Skip to main content
Log in

The role of self-organization in developmental evolution

  • Original Paper
  • Published:
Theory in Biosciences Aims and scope Submit manuscript

Abstract

In developmental and evolutionary biology, particular emphasis has been given to the relationship between transcription factors and the cognate cis-regulatory elements of their target genes. These constitute the gene regulatory networks that control expression and are assumed to causally determine the formation of structures and body plans. Comparative analysis has, however, established a broad sequence homology among species that nonetheless display quite different anatomies. Transgenic experiments have also confirmed that many developmentally important elements are, in fact, functionally interchangeable. Although dependent upon the appropriate degree of gene expression, the actual construction of specific structures appears not directly linked to the functions of gene products alone. Instead, the self-formation of complex patterns, due in large part to epigenetic and non-genetic determinants, remains a persisting theme in the study of ontogeny and regenerative medicine. Recent evidence indeed points to the existence of a self-organizing process, operating through a set of intrinsic rules and forces, which imposes coordination and a holistic order upon cells and tissue. This has been repeatedly demonstrated in experiments on regeneration as well as in the autonomous formation of structures in vitro. The process cannot be wholly attributed to the functional outcome of protein–protein interactions or to concentration gradients of diffusible chemicals. This phenomenon is examined here along with some of the methodological and theoretical approaches that are now used in understanding the causal basis for self-organization in development and its evolution.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  • Alencar AM, Andrade JS, Lucena LS (1997) Self-organized percolation. Phys Rev E 56:R2379–R2382

    CAS  Google Scholar 

  • Alonso CR, Wilkins AS (2005) The molecular elements that underlie developmental evolution. Nat Rev Genet 6(9):709–715

    CAS  PubMed  Google Scholar 

  • Amemiya CT et al (2013) The African coelacanth genome provides insights into tetrapod evolution. Nature 496(7445):311–316

    CAS  PubMed Central  PubMed  Google Scholar 

  • Angst B, Marcozzi C, Magee A (2001) The cadherin superfamily: diversity in form and function. J Cell Sci 114:629–641

    CAS  PubMed  Google Scholar 

  • Attanasio C, Nord AS, Zhu Y, Blow MJ, Li Z, Liberton DK, Morrison H, Plajzer-Frick I, Holt A, Hosseini R, Phouanenavong S, Akiyama JA, Shoukry M, Afzal V, Rubin EM, FitzPatrick DR, Ren B, Hallgrímsson B, Pennacchio LA, Visel A (2013) Fine tuning of craniofacial morphology by distant-acting enhancers. Science 342(6157):1241006

    PubMed Central  PubMed  Google Scholar 

  • Ayyar S, Negre B, Simpson P, Stollewerk A (2010) An arthropod cis-regulatory element functioning in sensory organ precursor development dates back to the Cambrian 8:127

    Google Scholar 

  • Baker RE, Schnell S, Maini PK (2006) A clock and wavefront mechanism for somite formation. Dev Biol 293(1):116–126

    CAS  PubMed  Google Scholar 

  • Balleza E, López-Bojorquez LN, Martínez-Antonio A, Resendis-Antonio O, Lozada-Chávez I, Balderas-Martínez YI, Encarnación S, Collado-Vides J (2009) Regulation by transcription factors in bacteria: beyond description. FEMS Microbiol Rev 33(1):133–151

    CAS  PubMed Central  PubMed  Google Scholar 

  • Batten B, Salthe S, Boschetti F (2008) Visions of evolution: self-organization proposes what natural selection disposes. Biol Theory 3(1):17–29

    Google Scholar 

  • Beloussov LV (1997) Life of Alexander G Gurwitsch and his relevant contribution to the theory of morphogenetic fields. Int J Dev Biol 41(6):771–779

    CAS  PubMed  Google Scholar 

  • Belting HG, Shashikant CS, Ruddle FH (1998) Modification of expression and cis-regulation of Hoxc8 in the evolution of diverged axial morphology. Proc Natl Acad Sci USA 95(5):2355–2360

    CAS  PubMed Central  PubMed  Google Scholar 

  • Birney E et al (2012) An integrated encyclopedia of DNA elements in the human genome. Nature 489:57–74

    Google Scholar 

  • Bizzarri M, Pasqualato A, Cucina A, Pasta V (2013a) Physical forces and non linear dynamics mould fractal cell shape. Histol Histopathol 28(2):155e174

    Google Scholar 

  • Bizzarri M, Palombo A, Cucina A (2013b) Theoretical aspects of systems biology. Prog Biophys Mol Biol 112(1–2):33–43

