Abstract
Thouarella Gray, 1870, is one of the most speciose genera among primnoid gorgonians. It has a worldwide distribution that includes Antarctic and sub-Antarctic regions. Based on a combination of detailed morphological studies and analyses using mitochondrial and nuclear DNA markers, we describe and illustrate three new species of bottlebrush-shaped Thouarella from the Weddell Sea, Southern Ocean: T. islai sp. nov., T. weddellensis sp. nov. and T. polarsterni sp. nov. For the morphological description, we used macro-structural characters, such as branching pattern and polyp arrangement, along with axis and micro-structural characters, such as architecture and shapes of scales and their arrangement in polyps. Additionally, we amplified two mitochondrial (mtMutS and Cox1) and one nuclear loci (28S rDNA) obtaining optimal topologies under a Bayesian approach. Resulting molecular phylogenies corroborated the status of the new taxa and elucidated their relationships to closely related species. With the three new species here described, the global diversity of Thouarella has increased to 38 species, 12 of which are endemic to Antarctic and sub-Antarctic waters. The high number of species from higher latitudes of the Southern Hemisphere, the high grade of endemism in this biogeographic area and recent phylogenetic analyses support the idea that the Southern Ocean was likely a centre for Thouarella species radiation.
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Abbreviations
- BECA:
-
Biodiversidad y Ecología Acuática
- H:
-
Height
- H:W:
-
Ratio height/width of a scale
- IL:
-
Inner lateral scales
- L:
-
Length of a polyp
- M:
-
Marginal scale
- MZB:
-
Museu de Zoologia de Barcelona
- O:
-
Opercular scale
- OL:
-
Outer lateral scales
- SEM:
-
Scanning electron microscopy
- SM:
-
Submarginal
- W:
-
Width
References
Altuna Á, López-González PJ (2019) Description of two new species of bathyal Primnoidae (Octocorallia: Alcyonacea) from the Porcupine Bank (northeastern Atlantic). Zootaxa 4576:61–80. https://doi.org/10.11646/zootaxa.4576.1.3
Baco AR, Cairns SD (2012) Comparing molecular variation to morphological species designations in the deep-sea coral Narella reveals new insights into seamount coral ranges. PLoS One 7:e45555. https://doi.org/10.1371/journal.pone.0045555
Bayer FM, Grasshoff M, Verseveldt J (1983) Illustrated trilingual glossary of morphological and anatomical terms applied to Octocorallia. E.J. Brill/Dr. W, Backhuys, Leiden
Bayer FM, Stefani J (1988) Primnoidae (Gorgonacea) de Nouvelle-Calédonie. Bull Mus Natl Hist Nat 4:449–518
Bickford D, Lohman DJ, Sodhi NS, Ng PKL, Meier R, Winker K, Ingram KK, Das I (2007) Cryptic species as a window on diversity and conservation. Trends Ecol Evol 22:148–155. https://doi.org/10.1016/J.TREE.2006.11.004
Bilewitch JP, Degnan SM (2011) A unique horizontal gene transfer event has provided the octocoral mitochondrial genome with an active mismatch repair gene that has potential for an unusual self-contained function. BMC Evol Biol 11:1–14. https://doi.org/10.1186/1471-2148-11-228
Brandt A, De Broyer C, De Mesel I, Ellingsen KE, Gooday AJ, Hilbig B, Linse K, Thomson MRA, Tyler PA (2007) The biodiversity of the deep Southern Ocean benthos. Philos Trans R Soc B Biol Sci 362:39–66. https://doi.org/10.1098/rstb.2006.1952
