Folia Parasitologica 58[2] 135-148 (2011) | DOI: 10.14411/fp.2011.013

Phylogenetic relationships of some spirurine nematodes (Nematoda: Chromadorea: Rhabditida: Spirurina) parasitic in fishes inferred from SSU rRNA gene sequences

Eva Černotíková1,2, Aleš Horák1, František Moravec1
1 Institute of Parasitology, Biology Centre of the Academy of Sciences of the Czech Republic, Branišovská 31, 370 05 České Budějovice, Czech Republic
2 Faculty of Science, University of South Bohemia, Branišovská 31, 370 05 České Budějovice, Czech Republic

Small subunit rRNA sequences were obtained from 38 representatives mainly of the nematode orders Spirurida (Camallanidae, Cystidicolidae, Daniconematidae, Philometridae, Physalopteridae, Rhabdochonidae, Skrjabillanidae) and, in part, Ascaridida (Anisakidae, Cucullanidae, Quimperiidae). The examined nematodes are predominantly parasites of fishes. Their analyses provided well-supported trees allowing the study of phylogenetic relationships among some spirurine nematodes. The present results support the placement of Cucullanidae at the base of the suborder Spirurina and, based on the position of the genus Philonema (subfamily Philoneminae) forming a sister group to Skrjabillanidae (thus Philoneminae should be elevated to Philonemidae), the paraphyly of the Philometridae. Comparison of a large number of sequences of representatives of the latter family supports the paraphyly of­ the genera Philometra, Philometroides and Dentiphilometra. The validity of the newly included genera Afrophilometra and Caranginema is not supported. These results indicate geographical isolation has not been the cause of speciation in this parasite group and no coevolution with fish hosts is apparent. On the contrary, the group of South-American species of Alinema, Nilonema and Rumai is placed in an independent branch, thus markedly separated from other family members. Molecular data indicate that the skrjabillanid subfamily Esocineminae (represented by Esocinema bohemicum) should be either elevated to the rank of an independent family or Daniconematidae (Mexiconema africanum) should be decreased to Daniconematinae and transferred to the family Skrjabillanidae. Camallanid genera Camallanus and Procamallanus, as well as the subgenera Procamallanus and Spirocamallanus are confirmed to be paraphyletic. Paraphyly has also been found within Filarioidea, Habronematoidea and Thelazioidea and in Cystidicolidae, Physalopteridae and Thelaziidae. The results of the analyses also show that Neoascarophis, Spinitectus and Rhabdochona are monophyletic, in contrast to the paraphyletic genus Ascarophis. They further confirm the independence of two subgenera, Rhabdochona and Globochona, in the genus Rhabdochona. The necessity of further studies of fish-parasitizing representatives of additional nematode families not yet studied by molecular methods, such as Guyanemidae, Lucionematidae or Tetanonematidae, is underscored.

Keywords: Nematoda, Spirurina, SSU rRNA, phylogeny, taxonomy

Received: August 20, 2010; Accepted: February 11, 2011; Published: June 1, 2011  Show citation

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Černotíková, E., Horák, A., & Moravec, F. (2011). Phylogenetic relationships of some spirurine nematodes (Nematoda: Chromadorea: Rhabditida: Spirurina) parasitic in fishes inferred from SSU rRNA gene sequences. Folia Parasitologica58(2), 135-148. doi: 10.14411/fp.2011.013
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References

