Platyhelminthes. London, Taylor & Francis.Google Scholar
Littlewood, DTJ, Waeschenbach, A and Nikolov, PN (2008) In search of mitochondrial markers for resolving the phylogeny of cyclophyllidean tapeworms (Platyhelminthes, Cestoda) – a test study with Davaineidae. Acta Parasitologica 53, 133–144.CrossRefGoogle Scholar
Machida, RJ and Knowlton, N (2012) PCR primers for metazoan nuclear 18S and 28S ribosomal DNA sequences. PLoS One 7(9), e46180.CrossRefGoogle ScholarPubMed
Makarikov, AA and Georgiev, BB (2020) Review of records of hymenolepidids (Eucestoda: Hymenolepididae) from dormice (Rodentia: Gliridae) in Europe, with a redescription of Armadolepis spasskyi Tenora & Baruš, 1958 and the description of A. genovi n. sp. Systematic Parasitology 97, 83–98.CrossRefGoogle ScholarPubMed
Makarikov, AA, Mel'nikova, YA and Tkach, VV (2015) Description and phylogenetic affinities of two new species of Nomadolepis (Eucestoda, Hymenolepididae) from eastern palearctic. Parasitology International 64, 453–463.CrossRefGoogle ScholarPubMed
Makarikov, AA, Stakheev, VV and Tkach, VV (2018) Phylogenetic relationships of the genus Armadolepis Spassky, 1954 (Eucestoda, Hymenolepididae), with descriptions of two new species from Palaearctic dormice (Rodentia, Gliridae). Systematic Parasitology 95, 65–79.CrossRefGoogle Scholar
Makarikov, AA, Galbreath, KE, Eckerlin, RP and Hoberg, EP (2020) Discovery of Arostrilepis tapeworms (Cyclophyllidea: Hymenolepididae) and new insights for parasite species diversity from Eastern North America. Parasitology Research 119, 567–585.CrossRefGoogle ScholarPubMed
Makarikova, TA (2018) Vampirolepis kulkinae n. sp. (Cyclophyllidea: Hymenolepididae) from the common noctule bat Nyctalus noctula (Schreber) (Chiroptera: Vespertilionidae) in Kazakhstan. Systematic Parasitology 95, 105–113.CrossRefGoogle Scholar
Mariaux, J and Olson, PD (2001) Cestode systematics in the molecular era. pp. 127–134 in Littlewood, DTJ and Bray, RA (Eds) Interrelationships of the Platyhelminthes. London, Taylor & Francis.Google Scholar
Mariaux, J, Tkach, VV, Vasileva, GP, et al. (2017) Cyclophyllidea van Beneden in Braun, 1900. pp. 77–148 in Caira, JN and Jensen, K (Eds) Planetary biodiversity inventory (2008–2017): tapeworms from vertebrate bowels of the earth. Lawrence, Kansas, University of Kansas, Natural History Museum.Google Scholar
Montgomery, SSJ, Montgomery, WI and Dunn, TS (1987) Biochemical, physiological and morphological variation in unarmed hymenolepids (Eucestoda: Cyclophyllidae). Zoological Journal of the Linnean Society 91, 293–324.CrossRefGoogle Scholar
Neov, B, Vasileva, GP, Radoslavov, G, Hristov, P, Littlewood, DTJ and Georgiev, BB (2019) Phylogeny of hymenolepidid cestodes (Cestoda: Cyclophyllidea) from mammalian hosts based on partial 28S rDNA, with focus on parasites from shrews. Parasitology Research 118, 73–88.CrossRefGoogle ScholarPubMed
Nkouawa, A, Haukisalmi, V, Li, T, Nakao, M, Lavikainen, A, Chen, X, Henttonen, H and Ito, A (2016) Cryptic diversity in hymenolepidid tapeworms infecting humans. Parasitology International 65, 83–86.CrossRefGoogle ScholarPubMed
Nylander, JAA, Ronquist, F, Huelsenbeck, JP, Nieves-Aldrey, J and Buckley, T (2004) Bayesian phylogenetic analysis of combined data. Systematic Biology 53, 47–67.CrossRefGoogle ScholarPubMed
Olson, PD, Littlewood, DTJ, Bray, RA and Mariaux, J (2001) Interrelationships and evolution of the tapeworms (Platyhelminthes: Cestoda). Molecular Phylogenetics and Evolution 19, 443–467.CrossRefGoogle Scholar
Olson, PD, Yoder, K, Fajardo LG, LF, Marty, AM, van de Pas, S, Olivier, C and Relman, DA (2003) Lethal invasive cestodiasis in immunosuppressed patients. The Journal of Infectious Diseases 187, 1962–1966.CrossRefGoogle ScholarPubMed
