Hostname: page-component-848d4c4894-p2v8j Total loading time: 0 Render date: 2024-04-30T11:37:23.226Z Has data issue: false hasContentIssue false
  • English
  • Français

A “rays-as-appendages” model for the origin of pentamerism in echinoderms

Published online by Cambridge University Press:  20 May 2016

Frederick H. C. Hotchkiss
Frederick H. C. Hotchkiss*
Affiliation:
26 Sherry Road, Harvard, Massachusetts 01451. E-mail: hotchkissf@panametrics.com
Get access Rights & Permissions [Opens in a new window]

Abstract

A new hypothesis concerning the evolutionary origin of pentameral symmetry in echinoderms is presented. The BA-A-BA pattern of Lovén's law in echinoids and the 2-1-2 symmetry of the edrioasteroid Stromatocystites appear to be morphogenetically related, and this pattern appears to be locked into development. This pattern may have originated from a unirayed 0-1-0, —A—, ancestor. I propose that a duplication of the uniray occurred and resulted in the addition of a pair of rays that followed Bateson's rules of symmetry to form a three-rayed 0-1-2, —A-BA, construction. This change occurred on the side that corresponds to the left side of the organism. This event made the individual asymmetric with respect to its anterior-posterior axis. Therefore I propose that morphogenetic regulation of bilaterality of the organism then led to homeotic expression of a mirror-image pair of rays on the opposite side. These two morphogenetic steps achieved the 2-1-2, BA-A-BA pattern. “Appendage status” of rays is assumed necessary to invoke the Batesonian mirror-image duplications of the model.

Three robust morphological characters emerge from the “rays-as-appendages” model: (1) 2-1-2, BAo-A-BA, organization; (2) “locked-in” pentamerism; and (3) a 2-3 pattern of right and left rays. Results based on ray homology research are presented for echinoids, asteroids, ophiuroids, edrioasteroids, ophiocistioids, and holothurians. I speculate that helicoplacoids may have 0-1-2 triradiate construction, and that solutes may have 0-1-0 uniray construction. The model has limits; it does not explain 1-1, or 2-1, or 2-2 or 1-1-1 organization of ambulacra.

Type
Articles
Information
Paleobiology , Volume 24 , Issue 2 , Spring 1998 , pp. 200 - 214
Copyright
Copyright © The Paleontological Society 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Literature Cited

Abeloos, M. 1931. Les potentialités regeneratrices de la face dorsale des bras des Astéries. Trifurcation dorsal d'un bras chez Solaster papposus (Linck). Bulletin Biologique de la France et de la Belgique 65: 394–405.Google Scholar
Abeloos, M. 1934. Régénération triple d'un bras chez une Astérie, Henricia sanguinolenta (O. F. Muller). Bulletin de la Societé Linneanne de Normandie Caen 8(6): 89–89.Google Scholar
Basler, K. and Struhl, G. 1994. Compartment boundaries and the control of Drosophila limb pattern by hedgehog protein. Nature 368: 208–214.Google Scholar
Bateson, W. 1894. Materials for the study of variation treated with especial regard to discontinuity in the origin of species. Reprint 1992, Johns Hopkins University Press, Baltimore.Google Scholar
Bather, F. A. 1915a. Studies in Edrioasteroidea VII. Morphology and bionomics of the Edrioasteridae. Geological Magazine, new series, decade VI 2: 211–215. 259–266.Google Scholar
Bather, F. A. 1915b. Studies in Edrioasteroidea IX. The genetic relations to other echinoderms. Geological Magazine, new series, decade VI 2: 393–403.Google Scholar
