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Molecular Paleobiology of the Echinoderm Skeleton

Published online by Cambridge University Press:  04 November 2022

Jeffrey R. Thompson
Affiliation:
University of Southampton

Summary

The echinoderms are an ideal group to understand evolution from a holistic, interdisciplinary framework. The genetic regulatory networks underpinning development in echinoderms are some of the best known for any model group. Additionally, the echinoderms have an excellent fossil record, elucidating in in detail the evolutionary changes underpinning morphological evolution. In this Element, the echinoderms are discussed as a model group for molecular palaeobiological studies, integrating what is known of their development, genomes, and fossil record. Together, these insights shed light on the molecular and morphological evolution underpinning the vast biodiversity of echinoderms, and the animal kingdom more generally.
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Online ISBN: 9781009179768
Publisher: Cambridge University Press
Print publication: 01 December 2022

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References

Adomako-Ankomah, A. & Ettensohn, C. A. 2013. Growth factor-mediated mesodermal cell guidance and skeletogenesis during sea urchin gastrulation. Development, 140, 42144225.CrossRefGoogle ScholarPubMed
Adomako-Ankomah, A. & Ettensohn, C. A. 2014. Growth factors and early mesoderm morphogenesis: Insights from the sea urchin embryo. Genesis, 52, 158172.Google Scholar
Ameye, L., Hermann, R., Killian, C., Wilt, F. & Dubois, P. 1999. Ultrastructural localization of proteins involved in sea urchin biomineralization. Journal of Histochemistry & Cytochemistry, 47, 11891200.Google Scholar
Anstrom, J. A., Chin, J., Leaf, D. S., Parks, A. L. & Raff, R. A. 1987. Localization and expression of msp130, a primary mesenchyme lineage-specific cell surface protein in the sea urchin embryo. Development, 101, 255265.CrossRefGoogle ScholarPubMed
Arenas-Mena, C., Cameron, A. R. & Davidson, E. H. 2000. Spatial expression of Hox cluster genes in the ontogeny of a sea urchin. Development, 127, 46314643.Google Scholar
Arenas-Mena, C., Martinez, P., Cameron, R. A. & Davidson, E. H. 1998. Expression of the Hox gene complex in the indirect development of a sea urchin. Proceedings of the National Academy of Sciences, 95, 1306213067.CrossRefGoogle ScholarPubMed
Arendt, D. 2008. The evolution of cell types in animals: Emerging principles from molecular studies. Nature Reviews Genetics, 9, 868882.Google Scholar
Arendt, D., Musser, J. M., Baker, C. V. et al. 2016. The origin and evolution of cell types. Nature Reviews Genetics, 17, 744757.Google Scholar
Armstrong, A. F. & Grosberg, R. K. 2018. The developmental transcriptomes of two sea biscuit species with differing larval types. BMC Genomics, 19, 19.Google Scholar
Barsi, J. C., Tu, Q., Calestani, C. & Davidson, E. H. 2015. Genome-wide assessment of differential effector gene use in embryogenesis. Development, 142, 38923901.Google ScholarPubMed
Barsi, J. C., Tu, Q. & Davidson, E. H. 2014. General approach for in vivo recovery of cell type-specific effector gene sets. Genome Research, 24, 860868.Google Scholar
Bauer, J. E. 2021. Paleobiogeography, paleoecology, diversity, and speciation patterns in the Eublastoidea (Blastozoa: Echinodermata). Paleobiology, 47, 115.Google Scholar
Baughman, K. W., Mcdougall, C., Cummins, S. F. et al. 2014. Genomic organization of Hox and Para Hox clusters in the echinoderm, Acanthaster planci. Genesis, 52, 952958.Google Scholar
Boivin, S., Saucède, T., Laffont, R., Steimetz, E. & Neige, P. 2018. Diversification rates indicate an early role of adaptive radiations at the origin of modern echinoid fauna. Plos One, 13, e0194575.Google Scholar
Borges, R., Machado, J. P., Gomes, C., Rocha, A. P. & Antunes, A. 2019. Measuring phylogenetic signal between categorical traits and phylogenies. Bioinformatics, 35, 18621869.Google Scholar
Bottjer, D. J. 2017. Geobiology and palaeogenomics. Earth Science Reviews, 164, 182192.Google Scholar
Bottjer, D. J., Davidson, E. H., Peterson, K. J. & Cameron, R. A. 2006. Paleogenomics of echinoderms. Science, 314, 956960.Google Scholar
Brennand, H. S., Soars, N., Dworjanyn, S. A., Davis, A. R. & Byrne, M. 2010. Impact of ocean warming and ocean acidification on larval development and calcification in the sea urchin Tripneustes gratilla. PloS One, 5, e11372.CrossRefGoogle Scholar
Byrne, M., Ho, M. A., Koleits, L. et al.2013. Vulnerability of the calcifying larval stage of the Antarctic sea urchin Sterechinus neumayeri to near‐future ocean acidification and warming. Global Change Biology, 19, 22642275.Google Scholar
Byrne, M., Ho, M., Wong, E. et al. 2011. Unshelled abalone and corrupted urchins: Development of marine calcifiers in a changing ocean. Proceedings of the Royal Society B: Biological Sciences, 278, 23762383.Google Scholar
Byrne, M., Koop, D., Morris, V. B. et al. 2018. Expression of genes and proteins of the pax‐six‐eya‐dach network in the metamorphic sea urchin: Insights into development of the enigmatic echinoderm body plan and sensory structures. Developmental Dynamics, 247, 239249.Google Scholar
Byrne, M., Koop, D., Strbenac, D. et al. 2020. Transcriptomic analysis of sea star development through metamorphosis to the highly derived pentameral body plan with a focus on neural transcription factors. DNA Research, 27,dsaa007.Google Scholar
