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Developmental Ascendency: From Bottom-up to Top-down Control

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Abstract

Development is a process whereby a relatively unspecified system comprised of loosely connected lower level parts becomes organized into a coherent, higher-level agency. Its temporal corollaries are growth, increasingly deterministic behavior, and a progressive reduction of developmental potential. During immature stages with relatively low specification and high potential, development is largely controlled by local interactions from the “bottom-up,” whereas during more highly specified stages with reduced potential, emergent autocatalytic processes exert “top-down” control. Robert Ulanowicz has shown that this phenomenology of ascendency follows thermodynamic principles and can be described quantitatively using information theory, providing a general theory of development. However, the theory has not found a wide audience among developmental biologists, as genetic determinism encourages the popular reductionistic perception that ontogeny is controlled entirely by molecular mechanisms that exert efficient causality from the bottom-up. Nonetheless, measurements of metabolic rates and mRNA complexity in developing embryos, as well as functional analyses of gene regulatory systems, indicate that ontogeny fits the paradigm of developmental ascendency. Beyond informing biomedical research and the interpretation of large datasets obtained by systems-biological approaches, developmental ascendency helps explain the origin of life, and, being independent of scale, provides an overarching explanation for phylogenetic change that contextualizes Darwinian evolution.

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References

  • Akashi K, He X, Chen J, Iwasaki H, Niu C, Steenhard B, Zhang J, Haug J, Li L (2003) Transcriptional accessibility for genes of multiple tissues and hematopoietic lineages is hierarchically controlled during early hematopoiesis. Blood 101: 383–389.

    Article  Google Scholar 

  • Al-Hajj M, Becker MW, Wicha M, Weissman I, Clarke MF (2004) Therapeutic implications of cancer stem cells. Current Opinion in Genetics and Development 14: 43–47.

    Article  Google Scholar 

  • Arnone MI, Bogarad LD, Collazo A, Kirchhamer CV, Cameron RA, Rast JP, Gregorians A, Davidson EH (1997) Green Fluorescent Protein in the sea urchin: New experimental approaches to transcriptional regulatory analysis in embryos and larvae. Development 124: 4649–4659.

    Google Scholar 

  • Arnone MI, Davidson EH (1997) The hardwiring of development: Organization and function of genomic regulatory systems. Development 124: 1851–1864.

    Google Scholar 

  • Arnone MI, Martin EL, Davidson EH (1998) Cis-regulation downstream of cell type specification: A single compact element controls the complex expression of the CyIIa gene in sea urchin embryos. Development 125: 1381–1395.

    Google Scholar 

  • Bissell MJ, Labarge MA (2005) Context, tissue plasticity, and cancer: Are tumor stem cells also regulated by the microenvironment? Cancer Cell 7: 17–23.

    Google Scholar 

  • Blackstone NW (1998) Morphological, physiological and metabolic comparisons between runner-like and sheet-like inbred lines of a colonial hydroid. Journal of Experimental Biology 201(20): 2821–2831.

    Google Scholar 

  • Blackstone NW (1999) Redox control in development and evolution: Evidence from colonial hydroids. Journal of Experimental Biology 202(24): 3541–3553.

    Google Scholar 

  • Blackstone NW (2000) Redox control and the evolution of multicellularity. Bioessays 22: 947–953.

    Article  Google Scholar 

  • Blackstone NW (2003) Redox signaling in the growth and development of colonial hydroids. Journal of Experimental Biology 206(4): 651–658.

    Article  Google Scholar 

  • Buss LW (1987) The Evolution of Individuality. Princeton, NJ: Princeton University Press.

    Google Scholar 

  • Child CM (1941a) Patterns and Problems of Development. Chicago: University of Chicago Press.

    Book  Google Scholar 

  • Child CM (1941b) Formation and reduction of indophenol blue in development of an echinoderm. Proceedings of the National Academy of Sciences USA 27: 523–529.

    Article  Google Scholar 

  • Coffman JA (2005) On reductionism, organicism, somatic mutations and cancer. Bioessays 27: 459; author reply, 460–161.