    PubMed  Google Scholar 

  • Boettiger AN, Oster G (2009) Emergent complexity in simple neural systems. Commun Integr Biol 2(6):467–470

    PubMed Central  PubMed  Google Scholar 

  • Bolker JA (2000) Modularity in development and why it matters to evo-devo. Am Zool 40(5):770–776

    Google Scholar 

  • Bosch M, Bishop SA, Baguña J, Couso JP (2010) Leg regeneration in Drosophila abridges the normal developmental program. Int J Dev Biol 54(8–9):1241–1250

    PubMed Central  PubMed  Google Scholar 

  • Bozorgmehr JE (2012) The effect of functional compensation among duplicate genes can constrain their evolutionary divergence. J Genet 91(1):1–8

    PubMed  Google Scholar 

  • Brakefield PM (2011) Evo-devo and accounting for Darwin’s endless forms. Philos Trans R Soc Lond B Biol Sci 366(1574):2069–2075

    PubMed Central  PubMed  Google Scholar 

  • Britten RJ (2003) Only details determine. In: Müller GB, Newman SA (eds) Origination of organismal form: beyond the gene in developmental and evolutionary biology. MIT Press, Cambridge, pp 75–81

    Google Scholar 

  • Camazine S, Deneubourg JL, Franks NR, Sneyd J, Theraulaz G, Bonabeau E (2001) Self-organization in biological systems. Princeton University Press, Princeton

    Google Scholar 

  • Capellini TD, Zappavigna V, Selleri L (2011) Pbx homeodomain proteins: TALEnted regulators of limb patterning and outgrowth. Dev Dyn 240(5):1063–1086

    CAS  PubMed Central  PubMed  Google Scholar 

  • Carroll SB (2005) Endless forms most beautiful: the new science of evo devo and the making of the animal kingdom. W.W. Norton and Company, New York

    Google Scholar 

  • Carroll SB (2008) Evo-devo and an expanding evolutionary synthesis: a genetic theory of morphological evolution. Cell 134(1):25–36

    CAS  PubMed  Google Scholar 

  • Chandebois R, Faber J (1987) From DNA transcription to visible structure: what the development of multicellular animals teaches us. Acta Biotheor 36(2):61–120

    CAS  PubMed  Google Scholar 

  • Chanson L, Brownfield D, Garbe JC, Kuhn I, Stampfer MR, Bissell MJ, LaBarge MA (2011) Self-organization is a dynamic and lineage-intrinsic property of mammary epithelial cells. Proc Natl Acad Sci USA 108(8):3264–3269

    CAS  PubMed Central  PubMed  Google Scholar 

  • Chaplain MAJ, Singh GD, McLachlan JC (1999) On growth and form: spatio-temporal pattern formation in biology. Wiley, Chichester

    Google Scholar 

  • Cooke J, Zeeman EC (1976) A clock and wavefront model for control of the number of repeated structures during animal morphogenesis. J Theor Biol 58:455–476

    CAS  PubMed  Google Scholar 

  • Cooper GM, Brown CD (2008) Qualifying the relationship between sequence conservation and molecular function. Genome Res 18(2):201–205

    CAS  PubMed  Google Scholar 

  • Darwin C (1875) The variation of animals and plants under domestication. John Murray, London

    Google Scholar 

  • Davidson EH (2006) The regulatory genome: gene regulatory networks in development and evolution. Academic Press, Amsterdam

    Google Scholar 

  • Davidson EH, Erwin DH (2006) Gene regulatory networks and the evolution of animal body plans. Science 311(5762):796–800

    CAS  PubMed  Google Scholar 

  • Davidson EH, Levine MS (2008) Properties of developmental gene regulatory networks. Proc Natl Acad Sci USA 105(51):20063–20066

    CAS  PubMed Central  PubMed  Google Scholar 

  • Davies JA (2005) Mechanisms of morphogenesis: the creation of biological form. Elsevier Academic Press, Waltham

    Google Scholar 

  • Davies JA (2008) Synthetic morphology: prospects for engineered, self-constructing anatomies. J Anat 212(6):707–719

    CAS  PubMed Central  PubMed  Google Scholar 

  • Davies P (2013) The secret of life won’t be cooked up in a chemistry lab. Guardian online. http://www.guardian.co.uk/commentisfree/2013/jan/13/secret-life-unveiled-chemistry-lab

  • De Robertis EM (2008) Evo-devo: variations on ancestral themes. Cell 132(2):185–195

    PubMed Central  PubMed  Google Scholar 

  • Dias AS, de Almeida I, Belmonte JM, Glazier JA, Stern CD (2014) Somites without a clock. Science. doi:10.1126/science.1247575

