Skip to main content
SpringerLink
Log in

Morphological and genetic analyses of xeniid soft coral diversity (Octocorallia; Alcyonacea)

  • Original Article
  • Published:
Organisms Diversity & Evolution Aims and scope Submit manuscript

Abstract

Studies on the biodiversity and evolution of octocorals are hindered by the incomplete knowledge of their taxonomy, which is due to few reliable morphological characters. Therefore, assessment of true species diversity within abundant and ecologically important families such as Xeniidae is difficult. Mitochondrial genes provide a reliable solution to this problem for a wide range of taxa. However, low mutation rates of the mitochondrial DNA in octocorals result in insufficient variability for species discrimination. We compared the variation of a fragment of the Signal Recognition Particle 54 gene (SRP54, proposed for octocorals) and the mitochondrial ND6/ND3 marker among members of the xeniid genera Ovabunda, Xenia, Heteroxenia and Bayerxenia. The mean uncorrected pairwise sequence divergence was 39 % for SRP54 compared to 2 % for ND6/ND3. Morphological assignments were not always supported by genetics: Species diversity was underestimated (one case) or overestimated, probably reflecting intraspecific polymorphisms or hinting at recent speciations. ND6/ND3 is informative for some species-level assignments, whereas SRP54 shows the variability needed for species delimitations within this understudied taxon. Our results on both genes show their potential for evolutionary and biodiversity studies in Xeniidae.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Achituv, Y., & Benayahu, Y. (1990). Polyp dimorphism and functional, sequential hermaphroditism in the soft coral Heteroxenia fuscescens (Octocorallia). Marine Ecology Progress Series, 64, 263–269.

    Article  Google Scholar 

  • Affeld, S., Kehraus, S., Waegele, H., & Koenig, G. (2009). Dietary derived sesquiterpenes from Phyllodesmium lizardensis Burghardt, Schrödl & Wägele (Opisthobranchia, Nudibranchia, Aeolidoidea). Journal of Natural Products, 72, 298–300.

    Article  PubMed  CAS  Google Scholar 

  • Aguilar, C., & Sanchez, J. A. (2007). Phylogenetic hypotheses of gorgoniid octocorals according to ITS2 and their predicted RNA secondary structures. Molecular Phylogenetics and Evolution, 43, 774–786.

    Article  PubMed  CAS  Google Scholar 

  • Aharonovich, D., & Benayahu, Y. (2011). Microstructure of octocoral sclerites for diagnosis of taxonomic features. Marine Biodiversity. doi:10.1007/s12526-011-0102-3.

  • Alderslade, P. (2001). Six new genera and six new species of soft coral, and some proposed familial and subfamilial changes within the Alcyonacea (Coelenterata, Octocorallia). Bulletin of the Biological Society of Washington, 10, 15–65.

    Google Scholar 

  • Anta, C., González, N., Santafé, G., Rodríguez, J., & Jiménez, C. (2002). New Xenia diterpenoids from the Indonesian soft coral Xenia sp. Journal of Natural Products, 65, 766–768.

    Article  PubMed  CAS  Google Scholar 

  • Baco, A. R., & Cairns, S. D. (2012). Comparing molecular variation to morphological species designations in the deep-sea coral Narella reveals new insights into seamount coral ranges. PLoS One, 7(9), e45555. doi:10.1371/journal.pone.0045555.

    Article  PubMed  CAS  Google Scholar 

  • Benayahu, Y. (1990). Xeniidae (Cniadaria: Octocorallia) from the Red Sea, with the description of a new species. Zoologische Medelingen Leiden, 64, 113–120.

    Google Scholar 

  • Berntson, E. A., Bayer, F. M., McArthur, A. G., & France, S. C. (2001). Phylogenetic relationships within the Octocorallia (Cnidaria: Anthozoa) based on nuclear 18S rRNA sequences. Marine Biology, 138, 235–246.

    Article  CAS  Google Scholar 

  • Burghardt, I., & Waegele, H. (2004). A new solar powered species of the genus Phyllodesmium Ehrenberg, 1831 (Mollusca: Nudibranchia: Aeolidoidea) from Indonesia with analysis of its photosynthetic activity and notes on biology. Zootaxa, 596, 1–18.

