Abstract
Scleractinian corals ascribed to the family Agariciidae represent an important component of Red Sea coral reef fauna, though little genetic data are currently available for this group, and existing information shows polyphyly in the examined mesophotic taxa from the Pacific Ocean. In this work, we provide a first genetic survey of Agariciidae from the Saudi Arabian Red Sea, based on a collection of shallow-water material (<30 m) from the Gulf of Aqaba to the Farasan Islands. Two molecular markers were sequenced to infer morphospecies monophyly and relationships, the intergenic region between COI and 16S rRNA from mitochondrial DNA and the ribosomal ITS1 region from nuclear DNA. A total of 20 morphospecies were identified based on classical macromorphological characters. Six, namely Gardineroseris planulata, Pavona maldivensis, Pavona clavus, Pavona decussata, Leptoseris fragilis, and Leptoseris yabei, were resolved with both DNA loci. The molecular boundaries among the remaining 14 species remain unclear. Our results further confirm that the morphology-based taxonomy of most agariciid species is in disagreement with genetics. In order to disentangle the systematics of these taxa, the inclusion of more sampling locations, additional variable loci, and a micromophological approach are likely needed. Our genetic data represent a first step towards the comparison of biodiversity and connectivity between the Red Sea and the rest of the Indo-Pacific.
Similar content being viewed by others
References
Arrigoni R, Stefani F, Pichon M, Galli P, Benzoni F (2012) Molecular phylogeny of the robust clade (Faviidae, Mussidae, Merulinidae, and Pectiniidae): an Indian Ocean perspective. Mol Phylogenet Evol 65:183–193
Arrigoni R, Berumen ML, Terraneo TI, Caragnano A, Bouwmeester J, Benzoni F (2015) Forgotten in the taxonomic literature: resurrection of the scleractinian coral genus Sclerophyllia (Scleractinia, Lobophylliidae) from the Arabian peninsula and its phylogenetic relationships. Syst Biodivers 13:140–163
Arrigoni R, Berumen ML, Chen CA, Terraneo TI, Baird AH, Payri C, Benzoni F (2016a) Species delimitation in the reef coral genera Echinophyllia and Oxypora (Scleractinia, Lobophylliidae) with a description of two new species. Mol Phylogenet Evol 105:146–159
Arrigoni R, Benzoni F, Huang D, Fukami H, Chen CA, Berumen ML, Hoogenboom M, Thomson DP, Hoeksema BW, Budd AF, Zayasu Y, Terraneo TI, Kitano YF, Baird AH (2016b) When forms meet genes: revision of the scleractinian genera Micromussa and Homophyllia (Lobophylliidae) with a description of two new species and one new genus. Contrib Zool 85:387–422
Arrigoni R, Benzoni F, Terraneo TI, Caragnano A, Berumen ML (2016c) Recent origin and semi-permeable species boundaries in the scleractinian coral genus Stylophora from the Red Sea. Sci Rep 6:34612
Arrigoni R, Berumen ML, Huang D, Terraneo TI, Benzoni F (2017) Cyphastrea (Cnidaria: Scleractinia: Merulinidae) in the Red Sea: phylogeny and a new reef coral species. Invertebr Syst 31:141–156
Benzoni F, Arrigoni R, Stefani F, Stolarski J (2012) Systematics of the coral genus Craterastrea (Cnidaria, Anthozoa, Scleractinia) and description of a new family through combined morphological and molecular analyses. Syst Biodivers 10:417–433
Berumen ML, Hoey AS, Bass WH, Bouwmeester J, Catania D, Cochran JE, Khalil MT, Miyake S, Mughal MR, Spaet JL, Saenz-Agudelo P (2013) The status of coral reef ecology research in the Red Sea. Coral Reefs 32:737–748