    Google Scholar 

  • Dobrescu R, Purcarea VL (2011) Emergence, self-organization and morphogenesis in biological structures. J Med Life 4(1):82–90

    CAS  PubMed Central  PubMed  Google Scholar 

  • Dowell R (2011) The similarity of gene expression between human and mouse tissues. Genome Biol 12:101

    PubMed Central  PubMed  Google Scholar 

  • Driesch H (1908) The science and philosophy of the organism. Adam and Charles Black, London

    Google Scholar 

  • Edelmann JB, Denton MJ (2007) The uniqueness of biological self-organization: challenging the Darwinian paradigm. Biol Philos 22(4):579–601

    Google Scholar 

  • Eguchi G, Eguchi Y, Nakamura K, Yadav MC, Millán JL, Tsonis PA (2011) Regenerative capacity in newts is not altered by repeated regeneration and ageing. Nat Commun 2:384

    PubMed Central  PubMed  Google Scholar 

  • Eiraku M et al (2008) Self-organized formation of polarized cortical tissues from ESCs and its active manipulation by extrinsic signals. Cell Stem Cell 3:519–532

    CAS  PubMed  Google Scholar 

  • Eiraku M, Takata N, Ishibashi H, Kawada M, Sakakura E, Okuda S, Sekiguchi K, Adachi T, Sasai Y (2011) Self-organizing optic-cup morphogenesis in three-dimensional culture. Nature 472(7341):51–56

    CAS  PubMed  Google Scholar 

  • Eiraku M, Adachi T, Sasai Y (2012) Relaxation-expansion model for self-driven retinal morphogenesis: a hypothesis from the perspective of biosystems dynamics at the multi-cellular level. BioEssays 1:17–25

    Google Scholar 

  • Elowitz MB, Levine AJ, Siggia ED, Swain PS (2002) Stochastic gene expression in a single cell. Science 297:1183–1186

    CAS  PubMed  Google Scholar 

  • Elsner JB, Tsonis PA (1989) On the dynamics of a forced reaction-diffusion model for biological pattern formation. Proc Natl Acad Sci USA 86(13):4938–4942

    PubMed Central  PubMed  Google Scholar 

  • Faucourt M, Houliston E, Besnardeau L, Kimelman D, Lepage T (2001) The pitx2 homeobox protein is required early for endoderm formation and nodal signaling. Dev Biol 229(2):287–306

    CAS  PubMed  Google Scholar 

  • Fisher EM, O’Doherty A, Ruf S, Mulligan C, Hildreth V, Errington ML, Cooke S, Sesay A, Modino S, Vanes L, Hernandez D, Linehan JM, Sharpe PT, Brandner S, Bliss TV, Henderson DJ, Nizetic D, Tybulewicz VL (2005) An aneuploid mouse strain carrying human chromosome 21 with Down syndrome phenotypes. Science 309(5743):2033–2037

    PubMed Central  PubMed  Google Scholar 

  • Frankel N, Erezyilmaz DF, McGregor AP, Wang S, Payre F, Stern DL (2011) Morphological evolution caused by many subtle-effect substitutions in regulatory DNA. Nature 474(7353):598–603

    CAS  PubMed Central  PubMed  Google Scholar 

  • Freitas R, Gómez-Marín C, Wilson JM, Casares F, Gómez-Skarmeta JL (2012) Hoxd13 contribution to the evolution of vertebrate appendages. Dev Cell 23(6):1219–1229

    CAS  PubMed  Google Scholar 

  • Gehring WJ (2002) The genetic control of eye development and its implications for the evolution of the various eye-types. Int J Dev Biol 46:65–73

    PubMed  Google Scholar 

  • Gellon G, McGinnis W (1998) Shaping animal body plans in development and evolution by modulation of Hox expression patterns. BioEssays 20(2):116–125

    CAS  PubMed  Google Scholar 

  • Gerhart J, Kirschner M (1997) Cells, embryos, and evolution. Blackwell Science, Malden

    Google Scholar 

  • Gerstman BS, Chapagain PP (2005) Self-organization in protein folding and the hydrophobic interaction. J Chem Phys 123:054901

    PubMed  Google Scholar 

  • Gilbert SF (2006) Developmental biology, 8th edn. Mass: Sinauer Associates, Sunderland, pp 65–66

    Google Scholar 

  • Gilbert SF, Opitz JM, Raff RA (1996) Resynthesizing evolutionary and developmental biology. Dev Biol 173(2):357–372

    CAS  PubMed  Google Scholar 

  • Goodwin BC (1985) Developing organisms as self-organizing fields. In: Antonelli PL (ed) Mathematical essays on growth and the emergence of form. Univer-sity of Alberta Press, Alberta

