Hostname: page-component-cd9895bd7-mkpzs Total loading time: 0 Render date: 2024-12-18T10:54:25.909Z Has data issue: false hasContentIssue false
  • English
  • Français

Phylogenetics of Trachylina (Cnidaria: Hydrozoa) with new insights on the evolution of some problematical taxa

Published online by Cambridge University Press:  08 September 2008

Allen G. Collins ,
Bastian Bentlage ,
Alberto Lindner ,
Dhugal Lindsay ,
Steven H.D. Haddock ,
Gerhard Jarms ,
Jon L. Norenburg ,
Thomas Jankowski  and
Paulyn Cartwright
Allen G. Collins*
Affiliation:
NMFS, National Systematics Laboratory, National Museum of Natural History, MRC-153, Smithsonian Institution, PO Box 37012, Washington, DC 20013-7012, USA
Bastian Bentlage
Affiliation:
Department of Ecology and Evolutionary Biology, University of Kansas, 1200 Sunnyside Avenue, Lawrence, KS 66045, USA
Alberto Lindner
Affiliation:
Centro de Biologia Marinha—USP–Rodovia Manoel Hipólito do Rego, Km 131, 5—São Sebastião, SP, Brazil
Dhugal Lindsay
Affiliation:
Japan Agency for Marine-Earth Science and Technology (JAMSTEC), Yokosuka, Japan
Steven H.D. Haddock
Affiliation:
Monterey Bay Aquarium Research Institute, 7700 Sandholdt Road, Moss Landing, CA 95039, USA
Gerhard Jarms
Affiliation:
Biozentrum Grindel und Zoologisches Museum, Universität Hamburg, Martin-Luther-King Platz 3, 20146 Hamburg, Germany
Jon L. Norenburg
Affiliation:
Smithsonian Institution, PO Box 37012, Invertebrate Zoology, NMNH, W-216, MRC163, Washington, DC 20013-7012, USA
Thomas Jankowski
Affiliation:
Federal Institute of Aquatic Science and Technology, Dübendorf 8600, Switzerland
Paulyn Cartwright
Affiliation:
Department of Ecology and Evolutionary Biology, University of Kansas, 1200 Sunnyside Avenue, Lawrence, KS 66045, USA
*
Correspondence should be addressed to: Allen G. Collins, NMFS, National Systematics Laboratory, National Museum of Natural History, MRC-153, Smithsonian Institution, PO Box 37012, Washington, DC 20013-7012, USA email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Some of the most interesting and enigmatic cnidarians are classified within the hydrozoan subclass Trachylina. Despite being relatively depauperate in species richness, the clade contains four taxa typically accorded ordinal status: Actinulida, Limnomedusae, Narcomedusae and Trachymedusae. We bring molecular data (mitochondrial 16S and nuclear small and large subunit ribosomal genes) to bear on the question of phylogenetic relationships within Trachylina. Surprisingly, we find that a diminutive polyp form, Microhydrula limopsicola (classified within Limnomedusae) is actually a previously unknown life stage of a species of Stauromedusae. Our data confirm that the interstitial form Halammohydra sp. (Actinulida) is derived from holopelagic direct developing ancestors, likely within the trachymedusan family Rhopalonematidae. Trachymedusae is shown to be diphyletic, suggesting that the polyp stage has been lost independently at least two times within trachyline evolution. Narcomedusae is supported as a monophyletic group likely also arising from trachymedusan ancestors. Finally, some data, albeit limited, suggest that some trachyline species names refer to cryptic species that have yet to be sorted taxonomically.

Keywords

phylogeneticsTrachylinaproblematic taxa
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 88 , Special Issue 8: Hydrozoans , December 2008 , pp. 1673 - 1685
Copyright
Copyright © Marine Biological Association of the United Kingdom 2008

