Abstract
Octocorals (Octocorallia, Alcyonacea) are distributed worldwide and their taxonomy in the Persian Gulf has been a subject of controversy among experts due to their cryptic features. Here, we present a primary review of the Alcyonacea in the Iranian Persian Gulf with molecular documentation to provide insight into the real diversity within this order. Our molecular study was based on two mitochondrial protein-coding (COI and mtMuts) and one nuclear (28S rDNA) gene sequences, which identified seven families, 14 genera, and 21 species of Octocorallia in the Persian Gulf that were well-supported by maximum likelihood and Bayesian analyses. Our results indicate consistency between morphological and molecular characteristics at the species level. We conclude the presence of some heterogeneous groups of genera creates ambiguity in our analysis.
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Avise JC (2012) Molecular markers, natural history and evolution. Springer US. pp 511
Bayer FM (1961) The shallow-water Octocorallia of the west Indian region. Stud Fauna Curaçao Carib Isl 12:1–373
Bayer FM (1973) Colonial organization in octocorals. In: Boardman RS, Cheetham AH, Oliver WA (eds). Animal Colonies. Dowden, Hutchinson and Ross, Stroudsburg, pp 69–94
Bayer FM (1981) Key to the genera of Octocorallia exclusive of Pennatulacea (Coelenterata: Anthozoa), with diagnosis of new taxa. P Biol Soc Wash 94(3):902–947
Bayer FM, Grasshoff M (1994) The genus group taxa of the family Ellisellidae, with clarification of the genera established by JE gray (Cnidaria; Octocorallia). Senck biol 74:21–45
Benayahu Y (1985) Faunistic composition and patterns in the distribution of soft corals (Octocorallia: Alcyonacea) along the coral reefs of Sinai Peninsula. Proc 5th Int Coral Reef Congr 6:255–260
Benayahu Y (1990) Xeniidae (Cnidaria: Octocorallia) from the Red Sea with description of a new species. Zool Meded 64:113–120
Benayahu Y (1995) Species composition of soft corals (Octocorallia: Alcyonacea) on the coral reefs of Sesoko Island, Ryukyu Archipelago, Japan. Galaxea 12:103–124
Benayahu Y (2002) Soft corals (Octocorallia: Alcyonacea) of the southern Ryukyu Archipelago: the families Tubiporidae, Clavulariidae. Alcyoniidae and Briareidae Galaxea JSRS 4:11–32
Benayahu Y, Achituv Y, Berner T (1989) Metamorphosis of an octocoral primary polyp and its infection by algal symbiosis. Symbiosis 7:159–169
Benayahu Y, Loya Y (1981) Competition for space among coral-reef sessile organisms at Eilat, Red Sea. Bull Mar Sci 31:514–522
Benayahu Y, Bridge TC, Colin PL, Liberman R, McFadden CS, Pizarro O, Schleyer MH, Shoham E, Reijnen BT, Weis M (2019) Octocorals of the Indo-Pacific. In: Loya Y, Puglise KA, Bridge TCL (eds) “Mesophotic coral ecosystems”, Springer, pp 709–728
Benayahu Y, McFadden CS, Shoham E (2017) Search for mesophotic octocorals (Cnidaria, Anthozoa) and their phylogeny: I. a new sclerite-free genus from Eilat, northern Red Sea. ZooKeys 676:1–12
Benayahu Y, Ofwegen LP, McFadden CS (2018) Evaluating the genus Cespitularia MilneEdwards & Haime, 1850 with descriptions of new genera of the family Xeniidae (Octocorallia, Alcyonacea). ZooKeys 754, 63–101.