    Google Scholar 

  • Goodwin BC, Trainor LE (1980) A field description of the cleavage process in embryogenesis. J Theor Biol 85:757–770

    CAS  PubMed  Google Scholar 

  • Green AA, Kennaway JR, Hanna AI, Bangham JA, Coen E (2010) Genetic control of organ shape and tissue polarity. PLoS Biol 8:e1000537

    PubMed Central  PubMed  Google Scholar 

  • Guo CL (2013) Mechanical models for the self-organization of tubular patterns. Biomatter 3(3):e24926

    Google Scholar 

  • Guttman M, Donaghey J, Carey BW, Garber M, Grenier JK, Munson G, Young G, Lucas AB, Ach R, Bruhn L, Yang X, Amit I, Meissner A, Regev A, Rinn JL, Root DE, Lander ES (2011) lincRNAs act in the circuitry controlling pluripotency and differentiation. Nature 477(7364):295–300

    CAS  PubMed Central  PubMed  Google Scholar 

  • Halder G, Callaerts P, Gehring WJ (1995) Induction of ectopic eyes by targeted expression of the eyeless gene in Drosophila. Science 267:1788–1792

    CAS  PubMed  Google Scholar 

  • Hall BK (2003) Unlocking the black box between genotype and phenotype: Cell condensations as morphogenetic (modular) units. Biol Philos 18(2):219–247

    Google Scholar 

  • Halley JD, Winkler D (2008) Consistent concepts of self-organization and self-assembly. Complexity 14(2):10–17

    Google Scholar 

  • Harold FM (2005) Molecules into cells: specifying spatial architecture. Microbiol Mol Biol Rev 69(4):544–564

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hayashi T, Mizuno N, Ueda Y, Okamoto M, Kondoh H (2004) FGF2 triggers iris-derived lens regeneration in newt eye. Mech Dev 121(6):519–526

    CAS  PubMed  Google Scholar 

  • Heisenberg W (1930) The physical principles of the quantum theory. University of Chicago Press, Chicago, IL

  • Held LI (2009) Quirks of human anatomy. In: An Evo-Devo Look at the Human Body, Cambridge University Press, Cambridge

  • Held LI (2010) The evolutionary geometry of human anatomy: discovering our inner fly. Evol Anthropol 19:227–235

    Google Scholar 

  • Henry JJ, Tsonis PA (2010) Molecular and cellular aspects of amphibian lens regeneration. Prog Retin Eye Res 29(6):543–555

    CAS  PubMed Central  PubMed  Google Scholar 

  • Henry RW, Haldiman JT, Albert TF, Henk WG, Abdelbaki YZ, Duffield DW (1983) Gross anatomy of the respiratory system of the bowhead whale, Balaena mysticetus. Anat Rec 207(3):435–449

    CAS  PubMed  Google Scholar 

  • Herbert-Read JE, Perna A, Mann RP, Schaerf TM, Sumpter DJ, Ward AJ (2011) Inferring the rules of interaction of shoaling fish. Proc Natl Acad Sci USA 108(46):18726–18731

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hernando-Herraez I, Prado-Martinez J, Garg P, Fernandez-Callejo M, Heyn H, Hvilsom C, Navarro A, Esteller M, Sharp AJ, Marques-Bonet T (2013) Dynamics of DNA methylation in recent human and great ape evolution. PLoS Genet 9(9):e1003763

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hodgkin J (2001) What does a worm want with 20,000 genes? Genome Biol 2(11):comment2008.1–2008.4

  • Hoekstra HE, Coyne JA (2007) The locus of evolution: evo devo and the genetics of adaptation. Evolution 61(5):995–1016

    PubMed  Google Scholar 

  • Hood L, Galas D (2003) The digital code of DNA. Nature 421(6921):444–448

    PubMed  Google Scholar 

  • Howard J, Grill SW, Bois JS (2011) Turing’s next steps: the mechanochemical basis of morphogenesis. Nat Rev Mol Cell Biol 12(6):392–398

    PubMed  Google Scholar 

  • Huang S, Ingber DE (2000) Shape-dependent control of cell growth, differentiation, and apoptosis: switching between attractors in cell regulatory networks. Exp Cell Res 261:91–103

    CAS  PubMed  Google Scholar 

  • Hughes TR, Weirauch MT (2010) Conserved expression without conserved regulatory sequence: the more things change, the more they stay the same. Trends Genet 26(2):66–74

    PubMed  Google Scholar 

  • Hynes R (2002) Integrins: bidirectional, allosteric signaling machines. Cell 110(6):673–687

