The first modern solitary Agariciidae (Anthozoa, Scleractinia) revealed by molecular and microstructural analysis
Marcelo V. Kitahara A G , Jaroslaw Stolarski B , Stephen D. Cairns C , Francesca Benzoni D , Joel L. Stake E and David J. Miller F
+ Author Affiliations
- Author Affiliations
A Centro de Biologia Marinha, Universidade de São Paulo, São Sebastião, S.P. 11600-000, Brazil.
B Institute of Paleobiology, Polish Academy of Sciences, Twarda 51/55, PL-00-818 Warsaw, Poland.
C Department of Invertebrate Zoology, National Museum of Natural History, Smithsonian Institution, Washington, DC 20560, USA.
D Institut de Recherche pour le Développement, UMR227 Coreus2, 101 Promenade Roger Laroque, BP A5, 98848 Noumea Cedex, New Caledonia and Department of Biotechnology and Biosciences and University of Milano-Bicocca, Piazza della Scienza 2, 20126 Milan, Italy.
E Department of Biology, Rivier College, Nashua, NH 03060, USA.
F ARC Centre of Excellence for Coral Reef Studies and Coral Genomics Group, James Cook University, Townsville, Qld 4811, Australia.
G Corresponding author. Email: mvkitahara@yahoo.com.br
Invertebrate Systematics 26(3) 303-315 https://doi.org/10.1071/IS11053
Submitted: 21 December 2011 Accepted: 30 April 2012 Published: 21 September 2012
Abstract
Dactylotrochus cervicornis (= Tridacophyllia cervicornis Moseley, 1881), which occurs in Indo-Pacific waters between 73 and 852 m, was originally described as an astraeid but was later transferred to the Caryophylliidae. Assumed to be solitary, this species has no stolons and only one elongated fossa, and is unique among azooxanthellate scleractinians in often displaying extremely long thecal extensions that are septate and digitiform. Based on both molecular phylogenetic analyses (partial mitochondrial CO1 and 16S rDNA, and partial nuclear 28S rDNA) and morphological characteristics, we propose the transfer of D. cervicornis from the Caryophylliidae to the Agariciidae, making it the first extant representative of the latter family that is solitary and from deep water (azooxanthellate). The basal position of D. cervicornis within the agariciids implied by our analyses strengthens the case for inclusion of fossil species that were solitary, such as Trochoseris, in this family and suggests that the ancestor of this scleractinian family, extant members of which are predominantly colonial and zooxanthellate, may have been solitary and azooxanthellate.
References
Anisimova, M., and Gascuel, O. (2006). Approximate likelihood-ratio test for branches: a fast, accurate, and powerful alternative. Systematic Biology 55, 539–552.| Approximate likelihood-ratio test for branches: a fast, accurate, and powerful alternative.Crossref | GoogleScholarGoogle Scholar |
Barbeitos, M., Romano, S., and Lasker, H. R. (2010). Repeated loss of coloniality and symbiosis in scleractinian corals. Proceedings of the National Academy of Sciences of the United States of America 107, 11 877–11 882.
| Repeated loss of coloniality and symbiosis in scleractinian corals.Crossref | GoogleScholarGoogle Scholar |
Baron-Szabo, R. C. (2002). ‘Scleractinian Corals of the Cretaceous. A Guide to Cretaceous Forms with Descriptions, Illustrations, and Remarks on their Taxonomic Position.’ (Baron-Szabo: Knoxville, TN, USA.)
Baron-Szabo, R. C. (2008). Corals of the K/T-boundary: scleractinian corals of the suborders Dendrophylliina, Caryophylliina, Fungiina, Microsolenina, and Stylinina. Zootaxa 1952, 1–244.
Benzoni, F., Stefani, F., Stolarski, J., Pichon, M., Mitta, G., and Galli, P. (2007). Debating phylogenetic relationships of the scleractinian Psammocora: molecular and morphological evidences. Contributions to Zoology (Amsterdam, Netherlands) 76, 35–54.
Benzoni, F., Arrigoni, R., Stefani, F., and Pichon, M. (2011). Phylogeny of the coral genus Plesiastrea (Cnidaria, Scleractinia). Contributions to Zoology (Amsterdam, Netherlands) 80, 231–249.