  1. Anderson R.C. 2000: Nematode Parasites of Vertebrates. Their Development and Transmission. 2nd Ed. CABI Publishing, Wallingford, UK, 650 pp Go to original source...
  2. Anderson R.C., Chabaud A.G., Willmott S. 1974- 1983: Keys to the Nematode Parasites of Vertebrates. Nos. 1-10. Commonwealth Bureaux of Agriculture, Farnham Royal, Bucks, UK
  3. Anderson R.C., Chabaud A.G., Willmott S. 2009: Keys to the Nematode Parasites of Vertebrates. Archival Volume. CAB International, Wallingford, UK, 463 pp Go to original source...
  4. Blaxter M.L., De Ley P., Garey J.R., Liu L.X., Scheldeman P., Vierstraete A., Vanfleteren J.P., Mackey L.Y., Dorris M., Frisse L.M., Vida J.T., Thomas W.K. 1998: A molecular evolutionary framework for the phylum Nematoda. Nature 392: 71-75 Go to original source... Go to PubMed...
  5. Chabaud A.G. 1974: Class Nematoda. Keys to subclasses, orders and superfamilies. In: R.C. Anderson, A.G. Chabaud and S. Willmott (Eds.), CIH Keys to Nematode Parasites of Verte brates. No. 1. Commonwealth Bureaux of Agriculture, Farnham Royal, Bucks, UK, pp. 6-17
  6. Chabaud A.G. 1975: Keys to genera of the order Spirurida. Part 1. Camallanoidea, Dracunculoidea, Gnathostomatoidea, Physalopteroidea, Rictularoidea and Thelazioidea. In: R.C. Anderson, A.G. Chabaud and S. Willmott (Eds.), CIH Keys to the Nematode Parasites of Vertebrates, No. 3. Commonwealth Bureaux of Agriculture, Farnham Royal, Bucks (UK), 27 pp
  7. Chitwood B.G. 1933: A revised classification of the Nematoda. J. Parasitol. 20: 131
  8. Chitwood B.G. 1937: A revised classification of the Nematoda. In: Anonym (Ed.), Papers on Helminthology. 30 Year Jubilee K.I Skryabin. All-Union Lenin Academy of Agricultural Sciences, Moscow, pp. 67-79
  9. Chitwood B.G. 1950: An outline classification of the Nematoda. In: B.G. Chitwood and M.B. Chitwood (Eds.), Introduction to Nematology. University Park Press, Baltimore, Maryland, pp. 12-25
  10. De Ley P., Blaxter M.L. 2002: Systematic position and phylogeny. In: D.L. Lee (Ed.), The Biology of Nematodes. Tailor & Francis, London and New York, pp. 1-30
  11. De Ley P., Blaxter M.L. 2004: A new system for Nematoda: combining morphological characters with molecular trees, and translating clades into ranks and taxa. Nematol. Monogr. Perspect. 2: 633-653 Go to original source...
  12. Gibbons L.M. 2010: Keys to the Nematode Parasites of Vertebrates. Supplementary Volume. CABI, Wallingford, UK, 416 pp Go to original source...
  13. Hall T.A. 1999: BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Series 41: 95-98
  14. Holterman M., van der Wurff A., van den E lsen S., van Meg en H., Bongers T., Holovachov O., Bakker J., Helder J. 2006: Phylum-wide analysis of SSU rDNA reveals deep phylogenetic relationships among nematodes and accelerated evolution toward crown clades. Mol. Biol. Evol. 23: 1798-1800 Go to original source... Go to PubMed...
  15. 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 Go to original source... Go to PubMed...
  16. Ivashkin V.M., Khromova L.A. 1976: [Cucullanata and Gnathostomatata of Animals and Man and the Diseases Caused by Them. Essentials of Nematodology 27.] Nauka, Moscow, 436 pp. (In Russian.)
  17. Ivashkin V.M., Sobolev A.A., Khromova L.A. 1971: [Camallanata of Animals and Man and the Diseases Caused by Them. Essentials of Nematodology 22.] Nauka, Moscow, 388 pp. (In Russian.)
  18. Katoh K., Misawa K., Kuma K., Miyata T. 2002: MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 30: 3059-3066 Go to original source... Go to PubMed...
  19. Meldal B.H.M., Debenham N.J., De Ley P., De Ley I.T., Van fleteren J.R., Vierstraete A.R., Bert W., Borgonie G., Moens T., Tyler P.A., Austen M.C., Blaxter M.L., Rogers A.D., Lambshead P.J.D. 2007: An improved molecular phylogeny of the Nematoda with special emphasis on marine taxa. Mol. Phylogenet. Evol. 42: 622-636 Go to original source... Go to PubMed...
