Phylogenetic relationships and systematics of tapeworms of the family Davaineidae (Cestoda, Cyclophyllidea), with emphasis on species in rodents
Language English Country Czech Republic Media electronic
Document type Journal Article
PubMed
39022895
DOI
10.14411/fp.2024.011
PII: 2024.011
Knihovny.cz E-resources
- Keywords
- 28S, Anoplocephalidae, Davaineinae, Inermicapsifer, Inermicapsiferinae, Raillietina, nad1, phylogeny,
- MeSH
- Cestoda * classification genetics MeSH
- Cestode Infections * veterinary parasitology MeSH
- Phylogeny * MeSH
- Rodentia * parasitology MeSH
- NADH Dehydrogenase genetics MeSH
- Birds MeSH
- RNA, Ribosomal, 28S genetics analysis MeSH
- Animals MeSH
- Check Tag
- Animals MeSH
- Publication type
- Journal Article MeSH
- Names of Substances
- NADH Dehydrogenase MeSH
- RNA, Ribosomal, 28S MeSH
The present study aims at clarifying the poorly known phylogenetic relationships and systematics of cestodes of the family Davaineidae Braun, 1900 (Cyclophyllidea), primarily the genus Raillietina Fuhrmann, 1920 and of the subfamily Inermicapsiferinae (Anoplocephalidae) from mammals (mostly rodents, 31 new isolates) and birds (eight new isolates). Phylogenetic analyses are based on sequences of the large subunit ribosomal RNA gene (28S) and mitochondrial NADH dehydrogenase subunit 1 gene (nad1). The main phylogenetic pattern emerging from the present analysis is the presence of three independent lineages within the main clade of the subfamily Davaineinae, one of which is almost entirely confined to species from rodents and the other two show a mixture of species from birds and mammals. It is suggested that the major diversification of the main clade took place in birds, possibly in galliforms. The subsequent diversification included repeated host shifts from birds to mammals and to other birds, and from rodents to other mammals, showing that colonisation of new host lineages has been the main driver in the diversification of davaineine cestodes. It is also shown that all isolates of Inermicapsifer Janicki, 1910, mainly from rodents, form a monophyletic group positioned among Raillietina spp. in the "rodent lineage", indicating that the genus Inermicapsifer is a member of the family Davaineidae. This means that the subfamily Inermicapsiferinae and the family Inermicapsiferidae should be treated as synonyms of the Davaineidae, specifically the subfamily Davaineinae. Three additional genera generally included in the Inermicapsiferinae, i.e. Metacapsifer Spasskii, 1951, Pericapsifer Spasskii, 1951 and Thysanotaenia Beddard, 1911, are also assigned here to the Davaineidae (subfamily Davaineinae). Raillietina spp. were present in all three main lineages and appeared as multiple independent sublineages from bird and mammalian hosts, verifying the non-monophyly of the genus Raillietina and suggesting a presence of multiple new species and genera.
Department of Conservation Ecology and Entomology Stellenbosch University Matieland South Africa
Department of Helminthology Faculty of Tropical Medicine Mahidol University Bangkok Thailand
Faculty of Biological and Environmental Sciences Helsinki University Finland;
Institut de Recerca de la Biodiversitat Universitat de Barcelona Spain
IRL HealthDEEP CNRS Kasetsart University Mahidol University Bangkok Thailand
See more in PubMed
Baer J.G., Fain A. 1955: Les Cestodes des Pangolins. Bull. Soc. Neuchâtel. Sci. Nat. 78: 37-52.
Beveridge I. 1994: Family Anoplocephalidae Cholodkovsky, 1902. In: L.F. Khalil, A. Jones and R.A. Bray (Eds.), Keys to the Cestode Parasites of Vertebrates. CABI, Wallingford, pp. 315-366.
Butboonchoo P., Wongsawad C., Rojanapaibul A., Chai J.-Y. 2016: Morphology and molecular phylogeny of Raillietina spp. (Cestoda: Cyclophyllidea: Davaineidae) from domestic chickens in Thailand. Kor. J. Parasitol. 54: 777-786. DOI
Caira J.N., Jensen K. 2017: Planetary Biodiversity Inventory (2008-2017): Tapeworms from the Vertebrate Bowels of the Earth. University of Kansas, Natural History Museum, Special Publication No. 25, Lawrence, 464 pp.
Caira J.N., Jensen K., Barbeau E. (Eds.) 2024: Global Cestode Database. World Wide Web electronic publication, www.tapewormdb.uconn.edu.