    Article  Google Scholar 

  • Coffman JA, Davidson EH (2001) Oral-aboral axis specification in the sea urchin embryo: I. Axis entrainment by respiratory asymmetry. Developmental Biology 230: 18–28.

    Article  Google Scholar 

  • Coffman JA, McCarthy JJ, Dickey-Sims C, Robertson AJ (2004) Oral-aboral axis specification in the sea urchin embryo: II. Mitochondrial distribution and redox state contribute to establishing polarity in Strongylocentrotus purpuratus. Developmental Biology 273: 160–171.

    Article  Google Scholar 

  • Cox KH, Angerer LM, Lee JJ, Davidson EH, Angerer RC (1986) Cell lineage-specific programs of expression of multiple actin genes during sea urchin embryogenesis. Journal of Molecular Biology 188: 159–172.

    Article  Google Scholar 

  • Crawford DL (2001) Functional genomics does not have to be limited to a few select organisms. Genome Biology 2. http://genomebiolog.com/2001/2/1/interactions/1001/

  • Czihak G (1963) Entwicklungsphysiologische Untersuchungen an Echiniden (Verteilung und Bedeutung der Cytochromoxydase). Roux’ Archiy Für Entwicklungsmechanik 154: 272–292.

    Article  Google Scholar 

  • Davidson EH (1986) Gene Activity in Early Development. San Diego, CA: Academic Press.

    Google Scholar 

  • Davidson EH (1990) How embryos work: A comparative view of diverse modes of cell fate specification. Development 108: 365–389.

    Google Scholar 

  • Davidson EH (1991) Spatial mechanisms of gene regulation in metazoan embryos. Development 113: 1–26.

    Google Scholar 

  • Davidson EH (2001) Genomic Regulatory Systems: Development and Evolution. San Diego, CA: Academic Press.

    Google Scholar 

  • Davidson EH, Cameron RA, Ransick A (1998) Specification of cell fate in the sea urchin embryo: Summary and some proposed mechanisms. Development 125: 3269–3290.

    Google Scholar 

  • Davidson EH, McClay DR, Hood L (2003) Regulatory gene networks and the properties of the developmental process. Proceedings of the National Academy of Sciences USA 100: 1475–1480.

    Article  Google Scholar 

  • Davidson EH, Rast JP, Oliveri P, Ransick A, Calestani C, Yuh CH, Minokawa T, Amore G, Hinman V, Arenas-Mena C, Otim O, Brown T, Livi CB, Lee PY, Revilla R, Clarke PJC, Rust AG, Pan Z, Arnone MI, Rowen L, Cameron RA, McClay DR, Hood L, Bolouri H (2002a) A provisional regulatory gene network for specification of endomesoderm in the sea urchin embryo. Developmental Biology 246: 162–190.

    Article  Google Scholar 

  • Davidson EH, Rast JP, Oliveri P, Ransick A, Calestani C, Yuh C-H, Minokawa T, Amore G, Hinman V, Arenas-Mena C, Otim O, Brown CT, Livi CB, Lee PY, Revilla R, Rust AG, Pan Zj, Schilstra MJ, Clarke PJC, Arnone MI, Rowen L, Cameron RA, McClay DR, Hood L, Bolouri H (2002b) A genomic regulatory network for development. Science 295: 1669–1678.

    Article  Google Scholar 

  • Driesch H (1892) Entwicklungsmechanisme Studien: I. Der Werth der beiden ersten Furchungszellen in der Echinodermentwicklung. Experimentelle Erzeugen von Theil und Doppelbildung. Zeitschrift für wissenschaftliche Zoologie 53: 160–178; 183–184.

    Google Scholar 

  • Duboc V, Rottinger E, Besnardeau L, Lepage T (2004) Nodal and BMP2/4 signaling organizes the oral-aboral axis of the sea urchin embryo. Developmental Cell 6: 397–110.

    Article  Google Scholar 

  • Erwin DH, Davidson EH (2002) The last common bilaterian ancestor. Development 129: 3021–3032.

    Google Scholar 

  • Fontana W, Buss LW (1994) What would be conserved if “the tape were played twice”? Proceedings of the National Academy of Sciences USA 91: 757–761.

