Skip to main content

Molecular phylogeny of clade III nematodes reveals multiple origins of tissue parasitism

  • S. A. NADLER (a1), R. A. CARRENO (a2), H. MEJÍA-MADRID (a1), J. ULLBERG (a1), C. PAGAN (a1), R. HOUSTON (a3) and J.-P. HUGOT (a4)...

Molecular phylogenetic analyses of 113 taxa representing Ascaridida, Rhigonematida, Spirurida and Oxyurida were used to infer a more comprehensive phylogenetic hypothesis for representatives of ‘clade III’. The posterior probability of multiple alignment sites was used to exclude or weight characters, yielding datasets that were analysed using maximum parsimony, likelihood, and Bayesian inference methods. Phylogenetic results were robust to differences among inference methods for most high-level taxonomic groups, but some clades were sensitive to treatments of characters reflecting differences in alignment ambiguity. Taxa representing Camallanoidea, Oxyurida, Physalopteroidea, Raphidascarididae, and Skrjabillanidae were monophyletic in all 9 analyses whereas Ascaridida, Ascarididae, Anisakidae, Cosmocercoidea, Habronematoidea, Heterocheilidae, Philometridae, Rhigonematida and Thelazioidea were never monophyletic. Some clades recovered in all trees such as Dracunculoidea and Spirurina included the vast majority of their sampled species, but were non-monophyletic due to the consistent behaviour of one or few ‘rogue’ taxa. Similarly, 102 of 103 clade III taxa were strongly supported as monophyletic, yet clade III was paraphyletic due to the grouping of Truttaedacnitis truttae with the outgroups. Mapping of host ‘habitat’ revealed that tissue-dwelling localization of nematode adults has evolved independently at least 3 times, and relationships among Spirurina and Camallanina often reflected tissue predilection rather than taxonomy.

