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Hydrobiologia

, Volume 687, Issue 1, pp 11–20 | Cite as

Molecular phylogeny of glass sponges (Porifera, Hexactinellida): increased taxon sampling and inclusion of the mitochondrial protein-coding gene, cytochrome oxidase subunit I

  • Martin Dohrmann
  • Karri M. Haen
  • Dennis V. Lavrov
  • Gert Wörheide
Sponge Research Developments

Abstract

Marine sponges of the class Hexactinellida (glass sponges) are among the most understudied groups of Porifera, and molecular approaches to investigating their evolution have only recently emerged. Although these first results appeared reliable as they largely corroborated morphology-based hypotheses, they were almost exclusively based on ribosomal RNA genes (rDNA) and should, therefore, be further tested with independent types of genetic data, such as protein-coding genes. To this end, we established the mitochondrial-encoded cytochrome oxidase subunit I gene (COI) as an additional marker, and conducted phylogenetic analyses on DNA- and amino-acid level, as well as a supermatrix analysis based on combined COI DNA and rDNA alignments. Furthermore, we increased taxon sampling compared to previous studies by adding seven additional species. The COI-based phylogenies were largely congruent with the rDNA-based phylogeny but suffered from poor bootstrap support for many nodes. However, addition of the COI sequences to the rDNA data set increased resolution of the overall molecular phylogeny. Thus, although obtaining COI sequences from glass sponges turned out to be quite challenging, this gene appears to be a valuable supplement to rDNA data for molecular evolutionary studies of this group. Some implications of our extended phylogeny for the evolution and systematics of Hexactinellida are discussed.

Keywords

Porifera Hexactinellida Phylogeny Cytochrome oxidase subunit I Ribosomal DNA 

Notes

Acknowledgments

Work at the Wörheide lab was supported by the Deutsche Forschungsgemeinschaft (DFG; project Wo896/5-3). The DFG is further acknowledged for funding the Deep Down Under expedition (Project Wo896/7-1; www.deepdownunder.de). During writing of this manuscript, MD was supported by a Postdoctoral Fellowship of the Smithsonian Institution. Work at the Lavrov lab was supported by the National Science Foundation (NSF) through the Poriferan Tree of Life project (DEB-0828783; https://www.portol.org/). Shirley Pomponi (HBOI), Sally Leys, and Jean Vacelet are acknowledged for providing additional specimens. Our warmest thanks go to the organizers of the 8th World Sponge Conference for making this great meeting possible. Allen Collins and three anonymous reviewers provided comments that led to improvement of this manuscript. Finally, we would like to thank Alexandros Stamatakis for implementing paired-sites models in his amazing program, RAxML.

Supplementary material

10750_2011_727_MOESM1_ESM.doc (81 kb)
Supplementary material 1 (DOC 81 kb)