    Article  Google Scholar 

  • Fujiwara A, Kamata Y, Asami K, Yasumasu I (2000) Relationship between ATP level and respiratory rate in sea urchin embryos. Development, Growth and Differentiation 42: 155–165.

    Article  Google Scholar 

  • Fujiwara A, Yasumasu I (1997) Does the respiratory rate in sea urchin embryos increase during early development without proliferation of mitochondria? Development, Growth and Differentiation 39: 179–189.

    Article  Google Scholar 

  • Goodman AF, Bellato CM, Khidr L (2005) The uncertain future for central dogma. The Scientist 19(12): 20–21.

    Google Scholar 

  • Gould SJ (2002) The Structure of Evolutionary Theory. Cambridge, MA: Harvard University Press.

    Google Scholar 

  • Hall BK (2000) Evo-devo or devo-evo: Does it matter? Evolution and Development 2: 177–178.

    Article  Google Scholar 

  • Hardin J, Coffman JA, Black SD, McClay DR (1992) Commitment along the dorsoventral axis of the sea urchin embryo is altered in response to NiCl2. Development 116: 671–685.

    Google Scholar 

  • Kauffman S (1995) At Home in the Universe. New York: Oxford University Press.

    Google Scholar 

  • Keller EF (1999) Elusive locus of control in biological development: Genetic versus developmental programs. Journal of Experimental Zoology (Molecular and Developmental Evolution) 285: 283–290.

    Article  Google Scholar 

  • Kirk DL (2005) A twelve-step program for evolving multicellularity and a division of labor. Bioessays 27: 299–310.

    Article  Google Scholar 

  • Laland KN, Odling-Smee FJ, Feldman MW (1999) Evolutionary consequences of niche construction and their implications for ecology. Proceedings of the National Academy of Sciences USA 96: 10242–10247.

    Article  Google Scholar 

  • McDonald JW (2004) Repairing the damaged spinal cord: From stem cells to activity-based restoration therapies. Clinical Neurosurgery 51: 207–227.

    Google Scholar 

  • Murray AW (2000) Whither genomics? Genome Biology 1. http://genomebiolog.com/2000/1/1/comment/003/

  • Newman SA (2002) Developmental mechanisms: Putting genes in their place. Journal of Biosciences 27: 97–104.

    Article  Google Scholar 

  • Newman SA (2005) The pre-Mendelian, pre-Darwinian world: Shifting relations between genetic and epigenetic mechanisms in early multicellular evolution. Journal of Biosciences 30: 75–85.

    Article  Google Scholar 

  • Newman SA, Müller GB (2000) Epigenetic mechanisms of character origination. Journal of Experimental Zoology B 288: 304–317.

    Article  Google Scholar 

  • Nijhout HF (1990) Metaphors and the role of genes in development. Bioessays 12(9): 441–446.

    Article  Google Scholar 

  • Nijhout HF (2002) The nature of robustness in development. Bioessays 24: 553–563.

    Article  Google Scholar 

  • Pease DC (1941) Echinoderm bilateral determination in chemical concentration gradients: I. The effects of cyanide, ferricyanide, iodoacetate, picrate, dinitrophenol, urethane, iodine, malonate, etc. Journal of Experimental Zoology 86: 381–404.

    Article  Google Scholar 

  • Pease DC (1942a) Echinoderm bilateral determination in chemical concentration gradients: II. The effects of azide, pilocarpine, pyocyanine, diamine, cysteine, glutathione, and lithium. Journal of Experimental Zoology 89: 329–345.

    Article  Google Scholar 

  • Pease DC (1942b) Echinoderm bilateral deterimination in chemical concentration gradients: III. The effects of carbon monoxide and other gases. Journal of Experimental Zoology 89: 347–356.

    Article  Google Scholar 

  • Popper KR (1990) A World of Propensities. Bristol: Thoemmes.

    Google Scholar 

  • Ransick A, Ernst S, Britten RJ, Davidson EH (1993) Whole mount in situ hybridization shows Endo 16 to be a marker for the vegetal plate territory in sea urchin embryos. Mechanics of Development 42(3): 117–124.