    Google Scholar 

  • Burghardt, I., Stemmer, K., & Waegele, H. (2008). Symbiosis between Symbiodinium (Dinophyceae) and different taxa of Nudibranchia (Mollusca: Gastropoda) with analyses of longterm retention. Organisms, Diversity and Evolution, 8, 66–76.

    Article  Google Scholar 

  • Burghardt, I., Schroedl, M., & Waegele, H. (2008). Three new solar-powered species of the genus Phyllodesmium Ehrenberg, 1831 (Mollusca:Nudibranchia:Aeolidioidea) from the tropical Indo-Pacific, with analysis of their photosynthetic activity and notes on biology. Journal of Molluscan Studies, 74, 277–292.

    Article  Google Scholar 

  • Chen, I. P., Tang, C. Y., Chiou, C. Y., Hsu, J. H., Wei, N. V., Wallace, C. C., et al. (2008). Comparative analyses of coding and noncoding DNA regions indicate that Acropora (Anthozoa: Scleractinia) possesses a similar evolutionary tempo of nuclear vs. mitochondrial genomes as in plants. Marine Biotechnology, 11, 141–152.

    Article  PubMed  Google Scholar 

  • Concepcion, G. T., Crepeau, M. W., Wagner, D., Kahng, S. E., & Toonen, R. J. (2008). An alternative to ITS, a hypervariable, single-copy nuclear intron in corals, and its use in detecting cryptic species within the octocoral genus Carijoa. Coral Reefs, 27, 323–336.

    Article  Google Scholar 

  • Dorado, D., & Sanchez, J. A. (2009). Internal Transcribed Spacer 2 (ITS2) variation in the Gorgonian Coral Pseudopterogorgia bipinnata in Belize and Panama. Smithsonian Contributions to the Marine Sciences, 38, 173–179.

    Google Scholar 

  • Drummond, A. J., Ashton, B., Buxton, S., Cheung, M., Cooper, A., Duran, C., et al. (2012). Geneious v5.6. http://www.geneious.com.

  • Ehrenberg, G. G. (1831). Symbolae Physicae seu icones est descriptiones animalium evertebratorum sepositis insectis quae ex itinere per Agricam Borealem et Asiam Occidentalem. Decas 1 Moll.

  • Ehrenberg, C. G. (1834). Beiträge zur Kenntnis der Corallenthiere im allgemeinen, und besonderen des Rothen Meeres, nebst einem Versuche zur physiologischen Systematik derselben. Abhandlungen der Königlichen Akademie der Wissenschaft Berlin (1832), 1, 225–380.

    Google Scholar 

  • Flot, J.-F., Blanchot, J., Charpy, L., Cruaud, C., Licuanan, W. Y., Nakano, Y., et al. (2011). Incongruence between morphotypes and genetically delimited species in the coral genus Stylophora: phenotypic plasticity, morphological convergence, morphological stasis or interspecific hybridization? BMC Ecology, 11, 22.

    Article  PubMed  Google Scholar 

  • Forsmann, Z. H., Concepcion, G. T., Haverkort, R. D., Shaw, R. W., Maragos, J. E., & Toonen, R. J. (2010). Ecomorph or endangered coral? DNA and microstructure reveal Hawaiian species complexes: Montipora dilatata/ flabellata/turgescens & M. patula/verrilli. Plos One, 5, 12.

    Google Scholar 

  • France, S., & Hoover, L. (2001). Analysis of variation in mitochondrial DNA sequences (ND3, ND4L, MSH) among Octocorallia (Alcyonaria) (Cnidaria: Anthozoa). Bulletin of the Biological Society of Washington, 10, 110–118.

    Google Scholar 

  • France, S., & Hoover, L. (2002). DNA sequences of the mitochondrial COI gene have low levels of divergence among deep-sea octocorals (Cnidaria: Anthozoa). Hydrobiologia, 471, 1–3.

    Article  Google Scholar 

  • Fukami, H., Budd, H. F., Levitan, D. R., Jara, J., Kersanach, R., & Knowlton, N. (2004). Geographic differences in species boundaries among members of the Montastraea annularis complex based on molecular and morphological markers. Evolution, 58, 324–337.

