Abstract
Due to the dearth of molecular markers variable enough to distinguish species of black corals, species delimitation in Antipatharia is still mainly based on morphological traits. One of the few markers available, the internal transcribed spacer (ITS) region located in ribosomal DNA, has already been used several times to infer phylogenetic relationships among antipatharians. However, this region was never considered in population-scale studies of shallow-water black corals till now. Here, we sampled two phenotypic variants of 41 specimens of the shallow-water antipatharian Stichopathes cf. maldivensis along the SW of Madagascar. The sampling area represents 200 km of shore and encompasses the runoffs of three rivers. We used direct sequencing to determine the main ITS1 types present in the genomes of the collected specimens and retrieved sequences from GenBank for Indonesian specimens. Then, we constructed a haploweb to visualize possible species boundaries using the criterion of mutual allelic exclusivity. With this method, we confirm that the previously described phenotypic variants belong to a single species that apparently extends from Indonesia to Madagascar. Likewise, the three rivers that pour freshwater in southwestern Madagascar do not appear to act as a barrier for the larval dispersal of this species. This study highlights the usefulness of ITS markers within antipatharians at both species and population levels.
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References
Adjeroud M, Guérécheau A, Vidal-Dupiol J, Flot JF, Arnaud-Haond S, Bonhomme F (2014) Genetic diversity, clonality and connectivity in the scleractinian coral Pocillopora damicornis: a multi-scale analysis in an insular, fragmented reef system. Mar Biol 161:531–541
Aldegheri M (1972) Rivers and streams in Madagascar. In: Biogeography and ecology in Madagascar (pp. 261–310). Springer, Dordrecht.
Bandelt HJ, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16(1):37–48
Barrett NJ, Hogan RI, Allcock AL, Molodtsova T, Hopkins K, Wheeler AK, Yesson C (2020) Phylogenetics and mitogenome organisation in black corals (Anthozoa: Hexacorallia: Antipatharia): an order-wide survey inferred from complete mitochondrial genomes. Front Mar Sci 7:440
Bo M, Barucca M, Biscotti MA, Canapa A, Lapian HFN, Olmo E, Bavestrello G (2009) Description of Pseudocirrhipathes (Cnidaria: Anthozoa: Hexacorallia: Antipathidae) a new genus of whip black corals from the Indo-Pacific. Ital J Zool 76:392–402
Bo M, Bavestrello G, Barucca M, Makapedua DM, Poliseno A, Forconi M, Olmo E, Canapa A (2012) Morphological and molecular characterization of the problematic whip black coral genus Stichopathes (Hexacorallia: Antipatharia) from Indonesia (North Sulawesi, Celebes Sea). Zool J Linn Soc-Lond 166:1–13
Bo M, Barucca M, Biscotti MA, Brugler MR, Canapa A, Canese S, Lo Iacono C, Bavestrello G (2018) Phylogenetic relationships of Mediterranean black corals (Cnidaria: Anthozoa: Hexacorallia) and implications for classification within the order Antipatharia. Invertebr Syst 32:1102–1110
Brabec J, Kuchta R, Scholz T, Littlewood DTJ (2016) Paralogues of nuclear ribosomal genes conceal phylogenetic signals within the invasive Asian fish tapeworm lineage: evidence from next generation sequencing data. Int J Parasitol 46:555–562
Brugler MR, Opresko DM, France SC (2013) The evolutionary history of the order Antipatharia (Cnidaria: Anthozoa: Hexacorallia) as inferred from mitochondrial and nuclear DNA: implications for black coral taxonomy and systematics. Zool J Linn Soc-Lond 169(2):312–361
Calderón I, Garrabou J, Aurelle D (2006) Evaluation of the utility of COI and ITS markers as tools for population genetic studies of temperate gorgonians. J Exp Mar Biol Ecol 336(2):184–197
Cardona Y, Ruiz-Ramos DV, Baums IB, Bracco A (2016) Potential connectivity of coldwater black coral communities in the northern Gulf of Mexico. PloS one 11(5).
Dellicour S, Flot J-F (2018) The hitchhiker’s guide to single-locus species delimitation. Molecular Ecology Resources 18:1234–1246
de Souza JN, Nunes FL, Zilberberg C, Sanchez JA, Migotto AE, Hoeksema BW, Serrano XM, Baker AC, Lindner A (2017) Contrasting patterns of connectivity among endemic and widespread fire coral species (Millepora spp.) in the tropical Southwestern Atlantic. Coral Reefs 36(3): 701–716.