References

  1. Abascal, F., R. Zardoya & D. Posada, 2005. ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21: 2104–2105.PubMedCrossRefGoogle Scholar
  2. Akaike, H., 1974. A new look at the statistical model identifications. IEEE Transactions on Automatic Control 19: 716–723.CrossRefGoogle Scholar
  3. Bebenek, I. G., R. D. Gates, J. Morris, V. Hartenstein & D. K. Jacobs, 2004. sine oculis in basal Metazoa. Development Genes and Evolution 214: 342–351.PubMedCrossRefGoogle Scholar
  4. Borchiellini, C., N. Boury-Esnault, J. Vacelet & Y. Le Parco, 1998. Phylogenetic analysis of the Hsp70 sequences reveals the monophyly of Metazoa and specific phylogenetic relationships between animals and fungi. Molecular Biology and Evolution 15: 647–655.PubMedGoogle Scholar
  5. Bucklin, A., D. Steinke & L. Blanco-Bercial, 2011. DNA barcoding of marine Metazoa. Annual Review of Marine Science 3: 471–508.PubMedCrossRefGoogle Scholar
  6. Conejo, M., M. Bertin, S. A. Pomponi & W. R. Ellington, 2008. The early evolution of the phosphagen kinases – insights from choanoflagellate and poriferan arginine kinases. Journal of Molecular Evolution 66: 11–20.PubMedCrossRefGoogle Scholar
  7. de Queiroz, A. & J. Gatesy, 2007. The supermatrix approach to systematics. Trends in Ecology and Evolution 22: 34–41.PubMedCrossRefGoogle Scholar
  8. Dohrmann, M., O. Voigt, D. Erpenbeck & G. Wörheide, 2006. Non-monophyly of most supraspecific taxa of calcareous sponges (Porifera, Calcarea) revealed by increased taxon sampling and partitioned Bayesian analysis of ribosomal DNA. Molecular Phylogenetics and Evolution 40: 830–843.PubMedCrossRefGoogle Scholar
  9. Dohrmann, M., D. Janussen, J. Reitner, A. G. Collins & G. Wörheide, 2008. Phylogeny and evolution of glass sponges (Porifera, Hexactinellida). Systematic Biology 57: 388–405.PubMedCrossRefGoogle Scholar
  10. Dohrmann, M., A. G. Collins & G. Wörheide, 2009. New insights into the phylogeny of glass sponges (Porifera, Hexactinellida): monophyly of Lyssacinosida and Euplectellinae, and the phylogenetic position of Euretidae. Molecular Phylogenetics and Evolution 52: 257–262.PubMedCrossRefGoogle Scholar
  11. Dohrmann, M., C. Göcke, D. Janussen, J. Reitner, C. Lüter & G. Wörheide, 2011. Systematics and spicule evolution in dictyonal sponges (Hexactinellida: Sceptrulophora) with description of two new species. Zoological Journal of the Linnean Society (in press).Google Scholar
  12. Erpenbeck, D. & G. Wörheide, 2007. On the molecular phylogeny of sponges (Porifera). Zootaxa 1668: 107–126.Google Scholar
  13. Erpenbeck, D., J. N. A. Hooper & G. Wörheide, 2006. CO1 phylogenies in diploblasts and the ‘Barcoding of Life’ – are we sequencing a suboptimal partition? Molecular Ecology Notes 6: 550–553.CrossRefGoogle Scholar
  14. Felsenstein, J., 1985. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39: 783–791.CrossRefGoogle Scholar
  15. Göcke, C. & D. Janussen, 2011. ANT XXIV/2 (SYSTCO) Hexactinellida (Porifera) and bathymetric traits of Antarctic glass sponges (incorporating ANDEEP-material); including an emendation of the rediscovered genus Lonchiphora. Deep-Sea Research Part II: in press.Google Scholar
  16. Gouy, M., S. Guindon & O. Gascuel, 2010. SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Molecular Biology and Evolution 27: 221–224.PubMedCrossRefGoogle Scholar
  17. Gundacker, D., S. P. Leys, H. C. Schröder, I. M. Müller & W. E. G. Müller, 2001. Isolation and cloning of a C-type lectin from the hexactinellid sponge Aphrocallistes vastus: a putative aggregation factor. Glycobiology 11: 21–29.PubMedCrossRefGoogle Scholar
  18. Haen, K. M., B. F. Lang, S. A. Pomponi & D. V. Lavrov, 2007. Glass sponges and bilaterian animals share derived mitochondrial genomic features: a common ancestry or parallel evolution? Molecular Biology and Evolution 24: 1518–1527.PubMedCrossRefGoogle Scholar
  19. Hillis, D. M. & J. J. Bull, 1993. An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analysis. Systematic Biology 42: 182–192.Google Scholar
  20. Huelsenbeck, J. P. & B. Rannala, 2004. Frequentist properties of Bayesian posterior probabilities of phylogenetic trees under simple and complex substitution models. Systematic Biology 53: 904–913.PubMedCrossRefGoogle Scholar
  21. Ivanova, N. V., A. V. Borisenko & P. D. N. Hebert, 2009. Express barcodes: racing from specimen to identification. Molecular Ecology Resources 9(Supplement 1): 35–41.PubMedCrossRefGoogle Scholar
  22. Lanave, C., G. Preparata, C. Saccone & G. Serio, 1984. A new method for calculating evolutionary substitution rates. Journal of Molecular Evolution 20: 86–93.PubMedCrossRefGoogle Scholar
  23. Larkin, M. A., G. Blackshields, N. P. Brown, R. Chenna, P. A. McGettigan, H. McWilliam, F. Valentin, I. M. Wallace, A. Wilm, R. Lopez, J. D. Thompson, T. J. Gibson & D. G. Higgins, 2007. ClustalW and ClustalX version 2.0. Bioinformatics 23: 2947–2948.PubMedCrossRefGoogle Scholar
