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Empirical and theoretical study of atelostomate (Echinoidea, Echinodermata) plate architecture: using graph analysis to reveal structural constraints

Published online by Cambridge University Press:  04 May 2015

Thomas Saucède
Affiliation:
Biogéosciences, UMR CNRS 6282, Université de Bourgogne, 21000 Dijon, France. E-mail: [email protected]
Rémi Laffont
Affiliation:
Biogéosciences, UMR CNRS 6282, Université de Bourgogne, 21000 Dijon, France. E-mail: [email protected]
Catherine Labruère
Affiliation:
Institut de Mathématiques de Bourgogne, UMR CNRS 5584, Université de Bourgogne, 21000 Dijon, France
Ahmed Jebrane
Affiliation:
Institut de Mathématiques de Bourgogne, UMR CNRS 5584, Université de Bourgogne, 21000 Dijon, France
Eric François
Affiliation:
Biogéosciences, UMR CNRS 6282, Université de Bourgogne, 21000 Dijon, France. E-mail: [email protected]
Gunther J. Eble
Affiliation:
Biogéosciences, UMR CNRS 6282, Université de Bourgogne, 21000 Dijon, France. E-mail: [email protected]
Bruno David
Affiliation:
Biogéosciences, UMR CNRS 6282, Université de Bourgogne, 21000 Dijon, France. E-mail: [email protected]

Abstract

Describing patterns of connectivity among organs is essential for identifying anatomical homologies among taxa. It is also critical for revealing morphogenetic processes and the associated constraints that control the morphological diversification of clades. This is particularly relevant for studies of organisms with skeletons made of discrete elements such as arthropods, vertebrates, and echinoderms. Nonetheless, relatively few studies devoted to morphological disparity have considered connectivity patterns as a level of morphological organization or developed comparative frameworks with proper tools. Here, we analyze connectivity patterns among apical plates in Atelostomata, the most diversified clade among irregular echinoids. The clade comprises approximately 1600 fossil and Recent species (e.g., 25% of post-Paleozoic species of echinoids) and shows high levels of morphological disparity. Plate connectivity patterns were analyzed using tools and statistics of graph theory. To describe and explore the diversity of connectivity patterns among plates, we symbolized each pattern as a graph in which plates are coded as nodes that are connected pairwise by edges. We then generated a comparative framework as a morphospace of connections, in which the disparity of plate patterns observed in nature was mapped and analyzed. Main results show that apical plate patterns are both highly disparate between and within atelostomate groups and limited in number; overall, they also constitute small, compact, and simple structures compared to possible random patterns. Main traits of the evolution of apical plate patterns reveal the existence of strong morphogenetic constraints that are phylogenetically determined. In contrast, evolutionary radiations within atelostomates were accompanied by a clear increase in disparity, suggesting a release of some constraints at the origin of clades.

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Articles
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Copyright © 2015 The Paleontological Society. All rights reserved. 

