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Phylogeny of Cidaroida (Echinodermata: Echinoidea) based on mitochondrial and nuclear markers

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Abstract

We present the first molecular phylogeny of Cidaroida, one of the most problematic groups within the echinoids. Two genes—the nuclear ribosomal gene 28 S rRNA and the mitochondrial protein-encoding gene COI—were obtained from 21 specimens representing 17 genera and 20 species, among which 13 species belong to Cidaroida. Phylogenetic analyses of the combined molecular data using parsimony and maximum likelihood optimality criteria resulted in a well-resolved phylogeny. Our results are broadly compatible (with the notable exception of Cidaris cidaris) with previous results obtained from morphological data. We find that Cidaroida represent a monophyletic group sister to the non-cidaroid Echinoidea. The family Cidaridae sensu Mortensen (1928) and Fell (1966) is paraphyletic because of the placement of Psychocidaris ohshimai as sister-group to Histocidaris elegans. Inside the Stylocidarina, we show that the two Atlantic species Stylocidaris affinis and Stylocidaris lineata constitute a well-supported clade. However, these two taxa could also represent two morphotypes within a single species showing high morphological variation.

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References

  • Agassiz, A. (1879). Preliminary report of the Echini of the exploring expedition of H.M.S. Challenger. Proceedings of the American Academy of Arts and Sciences, 14, 190–212.

    Article  Google Scholar 

  • Altschul, S. F., Madden, T. L., Schaffer, A. A., Zhang, J., Zhang, Z., Miller, W., & Lipman, D. J. (1997). Gapped Blast and Psi-Blast: a new generation of protein database search programs. Nucleic Acids Research, 25, 3389–3402.

    Article  PubMed  CAS  Google Scholar 

  • Baroin, A., Perasso, R., Qu, L. H., Brugerolle, G., Bachellerie, J. P., & Adoute, A. (1988). Partial phylogeny of the unicellular eukaryotes based on rapid sequencing of a portion of 28 S ribosomal RNA. Proceedings of the National Academy of Sciences USA, 85, 3474–3478.

    Article  CAS  Google Scholar 

  • Bell, F. J. (1892). Description of a remarkable new sea urchin of the genus Cidaris from Mauritius. Transactions of the Zoological Society of London, 13, 303–304.

    Article  Google Scholar 

  • Bonhomme, M.G., (2002). Apport des données moléculaires dans la phylogénie des Cidaridae (Echinodermata, Echinoidea, Cidaroida). Master’s thesis, Muséum national d’Histoire naturelle.

  • Brosseau, O., (2005). Phylogénie moléculaire et analyse morphométrique des pédicellaires et du test des Cidaroida (Echinodermata, Echinoidea). Ph.D. thesis, Muséum national d’Histoire naturelle.

  • Cantatore, P., Ritrebo, M., Ridlania, M., Gagaleta, N., & Saccone, C. (1989). The complete nucleotide sequence, the gene organization and the genetic code of the mitochondrial genome of Paracentrotus lividus. Journal of Biological Chemistry, 264, 10965–10975.

    PubMed  CAS  Google Scholar 

  • Castresana, J. (2000). Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Molecular Biology and Evolution, 17, 540–552.

    Article  PubMed  CAS  Google Scholar 

  • Clark, A. H. (1907). Descriptions of new species of recent unstalked crinoids from the North Pacific Ocean. Proceedings of the US National Museum, 33, 69–84.

    Article  Google Scholar 

  • Clark, H. L. (1918). Report on the Cidaroidea and Echinoidea collected by the Bahama Expedition from the University of Iowa in 1893. Bulletin of the Laboratory of Natural History State University Iowa, 7, 1–37.

    Google Scholar 

  • De Giorgi, C., Martiradonna, A., Lanave, C., & Saccone, C. (1996). Complete sequence of the mitochondrial DNA in the sea urchin Arbacia lixula: conserved features of the echinoid mitochondrial genome. Molecular Phylogenetics and Evolution, 5, 323–332.

    Article  PubMed  Google Scholar 

  • De Meijere, J. C. H. (1904). Die Echinoidea der Siboga-Expedition. Mitteilung der Siboga Expedition, 43, 1–251.

    Google Scholar 

  • Dörderlein, L. (1901). Diagnosen einiger von der Valdivia–Expedition gesammelten Seeigel-Arten aus dem Indischen Ocean. Zoologische Anzeiger, 23, 19–23.

    Google Scholar 

  • Düben, M.W.V., Koren, J., (1844). Om Holothuriernas Hudskelet. Kongl. Svenska Vetenskapsakademiens Handlingar 211–228.

  • Durham, J. W., & Melville, R. V. (1957). A classification of echinoids. Journal of Paleontology, 31, 242–272.