Bongaerts P, Frade PR, Ogier JJ, Hay KB, Van Bleijswijk J, Englebert N, Vermeij MJ, Bak RP, Visser PM, Hoegh-Guldberg O (2013) Sharing the slope: depth partitioning of agariciid corals and associated Symbiodinium across shallow and mesophotic habitats (2–60 m) on a Caribbean reef. BMC Evol Biol 13:205
Bongaerts P, Frade PR, Hay KB, Englebert N, Latijnhouwers KR, Bak RP, Vermeij MJ, Hoegh-Guldberg O (2015) Deep down on a Caribbean reef: lower mesophotic depths harbor a specialized coral-endosymbiont community. Sci Rep 5:7652
Bouchon C (1981) Quantitative study of the scleractinian coral communities of a fringing reef of Reunion Island (Indian Ocean). Mar Ecol Prog Ser 4:273–288
Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17:540–552
Coleman RR, Eble JA, DiBattista JD, Rocha LA, Randall JE, Berumen ML, Bowen BW (2016) Regal phylogeography: range-wide survey of the marine angelfish Pygoplites diacanthus reveals evolutionary partitions between the Red Sea, Indian Ocean, and Pacific Ocean. Mol Phylogenet Evol 100:243–253
Crossland C (1952) Madreporaria, Hydrocorallinae, Heliopora and Tubipora. Br Mus Nat Hist 6:85–257
DiBattista JD, Berumen ML, Gaither MR, Rocha LA, Eble JA, Choat JH, Craig MT, Skillings DJ, Bowen BW (2013) After continents divide: comparative phylogeography of reef fishes from the Red Sea and Indian Ocean. J Biogeogr 40:1170–1181
DiBattista JD, Waldrop E, Rocha LA, Craig MT, Berumen ML, Bowen BW (2015) Blinded by the bright: a lack of congruence between colour morphs, phylogeography and taxonomy for a cosmopolitan Indo-Pacific butterflyfish, Chaetodon auriga. J Biogeogr 42:1919–1929
DiBattista JD, Howard Choat J, Gaither MR, Hobbs JP, Lozano-Cortés DF, Myers RF, Paulay G, Rocha LA, Toonen RJ, Westneat MW, Berumen ML (2016a) On the origin of endemic species in the Red Sea. J Biogeogr 43:13–30
DiBattista JD, Roberts MB, Bouwmeester J, Bowen BW, Coker DJ, Lozano-Cortés DF, Howard Choat J, Gaither MR, Hobbs JP, Khalil MT, Kochzius M, Myers RF, Paulay G, Robitzch VSN, Saenz-Agudelo P, Salas E, Sinclair-Taylor TH, Toonen RJ, Westneat MW, Williams ST, Berumen ML (2016b) A review of contemporary patterns of endemism for shallow water reef fauna in the Red Sea. J Biogeogr 43:423–439
Dinesen ZD (1980) A revision of the coral genus Leptoseris (Scleractinia: Fungiina: Agariciidae). Mem Queensl Mus 20:181–235
Ehrenberg CG (1834) Beiträge zur physiologischen Kenntniss der Corallenthiere im Allgemeinen, und besonders des Rothen Meeres, nebst einem Versuche zur physiologischen Systematik derselben. Abhandlungen der Königlichen Akademie der Wissenschaften, Berlin
Ekman S (1953) Zoogeography of the sea. Sidgwick & Jackson, London
Flot JF (2007) Champuru 1.0: a computer software for unraveling mixtures of two DNA sequences of unequal lengths. Mol Ecol Resour 7:974–977
Flot JF (2010) SeqPHASE: a web tool for interconverting PHASE input/output files and FASTA sequence alignments. Mol Ecol Resour 10:162–166
Forskål P (1775) Descriptiones animalium, avium, amphibiorum, piscium, insectorum, vermium; quæ in itinere orientali observavit Petrus Forskål. Hauniæ, Heineck et Faber, Copenhagen
Fricke HW, Knauer B (1986) Diversity and spatial pattern of coral communities in the Red Sea upper twilight zone. Oecologia 71:29–37
Fricke HW, Vareschi E, Schlichter D (1987) Photoecology of the coral Leptoseris fragilis in the Red Sea twilight zone (an experimental study by submersible). Oecologia 73:371–381