Bell, B. M. 1976. A study of North American Edrioasteroidea. New York State Museum and Science Service Memoir 21: 1–447. Albany.Google Scholar
Breder, C. M. Jr. 1955. Observations on the occurrence and attributes of pentagonal symmetry. Bulletin of the American Museum of Natural History 106: 173–220.Google Scholar
Bury, H. 1895. The metamorphosis of echinoderms. Quarterly Journal of Microscopical Science, new series 38: 45–136.Google Scholar
Carnevali, M. D. Candia and Bonosoro, F. 1995. Arm regeneration and pattern formation in crinoids. Pp. 245–253. Emson, R. H., Smith, A. B., Campbell, A. C.Echinoderm Research 1995. Balkema, Rotterdam.Google Scholar
Carter, G. S. 1961. A general zoology of the invertebrates, 4th ed. (revised). Sidgwick and Jackson, London.Google Scholar
Child, C. M. 1924. Physiological foundations of behavior. Henry Holdt, New York.Google Scholar
Clark, H. L. 1921. The echinoderm fauna of Torres Strait: its composition and its origin. Department of Marine Biology of the Carnegie Institution of Washington 10: 1–223. (Carnegie Institution of Washington Publication No. 214.).Google Scholar
Daley, P. E. J. 1996. The first solute which is attached as an adult: a Mid-Cambrian fossil from Utah with echinoderm and chordate affinities. Zoological Journal of the Linnean Society 117: 405–440.Google Scholar
David, B. and Mooi, R. 1996. Embryology supports a new theory of skeletal homologies for the phylum Echinodermata. Comptes Rendus Académie des Sciences Paris, Sciences de la vie/Life sciences 319: 577–584.Google Scholar
David, B., Mooi, R., and Telford, M. 1995. The ontogenetic basis of Lovén's rule clarifies homologies of the echinoid peristome. Pp. 155–164. Emson, R., Smith, A., Campbell, A.Echinoderm Research 1995. Balkema, Rotterdam.Google Scholar
Dawkins, R. 1996. Climbing mount improbable. W.W. Norton, New York.Google Scholar
Domantay, J. S. 1938. An unusual bud due to heteromorphosis in Echinaster luzonicus (Gray). The Philippine Journal of Science, Manila 64: 281–283. + plate i.Google Scholar
Eldredge, N. 1989. Macroevolutionary dynamics. McGraw-Hill, New York.Google Scholar
Emmel, V. E. 1907. Regenerated and abnormal appendages in the lobster. Thirty-Seventh Annual Report of the Commissioners of Inland Fisheries of Rhode Island (Special Paper No. 31). 99–152.Google Scholar
Erwin, D. H. 1994. The Permo-Triassic extinction. Nature 367: 231–236.Google Scholar
Erwin, D. H. 1996. The mother of mass extinctions. Scientific American 275: 72–78.Google Scholar
Erwin, D. H., Valentine, J., and Jablonski, D. 1997. The origin of animal body plans. American Scientist 85: 126–136.Google Scholar
Field, M. and Golubitsky, M. 1992. Symmetry in chaos, a search for pattern in mathematics, art and nature. Oxford University Press, Oxford.Google Scholar
Fischer, A. G. 1966. Spatangoids. Pp. U543–U628. Durham, J. W. et al Echinodermata 3, Asterozoa and Echinozoa. R. C. Moore Part U of Treatise on invertebrate paleontology. Geological Society of America and University of Kansas Press, New York.Google Scholar
Fisher, W. K. 1945. Unusual abnormalities in sea stars. Journal of the Washington Academy of Sciences 35: 296–298.Google Scholar
Foerste, A. F. 1914. Notes on Agelacrinidae and Lepadocystinae, with descriptions of Thresherodiscus and Brockocystis. Bulletin of the Scientific Laboratories of Denison University 7: 399–487.Google Scholar
