Skip to main content
Log in

Molecular characterization of the Indian poultry nodular tapeworm, Raillietina echinobothrida (Cestoda: Cyclophyllidea: Davaineidae) based on rDNA internal transcribed spacer 2 region

  • Original Article
  • Published:
Journal of Parasitic Diseases Aims and scope Submit manuscript

Abstract

The nodular tapeworm, Raillietina echinobothrida is a well studied avian gastrointestinal parasite of family Davaineidae (Cestoda: Cyclophyllidea). It is reported to be the largest in size and second most prevalent species infecting chicken in north-east India. In the present study, morphometrical methods coupled with the molecular analysis of the second internal transcribed spacer (ITS2) region of ribosomal DNA were employed for precise identification of the parasite. The annotated ITS2 region was found to be 446 bp long and further utilized to elucidate the phylogenetic relationships and its species-interrelationships at the molecular level. In phylogenetic analysis similar topology was observed among the trees obtained by distance-based neighbor-joining as well as character-based maximum parsimony tree building methods. The query sequence R. echinobothrida is well aligned and placed within the Davaineidae group, with all Raillietina species well separated from the other cyclophyllidean (taeniid and hymenolepid) cestodes, while Diphyllobothrium latum (Pseudophyllidea: Diphyllobothriidae) was rooted as an out-group. Sequence similarities indeed confirmed our hypothesis that Raillietina spp. are neighboring the position with other studied species of order Cyclophyllidea against the out-group order Pseudophyllidea. The present study strengthens the potential of ITS2 as a reliable marker for phylogenetic reconstructions.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Alvarez I, Wendel JF (2003) Ribosomal ITS sequences and plant phylogenetic inference. Mol Phylogenet Evol 29:417–434

    Article  CAS  PubMed  Google Scholar 

  • Ashokan KV, Pillai MM (2008) In silico characterization of silk fibroin protein using computational tools and servers. Asian J Exp Sci 22:265–274

    Google Scholar 

  • Beveridge I, Campbell RA, Palm HW (1999) Preliminary cladistic analysis of genera of the cestode order Trypanorhyncha Diesing, 1863. Syst Parasitol 42:29–49

    Article  CAS  PubMed  Google Scholar 

  • Bowles J, Blair D, McManus DP (1995) A molecular phylogeny of the genus Echinococcus. Parasitology 110:317–328

    Article  CAS  PubMed  Google Scholar 

  • Bray RA, Jones A, Hoberg EP (1999) Observations on the phylogeny of the cestode order Pseudophyllidea Carus, 1863. Syst Parasitol 42:13–20

    Article  CAS  PubMed  Google Scholar 

  • Brooks DR, Hoberg EP (2001) Parasite systematics in the 21st century: opportunities and obstacles. Trends Parasitol 17:273–275

    Article  CAS  PubMed  Google Scholar 

  • Coleman A (2003) ITS2 is a double-edged tool for eukaryotic evolutionary comparisons. Trends Genet 19:370–375

    Article  CAS  PubMed  Google Scholar 

  • Engelmann JC, Rahmann S, Wolf M, Schultz J, Fritzilas E, Kneitz S, Dandekar T, Müller T (2009) Modeling cross-hybridization on phylogenetic DNA microarrays increases the detection power of closely related species. Mol Ecol Resour 9:83–93

    Article  CAS  PubMed  Google Scholar 

  • Ghatani S, Shylla JA, Tandon V, Chatterjee A, Roy B (2012) Molecular characterization of pouched amphistome parasites (Trematoda: Gastrothylacidae) using ribosomal ITS2 sequence and secondary structures. J Helminthol 86:117–124

    Article  CAS  PubMed  Google Scholar 

  • Gogoi AR, Hazarika RN (1975) Tetramorium tortosum (Rog), an intermediate host of poultry tapeworms Raillietina echinobothrida and Raillietina tetragona. Indian Vet J 52:939–941

    Google Scholar 

  • Goswami LM, Prasad PK, Tandon V, Chatterjee A (2009) Molecular characterization of Gastrodiscoides hominis (Platyhelminthes: Trematoda: Digenea) inferred from ITS rDNA sequence analysis. Parasitol Res 104:1485–1490

