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An integrated morpho-molecular approach to delineate species boundaries of Millepora from the Red Sea

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Abstract

Fire corals of the hydrocoral genus Millepora provide an important ecological role as framework builders of coral reefs in the Indo-Pacific and the Atlantic. Recent works have demonstrated the incongruence between molecular data and the traditional taxonomy of Millepora spp. based on overall skeleton growth form and pores. In an attempt to establish a reliable and standardized approach for defining species boundaries in Millepora, we focused on those from the Red Sea. In this region, three species are currently recognized: the fan-shaped branching M. dichotoma, the blade-like M. platyphylla, and the massive/encrusting M. exaesa. A total of 412 colonies were collected from six localities. Two mitochondrial marker genes (COI and 16S rDNA) were sequenced to obtain phylogeny reconstructions and haplotype networks. Eight morphological traits of pores and the nematocysts of both polyp and eumedusoid stages were measured to determine whether significant morphological differences occur among the three species. Both markers clearly resolved M. dichotoma, M. platyphylla, and M. exaesa as distinct, monophyletic lineages in the Red Sea. Nevertheless, they also revealed deep genetic breaks with Southwestern Indian Ocean populations of the three species. In the Red Sea, the three species were further distinguished based on their pore and nematocyst features. A discriminant analysis revealed dactylopore density, number of dactylopores per gastropore, dactylopore distance, and gastropore diameter as the most informative discriminative characters. The heteronemes, the large and small stenoteles of polyps, and the distribution of mastigophores of eumedusoids also showed significant interspecific differences. An integrated morpho-molecular approach proved to be decisive in defining species boundaries of Millepora supported by a combination of pore and nematocyst characters, which may be phylogenetically informative.

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Acknowledgements

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 Amr 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. This project was supported by funding from KAUST (award #FCC/1/1973-21 and baseline research funds to MLB). TS would like to acknowledge Yossi Loya and the Israeli Taxonomy Initiative for funding his work. We are deeply grateful to the editor and three anonymous referees for their comments which greatly improved the manuscript.

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Authors and Affiliations

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

    Roberto Arrigoni, Tullia Isotta Terraneo, Matthew D. Tietbohl & Michael L. Berumen

  2. Dipartimento di Scienze dell’Ambiente e del Territorio (DISAT), Università degli Studi di Milano-Bicocca, Piazza della Scienza 1, 20126, Milan, Italy

    Davide Maggioni, Simone Montano & Davide Seveso

  3. Marine Research and High Education (MaRHE) Center, Faafu Magoodhoo, 12030, Maldives

    Davide Maggioni, Simone Montano & Davide Seveso

  4. Taxonomy and Systematics Group, Naturalis Biodiversity Center, P.O. Box 9517, 2300 RA, Leiden, The Netherlands

    Bert W. Hoeksema

  5. School of Zoology, The George S. Wise Faculty of Life Sciences, Tel-Aviv University, 69978, Tel-Aviv, Israel

    Tom Shlesinger

  6. College of Marine and Environmental Science, James Cook University, Townsville, QLD, 4811, Australia

    Tullia Isotta Terraneo

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  1. Roberto Arrigoni
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Fig. S1 a

COI and b 16S rDNA phylogeny reconstructions of Millepora inferred by Bayesian inference. The two trees are identical to the ones presented in Fig. 4 but the graphics are different: Each single tip represents a single sequence. The clade support values are Bayesian posterior probabilities (≥ 0.7) and maximum likelihood bootstrap replicates (≥ 70). Colors denote each distinct molecular lineage as reported in the figure box (PDF 73 kb)

Table S1

List of Millepora samples collected from the Red Sea for this study, including voucher number, depth, site, latitude, longitude, GenBank accession numbers of the two mitochondrial genes (COI and 16S rDNA) (XLSX 240 kb)

Table S2

Measurements of pore characters analyzed in this study for the three Red Sea Millepora species (XLSX 69 kb)

Table S3

Measurements of nematocyst characters of both polyp and medusa stages analyzed in this study for the three Red Sea Millepora species (XLSX 57 kb)

Table S4

Wilks’ lambda test for verifying differences among Millepora species with pore character measurements using the DFA (DOCX 12 kb)

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Arrigoni, R., Maggioni, D., Montano, S. et al. An integrated morpho-molecular approach to delineate species boundaries of Millepora from the Red Sea. Coral Reefs 37, 967–984 (2018). https://doi.org/10.1007/s00338-018-01739-8

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