Frankel, J. 1989. Pattern formation: ciliate studies and models. Oxford University Press, New York.Google Scholar
Ganong, W. F. 1890. Zoological notes. Report of the Committee on Marine Invertebrate Zoology. Bulletin of the Natural History Society of New Brunswick 9: 46–59.Google Scholar
Gee, H. 1996. Before the backbone: views on the origin of the vertebrates. Chapman and Hall, London.Google Scholar
Goodwin, B. C. 1996. How the leopard changed its spots: the evolution of complexity. Simon and Schuster, New York.Google Scholar
Gordon, I. 1929. Skeletal development in Arbacia, Echinarachnius and Leptasterias. Philosophical Transactions of the Royal Society of London B 217: 289–334.Google Scholar
Haude, R. 1994. Fossil holothurians: constructional morphology of the sea cucumber, and the origin of the calcareous ring. Pp. 517–522. David, B., Guille, A., Féral, J. P., Roux, M.Echinoderms through time. Balkema, Rotterdam.Google Scholar
Haude, R. 1995. Die Holothurien-Konstruktion: Evolutionsmodell und ältester Fossilbericht. Neues Jahrbuch für Geologie und Paläontologie Abhandlungen 195: 181–198.Google Scholar
Hinegardner, R. T. 1975. Morphology and genetics of sea urchin development. American Zoologist 15: 679–689.Google Scholar
Hotchkiss, F. H. C. 1978. Studies on echinoderm ray homologies: Lovén's law applies to Paleozoic ophiuroids. Journal of Paleontology 52: 537–544.Google Scholar
Hotchkiss, F. H. C. 1979. Case studies in the teratology of starfish. Proceedings of the Academy of Natural Sciences of Philadelphia 131: 139–157.Google Scholar
Hotchkiss, F. H. C. 1995. Lovén's law and adult ray homologies in echinoids, ophiuroids, edrioasteroids, and an ophiocistioid (Echinodermata: Eleutherozoa). Proceedings of the Biological Society of Washington 108: 401–435.Google Scholar
Hotchkiss, F. H. C. In press. Discussion on pentamerism: the five-part pattern of Stromatocystites, Asterozoa and Echinozoa. R. Mooi, M. Telford Echinoderms: San Francisco. Balkema, Rotterdam.Google Scholar
Hotchkiss, F. H. C. and Seegers, P. R. 1976. Variable symmetry in starfish. Thalassia Jugoslavica 12: 173–180.Google Scholar
Huxley, J. and De Beer, G. R. 1934. The elements of experimental embryology. Cambridge University Press, Cambridge.Google Scholar
Hyman, L. H. 1955. The invertebrates, Vol. IV. Echinodermata. McGraw-Hill, New York.Google Scholar
Jackson, R. T. 1912. Phylogeny of the Echini, with a revision of Palaeozoic species. Memoirs of the Boston Society of Natural History 7: 1–491.Google Scholar
Jackson, R. T. 1927. Studies of Arbacia punctulata and allies, and of nonpentamerous Echini. Memoirs of the Boston Society of Natural History 8: 437–565.Google Scholar
Jefferies, R. P. S. 1991. Two types of bilateral symmetry in the Metazoa: chordate and bilaterian. Pp. 94–127. Bock, G. R., Marsh, J.Biological asymmetry and handedness (Ciba Foundation Symposium 162). Wiley, Chichester.Google Scholar
Jefferies, R. P. S. 1994. The echinoderm stem group. P. 165–P. 165. David, B., Guille, A., Féral, J. P., Roux, M.Echinoderms through time. Balkema, Rotterdam.Google Scholar
Jefferies, R. P. S., Brown, N. A., and Daley, P. A. J. 1996. The early phylogeny of chordates and echinoderms and the origin of chordate left-right asymmetry and bilateral symmetry. Acta Zoologica (Stockholm) 77: 101–122.Google Scholar
