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Towards a rigorous species delimitation framework for scleractinian corals based on RAD sequencing: the case study of Leptastrea from the Indo-Pacific

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Abstract

Accurate delimitation of species and their relationships is a fundamental issue in evolutionary biology and taxonomy and provides essential implications for conservation management. Scleractinian corals are difficult to identify because of their ecophenotypic and geographic variation and their morphological plasticity. Furthermore, phylogenies based on traditional loci are often unresolved at the species level because of uninformative loci. Here, we attempted to resolve these issues and proposed a consistent species definition method for corals by applying the genome-wide technique Restriction-site Associated DNA sequencing (RADseq) to investigate phylogenetic relationships and species delimitation within the genus Leptastrea. We collected 77 colonies from nine localities of the Indo-Pacific and subjected them to genomic analyses. Based on de novo clustering, we obtained 44,162 SNPs (3701 loci) from the holobiont dataset and 62,728 SNPs (9573 loci) from the reads that map to coral transcriptome to reconstruct a robust phylogenetic hypothesis of the genus. Moreover, nearly complete mitochondrial genomes and ribosomal DNA arrays were retrieved by reference mapping. We combined concatenation-based phylogenetic analyses with coalescent-based species tree and species delimitation methods. Phylogenies suggest the presence of six distinct species, three corresponding to known taxa, namely Leptastrea bottae, Leptastrea inaequalis, Leptastrea transversa, one characterized by a remarkable skeletal variability encompassing the typical morphologies of Leptastrea purpurea and Leptastrea pruinosa, and two distinct and currently undescribed species. Therefore, based on the combination of genomic, morphological, morphometric, and distributional data, we herein described Leptastrea gibbosa sp. n. from the Pacific Ocean and Leptastrea magaloni sp. n. from the southwestern Indian Ocean and formally considered L. pruinosa as a junior synonym of L. purpurea. Notably, mitogenomes and rDNA yielded a concordant yet less resolved phylogeny reconstruction compared to the ones based on SNPs. This aspect demonstrates the strength and utility of RADseq technology for disentangling species boundaries in closely related species and in a challenging group such as scleractinian corals.