Dmitriev DA, Rakitov RA (2008) Decoding of superimposed traces produced by direct sequencing of heterozygous indels. PLoS Comput Biol 4(7):e1000113
Dong YW, Wang HS, Han GD, Ke CH, Zhan X, Nakano T, Williams GA (2012) The impact of Yangtze River discharge, ocean currents and historical events on the biogeographic pattern of Cellana toreuma along the China coast. PLoS ONE 7(4):e36178
Dover G (1982) A molecular drive through evolution. Bioscience 32:526–533
Doyle JJ (1995) The irrelevance of allele tree topologies for species delimitation, and a non-topological alternative. Syst Bot 20:574–588
Du X, Cai S, Yu C, Jiang X, Lin L, Gao T, Han Z (2016) Population genetic structure of mantis shrimps Oratosquilla oratoria: testing the barrier effect of the Yangtze River outflow. Biochem Syst Ecol 66:12–18
Flot JF (2007) Champuru 1.0: a computer software for unraveling mixtures of two DNA sequences of unequal lengths. Mol Ecol Resour 7(6): 974–977.
Flot JF (2010) SeqPHASE: a web tool for interconverting PHASE input/output files and FASTA sequence alignments. Mol Ecol Resour 10(1):162–166
Flot J-F (2015) Species delimitation’s coming of age. Syst Biol 64:897–899
Flot J-F (2020) Haploweb analysis of ITS sequences of Leiopathes glaberrima (Cnidaria: Antipatharia). Zenodo. https://doi.org/10.5281/zenodo.3960305
Flot JF, Tillier S (2006) Molecular phylogeny and systematics of the scleractinian genus Pocillopora in Hawaii. Proc 10th Int Coral Reef Symp 24–29.
Flot JF, Tillier A, Samadi S, Tillier S (2006) Phase determination from direct sequencing of length-variable DNA regions. Mol Ecol Resour 6(3):627–630
Flot JF, Couloux A, Tillier S (2010) Haplowebs as a graphical tool for delimiting species: a revival of Doyle’s “field for recombination” approach and its application to the coral genus Pocillopora in Clipperton. BMC Evol Biol 10:372
Flot JF, Blanchot J, Charpy L, Cruaud C, Licuanan WY, Nakano Y, Payri C, Tillier S (2011) Incongruence between morphotypes and genetically delimited species in the coral genus Stylophora: phenotypic plasticity, morphological convergence, morphological stasis or interspecific hybridization? BMC Ecol 11:22
Flot J-F, Dahl M, André C (2013) Lophelia pertusa corals from the Ionian and Barents seas share identical nuclear ITS2 and near-identical mitochondrial genome sequences. BMC Res Notes 6:144
Fontaneto D, Flot JF, Tang CQ (2015) Guidelines for DNA taxonomy, with a focus on the meiofauna. Mar Biodivers 45(3):433–451
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(1–3):149–155
Gaino E, Scoccia F (2009) Release of sperm clusters in spheres by the black coral Cupressopathes pumila (Anthozoa, Antipatharia). Coral Reefs 28(4):851–857
Huang W, Li M, Yu K, Wang Y, Li J, Liang J, Luo Y, Huang X, Qin Z, Wang G, Su H, Wei F (2018) Genetic diversity and large-scale connectivity of the scleractinian coral Porites lutea in the South China Sea. Coral Reefs 37:1259–1271
Hellberg ME (2006) No variation and low synonymous substitution rates in coral mtDNA despite high nuclear variation. BMC Evol Biol 6(1):24
Horowitz J, Brugler MR, Bridge TCL, Cowman PF (2020) Morphological and molecular descruption of a new genus and species of black coral (Cnidaria: Anthozoa: Hexacorallia: Antipatharia: Antipathidae: Blastopathes) from Papua New Guinea. Zootaxa 4821(3):553–569
Kang JH, Jang JE, Kim JH, Kim S, Keshavmurthy S, Agostini S, Reimer JD, Chen CA, Choi K-S, Park SR, Lee HJ (2020) The origin of the subtropical coral Alveopora japonica (Scleractinia: Acroporidae) in high-latitude environments. Front Ecol Evol 8:12
Katoh K, Kuma K, Toh H, Miyata T (2005) MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res 33(2):511–518
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33(7): 1870–1874.