Byrne, M., Martinez, P. & Morris, V. 2016. Evolution of a pentameral body plan was not linked to translocation of anterior Hox genes: The echinoderm HOX cluster revisited. Evolution & Development, 18, 137143.Google Scholar
Byrne, M. & Selvakumaraswamy, P. 2002. Phylum echinodermata: Ophiuroidea. In Young, C. M., Sewell, M. A. & Rice, M. E. (eds.) Atlas of marine invertebrate larvae. San Diego: Academic Press, 483–498.Google Scholar
Cameron, C. & Bishop, C. 2012. Biomineral ultrastructure, elemental constitution and genomic analysis of biomineralization-related proteins in hemichordates. Proceedings of the Royal Society B: Biological Sciences, 279, 30413048.CrossRefGoogle ScholarPubMed
Cameron, R. A., Rowen, L., Nesbitt, R. et al. 2006. Unusual gene order and organization of the sea urchin hox cluster. Journal of Experimental Zoology Part B: Molecular and Developmental Evolution, 306, 4558.CrossRefGoogle ScholarPubMed
Cannon, J. T., Kocot, K. M., Waits, D. S. et al. 2014. Phylogenomic resolution of the hemichordate and echinoderm clade. Current Biology, 24, 28272832.Google Scholar
Carter, H. F., Thompson, J. R., Elphick, M. R. & Oliveri, P. 2021. The development and neuronal complexity of bipinnaria larvae of the sea star Asterias rubens. Integrative and Comparative Biology, 61, 337351.Google Scholar
Cary, G. A., Mccauley, B. S., Zueva, O. et al. 2020. Systematic comparison of sea urchin and sea star developmental gene regulatory networks explains how novelty is incorporated in early development. Nature communications, 11(1), 1–9. .Google Scholar
Cheers, M. S. & Ettensohn, C. A. 2005. P16 is an essential regulator of skeletogenesis in the sea urchin embryo. Developmental Biology, 283, 384396.CrossRefGoogle ScholarPubMed
Chiaramonte, M., Russo, R., Costa, C., Bonaventura, R. & Zito, F. 2020. PI3K inhibition highlights new molecular interactions involved in the skeletogenesis of Paracentrotus lividus embryos. Biochimica et Biophysica Acta (BBA)-Molecular Cell Research, 1867, 118558.Google Scholar
Chipman, A. D. & Edgecombe, G. D. 2019. Developing an integrated understanding of the evolution of arthropod segmentation using fossils and evo-devo. Proceedings of the Royal Society B, 286, 20191881.Google Scholar
Chow, G. & Benson, S. C. 1979. Carbonic anhydrase activity in developing sea urchin embryos. Experimental Cell Research, 124, 451453.Google Scholar
Clark, E. G., Hutchinson, J. R., Bishop, P. J. & Briggs, D. E. 2020. Arm waving in stylophoran echinoderms: Three-dimensional mobility analysis illuminates cornute locomotion. Royal Society Open Science, 7, 200191.Google Scholar
Cole, S. R., Wright, D. F. & Ausich, W. I. 2019. Phylogenetic community paleoecology of one of the earliest complex crinoid faunas (Brechin Lagerstätte, Ordovician). Palaeogeography, Palaeoclimatology, Palaeoecology, 521, 8298.Google Scholar
Costa, C., Karakostis, K., Zito, F. & Matranga, V. 2012. Phylogenetic analysis and expression patterns of p16 and p19 in Paracentrotus lividus embryos. Development Genes and Evolution, 222, 245251.Google Scholar
Croce, J., Lhomond, G., Lozano, J.-C. & Gache, C. 2001. ske-T, a T-box gene expressed in the skeletogenic mesenchyme lineage of the sea urchin embryo. Mechanisms of Development, 107, 159162.Google Scholar
Czarkwiani, A., Dylus, D. V., Carballo, L. & Oliveri, P. 2021. FGF signalling plays similar roles in development and regeneration of the skeleton in the brittle star Amphiura filiformis. Development, 148(10), dev180760.Google Scholar
Czarkwiani, A., Dylus, D. V. & Oliveri, P. 2013. Expression of skeletogenic genes during arm regeneration in the brittle star Amphiura filiformis. Gene Expression Patterns, 13, 464472.Google Scholar
David, B. & Mooi, R. 2014. How Hox genes can shed light on the place of echinoderms among the deuterostomes. EvoDevo, 5, 22.Google Scholar
Davidson, E. H. 2006. The regulatory genome: Gene regulatory networks in development and evolution, Elsevier.Google Scholar
Davidson, E. H. & Erwin, D. H. 2006. Gene regulatory networks and the evolution of animal body plans. Science, 311, 796800.CrossRefGoogle ScholarPubMed
Davidson, P. L., Guo, H., Wang, L. et al. 2020. Chromosomal-level genome assembly of the sea urchin Lytechinus variegatus substantially improves functional genomic analyses. Genome Biology and Evolution, 12, 1080–1086.Google Scholar
Davidson, E. H. & Levine, M. S. 2008. Properties of developmental gene regulatory networks. Proceedings of the National Academy of Sciences, 105, 2006320066.Google Scholar
Davidson, E. H., Rast, J. P., Oliveri, P. et al. 2002a. A genomic regulatory network for development. Science, 295, 16691678.CrossRefGoogle ScholarPubMed
Davidson, E. H., Rast, J. P., Oliveri, P. et al. 2002b. A provisional regulatory gene network for specification of endomesoderm in the sea urchin embryo. Developmental Biology, 246, 162190.Google Scholar
Deflandre-Rigaud, M. 1946. Vestiges microscopiques des larves d’echinodermes de l’Oxfordien de Viller-sur-Mer. CR Acad. Sci. Paris, 222, 908910.Google Scholar
Deline, B. & Ausich, W. 2011. Testing the plateau: A reexamination of disparity and morphologic constraints in early Paleozoic crinoids. Paleobiology, 37, 214236.Google Scholar
Deline, B., Thompson, J. R., Smith, N. S. et al. 2020. Evolution and development at the origin of a phylum. Current Biology, 30, 1672–1679.Google Scholar
Dubois, P. & Jangoux, M. 1990. Stereom morphogenesis and differentiation during regeneration of adambulacral spines of Asterias rubens (Echinodermata, Asteroida). Zoomorphology, 109, 263272.Google Scholar