Jell, P. A. 1983. Early Devonian echinoderms from Victoria (Rhombifera, Blastoidea and Ophiocistioidea). Pp. 209–235. Roberts, J., Jell, P. A.Memoire 1. T. Dorothy Hill jubilee memoir: proceedings of a meeting organized by the Association of Australasian Palaeontologists at the University of Queensland, 9th and 10th September 1982. Association of Australasian Palaeontologists, Sydney.Google Scholar
Kauffman, S. A. 1993. The origins of order: self-organization and selection in evolution. Oxford University Press, New York.Google Scholar
Kier, P. M. 1968. Echinoids from the Middle Eocene Lake City Formation of Georgia. Smithsonian Miscellaneous Collections 153(2): 1–45. Washington, D. C.Google Scholar
Kolata, D., Strimple, H. L., and Levorson, C. O. 1977. Revision of the Ordovician carpoid family Iowacystidae. Palaeontology 20: 529–557.Google Scholar
Lane, N. G. and Webster, G. D. 1967. Symmetry planes of Paleozoic crinoids. The University of Kansas Paleontological Contributions 25: 14–16.Google Scholar
Littlewood, D. T. J., Smith, A. B., Clough, K. A., and Emson, R. H. 1997. The interrelationships of the echinoderm classes: morphological and molecular evidence. Biological Journal of the Linnean Society 61: 409–438.Google Scholar
Lovén, S. 1874. Études sur les echinoidées. Kongelige Svenska Vetenskaps-Akademiens Handlingar, New Series 11(7): 1–91.Google Scholar
Lowe, C. J. and Wray, G. A. 1997. Radical alterations in the roles of homeobox genes during echinoderm evolution. Nature 389: 718–721.Google Scholar
Marten, M., Chesterman, J., May, J., and Trux, J. 1977. Worlds within worlds, a journey into the unknown. Holt, Rinehart and Winston, New York.Google Scholar
Smith, J. Maynard and Sondhi, K. C. 1960. The genetics of a pattern. Genetics 45: 1039–1050.Google Scholar
McNamara, K. J. 1987. Plate translocation in spatangoid echinoids: its morphological, functional and phylogenetic significance. Paleobiology 13: 312–325.Google Scholar
Melville, R. V. and Durham, J. W. 1966. Skeletal morphology. Pp. U220–U257. Durham, J. W. et al Echinodermata 3, Asterozoa and Echinozoa R. C. Moore Part U of Treatise on invertebrate paleontology. Geological Society of America and University of Kansas Press, New York.Google Scholar
Mooi, R. and David, B. 1997. Skeletal homologies of echinoderms. Paleontological Society Papers 3: 305–335.Google Scholar
Moore, R. C. and Fell, H. B. 1966. Homology of echinozoan rays. Pp. U119–U131. Durham, J. W. et al Echinodermata 3, Asterozoa and Echinozoa R. C. Moore Part U of Treatise on invertebrate paleontology. Geological Society of America and University of Kansas Press, New York.Google Scholar
Munar, J. 1984. Anomalías en la simetría de los Asteroidea (Echinodermata). Casos observados en aguas de Mallorca. Bolletí de la Societat d'història Natural de les Balears 28: 59–66.Google Scholar
Neville, A. C. 1976. Animal asymmetry (The Institute of Biology's Studies in Biology No. 67). Edward Arnold, London.Google Scholar
Ohshima, H. 1918. Notes on the development of Cucumaria echinata. Annotationes Zoologicae Japonenses 9: 377–387.Google Scholar
Olsen, H. 1942. The development of the brittle-star Ophiopholis aculeata (O. Fr. Müller), with a short report on the outer hyaline layer. Bergens Museums Årbok 1942, Naturvidenskapelig rekke Nr. 6. Bergen.Google Scholar
Onoda, K. 1933. On the orientation of the regular sea-urchin Heliocidaris crassispina. Japanese Journal of Zoology 5: 159–164.Google Scholar
Panganiban, G., Irvine, S. M., Lowe, C., Roehl, H., Corley, L. S., Sherbon, B., Grenier, J. K., Fallon, J. F., Kimble, J., Walker, M., Wray, G. A., Swalla, B. J., Martindale, M. Q., and Carroll, S. B. 1997. The origin and evolution of animal appendages. Proceedings of the National Academy of Sciences USA 94: 5162–5166.Google Scholar