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References

Literature Cited

Agassiz, L. 1839. Description des échinodermes fossiles de la Suisse. 1. Spatangoïdes et Clypeasteroïdes. Nouveaux Mémoires de la Société Helvétique des Sciences Naturelles 3:1101.Google Scholar
Agassiz, L. 1840. Description des échinodermes fossiles de la Suisse. 2. Cidarides. Nouveaux Mémoires de la Société Helvétique des Sciences Naturelles 4:1107.Google Scholar
Agassiz, A. 1869. Preliminary report on the echini and starfishes dredged in deep water between Cuba and Florida reef by L. F. De Pourtalès, Assist. U.S. coast survey. Bulletin of the Museum of Comparative Zoology, Harvard College 1:253308.Google Scholar
Baglivo, J. A., and Graver, J. E. 1983. Incidence and symmetry in design and architecture. Cambridge University Press, Cambridge.Google Scholar
Barabási, A.-L., and Oltvai, Z. N. 2004. Network biology: understanding the cell’s functional organization. Nature Reviews Genetics 5:101113.CrossRefGoogle ScholarPubMed
Barras, C. G. 2007. Phylogeny of the Jurassic to Early Cretaceous ‘Disasteroid’ echinoids (Echinoidea; Echinodermata), and the origins of spatangoids and holasteroids. Journal of Systematic Palaeontology 5:133161.CrossRefGoogle Scholar
Barras, C. G. 2008. Morphological innovation associated with the expansion of atelostomate irregular echinoids into fine-grained sediments during the Jurassic. Palaeogeography, Palaeoclimatology, Palaeoecology 263:4457.CrossRefGoogle Scholar
Beck, M., Benkö, G., Eble, G. J., Flamm, C., Müller, S., and Stadler, P. F. 2004. Graph grammars as models for the evolution of developmental pathways. Pp. 815in H. Schaub, F. Deetje, and U. Brüggemann, eds. The logic of artificial life: abstracting and synthesizing the principles of living systems (Proceedings of the 6th German workshop on artificial life, April 14–16, 2004, Bamberg, Germany. IOS Press, Akademische Verlagsgesellschaft, Berlin, Germ.Google Scholar
Bodirsky, M., Groepl, C., and Kang, M. 2003. Generating labeled planar graphs uniformly at random. Pp. 10951107in Automata, Languages and Programming. Springer, Berlin.CrossRefGoogle Scholar
Boyer, J. M., and Myrvold, W. J. 2004. On the cutting edge: simplified O(n) planarity by edge addition. Journal of Graph Algorithms and Applications 8:241273.CrossRefGoogle Scholar
Caro, Y., and Yuster, R. 2000. Graphs with large variance. Ars Combinatoria 57:151162.Google Scholar
Cheverud, J. M. 1996. Developmental integration and the evolution of pleiotropy. American Zoologist 36:4450.CrossRefGoogle Scholar
Cotteau, G. H. 1862. Echinides nouveaux ou peu connus. Revue et Magasin de Zoologie série 3 185201.Google Scholar
Cotteau, G. H. 1867–1874. Paléontologie Française. Terrain Jurassique 9. G. Masson, Paris.Google Scholar
Cotteau, G. H., Péron, P. A., and Gauthier, V. 1873–1891. Echinides fossiles de l’Algérie 2. Etages Tithonique et Néocomien. G. Masson, Paris.Google Scholar
David, B. 1985a. La variation chez les échinides irréguliers: dimensions ontogénétiques, écologiques, évolutives. Ph.D. dissertation, University of Burgundy, Dijon, France.Google Scholar
David, B. 1985b. Significance of architectural patterns in the deep-sea echinoids Pourtalesiidae. Pp. 237243in B. F. Keegan, and B.D.S. O’Connor, eds. Echinodermata. Balkema, Rotterdam.Google Scholar
David, B. 1987. Dynamics of plate growth in the deep-sea echinoid Pourtalesia miranda Agassiz: a new architectural interpretation. Bulletin of Marine Science 40:2947.Google Scholar
David, B. 1988. Origins of the deep-sea holasteroid fauna. Pp. 331346in C. R. C. Paul, and A. B. Smith, eds. Echinoderm phylogeny and evolutionary biology. Clarendon, Oxford.Google Scholar
