Skip to main content Skip to main navigation menu Skip to site footer
Type: Articles
Published: 2010-06-14
Page range: 1–19
Abstract views: 91
PDF downloaded: 3

Phylogenetic relationships in the genus Astropecten Gray (Paxillosida: Astropectinidae) on a global scale: molecular evidence for morphological convergence, species-complexes and possible cryptic speciation

Zoological Museum of the University of Zurich, Winterthurerstrasse 190, CH−8057 Zurich, Switzerland
Smithsonian Tropical Research Institute, Box 0843−03092, Balboa, Panama
Echinodermata global phylogeny Asteroidea mitochondrial DNA echinoderm marine invertebrates

Abstract

With over 150 described species, Astropecten Gray (Paxillosida:Astropectinidae) is one of the most species-rich genera among sea stars. This diversity is remarkable, because most species of Astropecten have a long-lived planktotrophic larval stage, which would be expected to lead to a low speciation rate. The taxonomy of this genus is complex and not well resolved, and phylogenetic relationships have only been addressed in the beginning of the last century. In order to resolve general taxonomic issues, identify speciation patterns and estimate species diversity within the genus Astropecten, we inferred a molecular phylogeny of 117 specimens of Astropecten belonging to 40 species from around the world using mitochondrial DNA (mtDNA) sequences of 12S rRNA, 16S rRNA and cytochrome oxidase subunit I (COI). We compared the resulting molecular phylogeny to a previously published morphological one by Döderlein and investigated the possibility of morphological convergence in species from different geographic regions. Finally, we also aimed at identifying potentially problematic descriptions and/or signs of cryptic speciation in Astropecten. The global molecular phylogeny exhibited three main clades, each containing specimens of the same geographic region: 1. the IndoPacific; 2. the Neotropics; and 3. the eastern Atlantic and Mediterranean. Phylogenetic inferences based on mtDNA indicate that morphological and ecological convergence has taken place in Astropecten, resulting in allopatric non-sister taxa with similar morphologies and habitat preferences. The comparison to Döderlein’s morphological phylogeny reveals congruence on the whole but many discrepancies on a local scale, indicating that meaningful morphological characters are not easily identified and categorized in Astropecten. Our results also reveal that A. polyacanthus Müller & Tröschel and A. indicus Döderlein are species-complexes; cryptic speciation may have occurred within each of these morphospecies. Furthermore, several variants, previously presumed to be conspecific, exhibit genetic distances large enough to justify recognizing them as separate species.

References

  1. Agassiz, A. (1877) North American starfishes. Memoires of the Museum of Comparative Zoology at Harvard, 5, 1−136.

    Bremer, K. (1988) The limits of amino-acid sequence data in angiosperm phylogenetic reconstruction. Evolution, 42, 795−803.

    Clark, A.M. & Downey, M.E. (1992) Starfishes of the Atlantic. Chapman & Hall, London, 794 pp.

    Colborn, J., Crabtree, R.E., Shaklee, J.B., Pfeiler, E. & Bowen, B.W. (2001) The evolutionary enigma of bonefishes (Albula spp.): cryptic species and ancient separation in a globally distributed shorefish. Evolution, 55, 807−820.

    Döderlein, L. (1917) Die Asteriden der Siboga-Expedition. I. Die Gattung Astropecten und ihre Stammesgeschichte. In: Brill, E.J. (ed) Siboga-Expeditie. Uitkomsten op zoölogisch, botanisch, ozeanographisch en geologisch gebied verzameld in Nederlandsch Oost-Indie 1899−1900 aan boord H.M. "Siboga", 46 (a), Leiden, pp 191.

    Farris, J.S., Källersjö, M., Kluge, A.G. & Bult, C. (1995) Constructing a significance test for incongruence. Systematic Biology, 44, 570−572.

    Fisher, W.K. (1906) New Starfishes from the Pacific Coast of North America. Proceedings of the Washington Academy of Sciences, 8, 11−139.

