Phylogenetic reconstruction of scleraxonian octocorals supports the resurrection of the family Spongiodermidae (Cnidaria, Alcyonacea)
Stephen D. Cairns A B and Herman H. Wirshing AA Department of Invertebrate Zoology, National Museum of Natural History, Smithsonian Institution, PO Box 37012, MRC 163, Washington, DC 20013-7012, USA.
B Corresponding author. Email: cairnss@si.edu
Invertebrate Systematics 29(4) 345-368 https://doi.org/10.1071/IS14063
Submitted: 10 December 2014 Accepted: 6 February 2015 Published: 28 August 2015
Abstract
The Scleraxonia are a group of octocorals that share similarities of their axis morphology. However, molecular phylogenetic analyses have shown this group to be largely polyphyletic. As a result, there is a significant lack of understanding of what constitutes distinct evolutionary units among members of this group, particularly at the family level. Prompted by the discovery of an unknown spongiodermid scleraxonian octocoral (Anthothelidae) from shallow water off the Pacific coast of lower Baja California, a phylogenetic analysis of the undescribed specimen, together with members of six scleraxonian families and an additional 29 non-scleraxonian octocorallian families was performed. Two mitochondrial loci (mtMutS and COI) and one nuclear locus (28S) supported a monophyletic spongiodermid clade (Homophyton, Callipodium, Diodogorgia, Titanideum and Sclerophyton, gen. nov.) at the family-level. The unknown scleraxonian was supported as a new genus and species within the spongiodermid clade, sister to the western Atlantic genus Titanideum. A morphological examination of the taxa within this clade revealed shared morphological similarities in solenial (boundary) canals, and medullar and cortical sclerites. A revision, with illustrations, of the Spongiodermidae was performed. Similar to previous studies, this study underscores the importance of combined morphological and molecular analyses in order to resolve unstable systematic relationships among octocorals.
References
Aguilar-Hurtado, C., Nonaka, M., and Reimer, J. D. (2012). The Melithaeidae (Cnidaria: Octocorallia) of the Ryukyu Archipelago: molecular and morphological examinations. Molecular Phylogenetics and Evolution 64, 56–65.| The Melithaeidae (Cnidaria: Octocorallia) of the Ryukyu Archipelago: molecular and morphological examinations.Crossref | GoogleScholarGoogle Scholar | 22465401PubMed |
Aurivillius, M. (1931). ‘The Gorgonarians from Dr. Sixten Bock’s Expedition to Japan and Bonin Islands 1914. Kungliga Svenska Vetenskaps-Akademiens Handlingar, Tredje Serien, Band 9.’ (Almqvist & Wiksell: Stockholm.)
Bayer, F. M. (1955). Contributions to the nomenclature, systematics, and morphology of the Octocorallia. Proceedings of the United States National Museum 105, 207–220.
| Contributions to the nomenclature, systematics, and morphology of the Octocorallia.Crossref | GoogleScholarGoogle Scholar |
Bayer, F. M. (1956). Octocorallia. In ‘Treatise on Invertebrate Paleontology’. (Ed. R. C. Moore.) pp. F166–189, 192–231. (University of Kansas Press: Lawrence, KS.)
Bayer, F. M. (1959). Octocorals from Surinam and the adjacent coasts of South America. Studies on the Fauna of Suriname and Other Guyanas 6, 1–43.
Bayer, F. M. (1961). The shallow-water Octocorallia of the West Indian region. Studies on the Fauna of Curaçao and Other Caribbean Islands 12, 1–373.
Bayer, F. M. (1981). Key to the genera of Octocorallia exclusive of Pennatulacea (Coelenterata: Anthozoa), with diagnoses of new taxa. Proceedings of the Biological Society of Washington 94, 902–947.
Bayer, F. M., Grasshoff, M., and Verseveldt, J. (1983). ‘Illustrated Trilingual Glossary of Morphological and Anatomical Terms Applied to Octocorallia.’ (E. J. Brill: Leiden.)
Boone, L. (1933). Scientific results of the cruise of the yachts “Eagle” and “Ara” 1921–1928. Coelenterata, Echinodermata and Mollusca. Bulletin of the Vanderbilt Marine Museum 4, 1–133.