Pistone, D, Lindgren, M, Holmstad, P, Ellingsen, NK, Kongshaug, H, Nilsen, F and Skorping, A (2017) The role of chewing lice (Phthiraptera: Philopteridae) as intermediate hosts in the transmission of Hymenolepis microps (Cestoda: Cyclophyllidea) from the willow ptarmigan Lagopus lagopus (Aves: Tetraonidae). Journal of Helminthology 92, 49–55.CrossRefGoogle Scholar
Pleijel, F, Jondelius, U, Norlinder, E, Nygren, A, Oxelman, B, Schander, C, Sundberg, P and Thollesson, M (2008) Phylogenies without roots? A plea for the use of vouchers in molecular phylogenetic studies. Molecular Phylogenetics and Evolution 48, 369–371.CrossRefGoogle Scholar
Ronquist, F, Teslenko, M, van der Mark, P, et al. (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61, 539–542.CrossRefGoogle ScholarPubMed
Schluter, D (2000) The ecology of adaptive radiation. 296 pp. Oxford, Oxford University Press.Google Scholar
Scholz, T, de Chambrier, A, Kuchta, R, Littlewood, DTJ and Waeschenbach, A (2013) Macrobothriotaenia ficta (Cestoda: Proteocephalidea), a parasite of sunbeam snake (Xenopeltis unicolor): example of convergent evolution. Zootaxa 3640, 485–499.CrossRefGoogle ScholarPubMed
Swan, DC (1936) Berlese's fluid: remarks upon its preparation and use as a mounting medium. Bulletin of Entomological Research 27, 389–391.CrossRefGoogle Scholar
Tkach, VV, Vasileva, GP and Genov, T (2003) Description of Vaucherilepis trichophorus sp. nov., gen. nov. (Cyclophyllidea, Hymenolepididae) from water shrews and gammarid crustaceans in Bulgaria and Ukraine. Acta Parasitologica 48, 87–97.Google Scholar
Tkach, VV, Makarikov, AA and Kinsella, JM (2013) Morphological and molecular differentiation of Staphylocystis clydesengeri n. sp. (Cestoda, Hymenolepididae) from the vagrant shrew, Sorex vagrans (Soricomorpha, Soricidae), in North America. Zootaxa 3691, 389–400.CrossRefGoogle Scholar
Tkach, VV, Kinsella, JM and Greiman, SE (2018) Two new species of Staphylocystoides Yamaguti, 1959 (Cyclophyllidea: Hymenolepididae) from the masked shrew Sorex cinereus in North America. Journal of Parasitology 104, 157–167.CrossRefGoogle ScholarPubMed
Tsai, IJ, Zarowiecki, M, Holroyd, N, et al. (2013) The genomes of four tapeworm species reveal adaptations to parasitism. Nature 496, 57–63.CrossRefGoogle ScholarPubMed
Vasileva, GP, Tkach, VV and Genov, T (2005) Two new hymenolepidid species (Cestoda, Hymenolepididae) from water shrews Neomys fodiens Pennant (Insectivora, Soricidae) in Bulgaria. Acta Parasitologica 50, 56–64.Google Scholar
Vaucher, C (1971) Les Cestodes parasites des soricidae d'Europe. Etude anatomique, révision taxonomique et biologie. Revue Suisse de Zoologie 78, 1–113.CrossRefGoogle Scholar
von Nickisch-Rosenegk, M, Brown, WM and Boore, JL (2001) Complete sequence of the mitochondrial genome of the tapeworm Hymenolepis diminuta: gene arrangements indicate that platyhelminths are eutrochozoans. Molecular Biology and Evolution 18, 721–730.CrossRefGoogle ScholarPubMed
Waeschenbach, A and Littlewood, DTJ (2017) A molecular framework for the Cestoda. pp. 431–451 in Caira, JN and Jensen, K (Eds) Planetary biodiversity inventory (2008–2017): tapeworms from vertebrate bowels of the earth. Lawrence, Kansas, University of Kansas, Natural History Museum.Google Scholar
Williams, BD, Schrank, B, Huynh, C, Shownkeen, R and Waterston, RH (1992) A genetic mapping system in Caenorhabditis elegans based on polymorphic sequence-tagged sites. Genetics 131, 609–624.CrossRefGoogle ScholarPubMed
Zhao, GH, Wang, HB, Jia, YQ, Zhao, W, Hu, XF, Yu, SK and Liu, GH (2016) The complete mitochondrial genome of Pseudanoplocephala crawfordi and a comparison with closely related cestode species. Journal of Helminthology 90, 588–595.CrossRefGoogle Scholar