    PubMed  CAS  Google Scholar 

  • Gohar, H. A. F. (1940). Studies on the Xeniidae of the Red Sea. Their ecology, physiology, taxonomy and phylogeny. Publications of the Marine Biological Station, Al Ghardaqa, Egypt, 2, 25–118.

    Google Scholar 

  • Hatta, M., Fukami, H., Wang, W., Omori, M., Schimoike, K., Hayashibara, T., et al. (1999). Reproductive and genetic evidence for a reticulate evolutionary history of mass-spawning corals. Molecular Biology and Evolution, 16, 1607–1613.

    Article  PubMed  CAS  Google Scholar 

  • Hebert, P. D. N., Cywinska, A., Ball, S. L., & deWaard, J. R. (2003). Biological identifications through DNA barcodes. Proceedings of the Royal Society of London B, 270, 313–321.

    Article  CAS  Google Scholar 

  • Hebert, P. D. N., Ratnasingham, S., & de Waard, J. R. (2003). Barcoding animal life: cytochrom C oxidase subunit 1 divergences among closely related species. Proceedings of the Royal Society of London B, 270, 596–599.

    Article  Google Scholar 

  • Hebert, P. D. N., Stoeckle, M. Y., Zemlak, T. S., & Francis, C. M. (2004). Identification of birds through DNA barcodes. PLoS Biology. doi:10.1371/journal.pbio.0020312.

  • Hellberg, M. E. (2006). No variation and low synonymous substitution rates in coral mtDNA despite high nuclear variation. BMC Evolutionary Biology, 6, 24.

    Article  PubMed  Google Scholar 

  • Huang, D., Meier, R., Todd, P. A., & Ming Chou, L. (2008). Slow mitochondrial COI sequence evolution at the base of the metazoan tree and its implications for DNA barcoding. Journal of Molecular Evolution, 66, 167–174.

    Article  PubMed  CAS  Google Scholar 

  • Huelsenbeck, J. P. (2001). MrBayes: A program for the Bayesian inference of phylogeny. Manual.

  • Huelsken, T., Waegele, H., Peters, B., Mather, A., & Hollmann, M. (2011). Molecular analysis of adults and egg masses reveals two independent lineages within the infaunal gastropod Naticarius onca (Röding, 1798) (Caenogastropoda: Naticidae). Molluscan Research, 3, 141–151.

    Google Scholar 

  • Katho, K., Misawa, K., Kuma, K., & Miyata, T. (2002). Mafft: a novel method for rapid multiple alignment based on fast Furier transform. Nucleic Acids Research, 30, 3059–3066.

    Article  Google Scholar 

  • Koelliker, A. (1874). Die Pennatulidae Umbellula und zwei neue Typen der Alcyonarien. Festschrift zur Feier des 25-jährigen Bestehens der Physikalisch-Medizinischen Gesellschaft 5–23.

  • Lamarck, J. B. P. A. (1816). Polypes tubiferes. In Histoire naturelle des animeaux sans vertebres. IV + 568 pp. Paris, Verdiere

  • McFadden, C. S., & Hutchinson, M. B. (2004). Molecular evidence for the hybrid origin of species in the soft coral genus Alcyonium (Cnidaria: Anthozoa: Octocorallia). Molecular Ecology, 13, 1495–1505.

    Article  PubMed  CAS  Google Scholar 

  • McFadden, C. S., Donahue, R., Hadland, B. K., & Weston, R. (2001). A molecular phylogenetic analysis of reproductive trait evolution in the soft coral genus Alcyonium. Evolution, 55, 54–67.

    PubMed  CAS  Google Scholar 

  • McFadden, C. S., Tullis, I. D., Hutchinson, M. B., Winner, K., & Sohm, J. A. (2004). Variation in coding (NADH Dehydrogenase Subunits 2, 3 and 6) and noncoding intergenetic spacer regions of the mitochondrial genome in Octocorallia (Cnidaria: Anthozoa). Marine Biotechnology, 6, 516–526.

    Article  PubMed  CAS  Google Scholar 

  • McFadden, C. S., France, S. C., Sánchez, J. A., & Alderslade, P. (2006). A molecular phylogenetic analysis of the Octocorallia (Cnidaria: Anthozoa) based on mitochondrial protein-coding sequences. Molecular Phylogenetics and Evolution, 41, 513–527.