    CAS  PubMed  Google Scholar 

  • Ingber DE (2005) Mechanical control of tissue growth: function follows form. Proc Natl Acad Sci USA 102(33):11571–11572

    CAS  PubMed Central  PubMed  Google Scholar 

  • Jacob F (1977) Evolution and tinkering. Science 196(4295):1161–1166

    CAS  PubMed  Google Scholar 

  • Jaenisch R, Bird A (2003) Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat Genet 33(Suppl):245–254

    CAS  PubMed  Google Scholar 

  • Jimenez SK, Sheikh F, Jin Y, Detillieux KA, Dhaliwal J, Kardami E, Cattini PA (2004) Transcriptional regulation of FGF-2 gene expression in cardiac myocytes. Cardiovasc Res 62(3):548–557

    CAS  PubMed  Google Scholar 

  • Jonsson H, Peng SL (2005) Forkhead transcription factors in immunology. Cell Mol Life Sci 62(4):397–409

    CAS  PubMed  Google Scholar 

  • Kadoshima T, Sakaguchi H, Nakano T, Soen M, Ando S, Eiraku M, Sasai Y (2013) Self-organization of axial polarity, inside-out layer pattern, and species-specific progenitor dynamics in human ES cell-derived neocortex. Proc Natl Acad Sci USA 110(50):20284–20289

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kaern M, Miguez DG, Munuzuri AP, Menzinger M (2004) Control of chemical pattern formation by a clock-and-wavefront type mechanism. Biophys Chem 110:231–238

    CAS  PubMed  Google Scholar 

  • Karsenti E (2008) Self-organization in cell biology: a brief history. Nat Rev Mol Cell Biol 9:255–262

    CAS  PubMed  Google Scholar 

  • Kauffman S (1993) Origins of order: self-organization and selection in evolution. Oxford University Press, Oxford

    Google Scholar 

  • Keim B (2010) Early reports from the “Dark Matter” of the genome. Wired Science. http://www.wired.com/wiredscience/2010/12/genomic-dark-matter/

  • Keller R (2006) Mechanisms of elongation in embryogenesis. Development 133:2291–2302

    CAS  PubMed  Google Scholar 

  • Keller R, Davidson L, Shook D (2003) How we are shaped: the biomechanics of gastrulation. Differentiation 7:171–205

    Google Scholar 

  • Kerszberg M, Wolpert L (2007) Specifying positional information in the embryo: looking beyond morphogens. Cell 130(2):205–209

    CAS  PubMed  Google Scholar 

  • Khavari DA, Sen GL, Rinn JL (2010) DNA methylation and epigenetic control of cellular differentiation. Cell Cycle 9(19):3880–3883

    CAS  PubMed  Google Scholar 

  • Klingenberg CP, Leamy LJ (2001) Quantitative genetics of geometric shape in the mouse mandible. Evolution 55:2342–2352

    CAS  PubMed  Google Scholar 

  • Kondo S, Miura T (2010) Reaction-diffusion model as a framework for understanding biological pattern formation. Science 329(5999):1616–1620

    CAS  PubMed  Google Scholar 

  • Kostka D, Hubisz MJ, Siepel A, Pollard KS (2012) The role of GC-biased gene conversion in shaping the fastest evolving regions of the human genome. Mol Biol Evol 29(3):1047–1057

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lavagnino M, Arnoczky SP (2005) In vitro alterations in cytoskeletal tensional homeostasis control gene expression in tendon cells. J Orthop Res 23(5):1211–1218

    CAS  PubMed  Google Scholar 

  • Lecuit T (2008) Developmental mechanics: cellular patterns controlled by adhesion, cortical tension and cell division. HFSP J 2(2):72–78

    PubMed Central  PubMed  Google Scholar 

  • Levin M (2011) The wisdom of the body: future techniques and approaches to morphogenetic fields in regenerative medicine, developmental biology and cancer. Regen Med 6(6):667–673

    PubMed  Google Scholar 

  • Levin M (2012a) Morphogenetic fields in embryogenesis, regeneration, and cancer: non-local control of complex patterning. Biosystems 109(3):243–261

    PubMed Central  PubMed  Google Scholar 

  • Levin M (2012b) Molecular bioelectricity in developmental biology: new tools and recent discoveries. BioEssays 34(3):205–217

    CAS  PubMed Central  PubMed  Google Scholar 

  • Levin M, Stevenson CG (2012) Regulation of cell behavior and tissue patterning by bioelectrical signals: challenges and opportunities for biomedical engineering. Annu Rev Biomed Eng 14:295–323

    CAS  PubMed  Google Scholar 

  • Levine M (2010) Transcriptional enhancers in animal development and evolution. Curr Biol 20(17):R754–R763