Broyer C, Koubbi P, Griffiths HJ, Raymond B, Udekem d’Acoz, C d’, Van de Putte AP, Danis B, David B, Grant S, Gutt J, Held C, Hosie G, Huettmann F, Post A, Ropert-Coudert Y (2014) Biogeographic atlas of the Southern Ocean. Cambridge. SCAR, Cambridge
Cairns SD (2006) Studies on western Atlantic Octocorallia (Coelenterata: Anthozoa). Part 6: the genera Primnoella Gray, 1858; Thouarella Gray, 1870; Dasystenella Versluys, 1906. Proc Biol Soc Wash 119:161–194. https://doi.org/10.2988/0006-324X(2006)119[161:SOWAOC]2.0.CO;2
Cairns SD (2011) A revision of the Primnoidae (Octocorallia: Alcyonacea) from the Aleutian Islands and Bering Sea. Smiths Contrib Zool 634:1–55. https://doi.org/10.5479/si.00810282.634
Cairns SD, Bayer FM (2009) A generic revision and phylogenetic analysis of the Primnoidae (Cnidaria: Octocorallia). Smiths Contrib Zool 629:1–79. https://doi.org/10.5479/si.00810282.629
Cairns SD, Stone RP, Moon H-W, Lee JH (2018) Primnoidae (Octocorallia: Calcaxonia) from the Emperor Seamounts, with notes on Callogorgia elegans (Gray, 1870). Pac Sci 72:125–142. https://doi.org/10.2984/72.1.8
Cairns SD, Wirshing HH (2018) A phylogenetic analysis of the Primnoidae (Anthozoa: Octocorallia: Calcaxonia) with analyses of character evolution and a key to the genera and subgenera. BMC Evol Biol 18:66. https://doi.org/10.1186/s12862-018-1182-5
Chenuil A, Saucède T, Hemery LG, Eléaume M, Féral JP, Améziane N, David B, Lecointre G, Havermans C (2018) Understanding processes at the origin of species flocks with a focus on the marine Antarctic fauna. Biol Rev 93:481–504. https://doi.org/10.1111/brv.12354
Chown SL, Clarke A, Fraser CI, Cary SC, Moon KL, McGeoch MA (2015) The changing form of Antarctic biodiversity. Nature 522:431–438. https://doi.org/10.1038/nature14505
Clarke A, Crame JA (1992) The Southern Ocean benthic fauna and climate change: a historical perspective. Philos Trans R Soc B Biol Sci 338:299–309. https://doi.org/10.1098/rstb.1992.0150
Cristini L, Grosfeld K, Butzin M, Lohmann G (2012) Influence of the opening of the Drake Passage on the Cenozoic Antarctic Ice Sheet: a modeling approach. Palaeogeogr Palaeoclimatol Palaeoecol 339:66–73. https://doi.org/10.1016/J.PALAEO.2012.04.023
Darriba D, Taboada GL, Doallo R, Posada D (2012) JModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772. https://doi.org/10.1038/nmeth.2109
De Queiroz K (2007) Species concepts and species delimitation. Syst Biol 56:879–886. https://doi.org/10.1080/10635150701701083
De Queiroz K (2005) A unified concept of species and its consequences for the future of taxonomy. Proc Calif Acad Sci 56:196–215
Dueñas LF, Alderslade P, Sánchez JA (2014) Molecular systematics of the deep-sea bamboo corals (Octocorallia: Isididae: Keratoisidinae) from New Zealand with descriptions of two new species of Keratoisis. Mol Phylogenet Evol 74:15–28. https://doi.org/10.1016/j.ympev.2014.01.031
France SC, Hoover LL (2001) Analysis of variation in mitochondrial DNA sequences (ND3, ND4L, MSH) among Octocorallia (=Alcyonaria) (Cnidaria: Anthozoa). Bull Biol Soc Wash 10:110–118
Grasshoff M (1999) The shallow water gorgonians of New Caledonia and adjacent islands (Coelenterata: Octocorallia). Senckenberg Biol 78:1–245
Gray JE (1870) Catalogue of the lithophytes or stony corals in the collection of the British Museum, London