Berntson E, Bayer FM, McArthur A, France S (2001) Phylogenetic relationships within the Octocorallia (Cnidaria: Anthozoa) based on nuclear 18S rRNA sequences. Mar Biol 138:235–246
Bilewitch JP, Ekins M, Hooper J, Degnan SM (2014) Molecular and morphological systematics of the Ellisellidae (Coelenterata: Octocorallia): Parallel evolution in a globally distributed family of octocorals. Mol Phylogenet Evol 73:106–118
Brockman SA, McFadden CS (2012) The mitochondrial genome of Paraminabea aldersladei (Cnidaria: Anthozoa: Octocorallia) supports intramolecular recombination as the primary mechanism of gene rearrangement in octocoral mitochondrial genomes. Genome Biol Evol 4:994–1006
Buhl-Mortensen L, Mortensen PB (2005) Distribution and diversity of species associated with deep-sea gorgonian corals off Atlantic Canada. In: Freiwald A, Roberts JM (eds) Cold-water corals and ecosystems. Erlangen Earth Conference Series. Springer, Berlin, pp 849–879
Coelho M (2009) Phylogeography and phylogeny of european gorgoniids (Gorgoniidae: genera Eunicella and Leptogorgia). Master’s Thesis. University of Algarve, pp 50
Ehrenberg CG (1834) Beiträge zur Kenntnis der Corallenthiere im allgemeinen, und besonderen des Rothen Meeres, nebst einem Versuche zur physiologischen Systematik derselben. Abh Königlichen Akad Wiss Berl 1:225–380
Etsebeth K, Pooran S, Macdonald AHH (2017) Sinularia of the Isimangaliso Park, South Africa: do genetic proxies agree with morphological estimates of species diversity? NCBI. https://www.ncbi.nlm.nih.gov/nuccore/MF817930. Accessed 29 Nov 2020
Fabricius K, 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, Queensland, Australia.
Fatemi SMR, Shokri MR (2001) Iranian coral reefs status with particular reference to Kish Island, Persian gulf. In: Proceedings of international coral reef initiative (ICRI) regional workshop for the Indian Ocean, Maputo, Mozambique, 26–28
Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3:294–299
France SC, Hoover LL (2002) DNA sequences of the mitochondrial COI gene have low levels of divergence among deep-sea octocorals (Cnidaria: Anthozoa). Hydrobiologia 471:149–155
Gohar HAF (1948) A description and some biological studies of a new alcyonarian species Clavularia hamra. Pub Mar Biol Stat Ghardaqa (Red Sea) 6:3–33
Grasshoff M (2000) The gorgonians of the Sinai coast and the Strait of Gubal, Red Sea (Coelenterata, Octocorallia). Cour Forschungsinst Senckenberg 224:1–125
Haverkort-Yeh RD, McFadden CS, Benayahu Y, Berumen M, Halász A, Toonen RJ (2013) A taxonomic survey of Saudi Arabian Red Sea octocorals (Cnidaria: Alcyonacea). Mar Biodivers 43:279–291
Hebert PD, Cywinska A, Ball SL, Dewaard JR (2003) Biological identifications through DNA barcodes. P Roy Soc B-Biol Sci 270:313–321
Hellberg ME (2006) No variation and low synonymous substitution rates in coral mtDNA despite high nuclear variation. BMC Evol Biol 6:1–8
Herklots J (1863) Descriptions de deux especes nouvelles de pennatulides des Mers de la Chine. Nederlandsch Tijdschrift voor de Dierkunde 1, 31–34
Hiles IL (1899) The Gorgonacea collected by Dr. Willey. Willey Zool. Res 2(14):195–206
Huang D, Meier R, Todd PA, Chou LM (2008) Slow mitochondrial COI sequence evolution at the base of the metazoan tree and its implications for DNA barcoding. J Mol Evol 66:167–174
Katoh K, Rozewicki J, Yamada KD (2017) MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Brief Bioinform 20(4):1160–1166
Klunzinger CB (1877) Die Korallenthiere des Rothen Meeres. I: Die Alcyonarien und Malacodermen. Gutmann’schen, Berlin. 98pp