Cairns, S. D., and Bayer, F. M. (2009). Octocorallia (Cnidaria) of the Gulf of Mexico. In ‘Gulf of Mexico: Origin, Waters, and Biota’. (Eds D. L. Felder and D. K. Camp.) pp. 321–331. (Texas A&M Press: College Station, TX.)
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., Rodriguez, E., Romano, S., and Stake, J. (2007). The phylum Cnidaria: a review of phylogenetic patterns and diversity 300 years after Linnaeus. Zootaxa 1668, 1–766.
Deichmann, E. (1936). The Alcyonaria of the western part of the Atlantic Ocean. Memoirs of the Museum of Comparative Zoology at Harvard College 53, 1–317.
DeVictor, S. T., and Morton, S. L. (2010). Identification guide to the shallow water (0–200 m) octocorals of the South Atlantic Bight. Zootaxa 2599, 1–62.
Edgar, R. C. (2004). MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32, 1792–1797.
| MUSCLE: multiple sequence alignment with high accuracy and high throughput.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXisF2ks7w%3D&md5=5e5a51a2851e50039acd3b34601cddcbCAS | 15034147PubMed |
Ellis, J., and Solander, D. (1786). ‘The Natural History of Many Curious and Uncommon Zoophytes ... Systematically Arranged and Described by the late Daniel Solander.’ (Benjamin White and Son: London.)
Fabricius, K., and Alderslade, P. (2001). ‘Soft Corals and Sea Fans – A Comprehensive Guide to the Tropical Shallow-water Genera of the Central-West Pacific, the Indian Ocean and the Red Sea.’ (Australian Institute of Marine Science: Townsville.)
Figueroa, D. F., and Baco, A. R. (2015). Octocoral mitochondrial genomes provide insights into the phylogenetic history of gene order rearrangements, order reversals, and cnidarian phylogenetics. Genome Biology and Evolution 7, 391–409.
| Octocoral mitochondrial genomes provide insights into the phylogenetic history of gene order rearrangements, order reversals, and cnidarian phylogenetics.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXjt1Cntrw%3D&md5=f9689cb20da0e7682b713cf217b9015dCAS |
France, S. C., and Hoover, L. 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.
Gray, J. E. (1866). Description of two new forms of gorgonioid corals. Proceedings of the Zoological Society of London 1866, 24–27.
Hargitt, C. W., and Rogers, C. G. (1901). The Alcyonaria of Porto Rico. Bulletin of the U. S. Fish Commission 20, 265–287.
Herrera, S., Baco, A., and Sánchez, J. A. (2010). Molecular systematics of the bubblegum coral genera (Paragorgiidae, Octocorallia) and description of a new deep-sea species. Molecular Phylogenetics and Evolution 55, 123–135.
| Molecular systematics of the bubblegum coral genera (Paragorgiidae, Octocorallia) and description of a new deep-sea species.Crossref | GoogleScholarGoogle Scholar | 20025983PubMed |
Hickson, S. J. (1904). The Alcyonaria of the Cape of Good Hope. Part 2. Marine Investigations of South Africa 3, 211–239.
Katoh, M., and Kuma, M. (2002). MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Research 30, 3059–3066.
| MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XlslOqu7s%3D&md5=062ddb93ea5f1aa3de915bbe559e94aaCAS |
Kölliker, A. (1871). Beiträge zur Kenntniss der Polypen. Verhandlungen der Physikal-Medicin. Gesellschaft in Würzburg 2, 11–30.
Kükenthal, W. (1919). Gorgonaria. Wissenschaftliche Ergebnisse der Deutschen Tiefsee-Expedition auf dem Dampfer “Valdivia”, 1898–1899 13, 1–946.