Budd, A. F., and McNeill, D. F. (1998). Zooxanthellate scleractinian corals from the Bowden Shell Bed, SE Jamaica. Contributions to Tertiary and Quaternary Geology 35, 49–65.
Budd, A. F., and Smith, N. D. (2005). Diversification of a new Atlantic clade of scleractinian reef corals: insights from phylogenetic analysis of morphologic and molecular data. Paleontological Society Papers 11, 103–128.
Budd, A. F., and Stolarski, J. (2011). Corallite wall and septal microstructure in scleractinian reef corals: comparison of molecular clades within the family Faviidae. Journal of Morphology 272, 66–88.
| Corallite wall and septal microstructure in scleractinian reef corals: comparison of molecular clades within the family Faviidae.Crossref | GoogleScholarGoogle Scholar |
Budd, A. F., Romano, S. L., Smith, N. D., and Barbeitos, M. S. (2010). Rethinking the phylogeny of scleractinian corals: a review of morphological and molecular data. Integrative and Comparative Biology 50, 411–427.
| Rethinking the phylogeny of scleractinian corals: a review of morphological and molecular data.Crossref | GoogleScholarGoogle Scholar |
Cairns, S. D. (1999). Cnidaria Anthozoa: deep-water azooxanthellate Scleractinia from Vanuatu, and Wallis and Futuna Islands. Mémoires du Muséum National d’histoire naturelle 180, 31–167.
Cairns, S. D. (2001). A generic revision and phylogenetic analysis of the Dendrophylliidae (Cnidaria: Scleractinia). Smithsonian Contributions to Zoology 615.
Chevalier, J. P. (1961). Recherches sur les madréporaries et les formations récifals miocènes de la Mediterranée occidentale. Memoirs of the Geological Society of France 93, 1–562.
Chevalier, J. P. (1968). Expédition française sur les récifs coralliens de la Nouvelle Calédonie. Fond Singer-Polignac l, 1–155.
Chevalier, J. P., and Beauvais, L. (1987). Order des Scléractiniaires. In ‘Traité de Zoologie, Tome III, fasc. 3.’ (Ed. P. P. Grassé.) pp. 679–764. (Paris, Masson.)
Clamp, M., Cuff, J., Searle, S. M., and Barton, G. J. (2004). The Jalview Java Alignment Editor. Bioinformatics 20, 426–427.
| The Jalview Java Alignment Editor.Crossref | GoogleScholarGoogle Scholar |
Cuif, J. P., Lecointre, G., Perrin, C., Tillier, A., and Tillier, S. (2003). Patterns of septal biomineralization in Scleractinia compared with their 28S rRNA phylogeny: a dual approach for a new taxonomic framework. Zoologica Scripta 32, 459–473.
| Patterns of septal biomineralization in Scleractinia compared with their 28S rRNA phylogeny: a dual approach for a new taxonomic framework.Crossref | GoogleScholarGoogle Scholar |
Dai, C. F., and Horng, S. (2009). ‘Scleractinia Fauna of Taiwan I. The Complex Group.’ (National Taiwan University: Taipei, Taiwan.)
de Queiroz, K., and Gauthier, J. (1992). Phylogenetic taxonomy. Annual Review of Ecology and Systematics 23, 449–480.
| Phylogenetic taxonomy.Crossref | GoogleScholarGoogle Scholar |
Durham, J. W. (1949). Ontogenetic stages of some simple corals. University of California Publications in Geological Sciences 28, 137–172.
Fricke, H. W., Vareschi, E., and Schlichter, D. (1987). Photoecology of the coral Leptoseris fragilis in the Red Sea twilight zone (an experimental study by submersible). Oecologia 73, 371–381.
| Photoecology of the coral Leptoseris fragilis in the Red Sea twilight zone (an experimental study by submersible).Crossref | GoogleScholarGoogle Scholar |
Fukami, H., Chen, C. A., Budd, A. F., Collins, A., Wallace, C., Chuang, Y. Y., Chen, C., Dai, C. F., Iwao, K., Sheppard, C., and Knowlton, N. (2008). Mitochondrial and nuclear genes suggest that stony corals are monophyletic but most families of stony corals are not (Order Scleractinia, Class Anthozoa, Phylum Cnidaria). PLoS ONE 3, e3222.
| Mitochondrial and nuclear genes suggest that stony corals are monophyletic but most families of stony corals are not (Order Scleractinia, Class Anthozoa, Phylum Cnidaria).Crossref | GoogleScholarGoogle Scholar |
Gardiner, J. S. (1899). On the solitary corals, collected by Dr. A. Willey Zoological Results based on Material from New Britain, New Guinea, Loyalty Islands and Elsewhere 2, 161–180.