    CAS  PubMed  Google Scholar 

  • Lipton BH, Bensch KG, Karasek MA (1991) Microvessel endothelial cell transdifferentiation: phenotypic characterization. Differentiation 46(2):117–133

    CAS  PubMed  Google Scholar 

  • Liu J, Wang ZA (2012) Classical solutions and steady states of an attraction-repulsion chemotaxis in one dimension. J Biol Dyn 6(Suppl 1):31–41

    PubMed  Google Scholar 

  • Liu F, van der Lijn F, Schurmann C, Zhu G, Chakravarty MM et al (2012) A genome-wide association study identifies five loci influencing facial morphology in Europeans. PLoS Genet 8(9):e1002932

    CAS  PubMed Central  PubMed  Google Scholar 

  • Loehlin DQ, Werren JH (2012) Evolution of shape by multiple regulatory changes to a growth gene. Science 335(6071):943–947

    CAS  PubMed Central  PubMed  Google Scholar 

  • Maini PK, Crampin EJ, Hackborn WW (2002) Pattern formation in reaction–diffusion models with nonuniform domain growth. Bull Math Biol 64(4):747–769

    PubMed  Google Scholar 

  • Mandelbrot BB (1982) The fractal geometry of nature. WH Freeman and co, San Francisco

    Google Scholar 

  • Mansfield JH (2013) cis-regulatory change associated with snake body plan evolution. PNAS 110(26):10473–10474

    CAS  PubMed Central  PubMed  Google Scholar 

  • Marks DS, Colwell LJ, Sheridan R, Hopf TA, Pagnani A, Zecchina R, Sander C (2011) Protein 3D structure computed from evolutionary sequence variation. PLoS One 6(12):e28766

    CAS  PubMed Central  PubMed  Google Scholar 

  • Matthee CA, Burzlaff JD, Taylor JF, Davis SK (2001) Mining the mammalian genome for artiodactyl systematics. Syst Biol 50:367–390

    CAS  PubMed  Google Scholar 

  • McLean CY, Reno PL, Pollen AA, Bassan AI, Capellini TD, Guenther C, Indjeian VB, Lim X, Menke DB, Schaar BT, Wenger AM, Bejerano G, Kingsley DM (2011) Human-specific loss of regulatory DNA and the evolution of human-specific traits. Nature 471(7337):216–219

    CAS  PubMed Central  PubMed  Google Scholar 

  • McMahon AP, Ingham PW, Tabin CJ (2003) Developmental roles and clinical significance of hedgehog signaling. Curr Top Dev Biol 53:1–114

    CAS  PubMed  Google Scholar 

  • Meinhardt H (2012) Modeling pattern formation in hydra: a route to understanding essential steps in development. Int J Dev Biol 56(6–8):447–462

    CAS  PubMed  Google Scholar 

  • Meinhardt H, Gierer A (2000) Pattern formation by local self-activation and lateral inhibition. BioEssays 22:753–760

    CAS  PubMed  Google Scholar 

  • Merks RMH, Glazier JA (2005) A cell-centred approach to developmental biology. Phys A 352:113–130

    CAS  Google Scholar 

  • Minguillon C, Del Buono J, Logan MP (2005) Tbx5 and Tbx4 are not sufficient to determine limb-specific morphologies but have common roles in initiating limb outgrowth. Dev Cell 8(1):75–84

    CAS  PubMed  Google Scholar 

  • Minguillón C, Gardenyes J, Serra E, Castro LF, Hill-Force A, Holland PW, Amemiya CT, Garcia-Fernàndez J (2005) No more than 14: the end of the amphioxus Hox cluster. Int J Biol Sci 1(1):19–23

    PubMed Central  PubMed  Google Scholar 

  • Misteli T (2001) The concept of self-organization in cellular architecture. J Cell Biol 155(2):181–186

    CAS  PubMed Central  PubMed  Google Scholar 

  • Moens CB, Selleri L (2006) Hox co-factors in vertebrate development. Dev Biol 291:193–206

    CAS  PubMed  Google Scholar 

  • Monteiro A, Podlaha O (2009) Wings, horns, and butterfly eyespots: how do complex traits evolve? PLoS Biol 7(2):e37

    PubMed  Google Scholar 

  • Morelli LG, Uriu K, Ares S, Oates AC (2012) Computational approaches to developmental patterning. Science 336:187–191

    CAS  PubMed  Google Scholar 

  • Müller P, Rogers KW, Jordan BM, Lee JS, Robson D, Ramanathan S, Schier AF (2012) Differential diffusivity of nodal and lefty underlies a reaction-diffusion patterning system. Science 336(6082):721–724