Kükenthal, W. (1924). ‘Coelenterata: Gorgonaria.’ Das Tierreich 47. (Walter de Gruyter & Co.: Berlin.) [In German]
McFadden, C. S., and van Ofwegen, L. P. (2012). Stoloniferous octocorals (Anthozoa, Octocorallia) from South Africa, with descriptions of a new family of Alcyonacea, a new genus of Clavulariidae, and a new species of Cornularia (Cornulariidae). Invertebrate Systematics 26, 331–356.
| Stoloniferous octocorals (Anthozoa, Octocorallia) from South Africa, with descriptions of a new family of Alcyonacea, a new genus of Clavulariidae, and a new species of Cornularia (Cornulariidae).Crossref | GoogleScholarGoogle Scholar |
McFadden, C. S., and van Ofwegen, L. P. (2013). Molecular phylogenetic evidence supports a new family of octocorals and a new genus of Alcyoniidae (Octocorallia, Alcyonacea). ZooKeys 346, 59–83.
| Molecular phylogenetic evidence supports a new family of octocorals and a new genus of Alcyoniidae (Octocorallia, Alcyonacea).Crossref | GoogleScholarGoogle Scholar | 24223488PubMed |
McFadden, C. S., France, S. C., Sánchez, J. A., and 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.
| A molecular phylogenetic analysis of the Octocorallia (Cnidaria: Anthozoa) based on mitochondrial protein-coding sequences.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht1CgsbnF&md5=17852cf169dde903c6d0abdd6ddab2d5CAS | 16876445PubMed |
McFadden, C. S., Benayahu, Y., Pante, E., Thoma, J. N., Nevarez, P. A., and France, S. C. (2011). Limitations of mitochondrial gene barcoding in Octocorallia. Molecular Ecology Resources 11, 19–31.
| Limitations of mitochondrial gene barcoding in Octocorallia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXht1amu7k%3D&md5=1693b4351679cbe5374e0ddb48431924CAS | 21429097PubMed |
Möbius, K. (1861). Neue Gorgoniden des naturhistorischen Museums zu Hamburg. Nova Acta Academiae Caesareae Leopoldino Carolinae Germanicae Naturae Curiosorum 29, 1–12.
Nutting, C. C. (1911). The Gorgonacea of the Siboga Expedition. VIII. The Scleraxonia. Siboga-Expeditie, Monographie 13b5, 1–62.
Nylander, J. A. A. (2004). ‘MrAIC.pl.’ Program distributed by the author. (Evolutionary Biology Centre: Uppsala University.)
Pallas, P. S. (1766). ‘Elenchus Zoophytorum.’ (Comitum, P. van Cleef: Hague.)
Rambaut, A., and Drummond, A. J. (2009). ‘Tracer version 1.5.0.’ Available at http://tree.bio.ed.ac.uk/software/tracer/.
Reijnen, B. T., McFadden, C. S., Hermanlimianto, Y. T., and van Ofwegen, L. P. (2014). A molecular and morphological exploration of the generic boundaries in the family Melithaeidae (Coelenterata: Octocorallia) and its taxonomic consequences. Molecular Phylogenetics and Evolution 70, 383–401.
| A molecular and morphological exploration of the generic boundaries in the family Melithaeidae (Coelenterata: Octocorallia) and its taxonomic consequences.Crossref | GoogleScholarGoogle Scholar | 24120448PubMed |
Ronquist, F., and Huelsenbeck, J. P. (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574.
| MrBayes 3: Bayesian phylogenetic inference under mixed models.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXntlKms7k%3D&md5=6c22440a111ffd7c39b671a54462b45bCAS | 12912839PubMed |
Sanchez, J. A., Lasker, H. R., and Taylor, D. J. (2003). Phylogenetic analyses among octocorals (Cnidaria): mitochondrial and nuclear DNA sequences (lsu-rRNA, 16S and ssu-rRNA, 18S) support two convergent clades of branching gorgonians. Molecular Phylogenetics and Evolution 29, 31–42.
| Phylogenetic analyses among octocorals (Cnidaria): mitochondrial and nuclear DNA sequences (lsu-rRNA, 16S and ssu-rRNA, 18S) support two convergent clades of branching gorgonians.Crossref | GoogleScholarGoogle Scholar |
Shearer, T. L., Van Oppen, M. J. H., Romano, S. L., and Wörheide, G. (2002). Slow mitochondrial DNA sequence evolution in the Anthozoa (Cnidaria). Molecular Ecology 11, 2475–2487.
| Slow mitochondrial DNA sequence evolution in the Anthozoa (Cnidaria).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xpsl2ms7g%3D&md5=3d23dd68240859a197287d70ce01faa1CAS | 12453233PubMed |
Stamatakis, A. (2006). RAxML-VI-HPC maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22, 2688–2690.