Gill, G. A. (1967). Quelques précisions sur les septes perforés des Polypiers mésozoïques. Mémoires de la Société géologique de France (n.s.) 46, 58–81.
Gittenberger, A., Reijnen, B. T., and Hoeksema, B. W. (2010). A molecularly based phylogeny reconstruction of mushroom corals (Scleractinia: Fungiidae) with taxonomic consequences and evolutionary implications for life history traits. Contributions to Zoology (Amsterdam, Netherlands) 80, 107–132.
Glynn, P. W., Maté, J. L., and Stemann, T. A. (2001). Pavona chiriquiensis, a new species of zooxanthellate scleractinian coral (Cnidaria: Anthozoa: Agariciidae) from the eastern tropical Pacific. Proceedings of the Biological Society of Washington 10, 210–225.
Guindon, S., and Gascuel, O. (2003). A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52, 696–704.
| A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood.Crossref | GoogleScholarGoogle Scholar |
Hennig, W. (1957). Systematik und Phylogenese. In ‘Bericht über die Hundertjahrfeier der Deutschen Entomologischen Gesellschaft Belin’. (Ed. H. J. Hannemann.) pp. 50–71. (Akademie Verlag: Berlin, Germany.)
Hennig, W. (1966). ‘Phylogenetic Systematics.’ (University of Illinios Press: Urbana, IL, USA.)
Huelsenbeck, J. P., and Ronquist, F. (2001). MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17, 754–755.
| MRBAYES: Bayesian inference of phylogenetic trees.Crossref | GoogleScholarGoogle Scholar |
Kerr, A. M. (2005). Molecular and morphological supertree of stony corals (Anthozoa: Scleractinia) using matrix representation parsimony. Biological Reviews of the Cambridge Philosophical Society 80, 1–16.
| Molecular and morphological supertree of stony corals (Anthozoa: Scleractinia) using matrix representation parsimony.Crossref | GoogleScholarGoogle Scholar |
Kitahara, M. V., Cairns, S. D., Stolarski, J., Blair, D., and Miller, D. J. (2010a). A comprehensive phylogenetic analysis of the Scleractinia (Cnidaria, Anthozoa) based on mitochondrial CO1 sequence data. PLoS ONE 5, e11490.
| A comprehensive phylogenetic analysis of the Scleractinia (Cnidaria, Anthozoa) based on mitochondrial CO1 sequence data.Crossref | GoogleScholarGoogle Scholar |
Kitahara, M. V., Cairns, S. D., and Miller, D. J. (2010b). Monophyletic origin of the Caryophyllia (Scleractinia; Caryophylliidae), with description of six new species. Systematics and Biodiversity 8, 91–118.
| Monophyletic origin of the Caryophyllia (Scleractinia; Caryophylliidae), with description of six new species.Crossref | GoogleScholarGoogle Scholar |
Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P. A., McWilliam, H., Valentin, F., Wallace, I. M., Wilm, A., Lopez, R., Thompson, J. D., Gibson, T. J., and Higgins, D. G. (2007). Clustal W and Clustal X version 2.0. Bioinformatics 23, 2947–2948.
| Clustal W and Clustal X version 2.0.Crossref | GoogleScholarGoogle Scholar |
Le Goff-Vitry, M. C., Rogers, A. D., and Baglow, D. (2004). A deep-sea slant on the molecular phylogeny of the Scleractinia. Molecular Phylogenetics and Evolution 30, 167–177.
| A deep-sea slant on the molecular phylogeny of the Scleractinia.Crossref | GoogleScholarGoogle Scholar |
Licuanan, W. Y., and Aliño, P. M. (2009). Leptoseris kalayaanensis (Scleractinia: Agariciidae), a new coral species from the Philipines. The Raffles Bulletin of Zoology 57, 1–4.