David, B. 1990. Mosaic pattern of heterochronies: variation and diversity in Pourtalesiidae (deep-sea echinoids). Evolutionary Biology 24:297327.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 (série 3, 319:577584.Google Scholar
David, B., and Mooi, R. 1999. Comprendre les échinodermes: la contribution du modèle extraxial-axial. Bulletin de la Société Géologique de France 170:91101.Google Scholar
David, B., and Mooi, R. 2014. How Hox genes can shed light on the place of echinoderms among the deuterostomes. EvoDevo 5:22.CrossRefGoogle ScholarPubMed
David, B., Lefebvre, B., Mooi, R., and Parsley, R. 2000. Are homalozoans echinoderms?An answer from the extraxial-axial theory. Paleobiology 26:529555.2.0.CO;2>CrossRefGoogle Scholar
David, B., Mooi, R., Néraudeau, D., Saucède, T., and Villier, L. 2009. Evolution et radiations adaptatives chez les échinides. Comptes Rendus Palevol 8:189207.CrossRefGoogle Scholar
Dera, G., Eble, G. J., Neige, P., and David, B. 2008. The flourishing diversity of models in theoretical morphology: from current practices to future macroevolutionary and bioenvironmental challenges. Paleobiology 34:301317.CrossRefGoogle Scholar
Desor, E. 1842. Des Dysaster: monographies d’échinodermes vivans et fossils, par Louis Agassiz. Monograph 4. Petitpierre, Neuchâtel.Google Scholar
Devriès, A. 1960. Contribution à l’étude de quelques groupes d’échinides fossiles d’Algérie. Publications du Service de la Carte Géologique de l’Algérie (nouvelle série). Paléontologie Mémoire 3:1279.Google Scholar
Dommergues, J.-L., Laurin, B., and Meister, C. 1996. Evolution of ammonoid morphospace during the Early Jurassic radiation. Paleobiology 22:219240.CrossRefGoogle Scholar
Eble, G. J. 2000. Contrasting evolutionary flexibility in sister groups: disparity and diversity in Mesozoic atelostomate echinoids. Paleobiology 26:5679.2.0.CO;2>CrossRefGoogle Scholar
Erwin, D. H. 1993. The great Paleozoic crisis: life and death in the Permian. Columbia University Press, New York.Google Scholar
Erwin, D. H. 2007. Disparity: morphological pattern and developmental context. Palaeontology 50:5773.CrossRefGoogle Scholar
Esteve-Altava, B., and Rasskin-Gutman, D. 2014. Theoretical morphology of tetrapod skull networks. Comptes Rendus Palevol 13:4150.CrossRefGoogle Scholar
Esteve‐Altava, B., Marugán‐Lobón, J., Botella, H., and Rasskin‐Gutman, D. 2011. Network models in anatomical systems. Journal of Anthropological Sciences 89:175184.Google ScholarPubMed
Esteve‐Altava, B., Marugán‐Lobón, J., Botella, H., and Rasskin‐Gutman, D. 2013a. Structural constraints in the evolution of the tetrapod skull complexity: Williston’s law revisited using network models. Evolutionary Biology 40:209219.CrossRefGoogle Scholar
Esteve‐Altava, B., Marugán‐Lobón, J., Botella, H., and Rasskin‐Gutman, D. 2013b. Grist for Riedl’s Mill: a network model perspective on the integration and modularity of the human skull. Journal of Experimental Zoology B 320:489500.CrossRefGoogle Scholar
Fischer, A. G. 1966. Spatangoids. Pp. U543U628. in J. W. Durham et al.Echinodermata 3, Asterozoa–Echinozoa. Part U of R. C. Moore, ed. Treatise on invertebrate paleontology. Geological Society of America, New York, and University of Kansas Press, Lawrence.Google Scholar
Foote, M. J. 1993. Discordance and concordance between morphological and taxonomic diversity. Paleobiology 19:185204.CrossRefGoogle Scholar
Geoffroy Saint-Hilaire, E. 1818. Philosophie anatomique. J. B. Baillière, Paris.CrossRefGoogle Scholar
Gordon, I. 1926. The development of the calcareous test of Echinocardium cordatum. Philosophical Transactions of the Royal Society of London 215:255313.Google Scholar
Hosseini, S. M. H., Hoeft, F., and Kesler, S. R. 2012. GAT: a graph-theoretical analysis toolbox for analyzing between-group differences in large-scale structural and functional brain network graphs. PLoS ONE 7:e40709.CrossRefGoogle Scholar