    Google Scholar 

  • Fell, J.P., (1966). Cidaroids. In: Treatise on invertebrate paleontology. Part U. Echinodermata 3. University of Kansas, Lawrence, pp. U312–U339.

  • Felsenstein, J. (1985). Confidence limits on phylogenies: an approach using the bootstrap. Evolution, 39, 783–791.

    Article  Google Scholar 

  • Féral, J. P., & Derelle, E. (1991). Partial sequence of the 28 S ribosomal RNA and the echinid taxonomy and phylogeny—application to the Antarctic brooding schizasterids. In T. Yanagisawa (Ed.), Biology of Echinodermata: proceedings of the seventh international echinoderm conference, Atami, 9–14 September 1990 (pp. 331–337). Rotterdam: Balkema.

    Google Scholar 

  • Féral, J. P., Derelle, E., & Philippe, H. (1994). Inferred phylogenetic trees of antarctic brood-protecting schizasterid echinoids from partial 28 S ribosomal RNA sequences. In A. R. Beaumont (Ed.), Genetics and evolution of aquatic organisms (pp. 199–206). London: Chapman and Hall.

    Google Scholar 

  • Folmer, O., Black, M., Hoeh, W., Lutz, R., & Vrijenhoek, R. C. (1994). DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology, 3, 294–299.

    PubMed  CAS  Google Scholar 

  • Goloboff, P. A., Farris, J. S., & Nixon, K. (2008). TNT, a free program for phylogenetic analysis. Cladistics, 24, 774–786.

    Article  Google Scholar 

  • Guindon, S., Dufayard, J. F., Lefort, V., Anisimova, M., Hordijk, W., & Gascuel, O. (2010). New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology, 59, 307–321.

    Article  PubMed  CAS  Google Scholar 

  • Guindon, S., & Gascuel, O. (2003). A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology, 52, 696–704.

    Article  PubMed  Google Scholar 

  • Hall, T. A. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series, 41, 95–98.

    CAS  Google Scholar 

  • Hart, M. W., Abt, C. H. J., & Emlet, R. B. (2011). Molecular phylogeny of echinometrid sea urchins: more species of Heliocidaris with derived modes of reproduction. Invertebrate Biology, 130, 175–185.

    Article  Google Scholar 

  • Hoggett, A. K., & Rowe, F. W. E. (1986). South-west Pacific cidarid echinoids (Echinodermata) including two new species. Indo-Malayan Zoology, 3, 1–13.

    Google Scholar 

  • Ikeda, H. (1935). Preliminary report on a new cidarid sea-urchin from the Western Pacific. Proceedings of the Imperial Academy of Japan, 11, 386–388.

    Google Scholar 

  • Ikeda, H. (1936). Preliminary note on the new family of the Cidaroidea. Annotationes Zoologicae Japonenses, 15, 486–493.

    Google Scholar 

  • Janies, D. A., Voight, J. R., & Daly, M. (2011). Echinoderm phylogeny including Xyloplax, a progenetic asteroid. Systematic Biology, 60, 420–438.

    Article  PubMed  Google Scholar 

  • Jeffery, C. H., Emlet, R. B., & Littlewood, D. T. (2003). Phylogeny and evolution of development in temnopleurid echinoids. Molecular Phylogenetics and Evolution, 28, 99–118.

    Article  PubMed  CAS  Google Scholar 

  • Katoh, K., Katoh, K., Kuma, Ki, Toh, H., & Miyata, T. (2005). MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Research, 33, 511–518.

    Article  PubMed  CAS  Google Scholar 

  • Katoh, K., Misawa, K., Kuma, Ki, & Miyata, T. (2002). MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Research, 30, 3059–3066.

    Article  PubMed  CAS  Google Scholar 

  • Katoh, K., & Toh, H. (2008). Recent developments in the MAFFT multiple sequence alignment program. Briefings in Bioinformatics, 9, 286–298.

    Article  PubMed  CAS  Google Scholar 

  • Knott, K. E., & Wray, G. A. (2000). Controversy and consensus in asteroid systematics: new insights to ordinal and familial relationships. American Zoologist, 40, 382–392.

    Article  CAS  Google Scholar 

  • Kroh, A., Mooi, R., (2011). World Echinoidea Database. Available online at http://www.marinespecies.org/echinoidea. Accessed 20 January 2012.

  • Kroh, A., & Smith, A. B. (2010). The phylogeny and classification of post-Palaeozoic echinoids. Journal of Systematic Palaeontology, 8, 147–212.

    Article  Google Scholar 

  • Lamarck, J.B., (1816). Histoire naturelle des animaux sans vertèbres, vol 2. Verdière, Paris.

  • Lee, Y. H. (2003). Molecular phylogenies and divergence times of sea urchin species of Strongylocentrotidae, Echinoida. Molecular Biology and Evolution, 20, 1211–1221.