Griffiths HJ, Barnes DKA, Linse K (2009) Towards a generalized biogeography of the Southern Ocean benthos. J Biogeogr 36:162–177. https://doi.org/10.1111/j.1365-2699.2008.01979.x
Hourigan TF, Etnoyer PJ, Cairns SD (2017) The state of deep-sea coral and sponge ecosystems of the United States
Kaiser S, Brandão SN, Brix S, Barnes DKA, Bowden DA, Ingels J, Leese F, Schiaparelli S, Arango CP, Badhe R, Bax N, Blazewicz-Paszkowycz M, Brandt A, Brenke N, Catarino AI, David B, De Ridder C, Dubois P, Ellingsen KE, Glover AG, Griffiths HJ, Gutt J, Halanych KM, Havermans C, Held C, Janussen D, Lörz AN, Pearce DA, Pierrat B, Riehl T, Rose A, Sands CJ, Soler-Membrives A, Schüller M, Strugnell JM, Vanreusel A, Veit-Köhler G, Wilson NG, Yasuhara M (2013) Patterns, processes and vulnerability of Southern Ocean benthos: a decadal leap in knowledge and understanding. Mar Biol 160:2295–2317. https://doi.org/10.1007/s00227-013-2232-6
Kinoshita K (1908) Gorgonacea no ikka Primnoidae ni tsuite. Dobutsugaku zasshi 20:517–528
Kükenthal W (1907) Gorgoniden der Deutschen Tiefsee–Expedition. Zool Anz 31:202–212
Kükenthal W (1908) Diagnosen neuer Gorgoniden (4. Mitteilung). Zool Anz 33:9–20
Kükenthal W (1912) Die Alcyonaria der Deutschen Südpolar, Expedition 1901–1903. Dtsch Südpolar Exped 1901–1903, Zool 5:289–349
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/msw054
Lamouroux JVF (1812) Extrait d’un mémoire sur la classification des polypiers coralligènes non entierement pierreux. Nouv Bull des Sci par la Société Philomatique Paris 3:181–188
Leray M, Knowlton N, Ho S-L, Nguyen BN, Machida RJ (2019) GenBank is a reliable resource for 21st century biodiversity research. Proc Natl Acad Sci U S A 116:22651–22656. https://doi.org/10.1073/pnas.1911714116
López-González PJ, Gili JM, Orejas C (2002) A new primnoid genus (Anthozoa: Octocorallia) from the Southern Ocean. Sci Mar 66:383–397. https://doi.org/10.3989/scimar.2002.66n4383
Matsuoka K, Skoglund A, Roth G (2018) Quantarctica [Dataset]. Nor Polar Inst. doi: https://doi.org/10.21334/npolar.2018.8516e961
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. https://doi.org/10.1111/j.1755-0998.2010.02875.x
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. https://doi.org/10.1080/14772000.2014.902866
McFadden CS, Sanchez JA, France SC (2010) Molecular phylogenetic insights into the evolution of Octocorallia: a review. Integr Comp Biol 50:389–410. https://doi.org/10.1093/icb/icq056
McFadden CS, van Ofwegen LP (2013) A second, cryptic species of the soft coral genus Incrustatus (Anthozoa: Octocorallia: Clavulariidae) from Tierra del Fuego, Argentina, revealed by DNA barcoding. Helgol Mar Res 67:137–147. https://doi.org/10.1007/s10152-012-0310-7
Milne-Edwards H (1857) Histoire naturelle des coralliaires ou polypes proprement dits (Vol. 2). Librairie Encyclopédique de Roret, Paris
Nutting CC (1908) Descriptions of the Alcyonaria collected by the U.S. Bureau of Fisheries steamer Albatross in the vicinity of the Hawaiian Islands in 1902. Proc USNatl Mus 34:543–601. https://doi.org/10.5479/si.00963801.34-1624.543
Padial JM, Miralles A, De la Riva I, Vences M (2010) The integrative future of taxonomy. Front Zool 7:16. https://doi.org/10.1186/1742-9994-7-16
Pante E, Schoelinck C, Puillandre N (2015) From integrative taxonomy to species description: one step beyond. Syst Biol 64:152–160. https://doi.org/10.1093/sysbio/syu083