Dawson M.R., Marivaux L., Li C.-K., Beard K.C., Métais G. 2006: A recently discovered living rodent is a survivor of a family thought to have been extinct for 11 million years. Science 311: 1456-1458. DOI
Edgar R.C. 2004: MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucl. Acids Res. 32: 1792-1797. DOI
Hoberg E.P., Jones A., Bray R.A. 1999: Phylogenetic analysis among the families of the Cyclophyllidea (Eucestoda) based on comparative morphology, with new hypotheses for co-evolution in vertebrates. Syst. Parasitol. 42: 51-73. DOI
Huelsenbeck J.P., Ronquist F., Nielsen R., Bollback J.P. 2001: Bayesian inference of phylogeny and its impact on evolutionary biology. Science 294: 2310-2314. DOI
Hugot J.P., Feliu C., Douangboupha B., Ribas A. 2013: Laoxyuris laonasti n. gen., n. sp. (Nematoda: Syphaciinae) parasite of Laonastes aenigmamus (Rodentia: Diatomyidae): morphology, biology, taxonomy, phylogeny. Infect. Genet. Evol. 16: 113-121. DOI
Jones A., Bray R.A. 1994: Family Davaineidae Braun, 1900. In: L.F. Khalil, A. Jones, and R.A. Bray (Eds.), Keys to the Cestode Parasites of Vertebrates, CABI, Wallingford, pp. 407-441.
Joyeux C., Baer J. 1936: Helminthes des rats de Madagascar: contribution a l'etude de Davainea madagascarensis (Dav., 1869). Bull. Soc. Pathol. Exot. 29: 611-619.
Littlewood D.T.J., Waeschenbach A., Nikolov P.N. 2008: In search of mitochondrial markers for resolving the phylogeny of cyclophyllidean tapeworms (Platyhelminthes, Cestoda) - a test study with Davaineidae. Acta Parasitol. 53: 133-144. DOI
Lockyer A.E., Olson P.D., Littlewood D.T.J. 2003: Utility of complete large and small subunit rRNA genes in resolving the phylogeny of the Neodermata (Platyhelminthes): implications and a review of the cercomer theory. Biol. J. Linn. Soc. 78: 155-171. DOI
Lopez-Neyra C.R. 1954: Anoplocephalidae. Rev. Ibér. Parasitol. 14: 13-130, 22-290, 303-396.
Lopez-Neyra C.R. 1955: Anoplocephalidae. Rev. Ibér. Parasitol. 15: 33-84.
Mariaux J., Tkach V.V., Vasileva G.P., Waeschenbach A., Beveridge I., Dimitrova Y.D., Haukisalmi V., Greiman S.E., Littlewood D.T.J., Makarikov A.A., Phillips A.J., Razafiarisolo T., Widmer V., Georgiev B.B. 2017: Cyclophyllidea van Beneden in Braun, 1900. In: J.N. Caira and K. Jensen (Eds.), Planetary Biodiversity Inventory (2008-2017): Tapeworms from Vertebrate Bowels of the Earth. University of Kansas, Natural History Museum, Special Publication No. 25, Lawrence, pp. 77-148.
Mettrick D.F. 1959: A new tapeworm, Inermicapsifer rhodesiensis sp. nov. from a scaly ant-eater, Manis temminckii, in southern Rhodesia. J. Helminthol. 33: 273-276. DOI
Mettrick D.F., Weir J.S. 1963: Studies on the genus Inermicapsifer Janicki, 1910 with notes on some genera in the subfamilies Inermicapsiferinae, Linstowiinae, and Davaineinae. Proc. Helminthol. Soc. Wash. 30: 199-205.
Miquel J., Świderski Z., Feliu C. 2016: Spermatozoon ultrastructure of Thysanotaenia congolensis (Cyclophyllidea, Anoplocephalidae, Inermicapsiferinae): phylogenetic implications. Parasitol. Res. 115: 3083-3091. DOI
Movsesyan S.O. 2003a: [Davaineata - Tapeworms of Animals and Man. I]. Nauka, Moskva, 395 pp. (In Russian.)
Movsesyan S.O. 2003b: [Davaineata - Tapeworms of Animals and Man. II]. Nauka, Moskva, 262 pp. (In Russian.)
Nguyen D.X., Nguyen N.X., Nguyen D.D., Dinh T.H., Le D.T., Dinh D.H. 2014: Distribution and habitat of the Laotian rock rat Laonastes aenigmamus Jenkins, Kilpatrick, Robinson and Timmins, 2005 (Rodentia: Diatomyidae) in Vietnam. Biodivers. Data J. 2: e4188. DOI
Nicolas V., Herbreteau V., Couloux A., Keovichit K., Douangboupha B., Hugot J.-P. 2012: A remarkable case of micro-endemism in Laonastes aenigmamus (Diatomyidae, Rodentia) revealed by nuclear and mitochondrial DNA sequence data. PLoS One 7: e48145. DOI
O'Callaghan M. 2004: Studies on the systematics of the cestodes infecting the emu, Dromaius novaehollandiae (Latham, 1790). Ph. D. Thesis, The University of Adelaide, Adelaide, 236 pp.