    Article  PubMed  CAS  Google Scholar 

  • Lessios, H. A., Kessing, B. D., & Pearse, J. S. (2001). Population structure and speciation in tropical seas: global phylogeography of the sea urchin Diadema. Evolution, 55, 955–975.

    Article  PubMed  CAS  Google Scholar 

  • Lessios, H. A., Kessing, B. D., Robertson, D. R., & Paulay, G. (1999). Phylogeography of the pantropical sea urchin Eucidaris in relation to land barriers and ocean currents. Evolution, 53, 806–817.

    Article  Google Scholar 

  • Linnaeus, C. (1758). Systema naturae per regna tria naturae, secundum classes, ordines, genera, species cum characteribus, differentiis, synonymis, locis. Editio Decima, Reformata. Stockholm: Laurentius Salvius.

    Google Scholar 

  • Linnaeus, C. (1767). Systema naturae. Editio Duodecima Reformata, Tomus I, Pars II. Stockholm: Laurentius Salvius.

    Google Scholar 

  • Littlewood, D. T. J., & Smith, A. B. (1995). A combined morphological and molecular phylogeny for sea urchins (Echinoidea: Echinodermata). Philosophical Transactions of the Royal Society, London, Series B, 347, 213–234.

    Article  CAS  Google Scholar 

  • Marshall, C. R., & Swift, H. (1992). DNA–DNA hybridization phylogeny of sand dollars and highly reproducible extent of hybridation values. Journal of Molecular Evolution, 34, 31–44.

    Article  PubMed  CAS  Google Scholar 

  • Matsuoka, N. (1993). Review molecular approaches to the systematics of echinoderms. Reports of Fukushima Marine Biology Laboratory, 14, 5–16.

    Google Scholar 

  • Matsuoka, N., & Inamori, M. (1999). Phylogenetic relationships among four echinoids of the family Cidaridae (Cidaroida) based on allozymes. Zoological Science, 16, 529–534.

    Article  Google Scholar 

  • Mortensen, T. (1903). The Danish Ingolf Expedition, IV (1). Echinoidea. Copenhagen: H. Hagerup.

    Google Scholar 

  • Mortensen, T., (1910). The Echinoidea of the Swedish South polar expedition. In: Wissenschaftliche Ergebnisse der Schwedischen Südpolar Expedition. Vol. 6. Stockholm, Sweden, pp. 1–114.

  • Mortensen, T. (1927). Report on the Echinoidea collected by the United States Fisheries Steamer “Albatross” during the Philippine expedition, 1907–1910, Part I: The Cidaridae. United States National Museums Bulletin, 6, 241–312.

    Google Scholar 

  • Mortensen, T. (1928). A Monograph of the Echinoidea. I, Cidaroidea. Copenhagen: Reitzel.

    Google Scholar 

  • Mortensen, T. (1932). New contributions to the knowledge of the cidarids. Kongeliga Danske Videnskabernes Selskabs Skrifter, 4, 146–152.

    Google Scholar 

  • Mortensen, T. (1939). Report on the Echinoidea of the Murray expedition, I. Scientific Reports on the John Murray Expedition, 6, 1–28.

    Google Scholar 

  • Mortensen, T. (1951). A monograph of the Echinoidea. V. 2. Spatangoida. II. Amphisternata. II. Spatangidæ, Loveniidæ, Pericosmidæ, Schizasteridæ, Brissidæ. Copenhagen: Reitzel.

    Google Scholar 

  • Paradis, E., Claude, J., & Strimmer, K. (2004). APE: analyses of phylogenetics and evolution in R language. Bioinformatics, 20, 289–290.

    Article  PubMed  CAS  Google Scholar 

  • Phelan, T. (1970). A field guide to the cidaroid echinoids of the Northwestern Atlantic Ocean, Gulf of Mexico, and the Caribbean Sea. Smithsonian Contributions to Zoology, 40, 1–67.

    Article  Google Scholar 

  • Philip, G. M. (1964). The Tertiary echinoids of southeastern Australia. II, Cidaridae (2). Proceedings of the Royal Society of Victoria, 77, 433–477.

    Google Scholar 

  • Philippi, R.A., (1845). Verzeichniss der in der Gegend von Magdeburg bei Osterweddingen und Westeregeln vorkommenden Tertiär-Versteinerungen. Jahrbuch für Mineralogie, Geognosie, Geologie und Petrefakten-Kunde, 447–451.

  • Pisani, D., Feuda, R., Peterson, K. J., & Smith, A. B. (2012). Resolving phylogenetic signal from noise when divergence is rapid: a new look at the old problem of echinoderm class relationships. Molecular Phylogenetics and Evolution, 62, 27–34.

    Article  PubMed  Google Scholar 

  • Ratto, A., & Christen, R. (1990). Phylogénie moléculaire des échinodermes déduite des séquences partielles des ARN ribosomiques. Comptes Rendus de l'Académie des Sciences Series III–Sciences de la Vie, 310, 169–174.