Jeffery, C. H. 1997. Revision of the echinoid Enallopneustes from the Upper Cretaceous of North Africa. Cretaceous Research 18:237248.CrossRefGoogle Scholar
Jesionek-Szymańska, W. 1963. Echinides irréguliers du Dogger de Pologne. Acta Palaeontologica Polonica 8:293414.Google Scholar
Jesionek-Szymańska, W. 1970. On a new pygasterid (Echinoidea) from the Jurassic (middle Lias) of Nevada, U.S.A. Acta Palaeontologica Polonica 15:411423.Google Scholar
Kier, P. M. 1957. Tertiary Echinoidea from British Somaliland. Journal of Paleontology 31:839902.Google Scholar
Kier, P. M. 1974. Evolutionary trends and their functional significance in the post-Paleozoic echinoids. Journal of Paleontology 48:195.CrossRefGoogle Scholar
Kikuchi, Y., and Nikaido, A. 1985. The first occurrence of abyssal echinoid Pourtalesia from the Middle Miocene Tatsukuroiso mudstone in Ibaraki Prefecture, northeastern Honshu, Japan. Annual Report of the Institute of Geoscience, the University of Tsukuba 11:32–34.Google Scholar
Kirschner, M., and Gerhart, J. 1998. Evolvability. Proceedings of the National Academy of Sciences of the United States of America 95:84208427.CrossRefGoogle ScholarPubMed
Kroh, A., Lukeneder, A., and Gallemí, J. 2014. Absurdaster, a new genus of basal atelostomate from the Early Cretaceous of Europe and its phylogenetic position. Cretaceous Research 48:235249.CrossRefGoogle ScholarPubMed
Kroh, A., and Smith, A. B. 2010. The phylogeny and classification of post-Palaeozoic echinoids. Journal of Systematic Palaeontology 8:147212.CrossRefGoogle Scholar
Lambert, J. 1902. Description des echinides fossiles de la province de Barcelone. Mémoire de la Société Géologique de France 24:158.Google Scholar
Laurin, B., and David, B. 1988. L’évolution morphologique: un compromis entre contraintes du développement et ajustements adaptatifs. Comptes Rendus de l’Académie des Sciences de Paris série 2 843849.Google Scholar
Lesne, A. 2006. Complex network graphs: from graph theory to biology. Letters in Mathematical Physics 78:235262.CrossRefGoogle Scholar
Liem, K. F. 1974. Evolutionary strategies and morphological innovations: cichlid pharyngeal jaws. Systematic Zoology 22:425441.CrossRefGoogle Scholar
Masrour, M. 1987. Étude des échinides du Crétacé inférieur de la région de Tarhazoute (Haut-Atlas occidental, Maroc). Unpublished Ph.D. dissertation,University Claude Bernard, Lyon.Google Scholar
Meijere de, J. C. H 1902. Vorläufige Beschreibung der neuen, durch die Siboga-Expedition gesammelten Echiniden. Tijdschrift van de Nederlansche Dierkundige Vereeniging Leiden 2:116.Google Scholar
Mintz, L. W. 1966. The origins, phylogeny, descendants of the echinoid family Disasteridae A. Gras, 1848. Ph.D. dissertation. University of California, Berkeley.Google Scholar
Mooi, R., and David, B. 1996. Phylogenetic analysis of extreme morphologies: deep-sea holasteroid echinoids. Journal of Natural History 30:913953.CrossRefGoogle Scholar
Mooi, R., and David, B. 1997. Skeletal homologies of echinoderms. In J. A. Waters, and C. L. Maples, eds. Geobiology of echinoderms. Paleontological Society Papers 3, 305335. Paleontological Society, Pittsburgh.Google Scholar
Mooi, R., and David, B. 2008. Radial symmetry, the anterior/posterior axis, and echinoderm Hox genes. Annual Review of Ecology Evolution and Systematics 39:4362.CrossRefGoogle Scholar
Mortensen, T. 1950. A monograph of the Echinoidea V, 1. Spatangoida I. C. A. Reitzel, Copenhagen.Google Scholar
Mortensen, T. 1951. A monograph of the Echinoidea (V, 2. Spatangoida II. C. A. Reitzel, Copenhagen.Google Scholar
Moyne, S., Thierry, J., and Angenard, D. 2007. Architectural variability of the test in the genus Collyrites (Echinoidea, Disasteroida) during Middle Jurassic. Annales de Paléontologie 93:233247.CrossRefGoogle Scholar