O'Callaghan M.G., Davies M., Andrews R.H. 2000: Species of Raillietina Fuhrmann, 1920 (Cestoda: Davaineidae) from the emu, Dromaius novaehollandiae. Trans. R. Soc. S. Aust. 124: 105-116.
Oliveira Simões R., Simões S.B.E., Luque J.L., Iñiguez A.M., Maldonado Júnior A. 2017: First record of Raillietina celebensis (Cestoda: Cyclophyllidea) in South America: redescription and phylogeny. J. Parasitol. 103: 359-365. DOI
Olson P.D., Littlewood D.T., Bray R.A., Mariaux J. 2001: Interrelationships and evolution of the tapeworms (Platyhelminthes: Cestoda). Mol. Phylogenet. Evol. 19: 443-467. DOI
Panti-May J.A., Moguel-Chin W.I., Hernández-Mena D.I., Cárdenas-Vargas M.H., Torres-Castro M., García-Prieto L., Digiani M.C., Hernández-Betancourt S.F., Vidal-Martínez V.M. 2023: Helminths of small rodents (Heteromyidae and Cricetidae) in the Yucatan Peninsula, Mexico: an integrative taxonomic approach to their inventory. Zootaxa 5357: 205-240. DOI
Poux C., Madsen O., Marquard E., Vieites D.R., De Jong W.W., Vences M. 2005: Asynchronous colonisation of Madagascar by the four endemic clades of primates, tenrecs, carnivores, and rodents as inferred from nuclear genes. Syst. Biol. 54: 719-730. DOI
Ronquist F., Huelsenbeck J.P. 2003: MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572-1574. DOI
Schenk J.J., Rowe K.C., Steppan S.J. 2013: Ecological opportunity and incumbency in the diversification of repeated continental colonizations by muroid rodents. Syst. Biol. 62: 837-864. DOI
Schmidt G.D. 1986: CRC Handbook of Tapeworm Identification. CRC Press Inc., Boca Raton, 675 pp.
Siddiqui T.R., Hoque M.R., Roy B.C., Anisuzzaman, Alam M.Z., Khatun M.S., Dey A.R. 2023: Morphological and phylogenetic analysis of Raillietina spp. in indigenous chickens (Gallus gallus domesticus) in Bangladesh. Saudi J. Biol. Sci. 30: 103784. DOI
Spasskii A.A. 1951: Anoplocephalate Tapeworms of Domestic and Wild Animals (English translation). The Academy of Sciences of the USSR, Moscow, 783 pp.
Spasskii A.A. 1996: [On the systematics of davaineids (Cestoda: Cyclophyllidea)]. In: Parazitologiya v Ukraine. Materiali konf. URNOP, posvyashh. 90-letiyu A. P. Markevicha, Kiev, pp. 88-91. (In Russian.)
Świderski Z., Miquel J., Conn D.B. 2015a: Functional ultrastructure of eggs and cellular organization of hexacanths of the cyclophyllidean cestode Thysanotaenia congolensis: a phylogenetic implication of obtained results. Parasitology 143: 320-333. DOI
Świderski Z., Miquel J., Feliu C. 2015b: Functional ultrastructure of the parenchymatic capsules of the cestode Thysanotaenia congolensis (Cyclophyllidea, Anoplocephalidae, Inermicapsiferinae). Parasitol. Res. 114: 297-303. DOI
Tamura K., Stecher G., Kumar S. 2021: MEGA11: Molecular Evolutionary Genetics Analysis Version 11. Mol. Biol. Evol. 38: 3022-3027. DOI
Tuli M.D., Li H., Pan X., Li S., Zhai J., Wu Y., Chen W., Huang W., Feng Y., Xiao L., Yuan D. 2022: Heteroplasmic mitochondrial genomes of a Raillietina tapeworm in wild pangolin. Parasit. Vectors 15: 204. DOI
Van der Auwera G., Chapelle S., De Wachter R. 1994: Structure of the large ribosomal subunit RNA of Phytophthora megasperma, and phylogeny of oomycetes. FEBS Letters 338: 133-136. DOI
Waeschenbach A., Littlewood D.T.J. 2017: A molecular framework for the Cestoda. In: J.N. Caira and K. Jensen (Eds.), Planetary Biodiversity Inventory (2008-2017): Tapeworms from Vertebrate Bowels of the Earth. University of Kansas, Natural History Museum, Special Publication No. 25, Lawrence, pp. 431-451.
Waeschenbach A., Webster B.L., Bray R.A., Littlewood D.T.J. 2007: Added resolution among ordinal level relationships of tapeworms (Platyhelminthes: Cestoda) with complete small and large subunit nuclear ribosomal RNA genes. Mol. Phylogenet. Evol. 45: 311-325. DOI