Prada C, Schizas NV, Yoshioka PM (2008) Phenotypic plasticity or speciation? A case from a clonal marine organism. BMC Evol Biol 8:47. https://doi.org/10.1186/1471-2148-8-47
Rambaut A, Drummond A (2010) TreeAnnotator version 1.6.1
Rambaut A, Drummond AJ, Xie D, Baele G, Suchard MA (2018) Posterior summarization in Bayesian Phylogenetics using Tracer 1.7. Syst Biol 67:901–904. https://doi.org/10.1093/sysbio/syy032
Rogers AD (2007) Evolution and biodiversity of Antarctic organisms: a molecular perspective. Philos Trans R Soc B Biol Sci 362:2191–2214. https://doi.org/10.1098/rstb.2006.1948
Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574. https://doi.org/10.1093/bioinformatics/btg180
Roule L (1908) Alcyonaires. Exped Antarct Fr (1903–1905). Sci Nat Doc Sci 15:1–6
Soler-Hurtado MM, López-González PJ, Machordom A (2017) Molecular phylogenetic relationships reveal contrasting evolutionary patterns in Gorgoniidae (Octocorallia) in the Eastern Pacific. Mol Phylogenet Evol 111:219–230. https://doi.org/10.1016/j.ympev.2017.03.019
Starmans A, Gutt J, Arntz WE (1999) Mega-epibenthic communities in Arctic and Antarctic shelf areas. Mar Biol 135:269–280. https://doi.org/10.1007/s002270050624
Studer T (1878) Übersicht der Anthozoa Alcyonaria, welche während der Reise S.M.S Gazelle um die Erde gesammelt wurden. Monatsbericht der Königlic Preuss Akad der Wissenschaften zu Berlin 632–688
Taylor ML, Cairns SD, Agnew DJ, Rogers AD (2013) A revision of the genus Thouarella Gray, 1870 (Octocorallia: Primnoidae), including an illustrated dichotomous key, a new species description, and comments on Plumarella Gray, 1870 and Dasystenella, Versluys, 1906. Zootaxa 3602:1–105
Taylor ML, Rogers AD (2017) Primnoidae (Cnidaria: Octocorallia) of the SW Indian Ocean: new species, genus revisions and systematics. Zool J Linnean Soc 181:70–97. https://doi.org/10.1093/zoolinnean/zlx003
Taylor ML, Rogers AD (2015) Evolutionary dynamics of a common sub-Antarctic octocoral family. Mol Phylogenet Evol 84:185–204. https://doi.org/10.1016/j.ympev.2014.11.008
Thomson JA (1911) Zoological studies chiefly on alcyonarians (fifth and sixth series). Aberdeen Univ Stud 48:1–177. https://doi.org/10.5962/bhl.title.27083
Thomson JA, Richie J (1906) The Alcyonarians of the Scottish National Antarctic Expedition. Trans R Soc Edinburgh 41:851–860
Tu TH, Dai CF, Jeng MS (2015) Phylogeny and systematics of deep-sea precious corals (Anthozoa: Octocorallia: Coralliidae). Mol Phylogenet Evol 84:173. https://doi.org/10.1016/j.ympev.2014.09.031
Valenciennes A (1846) Atlas of zoophytes. In: Dupetit-Thouars (ed) Voyage autour du monde sur la frégate la Vénus, pendant les annees. Atlas de Zoologie Gide et Cie, Paris, pp 1836–1839
Vargas S, Guzman HM, Breedy O, Wörheide G (2014) Molecular phylogeny and DNA barcoding of tropical eastern Pacific shallow-water gorgonian octocorals. Mar Biol 161:1027–1038. https://doi.org/10.1007/s00227-014-2396-8
Versluys J (1906) Die Gorgoniden der Siboga-Expedition. Siboga-Expeditie 13a:1–187
Wright EP, Studer T (1889) Report on the Alcyonaria collected by H.M.S. challenger during the years 1873–1876. Rep Sci c results Voyag HMS Chall Dur years 1873–76, Zool 31:1–314
