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Ontogeny in the fossil record: diversification of body plans and the evolution of “aberrant” symmetry in Paleozoic echinoderms

Published online by Cambridge University Press:  08 April 2016

Colin D. Sumrall
Affiliation:
Department of Earth and Planetary Sciences, University of Tennessee, Knoxville, Tennessee 37996-1410. E-mail: csumrall@utk.edu
Gregory A. Wray
Affiliation:
Department of Biology, Duke University, Box 90325, Durham, North Carolina 27708-0325. E-mail: gwray@duke.edu

Abstract

Echinoderms have long been characterized by the presence of ambulacra that exhibit pentaradiate symmetry and define five primary body axes. In reality, truly pentaradial ambulacral symmetry is a condition derived only once in the evolutionary history of echinoderms and is restricted to eleutherozoans, the clade that contains most living echinoderm species. In contrast, early echinoderms have a bilaterally symmetrical 2-1-2 arrangement, with three ambulacra radiating from the mouth. Branching of the two side ambulacra during ontogeny produces the five adult rays. During the Cambrian Explosion and Ordovician Radiation, some 30 clades of echinoderms evolved, many of which have aberrant ambulacral systems with one to four rays. Unfortunately, no underlying model has emerged that explains ambulacral homologies among disparate forms. Here we show that most Paleozoic echinoderms are characterized by uniquely identifiable ambulacra that develop in three distinct postlarval stages. Nearly all “aberrant” echinoderm morphologies can be explained by the paedomorphic ambulacra reduction (PAR) model through the loss of some combination of these growth stages during ontogeny. Superficially similar patterns of ambulacral reduction in distantly related clades have resulted from the parallel loss of homologous ambulacra during ontogeny. Pseudo-fivefold symmetry seen in Blastoidea and the true fivefold symmetry seen in Eleutherozoa result from great reduction and total loss, respectively, of the 2–1–2 symmetry early in ontogeny. These ambulacral variations suggest that both developmental and ecological constraints affect the evolution of novel echinoderm body plans.

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Articles
Copyright
Copyright © The Paleontological Society 