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Acknowledgements

This project was supported by funding from KAUST (award # FCC/1/1973-21 and baseline research funds to MLB). This research was undertaken in accordance with the policies and procedures of 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 A Gusti (KAUST), the captain and crew of the MV Dream-Master, and the KAUST Coastal and Marine Resources Core Laboratory for fieldwork logistics in the Red Sea. In Yemen, fieldwork organization, logistics, and sampling permits from the relevant authorities were possible thanks to the collaboration of E Dutrieux (Creocean), CH Chaineau (Total SA), R Hirst, and M Abdul Aziz (YLNG). We are grateful to E Karsenti (EMBL) and E Bougois (Tara Expeditions), the OCEANS Consortium for allowing sampling during the Tara Oceans expedition in Djibouti, the Gambier Archipelago, French Polynesia, and Mayotte. We thank the commitment of the following people and additional sponsors who made this singular expedition possible: CNRS, EMBL, Genoscope/CEA, VIB, Stazione Zoologica Anton Dohrn, UNIMIB, ANR (projects POSEIDON/ANR-09-BLAN-0348, BIOMARKS/ANR-08-BDVA-003, PROMETHEUS/ANR-09-GENM-031, and TARA-GIRUS/ANR-09-PCS-GENM-218), EU FP7 (MicroB3/No.287589), FWO, BIO5, Biosphere 2, agnès b., the Veolia Environment Foundation, Region Bretagne, World Courier, Illumina, Cap L’Orient, the EDF Foundation EDF Diversiterre, FRB, the Prince Albert II de Monaco Foundation, Etienne Bourgois, the Tara schooner, and its captain and crew. Tara Oceans would not exist without continuous support from 23 institutes (https://oceans.taraexpeditions.org). This article is contribution number 103 of the Tara Oceans Expedition 2009–2012. New Caledonia data and specimens were obtained during the IRD CORALCAL1 (https://dx.doi.org/10.17600/7100020), CORALCAL2 (https://dx.doi.org/10.17600/8100050), CORALCAL3 (https://dx.doi.org/10.17600/9100010), CORALCAL4 (https://dx.doi.org/10.17600/12100060), BIBELOT (https://dx.doi.org/10.17600/14003700), and CORALCAL5 (https://dx.doi.org/10.17600/15004300) expeditions on the RV Alis. We are grateful to the chief scientists and cruise organizers C Payri (IRD), C Fauvelot (IRD) for invitation and financial support to join and valuable help with sampling authorizations. Material from Madagascar was collected during the MAD (https://dx.doi.org/10.17600/16004700) expedition on the RV Antea organized by H Magalon (ULR). The MADANG expedition specimens were obtained during the "Our Planet Reviewed" Papua Niugini expedition (https://dx.doi.org/10.17600/12100070) organized by Muséum National d'Histoire Naturelle (MNHN), Pro Natura International (PNI), Institut de Recherche pour le Développement (IRD), and University of Papua New Guinea (UPNG), Principal Investigators P Bouchet, C Payri, and S Samadi. The organizers acknowledge funding from the Total Foundation, Prince Albert II of Monaco Foundation, Fondation EDF, Stavros Niarchos Foundation, and Entrepose Contracting, and in-kind support from the Divine Word University (DWU). Material from Kavieng, PNG, was sampled during the KAVIENG Expedition (https://doi.org/10.17600/14004400). The expedition operated under a permit delivered by the Papua New Guinea Department of Environment and Conservation. Material from the Coral Sea, Australia, was sampled in under Permit No. AU-COM2018-437. The authors wish to thank A.H. Baird (JCU), M. Pratchett (JCU), and Hugo Harrison (JCU), and the relevant staff at Parks Australia, for material collected in the Coral Sea. We are grateful to A. Andouche (MNHN), M. Castellin (MNHN), P. Lozouet (MNHN), C. Lüter (ZMB), T. Bridge (MTQ), P. Muir (MTQ), M. Lowe (NHM), and A. Cabrinovic (NHM) for allowing the study of the museum reference collections. The views expressed are purely those of the writers and may not in any circumstance be regarded as stating an official position of the European Commission, nor of Parks Australia, the Director of National Parks or the Australian Government. We are grateful to Z.H. Forsman (UH Manoa) and one anonymous reviewer for their useful corrections and suggestions.

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Authors and Affiliations

  1. Department of Biology and Evolution of Marine Organisms (BEOM), Stazione Zoologica Anton Dohrn Napoli, Villa Comunale, 80121, Naples, Italy

    Roberto Arrigoni

  2. Red Sea Research Center, Division of Biological and Environmental Science and Engineering, King Abdullah University of Science and Technology, Thuwal, 23955-6900, Saudi Arabia

    Roberto Arrigoni, Michael L. Berumen, Kiruthiga G. Mariappan, Ann Marie Hulver, Tullia Isotta Terraneo & Francesca Benzoni

  3. European Commission, Joint Research Centre (JRC), Ispra, Italy

    Roberto Arrigoni & Pieter S. A. Beck

  4. Dipartimento Di Scienze Dell’Ambiente E del Territorio, Università Degli Studi Di Milano-Bicocca, Piazza della Scienza 1, 20126, Milan, Italy

    Simone Montano

  5. Marine Research and High Education Center, Magoodhoo Island, Faafu Atoll, Maldives

    Simone Montano

  6. Queensland Museum, Biodiversity and Geosciences, Townsville, QLD, 4810, Australia

    Michel Pichon

  7. Research Centre for Ecological Change, University of Finland, 00014, Helsinki, Finland

    Giovanni Strona

  8. ARC Centre of Excellence for Coral Reef Studies, James Cook University, Townsville, QLD, 4810, Australia

    Tullia Isotta Terraneo

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  1. Roberto Arrigoni
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  2. Michael L. Berumen
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  3. Kiruthiga G. Mariappan
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  9. Tullia Isotta Terraneo
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  10. Francesca Benzoni
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Data S1