    PubMed Central  PubMed  Google Scholar 

  • Murata S, Yashiroda H, Tanaka K (2009) Molecular mechanisms of proteasome assembly. Nat Rev Mol Cell Biol 10(2):104–115

    CAS  PubMed  Google Scholar 

  • Naiche LA, Papaioannou VE (2007) Tbx4 is not required for hindlimb identity or post-bud hindlimb outgrowth. Development 134(1):93–103

    CAS  PubMed  Google Scholar 

  • Nelson TR, Manchester DK (1988) Modeling of lung morphogenesis using fractal geometries. IEEE Trans Med Imaging 7(4):321–327

    CAS  PubMed  Google Scholar 

  • Newman SA (2012) Physico-genetic determinants in the evolution of development. Science 338(6104):217–219

    CAS  PubMed  Google Scholar 

  • Newman SA, Bhat R (2008) Dynamical patterning modules: physico-genetic determinants of morphological development and evolution. Phys Biol 5(1):015008

    PubMed  Google Scholar 

  • Newman SA, Linde-Medina M (2013) Physical determinants in the emergence and inheritance of multicellular form. Biological Theory 8(3):274–285

    Google Scholar 

  • Nicolis G (1977) Self-organization in non-equilibrium systems. Wiley, Prigogine

    Google Scholar 

  • Niehrs C (2010) On growth and form: a Cartesian coordinate system of Wnt and BMP signaling specifies bilaterian body axes. Development 137:845–857

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Noble D (2013) Physiology is rocking the foundations of evolutionary biology. Exp Physiol 98(8):1235–1243

    PubMed  Google Scholar 

  • Pai VP, Aw S, Shomrat T, Lemire JM, Levin M (2011) Transmembrane voltage potential controls embryonic eye patterning in Xenopus laevis. Development 139(3):623

    Google Scholar 

  • Papaseit C, Pochon N, Tabony J (2000) Microtubule self-organization is gravity-dependent. Proc Natl Acad Sci USA 97:8364–8368

    CAS  PubMed Central  PubMed  Google Scholar 

  • Paternoster L, Zhurov AI, Toma AM, Kemp JP, St Pourcain B et al (2012) Genome-wide association study of three-dimensional facial morphology identifies a variant in PAX3 associated with nasion position. Am J Hum Genet 90:478–485

    CAS  PubMed Central  PubMed  Google Scholar 

  • Pauli A, Rinn JL, Schier AF (2011) Non-coding RNAs as regulators of embryogenesis. Nat Rev Genet 12(2):136–149

    CAS  PubMed Central  PubMed  Google Scholar 

  • Paulsen M, Legewie S, Eils R, Karaulanov E, Niehrs C (2011) Negative feedback in the bone morphogenetic protein 4 (BMP4) synexpression group governs its dynamic signaling range and canalizes development. Proc Natl Acad Sci USA 108:10202–10207

    CAS  PubMed Central  PubMed  Google Scholar 

  • Pennacchio LA, Ahituv N, Moses AM, Prabhakar S, Nobrega MA, Shoukry M, Minovitsky S, Dubchak I, Holt A, Lewis KD (2006) In vivo enhancer analysis of human conserved non-coding sequences. Nature 444:499–502

    CAS  PubMed  Google Scholar 

  • Piotrowska K, Zernicka-Goetz M (2001) Role for sperm in spatial patterning of the early mouse embryo. Nature 409(6819):517–521

    CAS  PubMed  Google Scholar 

  • Pivar S (2009) On the origin of form: evolution by self-organization. North Atlantic Books, Berkeley

    Google Scholar 

  • Pivar S (2011) The origin of the vertebrate skeleton. Int J Astrobiol 10:45–65

    Google Scholar 

  • Pletikos M, Sousa AM, Sedmak G, Meyer KA, Zhu Y, Cheng F, Li M, Kawasawa YI, Sestan N (2014) Temporal Specification and Bilaterality of Human Neocortical Topographic Gene Expression. Neuron 81(2):321–332. doi: 10.1016/j.neuron.2013.11.018

    Google Scholar 

  • Poyton RO (1983) Memory and membranes: expression of genetic and spatial memory during the assembly of organelle macrocompartments. Mod Cell Biol 2:15–72

    CAS  Google Scholar 

  • Prost J, Guérin T, Martin P, Joanny JF (2010) Coordination and collective properties of molecular motors: theory. Curr Opin Cell Biol 22:14–20

    PubMed  Google Scholar 

  • Razeto-Barry P, Maldonado K (2011) Adaptive cis-regulatory changes may involve few mutations. Evolution 65(11):3332–3335