Duloquin, L., Lhomond, G. & Gache, C. 2007. Localized VEGF signaling from ectodetm to mesenchyme cells controls morphogenesis of the sea urchin embryo skeleton. Development, 134, 22932302.Google Scholar
Dylus, D. V., Blowes, L. M., Czarkwiani, A., Elphick, M. R. & Oliveri, P. 2018. Developmental transcriptomics of the brittle star Amphiura filiformis reveals gene regulatory network rewiring in echinoderm larval skeleton evolution. Genome Biology, 19, 26.Google Scholar
Dylus, D. V., Czarkwiani, A., Stångberg, J. et al. 2016. Large-scale gene expression study in the ophiuroid Amphiura filiformis provides insights into evolution of gene regulatory networks. Evodevo, 7, 1.CrossRefGoogle ScholarPubMed
Edgar, A., Byrne, M., Mcclay, D. R. & Wray, G. A. 2019a. Evolution of abbreviated development in Heliocidaris erythrogramma dramatically re-wired the highly conserved sea urchin developmental gene regulatory network to decouple signaling center function from ultimate fate. BioRxiv, 712216.Google Scholar
Edgar, A., Byrne, M. & Wray, G. A. 2019b. Embryo microinjection of the lecithotrophic sea urchin Heliocidaris erythrogramma. Journal of Biological Methods, 6, e119.Google Scholar
Erkenbrack, E. M., Ako-Asare, K., Miller, E. et al. 2016. Ancestral state reconstruction by comparative analysis of a GRN kernel operating in echinoderms. Development Genes and Evolution, 226, 3745.Google Scholar
Erkenbrack, E. M. & Davidson, E. H. 2015. Evolutionary rewiring of gene regulatory network linkages at divergence of the echinoid subclasses. Proceedings of the National Academy of Sciences, 112, E4075E4084.Google Scholar
Erkenbrack, E. M. & Petsios, E. 2017. A conserved role for VEGF signaling in specification of homologous mesenchymal cell types positioned at spatially distinct developmental addresses in early development of sea urchins. Journal of Experimental Zoology Part B: Molecular and Developmental Evolution, 328, 423432.Google Scholar
Erkenbrack, E. M. & Thompson, J. R. 2019. Cell type phylogenetics informs the evolutionary origin of echinoderm larval skeletogenic cell identity. Communications Biology, 2, 160.Google Scholar
Erwin, D. H. 2020. The origin of animal body plans: A view from fossil evidence and the regulatory genome. Development, 147, dev182899.Google Scholar
Erwin, D. H. & Davidson, E. H. 2009. The evolution of hierarchical gene regulatory networks. Nature Reviews Genetics, 10, 141148.Google Scholar
Ettensohn, C. A. 2009. Lessons from a gene regulatory network: Echinoderm skeletogenesis provides insights into evolution, plasticity and morphogenesis. Development, 136, 1121.Google Scholar
Ettensohn, C. A. 2014. Horizontal transfer of the msp130 gene supported the evolution of metazoan biomineralization. Evolution & Development, 16, 139148.Google Scholar
Ettensohn, C. A. & Dey, D. 2017. KirrelL, a member of the lg-domain superfamily of adhesion proteins, is essential for fusion of primary mesenchyme cells in the sea urchin embryo. Developmental Biology, 421, 258270.Google Scholar
Ettensohn, C. A., Illies, M. R., Oliveri, P. & De jong, D. L. 2003. Alx1, a member of the Cart1/Alx3/Alx4 subfamily of Paired-class homeodomain proterins, is an essential component of the gene regulatory network controlling skeletogenic fate specification in the sea urchin embryo. Development, 130, 29172928.Google Scholar
Fleming, J. F., Kristensen, R. M., Sørensen, M. V. et al. 2018. Molecular palaeontology illuminates the evolution of ecdysozoan vision. Proceedings of the Royal Society B, 285, 20182180.Google Scholar
Foote, M. 1991. Morphological and Taxonomic diversity in a clade’s history: The blastoid record and stochastic simulations. Contributions from the museum of Paleontology The University of Michigan, 28, 101140.Google Scholar
Foote, M. 1992. Paleozoic record of morphological diversity in blastozoan echinoderms. Proceedings of the National Academy of Sciences of the United States of America, 89, 73257329.Google Scholar
Gao, F. & Davidson, E. H. 2008. Transfer of a large gene regulatory apparatus to a new developmental address in echinoid evolution. Proceedings of the National Academy of Sciences, 105, 60916096.Google Scholar
Gao, F., Thompson, J. R., Petsios, E. et al. 2015. Juvenile skeletogenesis in anciently diverged sea urchin clades. Developmental Biology, 400, 148158.Google Scholar
Garner, S., Zysk, I., Byrne, G. et al. 2016. Neurogenesis in sea urchin embryos and the diversity of deuterostome neurogenic mechanisms. Development, 143, 286297.Google Scholar
Garwood, R. J., Sharma, P. P., Dunlop, J. A. & Giribet, G. 2014. A Paleozoic stem group to mite harvestmen revealed through integration of phylogenetics and development. Current Biology, 24, 10171023.Google Scholar
Gilbert, S. F. 2006. Developmental biology. 8th ed. Sunderland, MA: Sinauer Associates.Google Scholar
Gliznutsa, L. & Dautov, S. S. 2011. Cell differentiation during the larval development of the ophiuroid Amphipholis kochii Lütken, 1872 (Echinodermata: Ophiuroidea). Russian Journal of Marine Biology, 37, 384400.CrossRefGoogle Scholar
Gorzelak, P. 2021. Functional micromorphology of the echinoderm skeleton. Cambridge Elements.Google Scholar
Grun, T. B. & Nebelsick, J. H. 2018. Structural design of the minute clypeasteroid echinoid Echinocyamus pusillus. Royal Society Open Science, 5, 171323.Google Scholar
Guss, K. & Ettensohn, C. A. 1997a. Skeletal morphogenesis in the sea urchin embryo: Regulation of primary mesenchyme gene expression and skeletal rod growth by ectoderm-derived cues. Development, 124, 18991908.Google Scholar