    Article  PubMed  CAS  Google Scholar 

  • McFadden, C. S., Sanchez, J., & France, S. (2010a). Molecular phylogenetic insights into the evolution of Octocorallia: a review. Integr Comp Biol, 1–22.

  • McFadden, C. S., Benayahu, Y., Pante, E., Thoma, J. N., Nevarez, A., & France, S. (2010). Limitations of mitochondrial gene barcoding in Octocorallia. Molecular Ecology Resources. doi:10.1111/j.1755-0998.2010.02875.x.

  • Park, E., Hwang, D. S., Lee, J. S., Song, J. I., Seo, T. K., & Won, Y. J. (2012). Estimation of divergence times in cnidarian evolution based on mitochondrial protein-coding genes and the fossil record. Molecular Phylogenetics and Evolution, 62, 329–345.

    Article  PubMed  Google Scholar 

  • Pillay, K. R. M., Asahida, T., Chen, C. A., Terashima, H., & Ida, H. (2006). ITS ribosomal DNA distinctions and the genetic structures of populations of two sympatric species of Pavona (Cnidaria; Scleractinia) from Mauritius. Zoological Studies, 45, 132–144.

    CAS  Google Scholar 

  • Posada, D. (2008). jModelTest: phylogenetic model averaging. Molecular Biology and Evolution, 25, 1253–1256.

    Article  PubMed  CAS  Google Scholar 

  • Reinicke, G. B. (1995). Xeniidae des Roten Meeres (Octocorallia, Alcyonacea)—Beiträge zur Systematik und Ökologie. Essener Ökologische Schriften, 6, 1–168.

    Google Scholar 

  • Reinicke, G. B. (1997). Xeniidae (Coelenterata, Octocorallia) of the Red Sea, with descriptions of six new species of Xenia. Fauna of Saudi Arabia, 16, 5–62.

    Google Scholar 

  • Roxas, H. A. (1933). The Philippine Alcyonaria. The families Cornulariidae and Xeniidae. Philippine Journal of Science, 50, 49–110.

    Google Scholar 

  • Shearer, T. L., & Coffroth, M. A. (2008). Barcoding corals: limited by interspecific divergence, not intraspecific variation. Molecular Ecology Resources, 8, 247–255.

    Article  PubMed  CAS  Google Scholar 

  • Shearer, T. L., vanOppen, M. J. H., Romano, S. L., & Woerheide, G. (2002). Slow mitochondrial DNA sequence evolution in the Anthozoa (Cnidaria). Molecular Ecology, 11, 2475–2487.

    Article  PubMed  CAS  Google Scholar 

  • Stamatakis, A. (2006). RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics, 22, 2688–2690.

    Article  PubMed  CAS  Google Scholar 

  • Strychar, K. B., Coates, M., Sammarco, P. W., Piva, T. J., & Scott, P. T. (2005). Loss of Symbiodinium from bleached soft corals Sarcophyton ehrenbergi, Sinularia sp. and Xenia sp. Journal of Experimental Marine Biology and Ecology, 320, 159–177.

    Article  Google Scholar 

  • Van Oppen, M. J. H., Willis, B. L., Van Vugt, H., & Miller, D. J. (2000). Examination of species boundaries in the Acropora cervicornis group (Scleractinia, Cnidaria) using nuclear DNA sequence analyses. Molecular Ecology, 9, 1363–1373.

    Article  PubMed  CAS  Google Scholar 

  • Van Oppen, M. J. H., McDonald, B. J., Willis, B., & Miller, D. J. (2001). The evolutionary history of the coral genus Acropora (Scleractinia, Cnidaria) based on a mitochondrial and a nuclear marker: reticulation, incomplete lineage sorting, or morphological convergence? Molecular Biology and Evolution, 18, 1315–1329.

    Article  PubMed  Google Scholar 

  • Van Oppen, M. J. H., Willis, B. L., Van Rheede, T., & Miller, D. J. (2002). Spawning times, reproductive compatibilities and genetic structuring in the Acropora aspera group: evidence for natural hybridization and semi-permeable species boundaries in corals. Molecular Ecology, 11, 1363–1376.