Fukami H, Chen CA, Budd AF, Collins A, Wallace C, Chuang YY, Chen C, Dai CF, Iwao K, Sheppard C, 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
Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98
Hellberg ME (2006) No variation and low synonymous substitution rates in coral mtDNA despite high nuclear variation. BMC Evol Biol 6:24
Hinderstein LM, Marr JCA, Martinez FA, Dowgiallo MJ, Puglise KA, Pyle RL, Zawada DG, Appeldoorn R (2010) Theme section on “Mesophotic coral ecosystems: characterization, ecology, and management”. Coral Reefs 29:247–251
Hodge JR, van Herwerden L, Bellwood DR (2014) Temporal evolution of coral reef fishes: global patterns and disparity in isolated locations. J Biogeogr 41:2115–2127
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
Kahng SE, Kelley CD (2007) Vertical zonation of megabenthic taxa on a deep photosynthetic reef (50–140 m) in the Au’au Channel, Hawaii. Coral Reefs 26:679–687
Kahng SE, Garcia-Sais JR, Spalding HL, Brokovich E, Wagner D, Weil E, Hinderstein L, Toonen RJ (2010) Community ecology of mesophotic coral reef ecosystems. Coral Reefs 29:255–275
Kahng SE, Copus JM, Wagner D (2014) Recent advances in the ecology of mesophotic coral ecosystems (MCEs). Curr Opin Environ Sustain 7:72–81
Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780
Kelchner SA (2000) The evolution of non-coding chloroplast DNA and its application in plant systematics. Ann Mo Bot Gard 87:482–498
Kitahara MV, Cairns SD, Stolarski J, Blair D, Miller DJ (2010) A comprehensive phylogenetic analysis of the Scleractinia (Cnidaria, Anthozoa) based on mitochondrial CO1 sequence data. PLoS One 5(7):e11490. doi:10.1371/journal.pone.0011490
Kitahara MV, Stolarski J, Cairns SD, Benzoni F, Stake JL, Miller DJ (2012) The first modern solitary Agariciidae (Anthozoa, Scleractinia) revealed by molecular and microstructural analysis. Invertebr Syst 26:303–315
Kitahara MV, Fukami H, Benzoni F, Huang D (2016) The new systematics of Scleractinia: integrating molecular and morphological evidence. In: Goffredo S, Dubinsky Z (eds) The Cnidaria, past, present and future: the world of Medusa and her sisters. Springer, Dordrecht, pp 41–60
Kitano YF, Benzoni F, Arrigoni R, Shirayama Y, Wallace CC, Fukami H (2014) A phylogeny of the family Poritidae (Cnidaria, Scleractinia) based on molecular and morphological analyses. PLoS One 9:e98406
Klunzinger CB (1870) Synopsis der fische des Rothen Meeres. C. Ueberreuter’shBuchdruckerei, Wien
Klunzinger CB (1877) Die Korallthiere des Rothen Meeres. Gutmann’schen, Berlin
Ladner JT, Palumbi SR (2012) Extensive sympatry, cryptic diversity and introgression throughout the geographic distribution of two coral species complexes. Mol Ecol 21:2224–2238
Lamarck JBP (1816) Histoire naturelle des Animaux sans Vertèbres, présentant les caractères généraux et particuliers de ces animaux, leur distribution, leurs classes, leurs familles, leurs genres, et la citation des principales espèces qui s’y rapportent; précédée d’une Introduction offrant la détermination des caractères essentiels de l’animal, sa distinction du végétal et des autres corps naturels, enfin, l’exposition des principes fondomentaux de la zoologie. Déterville & Verdière, Paris
Lesser MP, Slattery M, Leichter JJ (2009) Ecology of mesophotic coral reefs. J Exp Mar Biol Ecol 375:1–8
Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452
