Hostname: page-component-78c5997874-t5tsf Total loading time: 0 Render date: 2024-11-10T10:45:05.076Z Has data issue: false hasContentIssue false
  • English
  • Français

Phylogeny of Dictyocaulus (lungworms) from eight species of ruminants based on analyses of ribosomal RNA data

Published online by Cambridge University Press:  09 October 2003

J. HÖGLUND ,
D. A. MORRISON ,
B. P. DIVINA ,
E. WILHELMSSON  and
J. G. MATTSSON
J. HÖGLUND
Affiliation:
Department of Parasitology (SWEPAR), National Veterinary Institute and Swedish University of Agriculture Sciences, 751 89 Uppsala, Sweden
D. A. MORRISON
Affiliation:
Department of Parasitology (SWEPAR), National Veterinary Institute and Swedish University of Agriculture Sciences, 751 89 Uppsala, Sweden
B. P. DIVINA
Affiliation:
Department of Parasitology (SWEPAR), National Veterinary Institute and Swedish University of Agriculture Sciences, 751 89 Uppsala, Sweden College of Veterinary Medicine, University of the Philippines Los Baños, College, Laguna, 4031 Philippines
E. WILHELMSSON
Affiliation:
Department of Parasitology (SWEPAR), National Veterinary Institute and Swedish University of Agriculture Sciences, 751 89 Uppsala, Sweden
J. G. MATTSSON
Affiliation:
Department of Parasitology (SWEPAR), National Veterinary Institute and Swedish University of Agriculture Sciences, 751 89 Uppsala, Sweden
Get access Rights & Permissions [Opens in a new window]

Abstract

In this study, we conducted phylogenetic analyses of nematode parasites within the genus Dictyocaulus (superfamily Trichostrongyloidea). Lungworms from cattle (Bos taurus), domestic sheep (Ovis aries), European fallow deer (Dama dama), moose (Alces alces), musk ox (Ovibos moschatus), red deer (Cervus elaphus), reindeer (Rangifer tarandus) and roe deer (Capreolus capreolus) were obtained and their small subunit ribosomal RNA (SSU) and internal transcribed spacer 2 (ITS2) sequences analysed. In the hosts examined we identified D. capreolus, D. eckerti, D. filaria and D. viviparus. However, in fallow deer we detected a taxon with unique SSU and ITS2 sequences. The phylogenetic position of this taxon based on the SSU sequences shows that it is a separate evolutionary lineage from the other recognized species of Dictyocaulus. Furthermore, the analysis of the ITS2 sequence data indicates that it is as genetically distinct as are the named species of Dictyocaulus. Therefore, either this taxon needs to be recognized as a new species, or D. capreolus, D. eckerti and D. viviparus need to be combined into a single species. Traditionally, the genus Dictyocaulus has been placed as a separate family within the superfamily Trichostrongyloidea. The present molecular phylogenetic analyses support the placement as a separate family, but the current data do not support the placement of the Dictyocaulidae within the Trichostrongyloidea without a reassessment of the placement of the superfamily Strongyloidea. While D. eckerti has been regarded as the one and only lungworm species of cervids, this study showed that 4 host species including 3 members of Cervidae (moose, reindeer, red deer) and 1 Bovidae (musk ox) were infected with this parasite. Host ranges of D. viviparus (cattle), D. filaria (sheep) and D. capreolus (moose and roe deer) were more restricted. No clear pattern of co-evolution between the dictyocaulid taxa and their bovid and cervid hosts could be determined.

Keywords

DictyocaulusStrongylidagenetic diversitygenotypesphylogentic analysisSSU rRNAITS2ruminantsScandinavia
Type
Research Article
Information
Parasitology , Volume 127 , Issue 2 , August 2003 , pp. 179 - 187
Copyright
2003 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