    Article  PubMed  Google Scholar 

  • Van Oppen, M. J. H., Koolmees, E. M., & Veron, J. E. N. (2004). Patterns of evolution in the scleractinian coral genus Montipora (Acroporidae). Marine Biology, 144, 9–18.

    Article  Google Scholar 

  • Verseveldt, J., & Cohen, J. (1971). Some new species of Octocorallia from the Gulf of Elat (Red Sea). Israel Journal of Zoology, 20, 53–67.

    Google Scholar 

  • Vollmer, S. V., & Palumbi, S. R. (2004). Testing the utility of internally transcribed spacer sequences in coral phylogenetics. Molecular Ecology, 13, 2763–2772.

    Article  PubMed  CAS  Google Scholar 

  • Waegele, H., Raupach, M. J., Haendeler, K., & Burghardt, I. (2010). Solar powered seaslugs: Incorporation of photosynthetic units—a key character enhancing radiation? In M. Glaubrecht & H. Schneider (Eds.), Evolution in action—adaptive radiations and the origins of biodiversity (pp. 263–282). Berlin: Springer.

    Google Scholar 

  • Ward, R. D., Zemlak, T. S., Innes, B. H., Last, P. R., & Hebert, P. D. N. (2005). DNA barcoding Australia’s fish species. Philosophical Transactions of the Royal Society B, 360, 1847–1857.

    Article  CAS  Google Scholar 

  • Wei, N. V., Wallace, C. C., Dai, C. F., Pillay, K. R. M., & Chen, C. A. (2006). Analyses of the ribosomal internal transcribed spacers (ITS) and the 5.8S gene indicate that extremely high rDNA heterogeneity is a unique feature in the scleractinian coral genus Acropora (Scleractinia; Acroporidae). Zoological Studies, 45, 404–418.

    CAS  Google Scholar 

Download references

Acknowledgments

We would like to thank our diving and collecting companions on Lizard Island (Australia), from Dimakya Island (Philippines), Dahab (Egypt) and Bali (Indonesia): Sebastian Striewski (Bochum), Christoph Haake (Munich), Sabrina Bleidissel (Wuppertal) and Martina Vogt (Cologne). We thank Kathrin P. Lampert for her support with any questions we had. Special thanks to the Lizard Island Research Station (LIRS) for their permanent support. Furthermore, we would like to thank our laboratory staff: Malgorzata Rudschewski, Beate Hackethal, Claudia Brefeld and Gabi Strieso (Ruhr University). The German Science Foundation supported the collecting trips to Lizard Island (Australia) for KS and HW (Wa 618/8).

Authors’ contributions

KS, FL, IB, HW and RT designed the study. KS and FL did the laboratory work. KS, FL and CM performed the computer analyses. IB and GR helped with the morphological investigations. KS, FL, CM and HW drafted the manuscript and interpreted the data. RT and GR made valuable contributions to the interpretation of the data. All authors have read and approved the final version of the manuscript.

Author information

Authors and Affiliations

  1. Department of Animal Ecology, Evolution and Biodiversity, Ruhr University Bochum, Bochum, Germany

    Kristina Stemmer, Christoph Mayer, Ralph Tollrian & Florian Leese

  2. Zoologisches Forschungsmuseum Alexander Koenig, Bonn, Germany

    Christoph Mayer & Heike Wägele

  3. Functional Ecology, Alfred Wegener Institute for Polar and Marine Research, Bremerhaven, Germany

    Kristina Stemmer

  4. Deutsches Meeresmuseum, Stralsund, Germany

    Götz B. Reinicke

  5. Leibniz-Center for Tropical Marine Ecology, Bremen, Germany

    Ingo Burghardt

Authors
  1. Kristina Stemmer
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ingo Burghardt
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Christoph Mayer
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Götz B. Reinicke
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Heike Wägele
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Ralph Tollrian
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Florian Leese
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Kristina Stemmer.

Additional information

Kristina Stemmer and Florian Leese contributed equally to this study.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(PDF 4437 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Stemmer, K., Burghardt, I., Mayer, C. et al. Morphological and genetic analyses of xeniid soft coral diversity (Octocorallia; Alcyonacea). Org Divers Evol 13, 135–150 (2013). https://doi.org/10.1007/s13127-012-0119-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13127-012-0119-x

Keywords

Search

Navigation