Corresponding author
*Corresponding author: Department of Nematology, University of California, Davis, CA 95616-8668, USA. Tel: 001 530 752 2121. Fax: 001 530 752 5674. E-mail:
Hide All
Alfaro M. E., Zoller S. and Lutzoni F. (2003). Bayes or Bootstrap? A simulation study comparing the performance of Bayesian Markov chain Monte Carlo sampling and bootstrapping in assessing phylogenetic confidence. Molecular Biology and Evolution 20, 255266.
Anderson R. C. (1984). The origins of zooparasitic nematodes. Canadian Journal of Zoology 62, 317328.
Anderson R. C. (1988). Nematode transmission patterns. The Journal of Parasitology 74, 3045.
Anderson R. C. (2000). Nematode Parasites of Vertebrates: their Development and Transmission, 2nd Edn. CABI Publishing, New York.
Anderson R. C. and Bain O. (Eds.) (1976). CIH Keys to the Nematode Parasites of Vertebrates. No. 3 Keys to Genera of the Order Spirurida. Part 3. Diplotriaenoidea, Aproctoidea and Filarioidea. Commonwealth Agricultural Bureaux, Farnham Royal, Slough.
Anderson R. C., Chabaud A. G., Willmott S. and Hartwich G. (Eds.) (1974). CIH Keys to the Nematode Parasites of Vertebrates. No. 2. Keys to Genera of the Ascaridoidea, Commonwealth Agricultural Bureaux, Farnham Royal, Slough.
Andrássy I. (1976). Evolution as a Basis for the Systematization of Nematodes. Pitman Publishing, London.
Berry V. and Gascuel O. (1996). On the interpretation of bootstrap trees: Appropriate threshold of clade selection and induced gain. Molecular Biology and Evolution 13, 9991011.
Bert W., Messiaen M., Manhout J., Houthoofd W. and Borgonie G. (2006). Evolutionary loss of parasitism by nematodes? Discovery of a free-living filaroid nematode. The Journal of Parasitology 92, 645647.
Blaxter M. (2003). Nematoda: genes, genomes and the evolution of parasitism. Advances in Parasitology 54, 101195.
Blaxter M. L., De Ley P., Garey J. R., Liu L. X., Scheldeman P., Vierstraete A., Vanfleteren J. R., Mackey L. Y., Dorris M., Frisse L. M., Vida J. T. and Thomas W. K. (1998). A molecular evolutionary framework for the phylum Nematoda. Nature, London 392, 7175.
Carreno R. A. and Nadler S. A. (2003). Phylogenetic analysis of the Metastrongyloidea (Nematoda: Strongylida) inferred from ribosomal RNA gene sequences. The Journal of Parasitology 89, 965973.
Casiraghi M., Bain O., Guerrero R., Martin C., Pocacqua V., Gardner S. L., Franceschi A. and Bandi C. (2004). Mapping the presence of Wolbachia pipientis on the phylogeny of filarial nematodes: evidence for symbiont loss during evolution. International Journal for Parasitology 34, 191203.
Chabaud A. G. (Ed.) (1974). CIH Keys to the Nematode Parasites of Vertebrates. Class Nematoda. Keys to Subclasses, Orders and Superfamilies. Commonwealth Agricultural Bureaux, Farnham Royal, Slough.
Chabaud A. G. and Bain O. (1994). The evolutionary expansion of the Spirurida. International Journal for Parasitology 24, 11791201.
Chilton N. B., Huby-Chilton F., Gasser R. B. and Beveridge I. (2006). The evolutionary origins of nematodes within the order Strongylida are related to predilection sites within hosts. Molecular Phylogenetics and Evolution 40, 118128.
Chitwood B. G. (1937). A revised classification of the Nematoda. In Papers on Helminthology Published in Commemoration of the 30 year Jubileum of the Scientific, Educational and Social Activities of the Honoured Worker of Science K. J. Skrjabin and of the Fifteenth Anniversary of the All-Union Institute of Helminthology (ed. Skrjabin K. J., Shults R. S. and Gnyedina M. P.), pp. 6980. All-Union Lenin Academy of Agricultural Sciences, Moscow.
Chitwood B. G. (1950). Nemic relationships. In An Introduction to Nematology (ed. Chitwood B. G. and Chitwood M. B.), pp. 191205. B. G. Chitwood, Baltimore.
De Ley P. and Blaxter M. (2002). Systematic position and phylogeny. In The Biology of Nematodes (ed. Lee D. L.), pp. 130. Taylor and Francis, London.
Erixon P., Svennblad B., Britton T. and Oxelman B. (2003). Reliability of Bayesian posterior probabilities and bootstrap frequencies in phylogenetics. Systematic Biology 52, 665673.
Felsenstein J. (1978). Cases in which parsimony and compatibility methods will be positively misleading. Systematic Zoology 27, 401410.
Felsenstein J. (1985). Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39, 783791.
Fitch D. H. (1997). Evolution of male tail development in rhabditid nematodes related to Caenorhabditis elegans. Systematic Biology 46, 145179.
Gill L. L., Hardman N., Chappell L., Qu L. H., Nicoloso M. and Bachellerie J. P. (1988). Phylogeny of Onchocerca volvulus and related species deduced from rRNA sequence comparisons. Molecular and Biochemical Parasitology 28, 6976.
Holterman M., Van Der Wurff A., Van Den Elsen S., Van Megen H., Bongers T., Holovachov O., Bakker J. and Helder J. (2006). Phylum-wide analysis of SSU rDNA reveals deep phylogenetic relationships among nematodes and accelerated evolution toward crown clades. Molecular Biology and Evolution 23, 17921800.
Huelsenbeck J. P. (1997). Is the Felsenstein zone a fly trap? Systematic Biology 46, 6974.
Inglis W. G. (1965). Patterns of evolution in parasitic nematodes. In Third Symposium of the British Society for Parasitology (ed. Taylor A. E. R.), pp. 79124. Blackwell Scientific Publications, London.
Inglis W. G. (1983). An outline classification of the phylum Nematoda. Australian Journal of Zoology 31, 243255.
Kim K. H., Eom K. S. and Park J. K. (2006). The complete mitochondrial genome of Anisakis simplex (Ascaridida: Nematoda) and phylogenetic implications. International Journal for Parasitology 36, 319328.
Lemmon A. R. and Moriarty E. C. (2004). The importance of proper model assumption in Bayesian phylogenetics. Systematic Biology 53, 265277.
Lorenzen S. (1981). Entwurf eines phylogenetischen Systems der freilebenden Nematoden. Veröffentlichungen des Institut für Meeresforschungen Bremerhaven. Suppl. 7, 1472.