Guss, K. A. & Ettensohn, C. A. 1997b. Skeletal morphogenesis in the sea urchin embryo: Regulation of primary mesenchyme gene expression and skeletal rod growth by ectoderm-derived cues. Development, 124, 18991908.CrossRefGoogle ScholarPubMed
Hara, Y., Yamaguchi, M., Akasaka, K. et al. 2006. Expression patterns of Hox genes in larvae of the sea lily Metacrinus rotundus. Development Genes and Evolution, 216, 797809.Google Scholar
Hart, M. W., Byrne, M. & Smith, M. J. 1997. Molecular phylogenetic analysis of life‐history evolution in asterinid starfish. Evolution, 51, 18481861.Google Scholar
Haude, R. & Langenstrassen, F. 1976. Rotasaccus dentifer n. g. n. sp., ein devonischer Ophiocistioide (Echinodermata) mit “holothuroiden” Wandskleriten und “echinoidem” Kauapparat. Paläontologische Zeitschrift, 50, 130150.Google Scholar
Heatfield, B. M. & Travis, D. F. 1975. Ultrastructural studies of regenerating spines of the sea urchin Strongylocentrotus purpuratus I. Cell types without spherules. Journal of Morphology, 145, 1349.Google Scholar
Hinman, V. F., Nguyen, A. T., Cameron, R. A. & Davidson, E. H. 2003. Developmental gene regulatory network architecture across 500 million years of echinoderm evolution. Proceedings of the National Academy of Sciences of the United States of America, 100, 1335613361.Google Scholar
Hopkins, M. J. & Smith, A. B. 2015. Dynamic evolutionary change in post-Paleozoic echinoids and the importance of scale when interpreting changes in rates of evolution. Proceedings of the National Academy of Sciences, 112, 37583763.Google Scholar
Howard, R. J., Puttick, M. N., Edgecombe, G. D. & Lozano-Fernandez, J. 2020. Arachnid monophyly: Morphological, palaeontological and molecular support for a single terrestrialization within Chelicerata. Arthropod Structure & Development, 59, 100997.Google Scholar
Jell, P. A. 1983. Early Devonian echinoderms from Victoria (Rhombifera, Blastoidea and Ophiocistioidea). Memoir of the Association of Australasian Palaeontologists, 1, 209235.Google Scholar
Khor, J. M. & Ettensohn, C. A. 2017. Functional divergence of paralogous transcription factors supported the evolution of biomineralization in echinoderms. Elife, 6, e32728.Google Scholar
Khor, J. M. & Ettensohn, C. A. 2020. Transcription factors of the Alx family: Evolutionarily conserved regulators of deuterostome skeletogenesis. Frontiers in Genetics, 11, 1405.Google Scholar
Khor, J. M., Guerrero-Santoro, J. & Ettensohn, C. A. 2019. Genome-wide identification of binding sites and gene targets of Alx1, a pivotal regulator of echinoderm skeletogenesis. Development, 146, dev180653.Google Scholar
Kikuchi, M., Omori, A., Kurokawa, D. & Akasaka, K. 2015. Patterning of anteroposterior body axis displayed in the expression of Hox genes in sea cucumber Apostichopus japonicus. Development Genes and Evolution, 225, 275286.Google Scholar
Killian, C. E. & Wilt, F. H. 2008. Molecular aspects of biomineralization of the echinoderm endoskeleton. Chemical Reviews, 108, 44634474.Google Scholar
Koga, H., Fujitani, H., Morino, Y. et al. 2016. Experimental approach reveals the role of alx1 in the evolution of the echinoderm larval skeleton. PLoS One, 11, e0149067.Google Scholar
Koga, H., Matsubara, M., Fujitani, H. et al. 2010. Functional evolution of Ets in echinoderms with focus on the evolution of echinoderm larval skeletons. Development Genes and Evolution, 220, 107115.CrossRefGoogle ScholarPubMed
Koga, H., Morino, Y. & Wada, H. 2014. The echinoderm larval skeleton as a possible model system for experimental evolutionary biology. Genesis, 52, 186192.Google Scholar
Koop, D., Cisternas, P., Morris, V. B. et al. 2017. Nodal and BMP expression during the transition to pentamery in the sea urchin Heliocidaris erythrogramma: Insights into patterning the enigmatic echinoderm body plan. BMC Developmental Biology, 17, 113.Google Scholar
Kurokawa, D., Kitajima, T., Mitsunaga-Nakatsubo, K. et al. 1999. HpEts, an ets-related transcription factor implicated in primary mesenchyme cell differentiation in the sea urchin embryo. Mechanisms of Development, 80, 4152.Google Scholar
Leaf, D. S., Anstrom, J. A., Chin, J. E. et al. 1987. Antibodies to a fusion protein identify a cDNA clone encoding msp130, a primary mesenchyme-specific cell surface protein of the sea urchin embryo. Developmental Biology, 121, 2940.Google Scholar
Levine, M. & Davidson, E. H. 2005. Gene regulatory networks for development. Proceedings of the National Academy of Sciences, 102, 49364942.Google Scholar
Li, Y., Omori, A., Flores, R. L. et al. 2020. Genomic insights of body plan transitions from bilateral to pentameral symmetry in Echinoderms. Communications Biology, 3, 110.CrossRefGoogle ScholarPubMed
Liu, D., Awazu, A., Sakuma, T., Yamamoto, T. & Sakamoto, N. 2019. Establishment of knockout adult sea urchins by using a CRISPR‐Cas9 system. Development, Growth & Differentiation, 61, 378388.Google Scholar
Livingston, B. T., Killian, C. E., Wilt, F. H. et al. 2006. A genome-wide analysis of biomineralization-related proteins in the sea urchin Strongylocentrotus purpuratus. Developmental Biology, 300, 335348.Google Scholar
Lozano-Fernandez, J., Carton, R., Tanner, A. R. et al. 2016. A molecular palaeobiological exploration of arthropod terrestrialization. Philosophical Transactions of the Royal Society B: Biological Sciences, 371, 20150133.Google Scholar
Mallo, M., Wellik, D. M. & DESCHAMPS, J. 2010. Hox genes and regional patterning of the vertebrate body plan. Developmental Biology, 344, 715.Google Scholar
Mann, K., Poustka, A. J. & Mann, M. 2008a. In-depth, high-accuracy proteomics of sea urchin tooth organic matrix. Proteome Science, 6, 33.CrossRefGoogle ScholarPubMed