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References

Literature Cited

Beaver, H. H., et al. 1968. Echinodermata 1. Part S of Moore, R. C., ed. Treatise on invertebrate paleontology. Geological Society of America, New York, and University of Kansas, Lawrence.Google Scholar
Bell, B. M. 1975. Ontogeny and systematics of Timeischytes casteri, n. sp.: an enigmatic Devonian edrioasteroid. Bulletins of American Paleontology 67:3356.Google Scholar
Bell, B. M. 1976a. Phylogenetic implications of ontogenetic development in the class Edrioasteroidea (Echinodermata). Journal of Paleontology 50:10011019.Google Scholar
Bell, B. M. 1976b. A study of North American Edrioasteroidea. New York State Museum Memoir 21.Google Scholar
Brett, C. E., Frest, T. J., Sprinkle, J., and Clement, C. R. 1983. Coronoidea: a new class of blastozoan echinoderms based on a taxonomic reevaluation of Stephanocrinus . Journal of Paleontology 57:627651.Google Scholar
Broadhead, T. W. 1974. Reevaluation of the morphology of Amecystis laevis (Raymond). Journal of Paleontology 48:670673.Google Scholar
Broadhead, T. W., and Sumrall, C. D. 2003. Heterochrony and paedomorphic morphology of Sprinkleocystis ektopios, new genus and species (Rhombifera, Glyptocystida) from the Middle Ordovician (Caradoc) of Tennessee. Journal of Paleontology 77:113120.2.0.CO;2>CrossRefGoogle Scholar
Budd, G. E., and Jensen, S. 2000. A critical reappraisal of the fossil record of the bilaterian phyla. Biological Reviews 75:253295.Google Scholar
Bury, H. 1895. The metamorphosis of echinoderms. Quarterly Journal of Microscopic Science 29: 409–136.Google Scholar
Cameron, R. A., and Hinegardner, R. T. 1978. Early events in sea urchin metamorphosis, description and analysis. Journal of Morphology 157:2132.Google Scholar
Cameron, C. B., Garey, J. R., and Swalla, B. J. 2000. Evolution of the chordate body plan: new insights from phylogenetic analyses of deuterostome phyla. Proceedings of the National Academy of Sciences USA 97:44694474.Google Scholar
Carpenter, P. H. 1884. Report on the Crinoidea—the stalked crinoids. Report on the scientific results of the voyage of the H. M. S. Challenger. Zoology 11:1440.Google Scholar
Ciampaglio, C. N. 2002. Determining the role that ecological and developmental constraints play in controlling disparity: examples from the crinoid and blastozoan fossil record. Evolution and Development 4:117.Google Scholar
David, B., and Mooi, R. 1996. Embryology supports a new theory of skeletal homologies for the phylum Echinodermata. Comptes Rendus de l'Académie des Sciences de Paris, ser. 3, 319:577584.Google Scholar
David, B., Mooi, R., and Telford, M. 1995. The ontogenetic basis of Lovén's Rule clarifies homologies of the echinoid peristome. Pp. 155164 in Emson, R. H., Smith, A. B., and Campbell, A. C., eds. Echinoderm research 1995. A. A. Balkema, Rotterdam.Google Scholar
David, B., Lefebvre, B., Mooi, R., and Parsley, R. L. 2000. Are homalozoans echinoderms? An answer from the extraxial-axial theory. Paleobiology 26:529555.2.0.CO;2>CrossRefGoogle Scholar
Derstler, K. L. 1985. Studies on the morphological evolution of echinoderms. . University of California, Davis.Google Scholar
Erwin, D. H., and Valentine, J. W. 1984. “Hopeful monsters,” transposons, and the Metazoan radiation. Proceedings of the National Academy of Sciences, USA 81:54825483.CrossRefGoogle ScholarPubMed
Foote, M. 1995. Morphological diversification of Paleozoic crinoids. Paleobiology 21:273299.CrossRefGoogle Scholar
Foote, M. 1999. Morphological diversity in the evolutionary radiation of Paleozoic and post-Paleozoic crinoids. Paleobiology Memoir 1(Suppl. to Vol. 25, No. 2).Google Scholar
Gee, H. 1996. Before the backbone: views on the origin of vertebrates. Chapman and Hall, London.Google Scholar
Gordon, I. 1929. Skeletal development in Arbacia, Echinarachnius and Leptasterias . Philosophical Transactions of the Royal Society of London B 217:289334.Google Scholar
Gould, S. J. 1989. Wonderful life. W. W. Norton, New York.Google Scholar
Gould, S. J. 1991. The disparity of the Burgess Shale arthropod fauna and the limits of cladistic analysis: why we must strive to quantify morphospace. Paleobiology 17:411423.Google Scholar
Guensburg, T. E., and Sprinkle, J. 1992. Rise of echinoderms in the Paleozoic Evolutionary Fauna: significance of paleoenvironmental controls. Geology 20:407410.Google Scholar