Lapian HFN, Barucca M, Bavestrello G, Biscotti MA, Bo M, Canapa A, Tazioli S, Olmo E (2007) A systematic study of some black corals species (Antipatharia, Hexacorallia) based on rDNA internal transcribed spacers sequences. Mar Biol 151:785–792
Lapian HFN (2009) Biodiversity study of black coral (order: Antipatharia) collected from Manado, Indonesia based on rDNA Internal Transcribed Spacer (ITS) sequences analysis. Biodiversitas 10(1):1–5
Lauretta D, Penchaszadeh PE (2017) Gigantic oocytes in the deep sea black coral Dendrobathypathes grandis (Antipatharia) from the Mar del Plata submarine canyon area (southwestern Atlantic). Deep Sea Res Part I Oceanogr 128:109–114
Leffler EM, Bullaughey K, Matute DR, Meyer WK, Ségurel L, Venkat A, Andolfatto P, Przeworski M (2012) Revisiting an old riddle: what determines genetic diversity levels within species? PLoS Biol 10:e1001388
McIsaac KG, Best M, Brugler MR, Kenchington ELR, Anstey LJ, Jordan T (2013) Telopathes magna gen. nov., spec. nov. (Cnidaria: Anthozoa: Antipatharia: Schizopathidae) from deep waters off Atlantic Canada and the first molecular phylogeny of the deep-sea family Schizopathidae. Zootaxa 3700(2): 237–258.
McFadden CS, Sánchez JA, France SC (2010) Molecular phylogenetic insights into the evolution of Octocorallia: a review. Integr Comp Biol 50(3):389–410
Miller KJ (1997) Genetic structure of black coral populations in New Zealand’s fiords. Mar Ecol Prog Ser 161:123–132
Miller KJ (1998) Short-distance dispersal of black coral larvae: inference from spatial analysis of colony genotypes. Mar Ecol Prog Ser 163:225–233
Miller K, Williams A, Rowden AA, Knowles C, Dunshea G (2010) Conflicting estimates of connectivity among deep-sea coral populations. Mar Ecol 31:144–157
Molodtsova T, Opresko D (2017) Black corals (Anthozoa: Antipatharia) of the Clarion-Clipperton Fracture Zone. Mar Biodivers 47:349–365
Molodtsova T, Opresko D (2019) World List of Antipatharia. Accessed through: World Register of Marine Species. http://www.marinespecies.org/
Navajas M, Boursot P (2003) Nuclear ribosomal DNA monophyly versus mitochondrial DNA polyphyly in two closely related mite species: the influence of life history and molecular drive. Proc R Soc Lond B 270:S124-127
Opresko DM, Goldman SL, Johnson R, Parra K, Nuttall M, Schmahl GP, Brugler MR (2020) Morphological and molecular characterization of a new species of black coral from Elvers Bank, north-western Gulf of Mexico (Cnidaria: Anthozoa: Hexacorallia: Antipatharia: Aphanipathidae: Distichopathes). J Mar Biol Assoc U K 100(4):559–566
Posada D (2006) ModelTest Server: a web-based tool for the statistical selection of models of nucleotide substitution online. Nucleic Acids Research, 34(suppl_2), W700–W703.