Mann, K., Poustka, A. J. & Mann, M. 2008b. The sea urchin (Strongylocentrotus purpuratus) test and spine proteomes. Proteome Science, 6, 110.Google Scholar
Mann, K., Wilt, F. H. & Poustka, A. J. 2010. Proteomic analysis of sea urchin (Strongylocentrotus purpuratus) spicule matrix. Proteome Science, 8, 112.Google Scholar
Marie, B., Zanella-Cléon, I., Guichard, N., Becchi, M. & Marin, F. 2011. Novel proteins from the calcifying shell matrix of the Pacific oyster Crassostrea gigas. Marine Biotechnology, 13, 11591168.Google Scholar
Märkel, K., Röser, U., Mackenstedt, U. & Klostermann, M. 1986. Ultrastructural investigation of matrix-mediated biomineralization in echinoids (Echinodermata, Echinoida). Zoomorphology, 106, 232243.Google Scholar
Märkel, K., Röser, U. & Stauber, M. 1989. On the ultrastructure and the supposed function of the mineralizing matrix coat of sea urchins (Echinodermata, Echinoida). Zoomorphology, 109, 7987.Google Scholar
Martinez, P., Rast, J. P., Arenas-Mena, C. & Davidson, E. H. 1999. Organization of an echinoderm Hox gene cluster. Proceedings of the National Academy of Sciences, 96, 14691474.Google Scholar
Mccauley, B. S., Wright, E. P., Exner, C., Kitazawa, C. & Hinman, V. F. 2012. Development of an embryonic skeletogenic mesenchyme lineage in a sea cucumber reveals the trajectory of change for the evolution of novel structures in echinoderms. EvoDevo, 3, 17.Google Scholar
Mcclay, D. R., Warner, J., Martik, M., Miranda, E. & Slota, L. 2020. Gastrulation in the sea urchin. Current Topics in Developmental Biology, 136, 195218.Google Scholar
Mcedward, L. R. & Miner, B. G. 2001. Larval and life-cycle patterns in echinoderms. Canadian Journal of Zoology, 79, 11251170.Google Scholar
Minokawa, T., Hamaguchi, Y. & Amemiya, S. 1997. Skeletogenic potential of induced secondary mesenchyme cells derived from the presumptive ectoderm in echinoid embryos. Development Genes and Evolution, 206, 472476.Google Scholar
Minsuk, S. B., Turner, F. R., Andrews, M. E. & Raff, R. A. 2009. Axial patterning of the pentaradial adult echinoderm body plan. Development Genes and Evolution, 219, 89101.Google Scholar
Mitsunaga, K., Akasaka, K., Shimada, H. et al. 1986. Carbonic anhydrase activity in developing sea urchin embryos with special reference to calcification of spicules. Cell Differentiation, 18, 257262.Google Scholar
Molina, M. D., De Crozé, N., Haillot, E. & Lepage, T. 2013. Nodal: Master and commander of the dorsal–ventral and left–right axes in the sea urchin embryo. Current Opinion in Genetics & Development, 23, 445453.CrossRefGoogle ScholarPubMed
Mongiardino Koch, N., Coppard, S. E., Lessios, H. A. et al. 2018. A phylogenomic resolution of the sea urchin tree of life. BMC Evolutionary Biology, 18, 189.Google Scholar
Mongiardino Koch, N. (2021). Exploring adaptive landscapes across deep time: A case study using echinoid body size. Evolution, 75(6), 1567–1581.Google Scholar
Mongiardino Koch, N. & Thompson, J. R. 2021. A Total-evidence dated phylogeny of echinoidea combining phylogenomic and paleontological data. Systematic Biology, 70, 421–439Google Scholar
Mooi, R. & David, B. 1994. Echinoderm skeletal homologies: Classical morphology meets modern phylogenetics. In David, B., Guille, A., Féral, J.-P. & Roux, M. (eds.) Echinoderms through time. Rotterdam: A. A. Balkema, 87–95.Google Scholar
Mooi, R. & David, B. 2008. Radial symmetry, the anterior/posterior axis, and echinoderm Hox genes. Annual Review of Ecology, Evolution, and Systematics, 39, 4362.Google Scholar
Mooi, R., David, B. & Wray, G. A. 2005. Arrays in rays: Terminal addition in echinoderms and its correlation with gene expression. Evolution & Development, 7, 542555.Google Scholar
Morgulis, M., Gildor, T., Roopin, M. et al. 2019. Possible cooption of a VEGF-driven tubulogenesis program for biomineralization in echinoderms. Proceedings of the National Academy of Sciences, 116, 12353–12362.Google Scholar
Morino, Y., Koga, H., Tachibana, K. et al. 2012. Heterochronic activation of VEGF signaling and the evolution of the skeleton in echinoderm pluteus larvae. Evolution & Development, 14, 428436.Google Scholar
Morris, V. B. 2007. Origins of radial symmetry identified in an echinoderm during adult development and the inferred axes of ancestral bilateral symmetry. Proceedings of the Royal Society B: Biological Sciences, 274, 15111516.Google Scholar
Morris, V. B. 2009. On the sites of secondary podia formation in a juvenile echinoid: Growth of the body types in echinoderms. Development Genes and Evolution, 219, 597608.Google Scholar
Morris, V. B. 2011. Coelomogenesis during the abbreviated development of the echinoid Heliocidaris erythrogramma and the developmental origin of the echinoderm pentameral body plan. Evolution & Development, 13, 370381.Google Scholar
Morris, V. B. 2012. Early development of coelomic structures in an echinoderm larva and a similarity with coelomic structures in a chordate embryo. Development Genes and Evolution, 222, 313323.Google Scholar
Morris, V. B. & Byrne, M. 2005. Involvement of two Hox genes and Otx in echinoderm body‐plan morphogenesis in the sea urchin Holopneustes purpurescens. Journal of Experimental Zoology Part B: Molecular and Developmental Evolution, 304, 456467.Google Scholar
Morris, V. B. & Byrne, M. 2014. Oral–aboral identity displayed in the expression of HpHox3 and HpHox11/13 in the adult rudiment of the sea urchin Holopneustes purpurescens. Development Genes and Evolution, 224, 111.Google Scholar