Loya Y, Genin A, el-Zibdeh M, Naumann MS, Wild C (2014) Reviewing the status of coral reef ecology of the Red Sea: key topics and relevant research. Coral Reefs 33:1179–1180
Luck DG, Forsman ZH, Toonen RJ, Leicht SJ, Kahng SE (2013) Polyphyly and hidden species among Hawaiʻi’s dominant mesophotic coral genera, Leptoseris and Pavona (Scleractinia: Agariciidae). Peer J 1:e132
Maragos JE, Jokiel PL (1986) Reef corals of Johnston atoll: one of the world’s most isolated reefs. Coral Reefs 4:141–150
Maté J (2003) Ecological, genetic, and morphological differences among three Pavona (Cnidaria: Anthozoa) species from the Pacific coast of Panama. Mar Biol 142:427–440
Moothien Pillay KR, Aasahida T, Chen CA, 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. Zool Stud 45:132–144
Nishihira M, Veron JEN (1995) Hermatypic corals of Japan. Kaiyusha, Tokyo
Obura D (2012) The diversity and biogeography of western Indian Ocean reef-building corals. PLoS One 7:e45013
Pante E, Abdelkrim J, Viricel A, Gey D, France SC, Boisselier MC, Samadi S (2015) Use of RAD sequencing for delimiting species. Heredity 114(5):450–459
Pillai CSG, Scheer G (1976) Report on the stony corals from the Maldive Archipelago. Results of the Xarifa Expedition 1957/58. Zoologica, Stuttgart 43(126):1–83
Pochon X, Forsman ZH, Spalding HL, Padilla-Gamiño JL, Smith CM, Gates RD (2015) Depth specialization in mesophotic corals (Leptoseris spp.) and associated algal symbionts in Hawai’i. R Soc Open Sci 2:140351
Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14(9):817–818
Rambaut A, Drummond AJ (2007) Tracer v1.4. Available from http://beast.bio.ed.ac.uk/Tracer
Richards ZT, Berry O, van Oppen MJ (2016) Cryptic genetic divergence within threatened species of Acropora Coral from the Indian and Pacific oceans. Conserv Genet 17:577–591
Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574
Rooney J, Donham E, Montgomery A, Spalding H, Parrish F, Boland R, Fenner D, Gove J, Vetter O (2010) Mesophotic coral ecosystems in the Hawaiian archipelago. Coral Reefs 29:361–367
Scheer G, Pillai CSG (1974) Report on the Scleractinia from the Nicobar Islands. E. Schweizerbart’sche Verlagsbuchhandlung, Stuttgart
Scheer G, Pillai CSG (1983) Report on the stony corals from the Red Sea. E. Schweizerbart’sche Verlagsbuchhandlung, Stuttgart
Shearer TL, Van Oppen MJH, Romano SL, Wörheide G (2002) Slow mitochondrial DNA sequence evolution in the Anthozoa (Cnidaria). Mol Ecol 11:2475–2487
Sheppard CRC, Sheppard ALS (1991) Corals and coral communities of Saudi Arabia. Fauna Saudi Arabia 12:1–170
Sheppard CRC, Price A, Roberts C (1992) Marine ecology of the Arabian region. Academic Press, London
Stefani F, Benzoni F, Yang SY, Pichon M, Galli P, Chen CA (2011) Comparison of morphological and genetic analyses reveals cryptic divergence and morphological plasticity in Stylophora (Cnidaria, Scleractinia). Coral Reefs 30:1033–1049
Stephens M, Smith N, Donnelly P (2001) A new statistical method for haplotype reconstruction from population data. Am J Hum Genet 68:978–989
Swofford DL (2002) PAUP*. Phylogenetic Analysis Using Parsimony (*and other methods). Version 4. Sinauer Associates, Sunderland
Terraneo TI, Berumen ML, Arrigoni R, Waheed Z, Bouwmeester J, Caragnano A, Stefani F, Benzoni F (2014) Pachyseris inattesa sp. n. (Cnidaria, Anthozoa, Scleractinia): a new reef coral species from the Red Sea and its phylogenetic relationships. ZooKeys 433:1–33