Pillay KRM, Asahida 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
Puillandre N, Lambert A, Brouillet S, Achaz G (2012) ABGD, Automatic Barcode Gap Discovery for primary species delimitation. Mol Ecol 21(8):1864–1877
Quattrini AM, Faircloth BC, Dueñas LF, Bridge TCL, Brugler MR, Calixto-Botia I, DeLeo DM, Forêt S, Herrera S, Lee SMY, Miller DJ, Prada C, Radis-Baptista G, Ramirez-Portilla C, Sanchez JA, Rodriguez E, McFadden C (2018) Universal target-enrichment baits for anthozoan (Cnidaria) phylogenomics: New approaches to long-standing problems. Mol Ecol Resour 18:281–295
Ramanantsoa JD, Penven P, Krug M, Gula J, Rouault M (2018) Uncovering a new current: the Southwest MAdagascar Coastal Current. Geophys Res Lett 45(4):1930–1938
Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19(12):1572–1574
Rozas J, Ferrer-Mata A, Sánchez-DelBarrio JC, Guirao-Rico S, Librado P, Ramos-Onsins SE, Sánchez-Gracia A (2017) DnaSP 6: DNA sequence polymorphism analysis of large data sets. Mol Biol Evol 34(12):3299–3302
Ruiz-Ramos DV, Saunders M, Fisher CR, Baums IB (2015) Home bodies and wanderers: sympatric lineages of the deep-sea black coral Leiopathes glaberrima. PLoS ONE 10:e0138989
Shearer TL, Coffroth MA (2008) Barcoding corals: limited by interspecific divergence, not intraspecific variation. Mol Ecol Resour 8(2):247–255
Spöri Y, Flot J (2020) HaplowebMaker and CoMa: two web tools to delimit species using haplowebs and conspecificity matrices. Methods Ecol Evol 11(11):1434–1438
Stephens M, Smith NJ, Donnelly P (2001) A new statistical method for haplotype reconstruction from population data. Am J Hum Genet 68(4):978–989
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: Molecular Evolutionary Genetics Analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28(10):2731–2739
Tazioli S, Bo M, Boyer M, Rotinsulu H, Bavestrello G (2007) Ecological observations of some common antipatharian corals in the marine park of Bunaken (North Sulawesi, Indonesia). Zool Stud 46(2):227–241
Terrana L, Eeckhaut I (2019) Sexual reproduction of the shallow-water black coral Cirrhipathes anguina (Dana, 1846) from Madagascar. Mar Biol Res 15(7):410–423
Terrana L, Bo M, Opresko D, Eeckhaut I (2020) Shallow-water black corals (Hexacorallia: Antipatharia) from SW Madagascar. Zootaxa, 4826(1), zootaxa-4826.
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
Untergasser A, Cutcutache I, Koressaar T, Ye J, Faircloth BC, Remm M, Rozen SG (2012) Primer3 – new capabilities and interfaces. Nucleic Acids Res 40(15):e115
van der Ven R, Flot J-F, Buitrago-Lopez C, Kochzius M (2020) Population genetics of the brooding coral Seriatopora hystrix reveals patterns of strong genetic differentiation in the Western Indian Ocean. Heredity.
van Oppen MJH, Wörheide G, Takabayashi M (2002) Nuclear markers in evolutionary and population genetic studies of scleractinian corals and sponges. Proc 9th Int Coral Reef Symp 1:131–138.
Wagner D, Brugler MR, Opresko DM, France SC, Montgomery AD, Toonen RJ (2010) Using morphometrics, in situ observations and genetic characters to distinguish among commercially valuable Hawaiian black coral species; a redescription of Antipathes grandis Verrill, 1928 (Antipatharia: Antipathidae). Invertebr Syst 24:271–290
Wagner D (2015) A taxonomic survey of the shallow-water (< 150 m) black corals (Cnidaria: Antipatharia) of the Hawaiian Islands. Front Mar Sci 2:24
Acknowledgements
The authors are grateful to the two anonymous reviewers for their interesting remarks and suggestions that improved the quality of this manuscript. The authors are grateful to the Institut Halieutique et des Sciences Marines (IHSM) of the University of Toliara for providing facilities. Many thanks to Gildas Todinanahary for the administrative support. Thank also to Emily Claereboudt, Guillaume Ghisbain and Radonirina Lebely for their help during underwater sampling and field trips, and to Iliana Baums and Dannise Ruiz-Ramos for sharing with us the chromatograms of their Leiopathes glaberrima study. LT was supported by a PhD grant from the Fonds pour la Formation à la Recherche dans l’Industrie et dans l’Agriculture (FRIA). This work was supported by the Fonds National de la Recherche Scientifique (FNRS) grant PDR/OL T.0084.18 and the Fonds Leopold III pour l’Exploration et la Conservation de la Nature.
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Terrana, L., Flot, JF. & Eeckhaut, I. ITS1 variation among Stichopathes cf. maldivensis (Hexacorallia: Antipatharia) whip black corals unveils conspecificity and population connectivity at local and global scales across the Indo-Pacific. Coral Reefs 40, 521–533 (2021). https://doi.org/10.1007/s00338-020-02049-8
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DOI: https://doi.org/10.1007/s00338-020-02049-8