Krieger KJ, Wing B (2002) Megafauna associations with deepwater corals (Primnoa spp.) in the Gulf of Alaska. Hydrobiologia 471:83–90
Kong S, Won YJ (2017) Korea Soft Coral Mitochondrial Gene. NCBI. https://www.ncbi.nlm.nih.gov/nuccore/HQ694694.2/. Accessed 29 Nov 2020
Kükenthal W (1913) Alcyonrien des Roten Meeres. In: Expeditionen S.M. Schiff“Pola”in das Rote Meer. Zool Ergeb 29:1–32
Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549
Lamarck JBPA (1816) Polypes tubiferes. In: Histoire naturelle des animeaux sans vertebres. Verdiere, Paris
Lewis J, Wallis E (1991) The function of surface sclerites in gorgonians (Coelenterata, Octocorallia). Biol Bull-US 181:275–288
McFadden CS, Benayahu Y, Pante E, Thoma JN, Nevarez PA, France SC (2011) Limitations of mitochondrial gene barcoding in Octocorallia. Mol Ecol Resour 11:19–31
McFadden CS, France SC, Sánchez JA, Alderslade P (2006) A molecular phylogenetic analysis of the Octocorallia (Cnidaria: Anthozoa) based on mitochondrial protein-coding sequences. Mol Phylogenet Evol 41:513–527
McFadden CS, van Ofwegen LP (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 (4):331
McFadden CS, van Ofwegen L (2013) Molecular phylogenetic evidence supports a new family of octocorals and a new genus of Alcyoniidae (Octocorallia, Alcyonacea). ZooKeys 346:59–83
McFadden CS, Reynolds AM, Janes MP (2014) DNA barcoding of xeniid soft corals (Octocorallia: Alcyonacea: Xeniidae) from Indonesia: species richness and phylogenetic relationships. Syst Biodivers 12:247–257
McFadden CS, Van Ofwegen LP, Beckman EJ, Benayahu Y, Alderslade P (2009) Molecular systematics of the speciose Indo-Pacific soft coral genus, Sinularia (Anthozoa: Octocorallia). Inverteb Biol 128:303–323
McFadden CS, Haverkort-Yeh R, Reynolds AM, Halàsz A, Quattrini AM, Forsman ZH, Benayahu Y, Toonen RJ (2017) Species boundaries in the absence of morphological, ecological or geographical differentiation in the Red Sea octocoral genus Ovabunda (Alcyonacea: Xeniidae). Mol Phylogenetics Evol 112:174–184
Moritz C (1994) Applications of mitochondrial DNA analysis in conservation: a critical review. Mol Ecol 3:401–411
Namin KS, Ofwegen L (2009) Some shallow water octocorals (Coelenterata: Anthozoa) of the Persian Gulf. Zootaxa 2058: 1-52.
Samimi-Namin K, Van Ofwegen L (2009) Some shallow water octocorals (Coelenterata: Anthozoa) of the Persian Gulf. Zootaxa 2058:1–52
Ofwegen LP (2000) Status of knowledge of the Indo Pacific soft coral genus Sinularia May, 1898 (Anthozoa, Octocorallia). In: Kasim Moosa, M., Soemodihardjo, S., Soegiarto, A., Romimohtarto, K., Nontji, A., Suharsono, S., eds. Proc. 9th Int. Coral reef symposium, Ministry of Environment, Indonesian Institute of Sciences, International Society for Reef Studies. Bali, Indonesia. 23-27 October 2000, Vol 1
van Ofwegen L, Benayahu Y, McFadden C (2013) Sinularia leptoclados (Ehrenberg, 1834) (Cnidaria: Octocorallia) re-examined. ZooKeys 272:29–59
Osorio CR, Collins MD, Romalde JL, Toranzo AE (2005) Variation in 16S-23S rRNA intergenic spacer regions in Photobacterium damselae: a mosaic-like structure. Appl Environ Microbiol 71:636–645
Pallas PS (1766) Elenchus zoophytorum sistens generum adumbrationes generaliores et specierum cognitarum succinctas descriptiones cum selectis auctorum synonymis. Hagae Comitum. 1–451
Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics (Oxford, England) 14:817–818
Quattrini AM, Rodríguez E, Faircloth BC, Cowman P, Brugler MR, Farfan G, Hellberg ME, Kitahara MV, Morrison CL, Paz-García DA, Reimer JD, McFadden CS (2020) Paleoclimate ocean conditions shaped diversification of coral skeletal composition through deep time. Nat Ecol Evol 4(11):1531–1538.