Morris, V. B., Selvakumaraswamy, P., Whan, R. & Byrne, M. 2009. Development of the five primary podia from the coeloms of a sea star larva: Homology with the echinoid echinoderms and other deuterostomes. Proceedings of the Royal Society B: Biological Sciences, 276, 12771284.Google Scholar
Mortensen, T. 1921. Studies of the development and larval forms of echinoderms, Copenhagen: G. E. C. GAD.Google Scholar
O’hara, T. D., Hugall, A. F., Thuy, B. & Moussalli, A. 2014. Phylogenomic resolution of the class Ophiuroidea unlocks a global microfossil record. Current Biology, 24, 18741879.Google Scholar
Okazaki, K. 1975. Spicule formation by isolated micromeres of the sea urchin embryo. American Zoologist, 15, 567581.Google Scholar
Oliveri, P., Carrick, D. M. & Davidson, E. H. 2002. A regulatory gene network that directs micromere specification in the sea urchin embryo. Developmental Biology, 246, 209228.Google Scholar
Oliveri, P., Tu, Q. & Davidson, E. H. 2008. Global regulatory logic for specification of an embryonic cell lineage. Proceedings of the National Academy of Sciences, 105, 59555962.Google Scholar
Pagel, M. 1999. Inferring the historical patterns of biological evolution. Nature, 401, 877884.Google Scholar
Pennington, J. T. & Strathmann, R. R. 1990. Consequences of the calcite skeletons of planktonic echinoderm larvae for orientation, swimming, and shape. The Biological Bulletin, 179, 121133.Google Scholar
Peter, I. S. & Davidson, E. H. 2011. Evolution of gene regulatory networks controlling body plan development. Cell, 144, 970985.Google Scholar
Peter, I. S. & Davidson, E. H. 2015. Genomic control process: Development and evolution, London: Academic Press.Google Scholar
Peter, I. S. & Davidson, E. H. 2016. Implications of developmental gene regulatory networks inside and outside developmental biology. Current Topics in Developmental Biology, 117, 237251.Google Scholar
Peter, I. S. & Davidson, E. H. 2017. Assessing regulatory information in developmental gene regulatory networks. Proceedings of the National Academy of Sciences, 114, 58625869.Google Scholar
Peterson, K. J., Arenas-Mena, C. & Davidson, E. H. 2000. The A/P axis in echinoderm ontogeny and evolution: Evidence from fossils and molecules. Evolution & Development, 2, 93101.Google Scholar
Peterson, K. J., Summons, R. E. & Donoghue, P. C. J. 2007. Molecular palaeobiology. Palaeontology, 50, 775809.Google Scholar
Piovani, L., Czarkwiani, A., Ferrario, C., Sugni, M. & Oliveri, P. 2021. Ultrastructural and molecular analysis of the origin and differentiation of cells mediating brittle star skeletal regeneration. BMC Biology, 19, 119.CrossRefGoogle ScholarPubMed
Raff, R. & Byrne, M. 2006. The active evolutionary lives of echinoderm larvae. Heredity, 97, 244252.Google Scholar
Rafiq, K., Cheers, M. S. & Ettensohn, C. A. 2012. The genomic regulatory control of skeletal morphogenesis in the sea urchin. Development, 139, 579590.Google Scholar
Rafiq, K., Shashikant, T., Mcmanus, C. J. & Ettensohn, C. A. 2014. Genome-wide analysis of the skeletogenic gene regulatory network of sea urchins. Development, 141, 950961.Google Scholar
Rahman, I. A., Thompson, J. R., Briggs, D. E. et al. 2019. A new ophiocistioid with soft-tissue preservation from the Silurian Herefordshire Lagerstätte, and the evolution of the holothurian body plan. Proceedings of the Royal Society B, 286, 20182792.Google Scholar
Reich, M. 2010. Evolution and diversification of ophiocistioids (Echinodermata: Echinozoa). In Harris, L. G., Böttger, S. A., Walker, C. W. & Lesser, M. P. (eds.) Echinoderms: Durham. London: Taylor & Francis, 51–54.Google Scholar
Reich, M. 2021. The first Cretaceous ophiopluteus skeleton (Echinodermata: Ophiuroidea). Journal of Paleontology, 95(6), 1284–1292.Google Scholar
Reich, M. & Smith, A. B. 2009. Origins and biomechanical evolution of teeth in echinoids and their relatives. Palaeontology, 52, 11491168.Google Scholar
Revilla-I-Domingo, R., Oliveri, P. & Davidson, E. H. 2007. A missing link in the sea urchin embryo gene regulatory network: HesC and hte double-negative specification of micromeres. Proceedings of the National Academy of Sciences, 104, 1238312388.Google Scholar
Riedl, R. 1977. A systems-analytical approach to macro-evolutionary phenomena. The Quarterly Review of Biology, 52, 351370.Google Scholar
Rizzo, F., Fernandez-Serra, M., Squarzoni, P., Archimandritis, A. & Arnone, M. I. 2006. Identification and developmental expression of the ets gene family in the sea urchin (Strongylocentrotus purpuratus). Developmental Biology, 300, 3548.Google Scholar
Röttinger, E., Saudemont, A., Duboc, V. et al. 2008. FGF signals guide migration of mesenchymal cells, controls skeletal morphogenesis and regulate gastrulation during sea urchin development. Development, 137, 353365.Google Scholar
Russo, R., Pinsino, A., Costa, C. et al. 2014. The newly characterized Pl‐jun is specifically expressed in skeletogenic cells of the Paracentrotus lividus sea urchin embryo. The FEBS Journal, 281, 38283843.Google Scholar
Saucéde, T., Mooi, R. & David, B. 2007. Phylogeny and origin of Jurassic irregular echinoids (Echinodermata: Echinoidea). Geological Magazine, 144, 333359.Google Scholar
Schirrmeister, B. E., Gugger, M. & Donoghue, P. C. 2015. Cyanobacteria and the great oxidation event: Evidence from genes and fossils. Palaeontology, 58, 769785.Google Scholar
Schoch, R. R. 2010. Riedl’s burden and the body plan: Selection, constraint, and deep time. Journal of Experimental Zoology Part B: Molecular and Developmental Evolution, 314, 110.Google Scholar