Lorenzen S. (1994). The Phylogenetic Systematics of Freeliving Nematodes. Ray Society, London.
Löytynoja A. and Milinkovitch M. C. (2003). A hidden Markov model for progressive multiple alignment. Bioinformatics, 19, 15051513.
Maddison D. R. and Maddison W. P. (2000). MacClade 4. Sinauer Associates, Inc., Sunderland.
Maggenti A. R. (1963). Comparative morphology in nemic phylogeny. In The Lower Metazoa, Comparative Biology and Phylogeny (ed. Dougherty E. C.), pp. 273282. University of California Press, Berkeley, USA.
Maggenti A. R. (1983). Nematode higher classification as influenced by species and family concepts. In Concepts in Nematode Systematics (ed. Stone A. R., Platt H. M. and Khalil L. F.), pp. 2540. Academic Press, London.
Micoletzky H. (1922). Die freilebenden Erd-Nematoden mit besonderer Berücksichtigung der Steiermark und der Bukowina, zugleich mit einer Revision samtlicher nicht marine, freilebender Nematoden in form von Genus-Beschreibungen und Bestimmungsschlusseln. Archiv für Naturgeschichte, Abteilung A, 87, 1650.
Moravec F., Molnar K. and 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 Parasitologica 45, 5661.
Nadler S. A. (1992). Phylogeny of some ascaridoid nematodes, inferred from comparison of 18S and 28S rRNA sequences. Molecular Biology and Evolution 9, 932944.
Nadler S. A., Bolotin E. and Stock S. P. (2006 a). Phylogenetic relationships of Steinernema Travassos, 1927 (Nematoda: Cephalobina: Steinernematidae) based on nuclear, mitochondrial and morphological data. Systematic Parasitology 63, 161181.
Nadler S. A., D'Amelio S., Fagerholm H. P., Berland B. and Paggi L. (2000). Phylogenetic relationships among species of Contracaecum Railliet & Henry, 1912 and Phocascaris Host, 1932 (Nematoda: Ascaridoidea) based on nuclear rDNA sequence data. Parasitology 121, 455463.
Nadler S. A., De Ley P., Mundo-Ocampo M., Smythe A. B., Patricia Stock S., Bumbarger D., Adams B. J., De Ley I. T., Holovachov O. and Baldwin J. G. (2006 b). Phylogeny of Cephalobina (Nematoda) : molecular evidence for recurrent evolution of probolae and incongruence with traditional classifications. Molecular Phylogenetics and Evolution 40, 696711.
Nadler S. A. and Hudspeth D. S. (1998). Ribosomal DNA and phylogeny of the Ascaridoidea (Nematoda: Secernentea) : implications for morphological evolution and classification. Molecular Phylogenetics and Evolution 10, 221236.
Nadler S. A. and Hudspeth D. S. (2000). Phylogeny of the Ascaridoidea (Nematoda: Ascaridida) based on three genes and morphology: hypotheses of structural and sequence evolution. The Journal of Parasitology 86, 380393.
Nixon K. C. (1999). The Parsimony Ratchet, a new method for rapid parsimony analysis. Cladistics 15, 407414.
Posada D. and Crandall K. A. (1998). MODELTEST: Testing the model of DNA substitution. Bioinformatics 14, 817818.
Qu L. H., Hardman N., Gill L., Chappell L., Nicoloso M. and Bachellerie J. P. (1986). Phylogeny of helminths determined by rRNA sequence comparison. Molecular and Biochemical Parasitology 20, 9399.
Read A. F. and Skorping A. (1995). The evolution of tissue migration by parasitic nematode larvae. Parasitology 111, 359371.
Ronquist F. and Huelsenbeck J. P. (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 15721574.
Sanderson M. J. and Shaffer H. B. (2002). Troubleshooting molecular phylogenetic analysis. The Annual Review of Ecology and Systematics 33, 4972.
Smythe A. B. and Nadler S. A. (2006). Molecular phylogeny of Acrobeloides and Cephalobus (Nematoda: Cephalobidae) reveals paraphyletic taxa and recurrent evolution of simple labial morphology. Nematology 8, 819836.
Smythe A. B., Sanderson M. J. and Nadler S. A. (2006). Nematode small subunit phylogeny correlates with alignment parameters. Systematic Biology 55, 972992.
Soltis P. S. and Soltis D. E. (2003). Applying the bootstrap in phylogeny reconstruction. Statistical Science 18, 256267.
Subbotin S. A., Sturhan D., Chizhov V. N., Volvas N. and Baldwin J. G. (2006). Phylogenetic analysis of Tylenchida Thorne, 1949 as inferred from D2 and D3 expansion fragments of the 28S rRNA gene sequences. Nematology 8, 455474.
Swofford D. L. (1998). PAUP*. Phylogenetic Anaylsis Using Parsimony (*and Other Methods). Sinauer Associates, Sunderland, MA, USA.
Taylor D. J. and Piel W. H. (2004). An assessment of accuracy, error, and conflict with support values from genome-scale phylogenetic data. Molecular Biology and Evolution 21, 15341537.
Wijová M., Moravec F., Horák A. and Lukes J. (2006). Evolutionary relationships of Spirurina (Nematoda: Chromadorea: Rhabditida) with special emphasis on dracunculoid nematodes inferred from SSU rRNA gene sequences. International Journal for Parasitology 36, 10671075.
Wijová M., Moravec F., Horák A., Modry D. and Lukes J. (2005). Phylogenetic position of Dracunculus medinensis and some related nematodes inferred from 18S rRNA. Parasitology Research 96, 133135.
Wilcox T. P., Zwickl D. J., Heath T. A. and Hillis D. M. (2002). Phylogenetic relationships of the dwarf boas and a comparison of Bayesian and bootstrap measures of phylogenetic support. Molecular Phylogenetics and Evolution 25, 361371.
Yamaguti S. (1961). The Nematodes of Vertebrates. Parts I and II. Interscience Publishers, New York.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

  • ISSN: 0031-1820
  • EISSN: 1469-8161
  • URL: /core/journals/parasitology
Please enter your name
Please enter a valid email address
Who would you like to send this to? *



Altmetric attention score

Full text views

Total number of HTML views: 13
Total number of PDF views: 99 *
Loading metrics...

Abstract views

Total abstract views: 420 *
Loading metrics...

* Views captured on Cambridge Core between September 2016 - 19th January 2018. This data will be updated every 24 hours.