Parsley, R. L. 1990. Aristocystites, a recumbent diploporid (Echinodermata) from the Middle and Late Ordovician of Bohemia, CSSR. Journal of Paleontology 64: 278–293.Google Scholar
Parsley, R. L. and Mintz, L. W. 1975. North American Paracrinoidea: (Ordovician: Paracrinozoa, new, Echinodermata). Bulletins of American Paleontology 68(288): 1–115.Google Scholar
Paul, C. R. C. and Smith, A. B. 1984. The early radiation and phylogeny of echinoderms. Biological Reviews 59: 443–481.Google Scholar
Polya, G. 1957. How to solve it, 2d ed.Princeton University Press, Princeton, N.J.Google Scholar
Raff, R. 1996. The shape of life. University of Chicago Press, Chicago.Google Scholar
Raff, R. and Kaufman, T. C. 1983. Embryos, genes, and evolution. Macmillan, New York.Google Scholar
Riddle, R. D., Johnson, R. L., Laufer, E., and Tabin, C. 1993. Sonic hedgehog mediates the polarizing activity of the ZPA. Cell 75: 1401–1416.Google Scholar
Rosen, J. 1975. Symmetry discovered, concepts and applications in nature and science. Cambridge University Press, Cambridge.Google Scholar
Runnström, S. 1927. Über die Entwicklung von Leptosynapta inhaerens (O. Fr. Müller). Bergens Museums Årbok 1927, Naturvidenskapelig rekke Nr. 1. Bergen.Google Scholar
Semon, R. 1888. Die Entwicklung der Synapta digitata und die Stammesgeschichte der Echinodermen. Jena Zeitschrift für Wissenschaftliche 22: 1–135.Google Scholar
Shubin, N., Tabin, C., and Carroll, S. 1977. Fossils, genes and the evolution of animal limbs. Nature 388: 639–648.Google Scholar
Smiley, S. 1986. Metamorphosis of Stichopus californicus (Echinodermata: Holothuroidea) and its phylogenetic implications. Biological Bulletin 171: 611–631.Google Scholar
Smith, A. B. 1984. Echinoid palaeobiology. Special topics in palaeontology 1. Allen and Unwin, London.Google Scholar
Smith, A. B. 1990. Evolutionary diversification of echinoderms during the early Palaeozoic. Pp. 265–286. Taylor, P. D., Larwood, G. P.Major evolutionary radiations (Systematics Association Special Volume No. 42). Clarendon Press, Oxford.Google Scholar
Sumrall, C. D. 1997. The role of fossils in the phylogenetic reconstruction of Echinodermata. Paleontological Society Papers 3: 267–288.Google Scholar
Waddington, C. H. 1956. Genetic assmilation of the bithorax phenotype. Evolution 10: 1–13.Google Scholar
Waddington, C. H. 1962. New patterns in genetics and development. Columbia University Press, New York.Google Scholar
Webster, G. and Goodwin, B. 1996. Form and transformation: generative and relational principles in biology. Cambridge University Press, Cambridge.Google Scholar
Wootton, D. M. 1949. The development of Thyonepsolus nutriens Clark. Ph.D. dissertation. Stanford University, Palo Alto, Calif.Google Scholar
Wray, G. In press. Origin and diversification of echinoderm body architecture: insights from the expression of body-patterning genes. R. Mooi, M. Telford Echinoderms: San Francisco. Balkema, Rotterdam. [Abstract.].Google Scholar
Yamamoto, M. and Yoshida, M. 1978. Fine structure of the ocelli of a synaptid holothurian, Opheodesoma spectabilis, and the effects of light and darkness. Zoomorphologie 90: 1–17.Google Scholar
Zavodnik, D. 1995. Odd symmetrical and teratological Asteroidea of the Center for Marine Research (Rovinj, Croatia). Natura Croatica 4: 151–161.Google Scholar