  20. Moravec F. 1994: Parasitic Nematodes of Freshwater Fishes of Europe. Academia and Kluwer Academic Publishers, Prague and Dordrecht, Boston, London, 473 pp
  21. Moravec F. 2004: Some aspects of the taxonomy and biology of dracunculoid nematodes parasitic in fishes: a review. Folia Parasitol. 51: 1-13 Go to original source... Go to PubMed...
  22. Moravec F. 2006: Dracunculoid and Anguillicoloid Nematodes Parasitic in Vertebrates. Academia, Prague, 634 pp
  23. Moravec F. 2007: Some aspects of the taxonomy and biology of adult spirurine nematodes parasitic in fishes: a review. Folia Parasitol. 54: 239-257 Go to original source... Go to PubMed...
  24. Moravec F., Charo -Karisa H., Jirku M. 2009: Philometrids (Nematoda: Philometridae) from fishes of Lake Turkana, Kenya, including two new species of Philometra and erection of Afrophilometra gen. n. Folia Parasitol. 56: 41-54 Go to original source... Go to PubMed...
  25. Moravec F., de Buron I. 2006: Two new species of philometrid nematodes (Nematoda: Philometridae) from the southern flounder Paralichthys lethostigma in the estuaries of South Carolina, USA. Folia Parasitol. 53: 139-146 Go to original source... Go to PubMed...
  26. Moravec F., Molnar K., Szekely C. 1998: Lucionema balatonense gen. et sp. n., a new nematode of a new family Lucionematidae fam. n. (Dracunculoidea) from the swimbladder of the European pikeperch, Stizostedion lucioperca (Pisces). Folia Parasitol. 45: 56-61
  27. Moravec F., Scholz T., Ash A., Kar P.K. 2010: New data on the morphology and taxonomy of three species of Rhabdochona (Nematoda: Rhabdochonidae) parasitizing fishes in India. Folia Parasitol. 57: 295-306 Go to original source... Go to PubMed...
  28. Moravec F., Taraschewski H., Anantaphruti M.T., Maipanich W., Laoprasert T. 2007: Heliconema longissimum (Ortlepp, 1923) (Nematoda: Physalopteridae) in Thailand, with remarks on the taxonomy of the Proleptinae Schulz, 1927. Syst. Parasitol. 66: 73-80 Go to original source... Go to PubMed...
  29. Nadler S.A., Carreno R.A., Mejia-Madrid H., Ullberg J., Pagan C., Houston R., Hugot J.-P. 2007: Molecular phylogeny of clade III nematodes reveals multiple origins of tissue parasitism. Parasitology 134: 1421-1442 Go to original source... Go to PubMed...
  30. Posada D., Crandall K.A. 1998: Modeltest: testing the model of DNA substitution. Bioinformatics 14: 817-818 Go to original source... Go to PubMed...
  31. Rudolphi C.A. 1808: Entozoorum Sive Vermium Intestinalium. Historia Naturalis, Vol. 1. Amstelaedami, 527 pp
  32. Sambrook J., Russell D.W. 2001: Molecular Cloning: A Laboratory Manual. 3rd Ed. Chapter 6. Protocol 1: 6.9-6.11. Cold Spring Harbor Laboratory Press, New York
  33. Shimodaira H. 2004: Approximately unbiased tests of regions using multistep-multiscale bootstrap resampling. Ann. Stat. 32: 2616-2641 Go to original source...
  34. Shimodaira H., Hasegawa M. 2001: CONSEL: for assessing the confidence of phylogenetic tree selection. Bioinformatics 17: 1246-1247 Go to original source... Go to PubMed...
  35. Stamatakis A. 2006: RAxML-VI-HPC: maximum likelihoodbased phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 2688-2690 Go to original source... Go to PubMed...
  36. van Megen H., van den E lsen S., Holterman M., Karssen G., Mooyman P., Bongers T., Holovachov O., Bakker J., Helder J. 2009: A phylogenetic tree of nematodes based on about 1200 full-length small subunit ribosomal DNA sequences. Nematology 11: 927-950 Go to original source...
  37. Wijova M., Moravec F., Horak A., Lukes J. 2006: Evolutionary relationships of Spirurina (Nematoda: Chromadorea: Rhabditida) with special emphasis on dracunculoid nematodes inferred from SSU rRNA gene sequences. Int. J. Parasitol. 36: 1067-1075 Go to original source... Go to PubMed...
  38. Yamaguti S. 1961: Nematodes of Vertebrates. Systema Helminthum 3. Interscience Publishers, New York - London, 1261 pp