Sewell, M. A. & Mceuen, F. S. 2002. Phylum echinodermata: Holothuroidea. In Young, C. M., Sewell, M. A. & Rice, M. E. (eds.) Atlas of marine invertebrate larvae. San Diego: Academic Press, 513–530.Google Scholar
Shackleton, J. D. 2005. Skeletal homologies, phylogeny and classification of the earliest asterozoan echinoderms. Journal of Systematic Palaeontology, 3, 29114.Google Scholar
Sharma, T. & Ettensohn, C. A. 2010. Activation of the skeletogenic gene regulatory network in the early sea urchin embryo. Development, 137, 11491157.Google Scholar
Shashikant, T., Khor, J. M. & Ettensohn, C. A. 2018. From genome to anatomy: The architecture and evolution of the skeletogenic gene regulatory network of sea urchins and other echinoderms. Genesis, 56, e23253.Google Scholar
Shimizu, M. 1997. Cellular elements of the test plates in the sea urchin stronglyocentrotus intermedius. Fisheries Science, 63, 161168.Google Scholar
Shubin, N., Tabin, C. & Carroll, S. 1997. Fossils, genes and the evolution of animal limbs. Nature, 388, 639648.Google Scholar
Shubin, N., Tabin, C. & Carroll, S. 2009. Deep homology and the origins of evolutionary novelty. Nature, 457, 818823.Google Scholar
Smith, A. B. 1980. Stereom microstructure of the echinoid test. Special Papers in Palaeontology, 25, 185.Google Scholar
Smith, A. B. 1988. Fossil evidence for the relationships of extant echinoderm classes and their times of divergence. In Paul, C. R. C. & Smith, A. B. (eds.) Echinoderm phylogeny and evolutionary biology. Oxford: Clarendon Press, 85–97.Google Scholar
Smith, A. B. 1990. Biomineralization in echinoderms. In Carter, J. G. (ed.) Skeletal biomineralization: Patterns, processes and evolutionary trends. Volume 1. New York: Van Nostrand Reinhold, 413–442.Google Scholar
Smith, A. B. 1997. Echinoderm larvae and phylogeny. Annual Review of Ecology and Systematics, 28, 219241.Google Scholar
Smith, A. B. & Reich, M. 2013. Tracing the evolution of the holothurian body plan through stem‐group fossils. Biological Journal of the Linnean Society, 109, 670681.Google Scholar
Sodergren, E., Weinstock, G. M., Davidson, E. H. et al. 2006. The genome of the sea urchin Strongylocentrotus purpuratus. Science, 314, 941952.Google Scholar
Sperling, E. A., Pisani, D. & Peterson, K. J. 2011. Molecular paleobiological insights into the origin of the Brachiopoda. Evolution & Development, 13, 290303.Google Scholar
Strathmann, R. & Eernisse, D. 1994. What molecular phylogenies tell us about the evolution of larval forms. American Zoologist, 34, 502512.Google Scholar
Strathmann, R. R. 1971. The feeding behavior of planktotrophic echinoderm larvae: Mechanisms, regulation, and rates of suspensionfeeding. Journal of Experimental Marine Biology and Ecology, 6, 109160.CrossRefGoogle Scholar
Strathmann, R. R. 1975. Larval feeding in echinoderms. American Zoologist, 15, 717730.Google Scholar
Stricker, S. A. 1985. The ultrastructure and formation of the calcareous ossicles in the body wall of the sea cucumber Leptosynapta clarki (Echinodermata, Holothuroida). Zoomorphology, 105, 209222.Google Scholar
Stricker, S. A. 1986. The fine structure and development of calcified skeletal elements in the body wall of holothurian echinoderms. Journal of Morphology, 188, 273288.Google Scholar
Sumrall, C. D. & Wray, G. A. 2007. Ontogeny in the fossil record: Diversification of body plans and the evolution of “aberrant” symmetry in Paleozoic echinoderms. Paleobiology, 33, 149163.Google Scholar
Syverson, V. J. & Baumiller, T. K. 2014. Temporal trends of predation resistance in Paleozoic crinoid arm branching morphologies. Paleobiology, 40, 417427.Google Scholar
Szabó, R. & Ferrier, D. E. 2015. Another biomineralising protostome with an msp130 gene and conservation of msp130 gene structure across Bilateria. Evolution & Development, 17, 195197.Google Scholar
Telford, M. J., Lowe, C. J., Cameron, C. B. et al. 2014. Phylogenomic analysis of echinoderm class relationships supports Asterozoa. Proceedings of the Royal Society B: Biological Sciences, 281, 20140479.Google Scholar
Thompson, J. R., Erkenbrack, E. M., Hinman, V. F. et al. 2017. Paleogenomics of echinoids reveals an ancient origin for the double-negative specification of micromeres in sea urchins. Proceedings of the National Academy of Sciences, 114, 58705877.Google Scholar
Thompson, J. R., Mirantsev, G. V., Petsios, E. & Bottjer, D. J. 2020. Phylogenetic analysis of the archaeocidaridae and palaeozoic miocidaridae (Echinodermata: Echinoidea) and the origin of crown group echinoids. Papers in Palaeontology, 6, 217249.Google Scholar
Thompson, J. R., Paganos, P., Benvenuto, G., Arnone, M. I. & Oliveri, P. 2021. Post-metamorphic skeletal growth in the sea urchin Paracentrotus lividus and implications for body plan evolution. EvoDevo, 12, 114.Google Scholar
Thompson, J. R., Petsios, E., Davidson, E. H. et al. 2015. Reorganization of sea urchin gene regulatory networks at least 268 million years ago as revealed by oldest fossil cidaroid echinoid. Scientific Reports, 5, 19.Google Scholar
Thompson, J. R., Cotton, L. J., Candela, Y., Kutscher, M., Reich, M., & Bottjer, D. J. 2022. The Ordovician diversification of sea urchins: systematics of the Bothriocidaroida (Echinodermata: Echinoidea). Journal of Systematic Palaeontology, 19(20), 13951448.Google Scholar
True, J. R. & Haag, E. S. 2001. Developmental system drift and flexibility in evolutionary trajectories. Evolution & Development, 3, 109119.Google Scholar
Tsuchimoto, J. & Yamaguchi, M. 2014. Hox expression in the direct‐type developing sand dollar Peronella japonica. Developmental Dynamics, 243, 10201029.Google Scholar