Mayr, E. (1969). The biological meaning of species. Biological Journal of the Linnean Society. Linnean Society of London 1, 311–320.
| The biological meaning of species.Crossref | GoogleScholarGoogle Scholar |
Morycowa, E., and Roniewicz, E. (1995). Microstructural disparity between Recent fungiine and Mesozoic microsolenine scleractinian. Acta Palaeontologica Polonica 40, 361–385.
Moseley, H. N. (1881). Report on certain hydroid, alcyonarian, and madreporarian corals procured during the voyage H. M. S. Challenger, in the years 1873–1876. Report on the Scientific Results of the Voyage of H. M. S. Challenger during the years 1873–79, Zoology 2.
Nemenzo, F. (1955). Systematic studies on Philippine shallow water scleractinians: I. Suborder Fungiida. Natural and Applied Sciences Bulletin 15, 3–84.
Nothdurft, L. D., and Webb, G. (2007). Microstructure of common reef- building coral genera Acropora, Pocillopora, Goniastrea and Porites: constraints on spatial resolution in geochemical sampling. Facies 53, 1–26.
| Microstructure of common reef- building coral genera Acropora, Pocillopora, Goniastrea and Porites: constraints on spatial resolution in geochemical sampling.Crossref | GoogleScholarGoogle Scholar |
Pandey, D. K., and Fürsich, F. T. (2005). Jurassic corals from southern Tunisia. Zitteliana A 45, 3–34.
Pandey, D. K., Fursich, F. T., Baron-Szabo, R. M., and Wilmsen, M. (2007). Lower Cretaceous corals from the Koppeh Dagh, NE-Iran. Zitteliana A 47, 3–52.
Romano, S. L., and Cairns, S. D. (2000). Molecular phylogenetic hypotheses for the evolution of scleractinian corals. Bulletin of Marine Science 67, 1043–1068.
Romano, S. L., and Palumbi, S. R. (1996). Evolution of scleractinian corals inferred from molecular systematics. Science 271, 640–642.
| Evolution of scleractinian corals inferred from molecular systematics.Crossref | GoogleScholarGoogle Scholar |
Romano, S. L., and Palumbi, S. R. (1997). Molecular evolution of a portion of the mitochondrial 16S ribosomal gene region in scleractinian corals. Journal of Molecular Evolution 45, 397–411.
| Molecular evolution of a portion of the mitochondrial 16S ribosomal gene region in scleractinian corals.Crossref | GoogleScholarGoogle Scholar |
Stefani, F., Benzoni, F., Pichon, M., Mitta, G., and Galli, P. (2008). Genetic and morphometric evidence for unresolved species boundaries in the coral genus Psammocora (Cnidaria; Scleractinia). Hydrobiologia 596, 153–172.
| Genetic and morphometric evidence for unresolved species boundaries in the coral genus Psammocora (Cnidaria; Scleractinia).Crossref | GoogleScholarGoogle Scholar |
Stolarski, J. (1995). Ontogenetic development of the thecal structures in Caryophylliinae scleractinian corals. Acta Palaeontologica Polonica 40, 19–44.
Stolarski, J. (2003). 3-Dimensional micro- and nanostructural characteristics of the scleractinian corals skeleton: a biocalcification proxy. Acta Palaeontologica Polonica 48, 497–530.
Stolarski, J., Kitahara, M. V., Miller, D. J., Cairns, S. D., Mazur, M., and Meibom, A. (2011). An ancient evolutionary origin of Scleractinia revealed by azooxanthellate corals. BMC Evolutionary Biology 11, 316.
| An ancient evolutionary origin of Scleractinia revealed by azooxanthellate corals.Crossref | GoogleScholarGoogle Scholar |
Veron, J. E. N. (1995). ‘Corals in Space and Time: Biogeography and Evolution of the Scleractinia.’ (Cornell University Press: Ithaca, NY, USA.)
Veron, J. E. N. (2000). ‘Corals of the World. Volume 2.’ (Australian Institute of Marine Science: Townsville.)
Wells, J. W. (1954). Recent corals of the Marshall Islands: Bikini and nearby atolls, Part 2: Oceanography (Biology). U.S. Geological Survey Professional Paper 260-I, 382–486.
Wells, J. W. (1956). Scleractinia. In ‘Treatise on Invertebrate Paleontology, Part F. Coelenterata’. (Ed. R. C., Moore.) pp. F328–F444. (Geological Society of America: Lawrence, KS, USA.)