Navarro, N. 2003. MDA: a MATLAB-based program for morphospace-disparity analysis. Computers and Geosciences 29:655664.CrossRefGoogle Scholar
Newman, M. E. J., Watts, D. J., and Strogatz, S.H. 2002. Random graph models of social network graphs. Proceedings of the National Academy of Sciences USA 99:25662572.CrossRefGoogle Scholar
Olson, E. C., and Miller, R. L. 1958. Morphological integration. University of Chicago Press, Chicago.Google Scholar
Pennant, T. 1777. British zoology.Vol. IV.Crustacea. Mollusca. Testacea. White, London.Google Scholar
Peterson, K. J., Arenas-Mena, C., and Davidson, E. H. 2000. The A/P axis in echinoderm ontogeny and evolution: evidence from fossils and molecules. Evolution and Development 2:93101.CrossRefGoogle ScholarPubMed
Poslavskaya, N. A., and Moskvin, M. M. 1960. Echinoids of the order Spatangoida in Danian and adjacent deposits of Crimea, Caucasus and the Transcaspian Region. Pp. 4782in A. L. Yanshin, and V. V. Menner, eds. International Geological Congress 21st session. Reports of Soviet Geologists, Problem 5: the Cretaceous-Tertiary boundary. Publishing House of the Academy of Sciences of the USSR, Moscow.Google Scholar
Poslavskaya, N. A., and Solovjev, A. N. 1964. Class Echinoidea: sea urchins. Order Spatangoida. Pp. 174189in Y. Orlov, ed. Principles of paleontology: Echinodermata, Hemichordata, Pogonophora, Chaetognatha. Nedra, Moscow.Google Scholar
R Development Core Team 2011. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna.Google Scholar
Rasskin-Gutman, D. 2003. Boundary constraints for the emergence of form. Pp. 305322in G. B. Müller and S. A. Newman, eds. Origination of organismal form: beyond the gene in developmental and evolutionary biology (Vienna Series in Theoretical Biology). MIT Press, Cambridge.CrossRefGoogle Scholar
Rasskin-Gutman, D. 2005. Modularity: jumping forms within morphospace. Pp. 207219in W. Callebaut and D. Rasskin‐Gutman, eds. Modularity: understanding the development and evolution of natural complex systems. MIT Press, Cambridge.CrossRefGoogle Scholar
Rasskin-Gutman, D., and Buscalioni, A. D. 2001. Theoretical morphology of the archosaur (Reptilia: Diapsida) pelvic girdle. Paleobiology 27:5978.2.0.CO;2>CrossRefGoogle Scholar
Rasskin-Gutman, D., and Esteve-Altava, B. 2014. Connecting the dots: anatomical network analysis in morphological EvoDevo. Biological Theory 9:178194.CrossRefGoogle Scholar
Rieppel, O. C. 1988. Fundamentals of comparative biology. Birkhäuser, Basel.Google Scholar
Roy, K., and Foote, M. 1997. Morphological approaches to measuring biodiversity. Trends in Ecology and Evolution 12:277281.CrossRefGoogle ScholarPubMed
Samadi, S., and Barberousse, A. 2006. The tree, the network graph, and the species. Biological Journal of the Linnean Society 89:509521.CrossRefGoogle Scholar
Saucède, T., David, B., and Mooi, R. 2003. The strange apical system of the genus Pourtalesia (Holasteroida, Echinoidea). Pp. 131136in J.-P. Féral and B. David, eds. Echinoderm research 2001. Balkema, Lisse, The Netherlands.Google Scholar
Saucède, T., Mooi, R., and David, B. 2004. Evolution to the extreme: origins of the highly modified apical system in pourtalesiid echinoids. Zoological Journal of the Linnean Society 140:137155.CrossRefGoogle Scholar
Saucède, T., Mooi, R., and David, B. 2007. Phylogeny and origin of Jurassic irregular echinoids (Echinodermata: Echinoidea). Geological Magazine 144:333359.CrossRefGoogle Scholar
Saucède, T., Mironov, A. N., Mooi, R., and David, B. 2009. The morphology, ontogeny, and inferred behaviour of the deep-sea echinoid Calymne relicta (Holasteroida). Zoological Journal of the Linnean Society 155:630648.CrossRefGoogle Scholar