Hotchkiss, F. H. C. 1998. A “rays-as-appendages” model for the origin of pentamerism in echinoderms. Paleobiology 24:200214.Google Scholar
Hughes, N. C. 2005. Trilobite construction: building a bridge across the micro and macroevolutionary divide. Pp. 139158 in Briggs, D. E. G., ed. Evolving form and function: fossils and development. Proceedings of a symposium honoring Adolph Seilacher for his contributions to paleontology, in celebration of his 80th birthday. Special Publication of the Peabody Museum of Natural History, Yale University, New Haven, Conn. Google Scholar
Jacobs, D. K. 1990. Selector genes and the Cambrian radiation of Bilateria. Proceedings of the National Academy of Sciences, USA 87:44064410.Google Scholar
Jefferies, R. P. S. 1968. The subphylum Calcichordata (Jefferies, 1967) primitive fossil chordates with echinoderm affinities. Bulletin of the British Museum (Natural History), Geology 16:243339.Google Scholar
Jefferies, R. P. S. 1986. The ancestry of the vertebrates. British Museum (Natural History) and Cambridge University Press, London.Google Scholar
Jefferies, R. P. S., Brown, N. A., and Daley, P. E. J. 1996. The early phylogeny of chordates and echinoderms and the origin of chordate left-right asymmetry and bilateral symmetry. Acta Zoologica 77:101122.CrossRefGoogle Scholar
Kesling, R. V. 1968. Cystoids. Pp. S85S267 in Beaver, et al. 1968.Google Scholar
Lefebvre, B. 2001. A critical comment on “ankyroids” (Echinodermata, Stylophora). Geobios 34:597627.CrossRefGoogle Scholar
Lefebvre, B. 2003. Functional morphology of stylophoran echinoderms. Palaeontology 46:511555.Google Scholar
Lovén, S. 1874. Études sur les echinoidées. Kongelige Svenska Vetenskaps-Akademiens Handlinger, new series 11:191.Google Scholar
Lowe, C. J., and Wray, G. A. 1997. Radical alterations in the roles of homeobox genes during echinoderm evolution. Nature 389:718721.Google Scholar
McEdward, L. R., and Miner, B. G. 2001. Larval and life cycle patterns in echinoderms. Canadian Journal of Zoology 79:11251170.Google Scholar
Mooi, R., David, B., and Marchand, D. 1994. Echinoderm skeletal homologies: classical morphology meets modern phylogenetics. Pp. 8795 in David, B., Guille, A., Féral, J., and Roux, M., eds. Echinoderms through time. A. A. Balkema, Rotterdam.Google Scholar
Moore, R. C., Lane, N. G., Strimple, H. L., Sprinkle, J., and Fay, R. O. 1978. Inadunata. Pp. T520T812 in Ubaghs, G. et al. Echinodermata 2. Part T of Moore, R. C. and Teichert, C., eds. Treatise on invertebrate paleontology. Geological Society of America, Boulder, Colo., and University of Kansas, Lawrence.Google Scholar
Parsley, R. L. 1997. The echinoderm classes Stylophora and Homoiostelea: non Calcichordata. In Waters, J. A. and Maples, C. G., eds. Geobiology of echinoderms. Paleontological Society Papers 3:225248.CrossRefGoogle Scholar
Parsley, R. L., and Zhao, Y. 2007. Long stalked eocrinoids in the basal Middle Cambrian Kaili Biota, Taijaing County Guizhou Province, China. Journal of Paleontology (in press).Google Scholar
Paul, C. R. C. 1977. Evolution of primitive echinoderms. Pp. 123158 in Hallam, A., ed. Patterns of evolution as illustrated by the fossil record. Elsevier, Amsterdam.Google Scholar
Paul, C. R. C. 1984. British Ordovician cystoids, Part 2. Monographs of the Palaeontographical Society, London.Google Scholar
Paul, C. R. C., and Smith, A. B. 1984. The early radiation and phylogeny of echinoderms. Biological Reviews 59:443481.Google Scholar
Peterson, K. J. 1995. A phylogenetic test of the calcichordate scenario. Lethaia 28:2537.CrossRefGoogle Scholar
Peterson, K. J., Arenas-Mena, C., and Davidson, E. H. 2000a. The A/P axis in echinoderm ontogeny and evolution: evidence from fossils and molecules. Evolution and Development 2:93101.Google Scholar
Peterson, K. J., Cameron, R. A., and Davidson, E. H. 2000b. Bilaterian origins: significance of new experimental observations. Developmental Biology 219:117.Google Scholar
Raff, R. A. 1996. The shape of life. University of Chicago Press, Chicago.Google Scholar
Raff, R. A., and Kaufman, T. C. 1983. Embryos, genes, and evolution. Macmillan, New York.Google Scholar
Rozhnov, S. V. 2002. Morphogenesis and evolution of crinoids and other pelmatozoan echinoderms in the Early Paleozoic. Paleontological Journal 6(Suppl.):S525S674.Google Scholar