REFERENCES

ANDERSON, R. C. (1992). Nematode Parasites of Vertebrates: their Development and Transmission. CABI Publishing, Cambridge.
BANDELT, H.-J. & DRESS, A. W. M. (1992). Split decomposition: a new and useful approach to phylogenetic analysis of distance data. Molecular Phylogenetics and Evolution 1, 242–252.CrossRefGoogle Scholar
BIENIOSCHEK, S., REHBEIN, S. & RIBBECK, R. (1996). Cross-infections between fallow deer and domestic ruminants with large lungworms (Dictyocaulus spp.). Applied Parasitology 37, 229–238.Google Scholar
BLAXTER, M. L., LEY, P. D., GAREY, J. R., LIU, L. X., SCHELDEMAN, P., VIERSTRAETE, A., VANFLETEREN, J. R., MACKAY, L. Y., DORRIS, M., FRISSE, L. M., VIDA, J. T. & KELLEY, T. W. (1998). A molecular evolutionary framework for the phylum Nematoda. Nature, London 392, 71–75.CrossRefGoogle Scholar
CAMPBELL, A. J. D., GASSER, R. B. & CHILTON, N. B. (1995). Differences in a ribosomal DNA sequence of Strongylus species allows identification of single eggs. International Journal for Parasitology 25, 359–365.CrossRefGoogle Scholar
CHARLESTON, M. A. (1998). Spectrum: spectral analysis of phylogenetic data. Bioinformatics 14, 98–99.CrossRefGoogle Scholar
DIVINA, B., WILHELMNSSON, E., MATTSSON, J. G., WALLER, P. & HÖGLUND, J. (2000). Identification of Dictyocaulus spp. in ruminants by morphological and molecular analyses. Parasitology 121, 193–201.Google Scholar
DIVINA, B. P. & HÖGLUND, J. (2002). Heterologous transmission of Dictyocaulus capreolus from roe deer (Capreolus capreolus) to cattle (Bos taurus). Journal of Helminthology 76, 125–130.CrossRefGoogle Scholar
DURETTE-DESSET, M. C., HUGONNET, L. & CHABAUD, A. G. (1988). Redescription de Dictyocaulus noerneri Railliet et Henry, 1907, parasite de Capreolus capreolus en Europe, comparison avec D. viviparus (Bloch, 1782) parasite du bétail. Annales de Parasitologie Humaine et Comparée 63, 285–295.CrossRefGoogle Scholar
EPE, C., BIENIOSCHEK, S., REHBEIN, S. & SCHNIEDER, T. (1995). Comparative RAPD-PCR analysis of lungworms (Dictyocaulidae) from fallow deer, cattle, sheep and horses. Journal of Veterinary Medicine 42, 187–191.CrossRefGoogle Scholar
EPE, C., SAMSON-HIMMELSTJERNA, G. V. & SCHNIEDER, T. (1997). Differences in a ribosomal DNA sequence of lungworm species (Nematoda: Dictyocaulidae) from fallow deer, cattle, sheep and donkeys. Research in Veterinary Science 62, 17–21.CrossRefGoogle Scholar
GIBBONS, L. & HÖGLUND, J. (2002). Dictyocaulus capreolus n. sp. (Nematoda, Trichostrongyloidea) from roe deer, Capreolus capreolus and moose, Alces alces in Sweden. Journal of Helminthology 76, 119–124.Google Scholar
GIBBONS, L. M. & KHALIL, L. F. (1988). A revision of the genus Dictyocaulus Railliet & Henry, 1907 (Nematoda: Trichostrongylidea) with the description of D. africanus n. sp. from African artiodactylids. Journal of African Zoology 102, 151–175.Google Scholar
HENDY, M. D. & PENNY, D. (1993). Spectral analysis of phylogenetic data. Journal of Classification 10, 5–24.CrossRefGoogle Scholar
HEISE, M., EPE, C. & SCHNEIDER, T. (1999). Differences in the second internal transcribed spacer (ITS-2) of eight species of gastrointestinal nematodes of ruminants. Journal of Parasitology 85, 431–435.CrossRefGoogle Scholar
HOSTE, H., CHILTON, N. B., GASSER, R. B. & BEVERIDGE, I. (1995). Differences in the second internal transcribed spacer (ribosomal DNA) between five species of Trichostrongylus (Nematoda: Trichostrongylidae). International Journal for Parasitology 25, 75–80.CrossRefGoogle Scholar
HUELSENBECK, J. P. & CRANDALL, K. A. (1997). Phylogeny estimation and hypothesis testing using maximum likelihood. Annual Review of Ecology and Systematics 28, 437–466.CrossRefGoogle Scholar
HUELSENBECK, J. P. & RONQUIST, F. (2001). MrBayes: Bayesian inference of phylogenetic trees. Bioinformatics 17, 754–755.CrossRefGoogle Scholar
HUFFMAN, B. (2003). The Ultimate Ungulate Page. http://www.ultimateungulate.com/Accessed on 2003-02-03.
HUSON, D. H. (1998). SplitsTree: analyzing and visualizing evolutionary data. Bioinformatics 14, 68–73.CrossRefGoogle Scholar
HÖGLUND, J., WILHELMSSON, E., CHRISTENSSON, D., MORNER, T., WALLER, P. & MATTSSON, J. G. (1999). ITS2 sequences of Dictyocaulus species from cattle, roe deer and moose in Sweden: molecular evidence for a new species. International Journal for Parasitology 29, 607–611.CrossRefGoogle Scholar
JACOBS, D. E., ZHU, X., GASSER, R. B. & CHILTON, N. B. (1997). PCR-based methods for identification of potentially zoonotic ascaridoid parasites of the dog, fox and cat. Acta Tropica 68, 191–200.CrossRefGoogle Scholar