| RAxML-VI-HPC maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtFKlsbfI&md5=df50a1f20f2be0cbcb0dff3c135f1b17CAS | 16928733PubMed |
Stiasny, G. (1937). Die Gorgonacea der Siboga-Expedition. Supplement II, Revision der Scleraxonia mit ausschuluss der Melitodidae und Coralliidae. Siboga-Expeditie, Monographie 13b8, 1–138. [In German]
Stiasny, G. (1941). Studien uber Alcyonaria und Gorgonaria (Parerga und Paralipomena). II. Zoologischer Anzeiger 134, 53–71.
Studer, T. (1878). Ubersicht der Steinkorallen aus der Familie der Madreporaria aporosa, Eupsammina, und Turbinaria, welche auf der Reise S. M. S. Gazelle um die Erde gesammelt wurden. Monatsberichte der Königlich Preussischen Akademie der Wissenschaften zu Berlin 1877, 625–654.
Swofford, D. L. (2004). ‘PAUP: Phylogenetic Analysis Using Parsimony, version 4.0b10.’ (Sinauer Associates: Sunderland, MA.)
Thomson, J. A. (1927). Alcyonaires provenant des campagnes scientifiques du Prince Albert 1er de Monaco. Résultats des Campagnes Scientifiques accomplies sur son yacht par Albert 1er, Monaco 73, 1–77.
Thomson, J. A., and Mackinnon, D. L. (1911). The Alcyonarians of the “Thetis” expedition. Australian Museum Memoirs 4, 661–695.
| The Alcyonarians of the “Thetis” expedition.Crossref | GoogleScholarGoogle Scholar |
Verrill, A. E. (1864a). List of the polyps and corals sent by the Museum of Comparative Zoology to other institutions in exchange, with annotations. Bulletin of the Museum of Comparative Zoology 1, 29–60.
Verrill, A. E. (1864b). Revision of the polypi of the eastern coast of the United States. Memoirs of the Boston Society of Natural History 1, 1–45.
Verrill, A. E. (1866). On the polyps and corals of Panama with descriptions of new species. Proceedings of the Boston Society of Natural History 10, 323–333.
Verrill, A. E. (1869). Review of the polyps and corals of the west coast of America. Transactions of the Connecticut Academy of Arts and Sciences 1, 423–502.
Verrill, A. E. (1872). On Radiata from the coast of North Carolina. American Journal of Science and Arts 3, 432–438.
| On Radiata from the coast of North Carolina.Crossref | GoogleScholarGoogle Scholar |
Verrill, A. E. (1876). Anthozoa. In ‘Contributions to Natural History of Kerguelen Island’. (Ed. J. H. Kidder.) Bulletin of the U. S. National Museum 3, 76–77.
Verseveldt, J. (1940). Studies on Octocorallia of the families Briareidae, Paragorgiidae and Anthothelidae. Temminkia 5, 1–142.
Williams, G. C. (1992a). The Alcyonaria of Southern Africa. Gorgonian Octocorals (Coelenterata, Anthozoa). Annals of the South African Museum 101, 181–296.
Williams, G. C. (1992b). Biogeography of the octocorallian coelenterate fauna of southern Africa. Biological Journal of the Linnean Society. Linnean Society of London 46, 351–401.
| Biogeography of the octocorallian coelenterate fauna of southern Africa.Crossref | GoogleScholarGoogle Scholar |
Williams, G. C. (1993). ‘Coral Reef Octocorals: An Illustrated Guide to the Soft Corals, Sea Fans, and Sea Pens Inhabiting the Coral Reefs of Northern Natal.’ (Natural Science Museum: Durban.)
Williams, G. C., and Cairns, S. D. (2014). ‘Systematic list of the valid octocoral genera.’ Available at http://researcharchive.calacademy.org/research/izg/OCTOCLASS.htm
Wright, E. P., and Studer, T. (1889). Report on the Alcyonaria collected by H.M.S. Challenger during the years 1873–76. Report on the Scientific Results of the Voyage of H.M.S. Challenger during the years 1873–76. Zoology 31, 1–314.