Tweedt, S. M. 2017. Gene regulatory networks, homology, and the early panarthropod fossil record. Integrative and Comparative Biology, 57, 477487.Google Scholar
Valentine, J. W. & Campbell, C. A. 1975. Genetic regulation and the fossil record: Evolution of the regulatory genome may underlie the rapid development of major animal groups. American Scientist, 63, 673680.Google Scholar
Valentine, J. W., Collins, A. G. & Meyer, C. P. 1994. Morphological complexity increase in metazoans. Paleobiology, 20, 131142.Google Scholar
Vinther, J., Sperling, E. A., Briggs, D. E. & Peterson, K. J. 2012. A molecular palaeobiological hypothesis for the origin of aplacophoran molluscs and their derivation from chiton-like ancestors. Proceedings of the Royal Society B: Biological Sciences, 279, 12591268.Google Scholar
Wagner, G. P. 2007. The developmental genetics of homology. Nature Reviews Genetics, 8, 473479.Google Scholar
Wang, L., Israel, J. W., Edgar, A. et al. 2020. Genetic basis for divergence in developmental gene expression in two closely related sea urchins. Nature Ecology & Evolution, 4, 831840.Google Scholar
Wang, X. & Sommer, R. J. 2011. Antagonism of LIN-17/Frizzled and LIN-18/Ryk in nematode vulva induction reveals evolutionary alterations in core developmental pathways. PLoS Biol, 9, e1001110.Google Scholar
Watson, J. D., Baker, T. A., Bell, S. P. et al. 2008. Molecular biology of the gene, San Francisco: Pearson Education.Google Scholar
Wessel, G. M., Kiyomoto, M., Shen, T.-L. & Yajima, M. 2020. Genetic manipulation of the pigment pathway in a sea urchin reveals distinct lineage commitment prior to metamorphosis in the bilateral to radial body plan transition. Scientific Reports, 10, 110.Google Scholar
Wilt, F., Croker, L., Killian, C. E. & Mcdonald, K. 2008. Role of LSM34/SpSM50 proteins in endoskeletal spicule formation in sea urchin embryos. Invertebrate Biology, 127, 452459.Google Scholar
Wilt, F., Killian, C. E., Croker, L. & Hamilton, P. 2013. SM30 protein function during sea urchin larval spicule formation. Journal of Structural Biology, 183, 199204.Google Scholar
Woodland, W. 1906. Memoirs: Studies in spicule formation: IV.–The scleroblastic development of the spicules in cucumariidæ; with a note relating to the plate-and-anchor spicules of synapta inhærens. Journal of Cell Science, 2, 533559.Google Scholar
Woodland, W. 1907a. Memoirs: Studies in spicule formation: V.–The scleroblastic development of the spicules in ophiuroidea and echinoidea, and in the genera antedon and synapta. Journal of Cell Science, 2, 3144.Google Scholar
Woodland, W. 1907b. Memoirs: Studies in spicule formation: VII.–The scleroblastic development of the plate-and-anchor spicules of synapta, and of the wheel spicules of the auricularia larva. Journal of Cell Science, 2, 483510.Google Scholar
Wörheide, G., Dohrmann, M. & Yang, Q. 2016. Molecular paleobiology—progress and perspectives. Palaeoworld, 25, 138148.Google Scholar
Wray, G. A. 1992. The evolution of larval morphology during the post-Paleozoic radiation of echinoids. Paleobiology, 18, 258287.Google Scholar
Wray, G. A., Hahn, M. W., Abouheif, E. et al. 2003. The evolution of transcriptional regulation in eukaryotes. Molecular Biology and Evolution, 20, 13771419.Google Scholar
Wray, G. A. & Lowe, C. J. 2000. Developmental regulatory genes and echinoderm evolution. Systematic Biology, 49, 2851.Google Scholar
Wray, G. A. & Mcclay, D. R. 1988. The origin of spicule-forming cells in a “primitive” sea urchin (Eucidaris tribuloides) which appears to lack primary mesenchyme cells. Development, 103, 305315.Google Scholar
Wright, D. F. 2017. Phenotypic innovation and adaptive constraints in the evolutionary radiation of Palaeozoic crinoids. Scientific Reports, 7, 110.Google Scholar
Wu, S. & Mcclay, D. R. 2007. The Snail repressor is required for PMC ingression in the sea urchin embryo. Development, 134, 10611070.Google Scholar
Wu, S. Y., Ferkowicz, M. & Mcclay, D. R. 2007. Ingression of primary mesenchyme cells of the sea urchin embryo: A precisely timed epithelial mesenchymal transition. Birth Defects Research Part C: Embryo Today: Reviews, 81, 241252.Google Scholar
Yaguchi, S., Yaguchi, J., Suzuki, H. et al. 2020. Establishment of homozygous knock-out sea urchins. Current Biology, 30, R427R429.Google Scholar
Yamazaki, A., Furuzawa, Y. & Yamaguchi, M. 2010. Conserved early expression patterns of micromere specification genes in two echinoid species belonging to the orders clypeasteroida and echinoida. Developmental Dynamics, 239, 33913403.Google Scholar
Yamazaki, A., Kidachi, Y., Yamaguchi, M. & Minokawa, T. 2014. Larval mesenchyme cell specification in the primitive echinoid occurs independently of the double-negative gate. Development, 141, 26692679.Google Scholar
Yamazaki, A. & Minokawa, T. 2015. Expession patterns of mesenchyme specification genes in two distantly related echinoids, Glyptocidaris crenularis and Echinocardium cordatum. Gene Expression Patterns, 17, 8797.Google Scholar
Yamazaki, A., Morino, Y., Urata, M. et al. 2020. Pmar1/phb homeobox genes and the evolution of the double-negative gate for endomesoderm specification in echinoderms. Development, 147, dev182139.Google Scholar
Zamora, S. & Rahman, I. A. 2014. Deciphering the early evolution of echinoderms with Cambrian fossils. Palaeontology, 57, 11051119.Google Scholar
Zhang, X., Sun, L., Yuan, J. et al. 2017. The sea cucumber genome provides insights into morphological evolution and visceral regeneration. PLoS Biology, 15, e2003790.Google Scholar

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