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

Bouillon, J. (1957) Limnocnida congoensis nouvelle espece de Limnomeduse du bassin du Congo. Revue de Zoologie et de Botanique Africaines 56, 388–395.Google Scholar
Bouillon, J. (1985) Essai de classification des Hydropolypes–Hydromeduses (Hydrozoa–Cnidaria). Indo-Malayan Zoology 1, 29–243.Google Scholar
Bouillon, J. (1987) Considérations sur le développement des Narcoméduses et sur leur position phylogénétique. Indo-Malayan Zoology 4, 189–278.Google Scholar
Bouillon, J. and Boero, F. (2000) The Hydrozoa: a new classification in the light of old knowledge. Thalassia Salentina 24, 1–45.Google Scholar
Bouillon, J. and Deroux, G. (1967) Remarques sur des Cnidaires du type de Microhydrula pontica Valkanov 1965, trouvés a Roscoff. Cahiers de Biologie Marine 8, 253–272.Google Scholar
Brooks, W.K. (1886) Life history of the Hydromedusae. A discussion of the medusae and of the significance of metagenesis. Memoirs of the Boston Society of Natural History 3, 359–430.Google Scholar
Browne, E.T. and Kramp, P.L. (1939) Hydromedusae from the Falkland Islands. Discovery Reports XVIII, 265–322.Google Scholar
Castresana, J. (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Molecular Biology and Evolution 17, 540–552.CrossRefGoogle ScholarPubMed
Clausen, C. (1971) Interstitial Cnidaria: present status of their systematics and ecology. Smithsonian Contributions to Zoology 76, 1–8.Google Scholar
Collins, A.G. (2002) Phylogeny of Medusozoa and the evolution of cnidarian life cycles. Journal of Evolutionary Biology 15, 418–432.Google Scholar
Collins, A.G., Schuchert, P., Marques, A.C., Jankowski, T., Medina, M. and Schierwater, B. (2006a) Medusozoan phylogeny and character evolution clarified by new large and small subunit rDNA data and an assessment of the utility of phylogenetic mixture models. Systematic Biology 55, 97–115.CrossRefGoogle Scholar
Collins, A.G., Bentlage, B., Matsumoto, G.I., Haddock, S.H.D., Osborn, K. and Schierwater, B. (2006b) Solution to the phylogenetic enigma of Tetraplatia, a worm-shaped cnidarian. Biology Letters 2, 120–124.CrossRefGoogle Scholar
Cunningham, C.W. and Buss, L.W. (1993) Molecular evidence for multiple episodes of pedomorphosis in the family Hydractiniidae. Biochemical Systematics and Ecology 21, 57–69.CrossRefGoogle Scholar
Daly, M., Brugler, M.R., Cartwright, P., Collins, A.G., Dawson, M.N., Fautin, D.G., France, S.C., McFadden, C.S., Opresko, D.M., Rodrigues, E., Romano, S.L. and Stake, J.L. (2007) The phylum Cnidaria: a review of phylogenetic patterns and diversity 300 years after Linnaeus. Zootaxa 1668, 127–182.CrossRefGoogle Scholar
Edgar, R.C. (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32, 1792–1797.CrossRefGoogle ScholarPubMed
Edwards, C. (1973) Contributory thoughts on form, function, habitat and classification of hydroids and hydromedusae. Publications of the Seto Marine Biological Laboratory 20, 11–22.Google Scholar
Gould, S.J. (1977) Ontogeny and phylogeny. Cambridge, MA: Belknap Press.Google Scholar
Govindarajan, A.F., Halanych, K.M. and Cunningham, C.W. (2005) Mitochondrial evolution and phylogeography in the hydrozoan Obelia geniculata (Cnidaria). Marine Biology 146, 213–222.CrossRefGoogle Scholar
Hand, C. (1955) A study of the structure, affinities, and distribution of Tetraplatia volitans Busch (Coelenterata: Hydrozoa: Pteromedusae). Pacific Science 9, 332–348.Google Scholar
Hashimoto, H. (1981) The fresh water hydroid Astrohydra japonica new genus new species. Annotationes Zoologicae Japoneses 54, 207–212.Google Scholar
Hashimoto, H. (1985) Medusa of fresh-water hydroid Astrohydra japonica. Annotationes Zoologicae Japoneses 2, 761–766.Google Scholar
Hyman, L.H. (1940) The invertebrates, vol. 1. Protozoa through Ctenophora. New York: McGraw-Hill.Google Scholar
Jankowski, T. (2001) The freshwater jellyfish of the world—a taxonomic and systematic literature study. Hydrobiologia 462, 91–113.CrossRefGoogle Scholar
Jankowski, T., Collins, A.G. and Campbell, R. (2008) Global diversity of inland water cnidarians. Hydrobiologia 595, 35–40.Google Scholar
Jarms, G. and Tiemann, H. (1996) On a hydropolyp without tentacles Microhydrula limopsicola n. sp., epibiontic on bivalve shells from the Antarctic. Scientia Marina 60, 109–115.Google Scholar
Kikinger, R. and Salvini-Plawen, L.V. (1995) Development from polyp to stauromedusa in Stylocoronella (Cnidaria: Scyphozoa). Journal of the Marine Biological Association of the United Kingdom 75, 899–912.CrossRefGoogle Scholar
Kramp, P.L. (1938) Die meduse von Ostroumovia inkermanica (Pal.-Ostr.) und die systematische stellung der olindiiden. Zoologischer Anzeiger 122, 103–108.Google Scholar