Terraneo TI, Benzoni F, Arrigoni R, Berumen ML (2016) Species delimitation in the coral genus Goniopora (Scleractinia, Poritidae) from the Saudi Arabian Red Sea. Mol Phylogenet Evol 102:278–294
Vaughan TW (1918) Some shoal-water corals from Murray Island (Australia), Cocos-Keeling Islands, and Fanning Island. Carnegie Institution of Washington, Washington
Vaughan TW, Wells JW (1943) Revision of the suborders, families, and genera of the Scleractinia. Geol Soc Am Special Paper 44:1–394
Veron JEN (2000) Corals of the world. Australian Institute of Marine Science, Townsville
Veron JEN, Pichon M (1980) Scleractinia of eastern Australia. Part III: families Agariciidae, Siderastreidae, Fungiidae, Oculinidae, Merulinudae, Mussidae, Pectiniidae, Caryophylliidae, Dendrophylliidae. Aust Inst Mar Sci Monogr 4:1–422
Veron J, Stafford-Smith M, DeVantier L, Turak E (2015) Overview of distribution patterns of zooxanthellate Scleractinia. Front Mar Sci 1:81
Waheed Z, Hoeksema BW (2014) Diversity patterns of scleractinian corals at Kota Kinabalu, Malaysia, in relation to exposure and depth. Raffles Bull Zool 62:66–82
Waheed Z, Benzoni F, van der Meij SE, Terraneo TI, Hoeksema BW (2015) Scleractinian corals (Fungiidae, Agariciidae and Euphylliidae) of Pulau Layang-Layang, Spratly Islands, with a note on Pavona maldivensis (Gardiner, 1905). ZooKeys 517:1–37
Wei NW, Wallace CC, Dai CF, Pillay KRM, Chen CA (2006) Analyses of the ribosomal internal transcribed spacers (ITS) and 5.8 S gene indicate that extremely high rDNA heterogeneity is a unique feature in the scleractinian coral genus Acropora (Scleractinia; Acroporidae). Zool Stud 45:404–418
Wells JW (1956) Scleractinia. In: Moore RC (ed) Treatise on invertebrate paleontology, part F (Coelenterata). The University of Kansas Press, Lawrence, pp F328–F444
WoRMS (2016) World register of marine species. Available from http://www.marinespecies.org at VLIZ. Accessed 29 Sep 2016
Yabe H, Sugiyama T (1941) Recent reef-building corals from Japan and the South Sea Islands under the Japanese mandate II. The Science reports of the Tôhoku Imperial University, Sendai. 2nd Series (Geologie) Special Volume 2:67–91
Ziegler M, Roder CM, Büchel C, Voolstra CR (2015) Mesophotic coral depth acclimatization is a function of host-specific symbiont physiology. Front Mar Sci 2:1–4
Acknowledgments
This research was undertaken in accordance with the policies and procedures of the King Abdullah University of Science and Technology (KAUST). Permissions relevant for KAUST to undertake the research have been obtained from the applicable governmental agencies in the Kingdom of Saudi Arabia. We wish to thank the captain and crew of the MV Dream Master, the KAUST Coastal and Marine Resources Core Lab, A. Gusti (KAUST), and T.H. Sinclair-Taylor (KAUST). T.I.T. and R.A. gratefully acknowledge J.D. DiBattista (CURTIN) and P. Saenz-Agudelo (UACH) for their assistance at KAUST. This project was supported by funding from KAUST (award nos. URF/1/1389-01-01 and FCC/1/1973-07, and baseline research funds to M.L.B.).
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by M. Sonnewald
Rights and permissions
About this article
Cite this article
Terraneo, T.I., Arrigoni, R., Benzoni, F. et al. Exploring the genetic diversity of shallow-water Agariciidae (Cnidaria: Anthozoa) from the Saudi Arabian Red Sea. Mar Biodiv 47, 1065–1078 (2017). https://doi.org/10.1007/s12526-017-0722-3
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12526-017-0722-3