  24. Leys, S. P. G. O., G. O. Mackie & H. M. Reiswig, 2007. The biology of glass sponges. Advances in Marine Biology 52: 1–145.PubMedCrossRefGoogle Scholar
  25. Manuel, M., Y. Le Parco & C. Borchiellini, 2004. Comparative analysis of Brachyury T-domains, with the characterization of two new sponge sequences, from a hexactinellid and a calcisponge. Gene 340: 291–301.PubMedCrossRefGoogle Scholar
  26. Mehl, D., 1992. Die Entwicklung der Hexactinellida seit dem Mesozoikum. Paläobiologie, Phylogenie und Evolutionsökologie. Berliner Geowissenschaftliche Abhandlungen Reihe E: Paläobiologie 2: 1–164.Google Scholar
  27. Philippe, H., R. Derelle, P. Lopez, K. Pick, C. Borchiellini, N. Boury-Esnault, J. Vacelet, E. Renard, E. Houliston, E. Quéinnec, C. Da Silva, P. Wincker, H. Le Guyader, S. Leys, D. J. Jackson, F. Schreiber, D. Erpenbeck, B. Morgenstern, G. Wörheide & M. Manuel, 2009. Phylogenomics revives traditional views on deep animal relationships. Current Biology 19: 706–712.PubMedCrossRefGoogle Scholar
  28. Pick, K. S., H. Philippe, F. Schreiber, D. Erpenbeck, D. J. Jackson, P. Wrede, M. Wiens, A. Alié, B. Morgenstern, M. Manuel & G. Wörheide, 2010. Improved phylogenomic taxon sampling noticeably affects non-bilaterian relationships. Molecular Biology and Evolution 27: 1983–1987.PubMedCrossRefGoogle Scholar
  29. Reiswig, H. M., 2002. Family Tretodictyidae Schulze, 1886. In Hooper, J. N. A. & R. W. M. van Soest (eds), Systema Porifera. A Guide to the Classification of Sponges. Plenum, New York: 1341–1354.CrossRefGoogle Scholar
  30. Rokas, A., N. King, J. Finnerty & S. B. Carroll, 2003. Conflicting phylogenetic signals at the base of the metazoan tree. Evolution and Development 5: 346–359.PubMedCrossRefGoogle Scholar
  31. Rosengarten, R. D., E. A. Sperling, M. A. Moreno, S. P. Leys & S. L. Dellaporta, 2008. The mitochondrial genome of the hexactinellid sponge Aphrocallistes vastus: evidence for programmed translational frameshifting. BMC Genomics 9: 33.PubMedCrossRefGoogle Scholar
  32. Savill, N. J., D. C. Hoyle & P. G. Higgs, 2001. RNA sequence evolution with secondary structure constraints: comparison of substitution rate models using maximum-likelihood methods. Genetics 157: 399–411.PubMedGoogle Scholar
  33. Siddall, M. E., F. M. Fontanella, S. C. Watson, S. Kvist & C. Erséus, 2009. Barcoding bamboozled by bacteria: convergence to metazoan mitochondrial primer targets by marine microbes. Systematic Biology 58: 445–451.PubMedCrossRefGoogle Scholar
  34. Sperling, E. A., K. J. Peterson & D. Pisani, 2009. Phylogenetic-signal dissection of nuclear housekeeping genes supports the paraphyly of sponges and the monophyly of Eumetazoa. Molecular Biology and Evolution 26: 2261–2274.PubMedCrossRefGoogle Scholar
  35. Stamatakis, A., 2006. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 2688–2690.PubMedCrossRefGoogle Scholar
  36. Stamatakis, A., P. Hoover & J. Rougemont, 2008. A rapid bootstrap algorithm for the RAxML web servers. Systematic Biology 57: 758–771.PubMedCrossRefGoogle Scholar
  37. Tabachnick, K. R., 2002a. Lyssacinosida incertae sedis. In Hooper, J. N. A. & R. W. M. van Soest (eds), Systema Porifera. A Guide to the Classification of Sponges. Plenum, New York: 1506–1509.CrossRefGoogle Scholar
  38. Tabachnick, K. R., 2002b. Family Rossellidae Schulze, 1885. In Hooper, J. N. A. & R. W. M. van Soest (eds), Systema Porifera. A Guide to the Classification of Sponges. Plenum, New York: 1441–1505.CrossRefGoogle Scholar
  39. Tabachnick, K. R., 2002c. Family Euplectellidae Gray, 1867. In Hooper, J. N. A. & R. W. M. van Soest (eds), Systema Porifera. A Guide to the Classification of Sponges. Plenum, New York: 1388–1434.CrossRefGoogle Scholar
  40. Tabachnick, K. R. & H. M. Reiswig, 2002. Dictionary of Hexactinellida. In Hooper, J. N. A. & R. W. M. van Soest (eds), Systema Porifera. A Guide to the Classification of Sponges. Plenum, New York: 1224–1229.CrossRefGoogle Scholar
  41. Yang, Z., 1994. Maximum likelihood phylogenetic estimation from DNA sequences with variable rates over sites: approximate methods. Journal of Molecular Evolution 39: 306–314.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • Martin Dohrmann
    • 1
    • 5
  • Karri M. Haen
    • 2
  • Dennis V. Lavrov
    • 2
  • Gert Wörheide
    • 1
    • 3
    • 4
  1. 1.Department of Earth & Environmental Sciences, Palaeontology & GeobiologyLMU MunichMunichGermany
  2. 2.Department of Ecology, Evolution & Organismal BiologyIowa State UniversityAmesUSA
  3. 3.GeoBio-CenterLMUMunichGermany
  4. 4.Bavarian State Collections of Palaeontology & GeologyMunichGermany
  5. 5.Department of Invertebrate ZoologySmithsonian National Museum of Natural HistoryWashingtonUSA

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