Marques, A.C. and Collins, A.G. (2004) Cladistic analysis of Medusozoa and cnidarian evolution. Invertebrate Biology 123, 23–42.CrossRefGoogle Scholar
Medina, M., Collins, A.G., Silberman, J.D. and Sogin, M.L. (2001) Evaluating hypotheses of basal animal phylogeny using complete sequences of large and small subunit rRNA. Proceedings of the National Academy of Sciences of the United States of America 98, 9707–9712.CrossRefGoogle ScholarPubMed
Medlin, L., Elwood, H.J., Stickel, S. and Sogin, M.L. (1988) The characterization of enzymatically amplified eukaryotic 16S-like rRNA-coding regions. Gene 71, 491–499.Google Scholar
Metschnikoff, E. (1886) Embryologische Studien an Medusen. Ein Beitrag Zur Genealogie der Primitiv-Organe. Wien: Alfred Hölder.Google Scholar
Miglietta, M.P., Piraino, S., Kubato, S. and Schuchert, P. (2007) Species in the genus Turritopsis (Cnidaria, Hydrozoa): a molecular evaluation. Journal of Zoological Systematics and Evolutionary Research 45, 11–19.CrossRefGoogle Scholar
Mühlhardt, C. (2003) Molekularbiologie—genomics. Heidelberg: Spektrum Akademischer Verlag.Google Scholar
Naumov, D.V. (1960) Hydroids and hydromedusae of the USSR. Jerusalem: Israel Programme for Scientific Translations. [Translated from Russian (1969).]Google Scholar
Norenburg, J.L. and Morse, M.P. (1983) Euphysa ruthae (Athecata, Corymorphidae) sp. n., a psammophilic solitary hydroid with statocysts and reversed polarity buds, with a discussion of euphysine characters. Transactions of the American Microscopical Society 102, 1–17.Google Scholar
Petersen, K.W. (1990) Evolution and taxonomy in capitate hydroids and medusae (Cnidaria: Hydrozoa). Zoological Journal of the Linnaean Society 100, 101–231.CrossRefGoogle Scholar
Posada, D. and Crandall, K.A. (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14, 817–818.Google Scholar
Raikova, E.V. (1994) Life cycle, cytology, and morphology of Polypodium hydriforme, a coelenterate parasite of the eggs of acipenseriform fishes. Journal of Parasitology 80, 1–22.Google Scholar
Rees, W.J. (1958) The relationships of Moerisia lyonsi Boulenger and the family Moerisiidae, with capitate hydroids. Proceedings of the Zoological Society of London 130, 537–545.CrossRefGoogle Scholar
Remane, A. (1927) Halammohydra, ein eigenartiges Hydrozoon der Nord- und Ostsee. Zeitschrift für Morphologie und Ökologie der Tiere 7, 643–677.Google Scholar
Salvini-Plawen, L.V. (1987) Mesopsammic Cnidaria from Plymouth (with systematic notes). Journal of the Marine Biological Association of the United Kingdom 67, 623–637.CrossRefGoogle Scholar
Schuchert, P. (1996) The marine fauna of New Zealand: athecate hydroids and their Medusae (Cnidaria: Hydrozoa). Wellington: New Zealand Oceanographic Institute.Google Scholar
Schuchert, P. (1998) How many hydrozoan species are there? Zoologische Verhandelingen 323, 209–219.Google Scholar
Schuchert, P. (2005) Species boundaries in the hydrozoan genus Coryne. Molecular Phylogenetics and Evolution 36, 194–199.CrossRefGoogle ScholarPubMed
Schuchert, P. (2007) The Hydrozoa Directory, Version 15, September 2007. (http://www.ville-ge.ch/musinfo/mhng/hydrozoa/hydrozoa-directory.htm).Google Scholar
Swedmark, B. (1964) The interstitial fauna of marine sand. Biological Reviews 39, 1–42.Google Scholar
Swedmark, B. and Teissier, G. (1958) Otohydra vagans n. g., n. sp., hydrozoaire des sables, apparanté aux Halammohydridées. Comptes Rendus Hebdomadaires des Séances de l'Académie des Sciences de Paris 247, 238–240.Google Scholar
Swedmark, B. and Teissier, G. (1966) The Actinulida and their evolutionary significance in the Cnidaria. In Rees, W.J. (ed.) The Cnidaria and their evolution. London: Academic Press, pp. 119–133.Google Scholar
Swofford, D.L. (2002) PAUP*: Phylogenetic Analysis Using Parsimony (*and Other Methods), version 4. Sunderland, MA: Sinauer Associates.Google Scholar
Voigt, O., Collins, A.G., Pearse, V.B., Hadrys, H. and Schierwater, B. (2004) Placozoa—no longer a phylum of one. Current Biology 14, R944–R945.Google Scholar
Werner, B. (1965) Halammohydra Remane, Medusennatur und Stellung im System. Zoologischer Anzeiger Supplement 28, 163–177.Google Scholar
Wiens, J.J., Bonett, R.M. and Chippindale, P.T. (2005) Ontogeny discombobulates phylogeny: paedomorphosis and higher-level salamander phylogeny. Systematic Biology 54, 91–110.CrossRefGoogle Scholar
Zagal, C.J. (2004) Population biology and habitat of the stauromedusan Haliclystus auricula in southern Chile. Journal of the Marine Biological Association of the United Kingdom 84, 331–336.Google Scholar
Zwickl, D.J. (2006) Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion. PhD thesis, The University of Texas, Austin, USA.Google Scholar