Zapata-Guardiola R, López-González PJ (2012) Revision and redescription of the species previously included in the genus Amphilaphis Studer and Wright in Studer, 1887 (Octocorallia: Primnoidae). Sci Mar 76:357–380. https://doi.org/10.3989/scimar.03278.18B
Zapata-Guardiola R, López-González PJ (2010a) Four new species of Thouarella (Anthozoa: Octocorallia: Primnoidae) from Antarctic waters. Sci Mar 74:131–146. https://doi.org/10.3989/scimar.2010.74n1131
Zapata-Guardiola R, López-González PJ (2010b) Two new species of Antarctic gorgonians (Octocorallia: Primnoidae) with a redescription of Thouarella laxa Versluys, 1906. Helgol Mar Res 64:169–180. https://doi.org/10.1007/s10152-009-0176-5
Acknowledgements
The authors wish to acknowledge the valuable assistance of the officers and crew of the RV Polarstern and many colleagues on board during the ANT XII/3 (1995), ANT XXIII/8 (2007), ANT XXIV/2 (2008), ANT XXVII-3 (2011), ANT-XXIX (2014) and ANT-XXXI/2 (2016) cruises. We extend our thanks to the cruise leaders and steering committee of the cruises especially Wolf E. Arntz and Julian Gutt (Alfred Wegener Institut, Bremerhaven), who kindly facilitated the work onboard, and for the opportunity to collaborate in these Antarctic programs. Special thanks to Josep Maria Gili, Rebeca Zapata-Guardiola, and Stefano Ambroso for helping in the collection of octocoral specimens during Polarstern cruises. We also acknowledge José Garrido for his help with the DNA extraction and amplification and Norwegian Polar Institute for making the Quantarctica package available. Finally, we thank the editor Bert W. Hoeksema and the two anonymous reviewers for their comments and suggestions that improved the final version of this manuscript.
Funding
This research is supported by the project CTM2017–83920-P (DIVERSICORAL), Spanish Ministry of Economy, Industry and Competitiveness. Different funds for the participation on these Polarstern cruises were provided by the Spanish CICYT projects—CLIMANT—POL2006–06399/CGL (ANT XXIII/8). M.N.F. acknowledges partial support from CONICYT-PCHA/Doctorado Nacional/2017–21,170,438, and Instituto Antártico Chileno (INACH) grant number DG_04_19. D.G.U. acknowledges partial support from Nucleo Milenio INVASAL funded through Chile’s Iniciativa Científica Milenio at Ministerio de Economía, Fomento & Turismo, Chile.
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Additional data, including primers used to amplify the regions of Cox1, mtMutS and 28S, GenBank accession numbers of the primnoids specimens used in the molecular analysis and additional phylogenetic results are in the Supplementary Files.
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M.N.F., P.L.G. and D.G.U. conceived and designed the study. M.N.F. performed scanning electron microscopy (SEM) and conducted morphological examinations and phylogenetic analysis. M.N.F. wrote the first draft of the manuscript that was improved in subsequent revisions by P.L.G and D.G.U. All authors gave final approval for publication.
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Núñez-Flores, M., Gomez-Uchida, D. & López-González, P.J. Molecular and morphological data reveal three new species of Thouarella Gray, 1870 (Anthozoa: Octocorallia: Primnoidae) from the Southern Ocean. Mar. Biodivers. 50, 30 (2020). https://doi.org/10.1007/s12526-020-01053-z
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DOI: https://doi.org/10.1007/s12526-020-01053-z