List of coral samples analyzed in this study with collection information and the sequencing and bioinformatics statistics summary. In particular, the collection information includes voucher numbers, museum/institute where the specimen is deposited, species identification, molecular clade based on SNPs phylogenies, and collection locality. The sequencing and bioinformatics statistics summary includes the total number of raw reads, the total number of reads after trimming and relative percentage, the percentage of trimmed reads mapped to reference sequences (coral transcriptome, coral mitochondrial genome, and coral nuclear ribosomal DNA), average deviation, standard deviation, and the percentage of reference sequence covered. Abbreviations: IRD = Institute de Recherche pour le Développement (Noumea, New Caledonia); KAUST = King Abdullah University of Science and Technology (Thuwal, Saudi Arabia); MNHN = Muséum National d’Histoire Naturelle (Paris, France); UNIMIB = University of Milano-Bicocca (Milan, Italy); refseq_percentage = percentage of reference sequence covered. (XLSX 23 kb)

Data S2

List of the Leptastrea specimens examined for the species treated in this study including museum and collected material in addition to those listed in the Taxonomic Account. Species synonymies and additional taxonomic references cited in the synonymies, but not in the main text, are provided. (DOCX 33 kb)

Data S3

Alignment of nearly complete mitochondrial genomes, including 10,837 bp. (TXT 826 kb)

Data S4

Alignment of nearly complete nuclear ribosomal DNA regions, including 5835 bp. (TXT 445 kb)

Data S5

Average (st. dev.) values of the six Leptastrea skeleton variables measured in this study: v1, maximum calice diameter; v2, minimum calice diameter; v3, maximum columella diameter; v4, minimum columella diameter perpendicular to v3; v5, distance between the centre of the columella and the centre of the columella of the closest adjacent corallite; v6, width of the groove among the corallites. The number of coralla examined per species is given in brackets below the species name. (DOCX 13 kb)

Figure S1

In situ images of colonies of the Leptastrea species analyzed in this study: S1_1 L. purpurea (a) UNIMIB MY143, Mayotte Island; (b) IRD HS3790, Isle of Pines, New Caledonia; (c) KAUST SA0056, Saudi Arabia; (d) KAUST SA0014, Al Lith, Saudi Arabia; (e) UNIMIB PFB776, Kavieng, Papua New Guinea; (f) lagoon pinnacle north of Magareva Island, Gambier Archipelago, French Polynesia (F. Benzoni, 05/07/2011); (g) Aqaba, Jordan (R. Joury, 17/07/2018); S1_2 L. transversa (a) UNIMIB PFB369, Madang, Papua New Guinea; (b) Nakety Bay, Grande Terre, New Caledonia (F. Benzoni, 22/04/2012); (c) KAUST SA0045, Farasan Banks, Saudi Arabia; (d) IRD HS3652, Isle of Pines, New Caledonia; (e) IRD HS3299, Grande Terre, New Caledonia; (f) KAUST SA1027, Magna, Saudi Arabia; (g) Aqaba, Jordan (R. Joury, 17/07/2018); S1_3 L. bottae (a) KAUST SA0736 Ras Al-Ubayd, Saudi Arabia; (b) KAUST SA0011, Al Lith, Saudi Arabia; (c) Aqaba, Jordan (F. Benzoni, 09/07/2018); (d) KAUST SA0044, Farasan Banks, Saudi Arabia; (e) UNIMIB DJ070, Oblal, Djibouti; (f) KAUST SA0011, Al Lith, Saudi Arabia; (g) Aqaba, Jordan (R. Joury, 16/07/2018); S1_4 L. inaequalis (a) UNIMIB BA079, Bir Ali, Yemen; (b) UNIMIB DJ047, Oblal, Djibouti; (c) Aqaba, Jordan (F. Benzoni, 15/07/2018); (d) KAUST SA0043, Farasan Banks, Saudi Arabia; (e) KAUST SA0042, Farasan Banks, Saudi Arabia; (f) Socotra Island, Yemen (F. Benzoni, 18/03/2010); (g) Aqaba, Jordan (R. Joury, 16/07/2018); S1_5 Leptastrea gibbosa sp. n. (a) Lifou Island, Loyalty Islands, New Caledonia (F. Benzoni, 18/02/2014); (b) outer reef south of the Grande Terre, New Caledonia (F. Benzoni, 08/11/2017); (c) IRD HS3167, Moneo, Grande Terre, New Caledonia; (d) UNIMIB PFB805, Kavieng, Papua New Guinea; (e) IRD HS3740, Isle of Pines, New Caledonia; (f) IRD HS3653, Isle of Pines, New Caledonia; (g) Mellish Reef, Australia (F. Benzoni, 02/12/2018); S1_6 Leptastrea magaloni sp. n. (a) IRD MD266, Nosy Sakatia, Madagascar; (b) IRD MD260, Nosy Be, Madagascar; (c) IRD MD222, Nosy Lava, Madagascar; (d) MNHN-IK-2012-9823, Bouzi, Mayotte Island; (e) IRD MD225, Nosy Lava, Madagascar; (f) IRD MD183, Nosy Mitsio, Madagascar; (g) IRD MD274, Nosy Sakatia, Madagascar; (h) same colony as in g with retracted tentacles. All in situ specimen images by F. Benzoni. For specimens, site and date metadata can be found in Data S1. (PDF 6043 kb)