    Article  CAS  PubMed  Google Scholar 

  • Haukisalmi V, Wickstrom LM, Hantula J, Henttonen H (2001) Taxonomy, genetic differentiation and Holarctic biogeography of Paranoplocephala spp. (Cestoda: Anoplocephallidae) in collared lemmings (Dicrostonyx; Arvicolinae). Biol J Linn Soc 74:171–196

    Article  Google Scholar 

  • Hershkovitz M, Lewis L (1996) Deep-level diagnostic value of the rDNA-ITS region. Mol Biol Evol 13:1276–1295

    Article  CAS  PubMed  Google Scholar 

  • Hoberg EP, Mariaux J, Justine JL, Brooks DR, Weekes PJ (1997) Phylogeny of the orders of the Eucestoda (Cercomeromorphae) based on comparative morphology: historical perspectives and a new working hypothesis. J Parasitol 83:1128–1147

    Article  CAS  PubMed  Google Scholar 

  • Hoberg EP, Jones A, Bray RA (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

    Article  CAS  PubMed  Google Scholar 

  • Hoberg EP, Mariaux J, Brooks DR (2001) Phylogeny among orders of the Eucestoda (Cercomeromorphae): integrating morphology, molecules and total evidence. In: Littlewood DJT, Bray RA (eds) Interrelationships of the Platyhelminthes. Taylor & Francis, London, pp 112–126

    Google Scholar 

  • Horsfall MW (1938) Observations on the Life History of Raillietina echinobothrida and of R. tetragona (Cestoda). J Parasitol 24:409–421

    Article  Google Scholar 

  • Huang A, Li JW, Shen ZQ, Wang XW, Jin M (2006) High-throughput identification of clinical pathogenic fungi by hybridization to oligonucleotide microarray. J Clin Microbiol 44:3299–3305

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Jones MF, Horsfall MW (1935) Ants as intermediate hosts for two species of Raillietina parasitic in chickens. J Parasitol 21:442–443

    Google Scholar 

  • Jyrwa DB, Tandon V, Lyngdoh RD (2009) Molecular characterization of Lytocestus spp. (Eucestoda: Caryophyllidea) from Clarias batrachus (L.) in Meghalaya. In: Tandon V, Yadav AK, Roy B (eds) Current trends in parasitology. Proceedings of the 20th national congress of parasitology, India, November 3–5, 2008. Panima Publishing Corporation, New Delhi, p 137–146

  • Khalil LF, Jones A, Bray RA (eds) (1994) Keys to the cestode parasites of vertebrates. Commonwealth Agriculture Bureaux International, Wallingford, pp 407–441

    Google Scholar 

  • Literak F, Tenora V, Letkova M, Goldova N, Torres J, Olson PD (2006) Mesocestoides litteratus (Batsch, 1786) (Cestoda: Cyclophyllidea: Mesocestoidae) from the red fox: morphological and 18S rDNA characterization of European isolates. Helminthologia 43:191–195

    Article  CAS  Google Scholar 

  • Littlewood DTJ, Olson PD (2001) Small subunit rDNA and the phylum Platyhelminthes: signal, noise, conflict and compromise. In: Littlewood DTJ, Bray RA (eds) Interrelationships of the Platyhelminthes. Taylor & Francis, London, pp 262–278

    Google Scholar 

  • Mariaux J (1996) Cestode systematics: any progress? Int J Parasitol 26:231–243

    Article  CAS  PubMed  Google Scholar 

  • Mariaux J (1998) A molecular phylogeny of the Eucestoda. J Parasitol 84:114–124

    Article  CAS  PubMed  Google Scholar 

  • Nei M, Kumar S (2000) Molecular evolution and phylogenetics. Oxford University Press, New York, p 333

    Google Scholar 

  • Park MH, Sim CJ, Baek J, Min GS (2007) Identification of genes suitable for DNA barcoding of morphologically indistinguishable Korean Halichondriidae sponges. Mol Cells 23:220–227

    CAS  PubMed  Google Scholar 

  • Prasad PK, Tandon V, Biswal DK, Goswami LM, Chatterjee A (2009a) Phylogenetic reconstruction using secondary structures and sequence motifs of ITS2 rDNA of Paragonimus westermani (Kerbert, 1878) Braun, 1899 (Digenea: Paragonimidae) and related species. BMC Genomics 10(Suppl 3):S25