Smith, A. B. 1984. Echinoid paleobiology (Special Topics in Palaeontology). Allen and Unwin, London.Google Scholar
Smith, A. B. 2004. Phylogeny and systematics of holasteroid echinoids and their migration into the deep-sea. Palaeontology 47:123150.CrossRefGoogle Scholar
Smith, A. B., and Anzalone, L. 2000. Loriolella, a key taxon for understanding the early evolution of irregular echinoids. Palaeontology 43:303324.CrossRefGoogle Scholar
Smith, A. B., and Jeffery, C. H. 2000. Maastrichtian and Palaeocene echinoids: a key to world faunas. Special Papers in Palaeontology 63:1406.Google Scholar
Smith, A. B., and Kroh, A. 2011. The echinoid directory. http://www.nhm.ac.uk/research-curation/projects/echinoid-directory [accessed 2014].Google Scholar
Smith, A. B., and Wright, C. W. 2003. British Cretaceous echinoids. Part 7, Atelostomata, 1. Holasteroida. Monographs of the Palaeontographical Society 156:440568.CrossRefGoogle Scholar
Smith, A. B., Gallemi., J., Jeffery, C. H., Ernst, G., and Ward, P. D. 1999. Late Cretaceous-early Tertiary echinoids from northern Spain: implications for the Cretaceous-Tertiary extinction event. Bulletin of the Natural History Museum, London (Geology Series) 55:81137.Google Scholar
Solovjev, A. N. 1971. Late Jurassic and Early Cretaceous disasterids of the USSR. Transactions of the Palaeontological Institute, Academy of Sciences of the USSR 131:1120.Google Scholar
Solovjev, A. N. 1974. Evolutionary features of the suborder Meridosternina (Echinoidea) and origin of the deep-water families Urechinidae and Pourtalesiidae. Pp. 60in The biology of marine molluscs and echinoderms. Soviet-Japanese symposium on marine biology. Far East Centre, USSR Academy of Sciences, Vladivostok.Google Scholar
Solovjev, A. N. 1994. Evolutionary trends of the fossil holasteroid echinoids with subanal fasciole. Pp. 877880in B. David, A. Guille, J.-P. Féral, and M. Roux, eds. Echinoderms through time (Echinoderms Dijon). Balkema, Rotterdam.Google Scholar
Thierry, J., and Néraudeau, D. 1994. Variations in Jurassic echinoid diversity at ammonite zone levels: stratigraphical and palaeoecological significance. Pp. 901909in B. David, A. Guille, J.-P. Féral, and M. Roux, eds. Echinoderms through time (Echinoderms Dijon). Balkema, Rotterdam.Google Scholar
Vermeij, G. J. 1974. Marine faunal dominance and molluscan shell form. Evolution 28:656664.CrossRefGoogle ScholarPubMed
Villier, L. 2001). Evolution du genre Heteraster dans le contexte de la radiation de l’ordre des Spatangoida (Echinoidea, Echinodermata) au Crétacé inférieur. Ph.D. dissertation. University of Burgundy, Dijon, France.Google Scholar
Villier, L., Néraudeau, D., Clavel, B., Neumann, C., and David, B. 2004. Phylogeny and early Cretaceous spatangoids (Echinodermata: Echinoidea) and taxonomic implications. Palaeontology 47:265292.CrossRefGoogle Scholar
Wagner, G. P., and Altenberg, L. 1996. Complex adaptations and the evolution of evolvability. Evolution 50:967976.CrossRefGoogle ScholarPubMed
Wagner, C. D., and Durham, J. W. 1966. Holasteroids. Pp. U523U543in J. W. Durham et al., Echinodermata 3, Asterozoa–Echinozoa. Part U of R. C. Moore, ed. Treatise on invertebrate paleontology. Geological Society of America. New York, and University of Kansas Press, Lawrence.Google Scholar
Wake, D. B. 1989. Homoplasy: the result of natural selection, or evidence of design limitations. American Naturalist 138:543567.CrossRefGoogle Scholar
Wills, M. A., Briggs, D. E. G., and Fortey, R. A. 1994. Disparity as an evolutionary index—a comparison of Cambrian and Recent arthropods. Paleobiology 20:93130.CrossRefGoogle Scholar
Zachos, L. G., and Sprinkle, J. 2011. Computational model of growth and development in Paleozoic echinoids. Pp. 7593in A. M. T. Elewa, ed. Computational paleontology. Springer, Berlin.CrossRefGoogle Scholar