Figure S2

Maximum Likelihood (ML) phylogenetic tree of Leptastrea estimated with RAxML v8.2.10 using (a) the concatenated “holobiont-min” supermatrix (2075 loci including a total of 2141 SNPs); (b) the concatenated “coral-min” supermatrix (2366 loci including a total of 2479 SNPs). Branch support is based on ML bootstrap analyses. (PDF 992 kb)

Figure S3

Maximum Likelihood (ML) phylogenetic tree of Leptastrea estimated with RAxML v8.2.10 using (a) the barcoding portion of the cytochrome oxidase subunit I gene of the mitochondrial genome (COI); (b) the complete ITS1, 5.8S, and ITS2 regions of the nuclear ribosomal DNA (ITS). Branch support is based on ML bootstrap analyses. (PDF 906 kb)

Figure S4

Variability of skeleton morphology across specimens of the Leptastrea species examined in this study included in the genomic and morphometric analyses: L. purpurea (a–h), L. transversa (i–l), L. gibbosa sp. n. (m–p), L. inaequalis (q–t), L. bottae (u–x), L. magaloni sp. n. (y-ab). (a) UNIMIB BA081; (b) UNIMIB MY247; (c) UNIMIB MY245; (d) IRD HS3045; (e) UNIMIB PFB776; (f) UNIMIB GA097; (g) UNIMIB GA170; (h) UNIMIB GA076; (i) UNIMIB DJ297; (j) UNIMIB MY202; (k) UNIMIB PFB252; (l) IRD HS3247; (m) UNIMIB PFB805; (n) IRD HS3740; (o) and (p) IRD HS2344; (q) UNIMIB DJ292; (r) UNIMIB BA044; (s) UNIMIB BA079; (t) UNIMIB DJ047; (u) UNIMIB AD040; (v) UNIMIB DJ070; (w) UNIMIB BAL144; (x) UNIMIB DJ335; (y) UNIMIB MY333; (z) IRD MD260; (aa) IRD MD183; (ab) IRD MD222. All images were taken at the same magnification (scale bar shown in a). Colour code same as in Figures 4, 5, 6 and 7. Collection metadata for L. magaloni sp. n. and L. gibbosa sp. n. specimens are in the Taxonomic Account, for all the other species in Data S1. (JPEG 411 kb)

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Arrigoni, R., Berumen, M.L., Mariappan, K.G. et al. Towards a rigorous species delimitation framework for scleractinian corals based on RAD sequencing: the case study of Leptastrea from the Indo-Pacific. Coral Reefs 39, 1001–1025 (2020). https://doi.org/10.1007/s00338-020-01924-8

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