    Article  Google Scholar 

  • Reynolds SD, Angerer LM, Palis J, Nasir A, Angerer RC (1992) Early mRNAs, spatially restricted along the animal-vegetal axis of sea urchin embryos, include one encoding a protein related to tolloid and BMP-1. Development 114: 769–786.

    Google Scholar 

  • Salthe SN (1993) Development and Evolution: Complexity and Change in Biology. Cambridge, MA: MIT Press.

    Google Scholar 

  • Smith E, Morowitz HJ (2004) Universality in intermediary metabolism. Proceedings of the National Academy of Sciences USA 101: 13168–13173.

    Article  Google Scholar 

  • Sole RV, Montoya JM, Erwin DH (2002) Recovery after mass extinction: Evolutionary assembly in large-scale biosphere dynamics. Philosophical Transactions of the Royal Society of London B 357: 697–707.

    Article  Google Scholar 

  • Sonnenschein C, Soto AM (1999) The Society of Cells: Cancer and Control of Cell Proliferation. Oxford: BIOS Scientific.

    Google Scholar 

  • Soto AM, Sonnenschein C (2004) The somatic mutation theory of cancer: Growing problems with the paradigm? Bioessays 26: 1097–1107.

    Article  Google Scholar 

  • Ulanowicz RE (1986) Growth and Development: Ecosystems Phenomenology. New York: Springer.

    Book  Google Scholar 

  • Ulanowicz RE (1997) Ecology: The Ascendent Perspective (Allen TFH, Roberts DW, eds). New York: Columbia University Press.

    Google Scholar 

  • Wedlich-Soldner R, Li R (2003) Spontaneous cell polarization: Undermining determinism. Nature Cell Biology 5: 267–270.

    Article  Google Scholar 

  • Wei Z, Angerer LM, Angerer RC (1997) Multiple positive cis elements regulate the asymmetric expression of the SpHE gene along the sea urchin embryo animal-vegetal axis. Developmental Biology 187: 71–78.

    Article  Google Scholar 

  • Wei Z, Angerer LM, Gagnon ML, Angerer RC (1995) Characterization of the SpHE promoter that is spatially regulated along the animal-vegetal axis of the sea urchin embryo. Developmental Biology 171: 195–211.

    Article  Google Scholar 

  • Weitzel HE, Illies MR, Byrum CA, Xu R, Wikramanayake AH, Ettensohn CA (2004) Differential stability of beta-catenin along the animal-vegetal axis of the sea urchin embryo mediated by dishevelled. Development 131: 2947–2956.

    Article  Google Scholar 

  • Yuh CH, Bolouri H, Davidson EH (2001) Cis-regulatory logic in the endo16 gene: Switching from a specification to a differentiation mode of control. Development 128: 617–629.

    Google Scholar 

  • Yuh CH, Davidson EH (1996) Modularcis-regulatory organization of Endo16, a gut-specific gene of the sea urchin embryo. Development 122: 1069–1082.

    Google Scholar 

  • Yuh CH, Dorman ER, Davidson EH (2005) Brn1/2/4, the predicted midgut regulator of the endo16 gene of the sea urchin embryo. Developmental Biology 281: 286–298.

    Article  Google Scholar 

  • Yuh CH, Ransick A, Martinez P, Britten RJ, Davidson EH (1994) Complexity and organization of DNA-protein interactions in the 5′ — regulatory region of an endoderm-specific marker gene in the sea urchin embryo. Mechanics of Development 47: 165–186.

    Article  Google Scholar 

  • Zeller RW, Cameron RA, Franks RR, Britten RJ, Davidson EH (1992) Territorial expression of three different trans-genes in early sea urchin embryos detected by a whole-mount fluorescence procedure. Developmental Biology 151: 382–390.

    Article  Google Scholar 

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Correspondence to James A. Coffman.

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Coffman, J.A. Developmental Ascendency: From Bottom-up to Top-down Control. Biol Theory 1, 165–178 (2006). https://doi.org/10.1162/biot.2006.1.2.165

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