Shubin, N. H., and Marshall, C. R. 2000. Fossils, genes, and the origin of novelty. In Erwin, D. H. and Wing, S. L., eds. Deep time: Paleobiology‘s perspective. Paleobiology 26(Suppl. to No. 4):324340.Google Scholar
Smith, A. B. 1984. Echinoid paleobiology. Allen and Unwin, London.Google Scholar
Smith, A. B. 1988. Fossil evidence for the relationships of extant echinoderm classes and their times of divergence. Pp. 85101 in Paul, C. R. C. and Smith, A. B., eds. Echinoderm phylogeny and evolution. Clarendon, Oxford.Google Scholar
Smith, A. B. 2005. The pre-radial history of echinoderms. Geological Journal 40:255280.Google Scholar
Smith, A. B., Peterson, K. J., Wray, G. A., and Littlewood, D. T. J. 2004. From bilateral symmetry to pentaradiality: the phylogeny of hemichordates and echinoderms. Pp. 365383 in Cra-craft, J. and Donoghue, M. J., eds. Assembling the tree of life. Oxford University Press, Oxford.Google Scholar
Sprinkle, J. 1973a. Morphology and evolution of blastozoan echinoderms. Harvard University Museum of Comparative Zoology Special Publication, Cambridge.CrossRefGoogle Scholar
Sprinkle, J. 1973b. Tripatocrinus, a new hybocrinid crinoid based on disarticulated plates from the Antelope Valley Limestone of Nevada and California. Journal of Paleontology 47:861882.Google Scholar
Sprinkle, J. 1980. An overview of the fossil record. Pp. 1526 in Broadhead, T. and Waters, J., eds. Echinoderms—notes for a short course. University of Tennessee, Knoxville.Google Scholar
Sprinkle, J., and Wilbur, B. C. 2005. Deconstructing helicopla-coids: reinterpreting the most enigmatic Cambrian echinoderms. Geological Journal 40:281293.Google Scholar
Strathmann, R. R. 1985. Feeding and nonfeeding larval development and life-history evolution in marine invertebrates. Annual Review of Ecology and Systematics 16:339361.Google Scholar
Strathmann, R. R. 1988. Larvae, phylogeny, and von Baer's law. Pp. 5367 in Paul, C. R. C. and Smith, A. B., eds. Echinoderm phylogeny and evolutionary biology. Clarendon, Oxford.Google Scholar
Sumrall, C. D. 1996. Late Paleozoic edrioasteroids (Echinodermata) from the North American mid-continent. Journal of Paleontology 70:969985.Google Scholar
Sumrall, C. D. 1997. The role of fossils in the phylogenetic reconstruction of Echinodermata. In Waters, J. A. and Maples, C. G., eds. Geobiology of echinoderms. Paleontological Society Papers 3:267288.Google Scholar
Sumrall, C. D. 2007. The origin of Lovén's Law in glyptocystitoid rhombiferans and its bearing on the plate homology and heterochronic evolution of the hemicosmitid peristomial border. In Ausich, W. I. and Webster, G. D., eds. Echinoderm paleobiology. Indiana University Press, Bloomington (in press).Google Scholar
Sumrall, C. D., and Schumacher, G. A. 2002. Cheirocystis fulto-nensis, a new glyptocystitoid rhombiferan from the Upper Ordovician of the Cincinnati Arch—comments on cheirocrinid ontogeny. Journal of Paleontology 76:843851.2.0.CO;2>CrossRefGoogle Scholar
Sumrall, C. D., and Sprinkle, J. 1998. Phylogenetic analysis of living Echinodermata based on primitive fossil taxa. Pp. 8187 in Mooi, R. and Telford, M., eds. Echinoderms: San Francisco. A. A. Balkema, Rotterdam.Google Scholar
Sumrall, C. D., and Sprinkle, J. 1999. Early ontogeny of the glyptocystitid rhombiferan Lepadocystis moorei. Pp. 409414 in Carnevali, M. D. C. and Bonasoro, F., eds. Echinoderm research 1998. A. A. Balkema., Rotterdam.Google Scholar
Sumrall, C. D., Sprinkle, J., and Guensburg, T. E. 2001. Comparison of flattened Pelmatozoa (Echinodermata): insights from the new Early Ordovician eocrinoid Haimacystis rozhnovi . Journal of Paleontology 75:985992.Google Scholar
Ubaghs, G. 1968a. General characters of Echinodermata. Pp. S3S59 in Beaver, et al. 1968.Google Scholar
Ubaghs, G. 1968b. Stylophora. Pp. S495S565 in Beaver, et al. 1968.Google Scholar
Valentine, J. W. 1995. Why no new phyla after the Cambrian? Genome and ecospace hypotheses revisited. Palaios 10:190194.Google Scholar
Valentine, J. W. 2004. On the origin of phyla. University of Chicago Press, Chicago.Google Scholar
Wray, G. A. 1997. Echinoderms. Pp. 309329 in Gilert, S. F. and Raunio, A. M., eds. Embryology: constructing the organism. Sinauer, Sunderland, Mass. Google Scholar