    CAS  Google Scholar 

  • Schliep, K. P. (2010). Phangorn: phylogenetic analysis in R. Bioinformatics, 27, 592–593.

    Article  PubMed  Google Scholar 

  • Scouras, A., & Smith, M. J. (2001). A novel mitochondrial gene order in the crinoid echinoderm Florometra serratissima. Molecular Biology and Evolution, 18, 61–73.

    Article  PubMed  CAS  Google Scholar 

  • Shimodaira, H., & Hasegawa, M. (1999). Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Molecular Biology and Evolution, 16, 1114–1116.

    Article  CAS  Google Scholar 

  • Smith, A.B., (2005). The echinoid directory. World Wide Web electronic publication. http://www.nhm.ac.uk/research-curation/projects/echinoid-directory/index [last accessed January 2012].

  • Smith, A. B., Lafay, B., & Christen, R. (1992). Comparative variation of morphological and molecular evolution through geologic time: 28 S rRNA versus morphology in echinoids. Philosophical Transactions of the Royal Society B, 338, 365–382.

    Article  CAS  Google Scholar 

  • Smith, A. B., Pisani, D., Mackensis-Dodds, J. A. B. S., Webster, B. L., & Littlewood, D. T. J. (2006). Testing the molecular clock: molecular and paleontological estimates of divergence times in the Echinoidea (Echinodermata). Molecular Biology and Evolution, 23, 1832–1851.

    Article  PubMed  CAS  Google Scholar 

  • Smith, A. B., & Wright, C. W. (1989). British cretaceaous echinoids. Part 1. General introduction and Cidaroida. Palaeontographical Society Monographs, 141, 1–101.

    Google Scholar 

  • Smith, M. J., Arndt, A., Gorski, S., & Fajber, E. (1993). The phylogeny of echinoderm classes based on mitochondrial gene arrangements. Journal of Molecular Evolution, 36, 545–554.

    Article  PubMed  CAS  Google Scholar 

  • Stockley, B., Smith, A. B., Littlewood, T., Lessios, H. A., & Mackensis-Dodds, J. A. (2005). Phylogenetic relationships of spatangoid sea urchins (Echinoidea): taxon sampling density and congruence between morphological and molecular estimates. Zoologica Scripta, 34, 447–468.

    Article  Google Scholar 

  • Suzuki, N., & Yoshino, K. (1992). The relationship between amino acid sequences of sperm activating peptides and the taxonomy of echinoids. Comparative Biochemistry and Physiology. Part B, Biochemistry & Molecular Biology, 102B, 690.

    Google Scholar 

  • Suzuki, N., Yoshino, K., Kurita, M., Yamaguchi, M., & Amemiya, S. (1988). Taxonomical significance of respiratory stimulation of sea urchin spermatozoa by egg associated substances. In R. D. Burke, P. V. Mladenov, P. Lambert, & R. L. Parsley (Eds.), Echinoderm biology (pp. 213–218). Rotterdam: Balkema.

    Google Scholar 

  • Winchell, C. J., Sullivan, J., Cameron, C. B., Swalla, B. J., & Mallatt, J. (2002). Evaluating hypotheses of deuterostome phylogeny and chordate evolution with new LSU and SSU ribosomal DNA data. Molecular Biology and Evolution, 19, 762–776.

    Article  PubMed  CAS  Google Scholar 

  • Zigler, K. S., & Lessios, H. A. (2003). Evolution of bindin in the pantropical sea urchin Tripneustes: comparisons to bindin of other genera. Molecular Biology and Evolution, 20, 220–231.

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We would like to thank M.-G. Bonhomme who initiated the sequencing project. Sequencing was carried out in the Molecular Systematics Service (MNHN) and the “Milieu et peuplement aquatiques” department (MNHN). Field work was supported by the program Deep Sea Benthos (MNHN/IRD). Some of the analytical work was performed in the lab EDB, part of the Laboratoires d’Excellence (LABEX) TULIP (ANR-10-LABX-41) and CEBA. We would like to thank the team and the cruise manager B. Richer-de-Forge (cruise Salomon 1). A. Ziegler’s comments greatly improved multiple versions of this work. Associate editor O. Bininda-Emonds, A. Smith, and an anonymous reviewer helped improve the quality of the manuscript. Financial support was provided by the French Ministry of Research. J.M. was supported by a Marie Curie International Outgoing Fellowship (grant 221099) within the 7th European Community Framework Program.

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Brosseau, O., Murienne, J., Pichon, D. et al. Phylogeny of Cidaroida (Echinodermata: Echinoidea) based on mitochondrial and nuclear markers. Org Divers Evol 12, 155–165 (2012). https://doi.org/10.1007/s13127-012-0087-1

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