    Fisher, W.K. (1911) Asteroidea of the North Pacific and adjacent waters. Part 1. Phanerozonia and Spinulosa. Bulletin of the U.S. National Museum, 76, pp. 420.

    Fisher, W.K. (1913) Four new genera and fifty-eight new species of starfishes from the Philippine Islands, Celebes, and the Moluccas. Proceedings of the U.S. National Museum, 43, 599−648.

    Folmer, O., Black, M., Hoeh, W., Lutz, R. & Vrijenhoek, R. (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology, 3, 5294-5299.

    Gray, J.E. (1841) A synopsis of the genera and species of the class Hypostoma (Asterias, Linnaeus). Annals and Magazine of Natural History, 1, 175−184.

    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.

    Hörstadius, S. (1938) Über die Entwicklung von Astropecten aranciacus L. Pubblicazioni della Stazione Zoologica Napoli, 17, 221−312.

    Jeanmougin, F., Thompson, J.D., Gouy, M., Higgins, D.G. & Gibson, T.J. (1998) Multiple sequence alignment with Clustal x. Trends in Biochemical Sciences, 23, 403−405.

    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.

    Koehler, R. (1909) Echinodermes provenant des campagnes du yacht Princesse-Alice. Resultats des campagnes scientifiques (Monaco), 34, 1−317.

    Koehler, R. (1910) Shallow-Water Asteroidea. Echinoderma of the Indian Museum, Calcutta, Indian Museum 191, 206 pp.

    Koehler, R. (1924) Les Echinodermes des Mers D'Europe. Librarie Octave Doin, Paris, 210 pp.

    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.

    Lessios, H.A. (2008) The great American schism: divergence of marine organisms after the final rise of the Central American Isthmus. Annual Review of Ecology, Evolution, and Systematics, 39, 63−91.

    Loytynoja, A. & Milinkovitch, M.C. (2001) SOAP, cleaning multiple alignments from unstable blocks. Bioinformatics 17, 573−574.

    Ludwig, H. (1897) Die Seesterne des Mittelmeeres. Fauna und Flora des Golfes von Neapel und der angrenzenden Meeres-Abschnitte. Zoologische Station zu Neapel, 24, 491 pp.

    Mortensen, T. (1921) Studies of the development and larval forms of echinoderms. Copenhagen, 253 pp.

    Mortensen, T. (1937) Contributions to the study of the development and larval forms of echinoderms III. Mémoires de l'Académie Royale des Sciences et des Lettres de Danemark, Copenhagen, 65 pp.

    Müller, J. & Troschel, F.H. (1842) System der Asteriden. Bieweg & Sohn, Braunschweig, 132 pp.

    Newth, H.G. (1925) The early development of Astropecten irregularis, with remarks on duplicity in Echinoderm larvae. Quarterly Journal of Microscopical Science, 69, 519−542.

    Palumbi, S.R. (1992) Marine Speciation on a Small Planet. Trends in Ecology and Evolution, 7, 114−118.

    Palumbi, S.R. (1994) Genetic-divergence, reproductive isolation, and marine speciation. Annual Review of Ecology and Systematics, 25, 547−572.

    Palumbi, S.R. (1996) PCR and molecular systematics. In: Hillis, D., Moritz, C., Mable, B.K. (eds). Molecular systematics, 2nd ed. Sunderland MA: Sinauer Press, 655 pp.

    Paulay, G. & Meyer, C. (2006) Dispersal and divergence across the greatest ocean region: Do larvae matter? Integrative and Comparative Biology, 46, 269−281.

    Perrier, E. (1875/6) Révision de la collection de Stellerides du Muséum d'Histoire Naturelle de Paris. Archives de Zoologie Experimentale et Génerale, 4, 265−450.

    Philippe, H., Snell, E.A., Bapteste, E., Lopez, P., Holland, P.W.H. & Casane, D. (2004) Phylogenomics of eukaryotes: impact of missing data on large alignments. Molecular Biology and Evolution, 21, 1740–1752.