Quattrini AM, Wu T, Soong K, Jeng M-S, Benayahu Y, McFadden CS (2019) A next generation approach to species delimitation reveals the role of hybridization in a cryptic species complex of corals. BMC Evol Biol 19:116
Rambaut A, Drummond A (2009) Tracer: MCMC trace analysis tool, version 1.5. University of Oxford, Oxford
Reinicke G (1997) Xeniidae (Coelenterata: Octocorallia) of the Red Sea, with descriptions of six new species of Xenia. Fauna Saudi Arab 16:5–62
Reynolds RM (1993) Physical oceanography of the Persian Gulf, strait of Hormuz, and the Gulf of Oman—results from the Mt. Mitchell expedition. Mar Pollut Bull 27:35–59
Riegl BM, Purkis SJ (2012) Coral reefs of the Gulf: adaptation to climatic extremes in the world’s hottest sea. In: Riegl BM, Purki SJ (eds) “coral reefs of the Gulf”, pp. 1–4. Springer
Reijnen BT, McFadden CS, Hermanlimianto YT, van Ofwegen LP (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
Rocheford T (1994) Change in ribosomal DNA intergenic spacer-length composition in maize recurrent selection populations. 1. Analysis of BS13, BSSS, and BSCB1. Theor Appl Genet 88:541–547
Ronquist F, Huelsenbeck JP, van der Mark P (2005) MrBayes 3.1 manual. pp 1–69
Ronquist F, Teslenko M, Van Der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol 61:539–542
Safaeian S, Esmaieili A, Sharifi S (2010) Study on main lipid of the sea pen Virgularia gustaviana in the Sorou estuary, Bandar Abbas coastal zone, the Persian Gulf. JMSTR. 5(3):31–40
Samimi-Namin K, van Ofwegen L (2012) The octocoral fauna of the Gulf. In: Riegl BM, Purki SJ (eds) “coral reefs of the Gulf”, Springer, pp 225–252
Sánchez J, McFadden CS, France S, Lasker H (2003) Molecular phylogenetic analyses of shallow-water Caribbean octocorals. Mar Biol 142:975–987
Shahbazi S, Sakhaei N, Zolgharnein H, McFadden CS (2019) First record of Viminella sp.(Anthozoa: Alcyonacea: Ellisellidae) in the Persian Gulf. Biodivers Data J 7:e33089
Shearer T, Coffroth M (2006) Genetic identification of Caribbean scleractinian coral recruits at the flower garden banks and the Florida Keys. Mar Ecol Prog Ser 306:133–142
Sotelo G, Morán P, Posada D (2009) Molecular phylogeny and biogeographic history of the European Maja spider crabs (Decapoda, Majidae). Mol Phylogenet Evol 53:314–319
Stiasny G (1940) Gorgonides et alcyonides des collections du Muséum National d'Histoire Naturelle (Première partie). Archives Muséum National d’Histoire Naturelle Paris (6) 16, 109–145.