    Article  PubMed Central  PubMed  Google Scholar 

  • Prasad PK, Tandon V, Biswal DK, Goswami LM, Chatterjee A (2009b) Use of sequence motifs as barcodes and secondary structures of internal transcribed spacer 2 (ITS2, rDNA) for identification of the Indian liver fluke, Fasciola (Trematoda: Fasciolidae). Bioinformation 3:314–320

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Prasad PK, Goswami LM, Tandon V, Chatterjee A (2011) PCR-based molecular characterization and in silico analysis of food-borne trematode parasites Paragonimus westermani, Fasciolopsis buski and Fasciola gigantica from northeast India using ITS2 rDNA. Bioinformation 6:64–68

    Article  PubMed Central  PubMed  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    CAS  PubMed  Google Scholar 

  • Sambrook J, Russel D (2001) Molecular cloning: a laboratory manual, 3rd edn. Cold Springs Harbour Press, New York

    Google Scholar 

  • Sawada I (1965) On the genus Raillietina fuhrmann 1920 (II). J Nara Gakugei Univ (Nat) 13:5–38

    Google Scholar 

  • Schmidt GD (1986) CRC Handbook of tapeworm identification. CRC Press, Boca Raton 675 pp

    Google Scholar 

  • Sharma SK, Dkhar J, Kumaria S, Tandon P, Rao SR (2012) Assessment of phylogenetic inter-relationships in the genus Cymbidium (Orchidaceae) based on internal transcribed spacer region of rDNA. Gene 495:10–15

    Article  CAS  PubMed  Google Scholar 

  • Soulsby EJL (1982) Helminths, Arthropods and Protozoa of domesticated animals, 7th edn. ELBS and Bailliere Tindall, London

    Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony method. Mol Biol Evol 28:2731–2739

    Article  CAS  PubMed  Google Scholar 

  • Tandon V, Biswal DK, Prasad PK, Malsawmtluangi C (2010) Reconstructing the phylogenetic relationships of the cyclophyllidean cestodes: a case study using ITS2 rDNA and sequence structure alignment. In: Fred A, Filipe J, Gamboa H (eds) Biomedical engineering systems and technologies. BIOSTEC 2010, CCIS 127. Springer, Berlin, pp 309–321

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Waeschenbach A, Webster BL, Bray RA, Littlewood DTJ (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

    Article  CAS  PubMed  Google Scholar 

  • Wiemers M, Keller A, Wolf M (2009) ITS2 secondary structure improves phylogeny estimation in a radiation of blue butterflies of the subgenus Agrodiaetus (Lepidoptera: Lycaenidae: Polyommatus). BMC Evol Biol 9:300

    Article  PubMed Central  PubMed  Google Scholar 

  • Woese CR, Fox GE (1977) Phylogenetic structure of the prokaryotic domain: the primary kingdoms. Proc Natl Acad Sci USA 74:5088–5090

    Article  CAS  PubMed  Google Scholar 

  • Wolf M, Achtziger M, Schultz J, Dandekar T, Müller T (2005) Homology modeling revealed more than 20,000 rRNA internal transcribed spacer 2 (ITS2) secondary structures. RNA 11:1616–1623

    Article  CAS  PubMed  Google Scholar 

  • Yadav AK, Tandon V (1991) Helminth parasitism of domestic fowl (Gallus domesticus L.) in a subtropical high-rainfall area of India. Beitr Trop Landwirtsch Veterinarmed 29:97–104

    CAS  PubMed  Google Scholar 

  • Yao H, Song J, Liu C, Luo K, Han J et al (2010) Use of ITS2 Region as the universal DNA barcode for plants and animals. Plos One 5:e13102

    Article  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

Authors thank the Department of Biotechnology (Government of India), New Delhi, for their financial support for the study. Thanks are also due to the Head, Department of Zoology, NEHU, for providing infrastructural facilities.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to V. Tandon.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ramnath, Jyrwa, D.B., Dutta, A.K. et al. Molecular characterization of the Indian poultry nodular tapeworm, Raillietina echinobothrida (Cestoda: Cyclophyllidea: Davaineidae) based on rDNA internal transcribed spacer 2 region. J Parasit Dis 38, 22–26 (2014). https://doi.org/10.1007/s12639-012-0184-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12639-012-0184-2

Keywords

Navigation