    Posada, D. & Crandall, K.A. (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics, 14, 817−818.

    Riginos, C. & Victor, B.C. (2001) Larval spatial distributions and other early life-history characteristics predict genetic differentiation in eastern Pacific blennioid fishes. Proceedings of the Royal Society of London Series B, 268, 1931−1936.

    Ronquist, F. & Huelsenbeck, J.P. (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19, 1572−1574.

    Say, T. (1825) On the species of the Linnean genus Asterias inhabiting the coast of the United States. Journal of the Academy of Natural Sciences of Philadelphia, 5, 151−154.

    Sladen, W.P. (1889) Report on the Asteroidea. Report on the scientific results of the voyage of the H. M. S. Challenger during the years 1873−1876. Zoology, 30, 1−893.

    Sponer, R. & Roy, M.S. (2002) Phylogeographic analysis of the brooding brittle star Amphipholis squamata (Echinodermata) along the coast of New Zealand reveals high cryptic genetic variation and cryptic dispersal potential. Evolution, 56, 1954−1967.

    Swofford, D.L. (2003) PAUP*. Phylogenetic Analysis Using Parsimony (*and other Methods). Version 4, Sinauer Associates, Sunderland, Massachusetts.

    Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F. & Higgins, D.G. (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research, 25, 4876−4882.

    Tortonese, E. (1965) Echinodermata Fauna d'Italia VI. Calderini, Bologna, 422 pp.

    Ventura, C.R.R., Falcao, A.P.C., Santos, J.S. & Fiori, C.S. (1997) Reproductive cycle and feeding periodicity in the starfish Astropecten brasiliensis in the Cabo Frio upwelling ecosystem (Brazil). Invertebrate Reproduction and Development, 31, 135−141.

    Verrill, A.E. (1914) Monograph of the shallow-water Starfishes of the North Pacific Coast from the Arctic Ocean to California. Harriman Alaska Series, 14, 1−420.

    Verrill, A.E. (1915) Report on the Starfishes of the West Indies, Florida, and Brazil. Bulletin from the Laboratories of Natural History of the State University of Iowa, 7, 2−232.

    Ward, R.D., Holmes, B.H. & O’Hara, T.D. (2008) DNA Barcoding discriminates echinoderm species. Molecular Ecology Resources, 8, 1202−1211.

    Waters, J.M., O'Loughlin, P.M. & Roy, M.S. (2004) Molecular systematics of some Indo-Pacific asterinids (Echinodermata, Asteroidea): does taxonomy reflect phylogeny? Molecular Phylogenetetics and Evolution, 30, 872−878.

    Wiens, J.J. (2003) Missing data, incomplete taxa, and phylogenetic accuracy. Systematic Biology, 52, 528−538.

    Wiens, J.J. (2005) Can incomplete taxa rescue phylogenetic analyses from long branch attraction? Systematic Biology, 54, 731–742.

    Wiens, J.J. (2006) Missing data and the design of phylogenetic analyses. Journal of Biomedical Informatics, 39, 34−42.

    Wiens, J.J. & Moen, D.S. (2008) Missing data and the accuracy of Bayesian phylogenetics. Journal of Systematics and Evolution, 46, 307–314.

    Wilson, N.G., Hunter, R.L., Lockhart, S.J. & Halanych, K.M. (2007) Multiple lineages and absence of panmixia in the "circumpolar" crinoid Promachocrinus kerguelensis from the Atlantic sector of Antarctica. Marine Biology, 152, 895−904.

    Ziesenhenne, F.C. (1939) The Templeton Crocker Expedition. X. Echinoderms from the West Coast of Lower California, the Gulf of California and Clarion Island. Zoologica, 22, 209−239.

    Zigler, K.S. & Lessios, H.A. (2004) Speciation on the coasts of the new world: Phylogeography and the evolution of bindin in the sea urchin genus Lytechinus. Evolution, 58, 1225−1241.