Stiasny GA (1938) Diagnosen einiger neuer Gorgonarien-Arten aus dem Roten Meere. Zool Anz 121(11/12):336–341
Swofford DL, Sullivan J (2003) Phylogeny inference based on parsimony and other methods using PAUP*. The Phylogenetic Handbook: A Practical Approach to DNA and Protein Phylogeny, cáp 7:160–206
Thomson JA, Simpson JJ (1909) An account of the Alcyonarians collected by the Royal Indian Marine Survey Ship Investigator in the Indian Ocean; with a report on the species of Dendronephthyaby W.D. Henderson. II. The Alcyonarians of the littoral area. Trustees of the Indian Museum. Calcutta, pp. 1–319
Tixier-Durivault A (1945) Les alcyonaires du Muséum: I. Famille des Alcyoniidae. II. Genre Sinularia. Bulletin du Muséum National d’Histoire Naturelle Paris 2:17, 1:55–63, 2:145–152, 3:243–250, 4:321–325
Tixier-Durivault A (1970) Les octocoralliaires de Nha-Trang (Viet-Nam). Cah Pacifique 14:115–236
Tursch B, Tursch A (1982) The soft coral community on a sheltered reef quadrat at Laing Island (Papua New Guinea). Mar Biol 68:321–332
Umar W, Jompa J, Tassakka ACMA (2018) Genetic diversity and geographical gene flow patterns of spawning broadcast coral Lobophyllia corymbosa in the Sulawesi waters as a coral triangle area. 3rd International Conference on Tropical and Coastal Region Eco Development 2017. IOP Conf. Series: Earth and Environmental Science 116: 012060.
Verseveldt J, Benayahu Y (1978) Descriptions of one old and five new species of Alcyonacea (Coelenterata: Octocorallia) from the Red Sea. Zool Meded 53:57–74
Verseveldt J, Cohen J (1971) Some new species of Octocorallia from the Gulf of Elat (Red Sea). Isr J Ecol Evol 20:53–67
Williams GC, Chen J (2014) Illustrated key to the shallow-water gorgonians and pennatulaceans of the Verde Island passage, northern Philippines, including synopses of the taxa and a glossary of terms (Cnidaria: Anthozoa: Octocorallia). In: Williams GC, Gosliner TM (eds) The coral triangle—the Hearst Philippine biodiversity expedition 2011. California Academy of Sciences, San Francisco, pp 67–128
Wirshing H, Messing CG, Douady C, Reed J, Stanhope M, Shivji MS (2005) Molecular evidence for multiple lineages in the gorgonian family Plexauridae (Anthozoa: Octocorallia). Mar Biol 147:497–508
Xia X, Xie Z (2001) DAMBE: software package for data analysis in molecular biology and evolution. J Hered 92:371–373
Zeevi-Ben-Yosef D, Benayahu Y (2008) Synergistic effects of UVR and temperature on survival of azooxanthellate and zooxanthellate early developmental stages of soft corals. Bull Mar Sci 83:401–414
Acknowledgments
We would like to acknowledge the Iranian Biological Resource Center. We greatly appreciate thank the Environment Protection Agencies (EPA) that provided us residency during sampling. We thank PhD candidate Neda Fahimi for their valuable assistance in this work. We are also very grateful to the anonymous reviewers, whose comments have allowed us to improve this paper.
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All necessary permits for sampling and observational field studies have been obtained by the authors from the competent authorities and are mentioned in the acknowledgements. Sample collection was carried out under permission No. 96/3357 on 5 February 2018, from the Department of Environment of Hormozgan Provincial Directorate.
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SS, NS, and HZ conceived and designed the research. SS collected specimens and laboratory activities. SS and CM analyzed the data and did the illustrations. SS and CM wrote and approved the manuscript and English editing of the manuscript by CM. All authors read and approved the manuscript.
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Shahbazi, S., Sakhaei, N., Zolgharnein, H. et al. A molecular systematic survey of the Iranian Persian Gulf octocorals (Cnidaria: Alcyonacea). Mar. Biodivers. 51, 11 (2021). https://doi.org/10.1007/s12526-020-01147-8
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DOI: https://doi.org/10.1007/s12526-020-01147-8