JANSEN, J. & BORGSTEEDE, F. H. (1990). Dictyocaulus species, lungworms in cattle and deer in The Netherlands. Tijdschrift voor Diergeneeskunde 115, 155–158.Google Scholar
LEGENDRE, P., DESDEVISES, Y. & BAZIN, E. (2002). A statistical test for host-parasite coevolution. Systematic Biology 51, 217–234.CrossRefGoogle Scholar
LICHTENFELS, J. R., PILITT, P. A. & LANCASTER, M. B. (1988). Systematics of the nematodes that cause ostertagiasis in cattle, sheep and goats in North America. Veterinary Parasitology 27, 3–12.CrossRefGoogle Scholar
MADDISON, W. P. & MADDISON, D. R. (1992). MacClade: Analysis of Phylogeny and Character Evolution. Sinauer Associates, Sunderland.
MORRISON, D. A. & ELLIS, J. T. (1997). Effects of nucleotide sequence alignment on phylogeny estimation: a case study of 18S rDNAs of Apicomplexa. Molecular Biology and Evolution 14, 428–441.CrossRefGoogle Scholar
NADLER, S. A. (1992). Phylogeny of some ascaridoid nematodes, inferred from comparison of 18S and 28S rRNA sequences. Molecular Biology and Evolution 9, 932–944.Google Scholar
NADLER, S. A. (2002). Species delimitation and nematode biodiversity: phylogenies rule. Nematology 4, 615–626.CrossRefGoogle Scholar
NYLANDER, J. A. A. (2002). Testing Models of Evolution – MrModeltest Version 1.1b. Department of Systematic Zoology, Evolutionary Biology Centre, Uppsala University, Uppsala.
PAGE, R. D. M. (1996). TreeView: an application to display phylogenetic trees on personal computers. Computer Applications in the Biosciences 12, 357–358.Google Scholar
RAILLIET, A. & HENRY, A. (1907). Sur les variations des strongyles de l'appareil respiratoire des mammifères. Comptes Rendus des Séances de la Société de Biologie 63, 751–753.Google Scholar
SCHNIEDER, T., EPE, C. & SAMSON-HIMMELSTJERNA, G. V. (1996). Species differentiation of lungworms (Dictyocaulidae) by polymerase chain reaction/restriction-fragment-length polymorphism of a second internal transcribed spacers of ribosomal DNA. Parasitology Research 82, 392–394.CrossRefGoogle Scholar
SKRJABIN, K. I., SHIKHOBALOVA, N. P. & SCHULTZ, R. S. (1954). Dictyocaulidae, Heligosomatidae and Ollulanidae in animals. In Essentials of Nematology (ed. Skrjabin, K. I.), Academy of Sciences, Moscow(in Russian). English translation (1971) by Israel Program of Scientific Translation, Jerusalem.
STEVENSON, L. A., CHILTON, N. B. & GASSER, R. B. (1995). Differentiation of Haemonchus placei from H. contortus (Nematoda: Trichostrongylidae) by the ribosomal DNA second internal transcribed spacer. International Journal for Parasitology 25, 483–488.Google Scholar
STEVENSON, L. A., GASSER, R. B. & CHILTON, N. B. (1996). The ITS-2 rDNA of Teladorsagia circumcincta, T. trifurcata and T. davtiani (Nematoda: Trichostrongylidae) indicates that these taxa are one species. International Journal for Parasitology 26, 1123–1126.Google Scholar
SWOFFORD, D. L. (1998). PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods), Version 4. Sinauer Associates, Sunderland, Massachussetts.
SWOFFORD, D. L., OLSEN, G. J., WADDELL, P. J. & HILLIS, D. M. (1996). Phylogenetic inference. In Molecular Systematics, 2nd Edn (ed. Hillis, D. M., Moritz, C. & Mable, B. K.), pp. 407–514. Sinauer Associates, Sunderland.
THOMPSON, J. D., GIBSON, T. J., PLEWNIAK, F., JEANMOUGIN, E. F. & HIGGINS, D. G. (1997). The CLUSTAL-X windows interface: Flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 25, 4876–4882.CrossRefGoogle Scholar
URQUHART, G. M., ARMOUR, J., DUNCAN, J. L., DUNN, A. M. & JENNINGS, F. W. (1996). Veterinary Parasitology. Blackwell Science Ltd, Oxford.
VON SAMSON-HIMMELSTJERNA, G., WOIDTKE, S., EPE, C. & SCHNIEDER, T. (1997). Species-specific polymerase chain reaction for the differentiation of larvae from Dictyocaulus viviparus and Dictyocaulus eckerti. Veterinary Parasitology 68, 119–126.CrossRefGoogle Scholar
WUYTS, J., VAN DE PEER, Y., WINKELMANS, T. & DE WACHTER, R. (2002). The European database on small subunit ribosomal RNA. Nucleic Acids Research 30, 183–185.CrossRefGoogle Scholar
ZARLENGA, D. S., HOBERG, E. P., STRINGFELLOW, F. & LICHTENFELS, J. R. (1998). Comparisons of two polymorphic species of Ostertagia and phylogenetic relationships within the Ostertagiinae (Nematoda: Trichostrongyloidea) inferred from ribosomal DNA repeat and mitochondrial DNA sequences. Journal of Parasitology 84, 806–812.CrossRefGoogle Scholar
ZARLENGA, D. S., LICHTENFELS, J. R. & STRINGFELLOW, F. (1994). Cloning and sequence analysis of the small subunit ribosomal RNA gene from Nematodirus battus. Journal of Parasitology 80, 342–344.CrossRefGoogle Scholar