    CAS  PubMed  Google Scholar 

  • Rebeiz M, Castro B, Liu F, Yue F, Posakony JW (2012) Ancestral and conserved cis-regulatory architectures in developmental control genes. Dev Biol 362(2):282–294

    CAS  PubMed Central  PubMed  Google Scholar 

  • Renfree MB, Chew KY, Yu H, Pask AJ, Shaw G (2012) HOXA13 and HOXD13 expression during development of the syndactylous digits in the marsupial Macropus eugenii. BMC Dev Biol 12:2

    PubMed Central  PubMed  Google Scholar 

  • Reversade B, De Robertis EM (2005) Regulation of ADMP and BMP2/4/7 at opposite embryonic poles generates a self-regulating morphogenetic field. Cell 123:1147–1160

    CAS  PubMed Central  PubMed  Google Scholar 

  • Rodriguez-Esteban C, Tsukui T, Yonei S, Magallon J, Tamura K, Izpisua Belmonte JC (1999) The T-box genes Tbx4 and Tbx5 regulate limb outgrowth and identity. Nature 398(6730):814–818

    CAS  PubMed  Google Scholar 

  • Roensch K, Tazaki A, Chara O, Tanaka EM (2013) Progressive specification rather than intercalation of segments during limb regeneration. Science 342(6164):1375–1379

    CAS  PubMed  Google Scholar 

  • Rohlf FJ (1986) Relationships among eigenshape analysis, Fourier analysis, and analysis of coordinates. Math Geol 18:845–854

    Google Scholar 

  • Rosette C, Karin M (1995) Cytoskeletal control of gene expression: depolymerization of microtubules activates NF-xB. J Cell Biol 128:1111–1119

    CAS  PubMed  Google Scholar 

  • Ruvinsky I, Ruvkun G (2003) Functional tests of enhancer conservation between distantly related species. Development 130(21):5133–5142

    CAS  PubMed  Google Scholar 

  • Sagai T, Hosoya M, Mizushina Y, Tamura M, Shiroishi T (2005) Elimination of a long-range cis-regulatory module causes complete loss of limb-specific Shh expression and truncation of the mouse limb. Development 132(4):797–803

    CAS  PubMed  Google Scholar 

  • Salazar-Ciudad I, Jernvall J, Newman SA (2003) Mechanisms of pattern formation in development and evolution. Development 130:2027–2037

    CAS  PubMed  Google Scholar 

  • Sansom R (2011) Ingenious genes: how gene regulation networks evolve to control development. MIT Press, Cambridge

    Google Scholar 

  • Schiffmann Y (1997) Self-organization in biology and development. Prog Biophys Mol Biol 68(2–3):145–205

    CAS  PubMed  Google Scholar 

  • Schiffmann Y (2012) Maternal-effect genes as the recording genes of Turing-Child patterns: sequential compartmentalization in Drosophila. Prog Biophys Mol Biol 109(1–2):16–32

    CAS  PubMed  Google Scholar 

  • Schneider I, Shubin NH, Aneas I, Gehrke AR, Dahn RD, Nobrega MA (2011) Appendage expression driven by the Hoxd Global Control Region is an ancient gnathostome feature. Proc Natl Acad Sci USA 108(31):12782–12786

    CAS  PubMed Central  PubMed  Google Scholar 

  • Scimone ML, Srivastava M, Bell GW, Reddien PW (2011) A regulatory program for excretory system regeneration in planarians. Development 138(20):4387–4398

    CAS  PubMed Central  PubMed  Google Scholar 

  • Shapiro MD, Marks ME, Peichel CL, Blackman BK, Nereng KS, Jónsson B, Schluter D, Kingsley DM (2004) Genetic and developmental basis of evolutionary pelvic reduction in threespine sticklebacks. Nature 428(6984):717–723

    CAS  PubMed  Google Scholar 

  • Shapiro MD, Bell MA, Kingsley DM (2006) Parallel genetic origins of pelvic reduction in vertebrates. Proc Natl Acad Sci USA 103(37):13753–13758

    CAS  PubMed Central  PubMed  Google Scholar 

  • Sheth R, Marcon L, Bastida MF, Junco M, Quintana L, Dahn R, Kmita M, Sharpe J, Ros MA (2012) Hox genes regulate digit patterning by controlling the wavelength of a Turing-type mechanism. Science 338(6113):1476–1480

    CAS  PubMed  Google Scholar 

  • Shi R, Borgens RB (1995) Three-dimensional gradients of voltage during develop-ment of the nervous system as invisible coordinates for the establishment of embryonic pattern. Dev Dyn 202:101–114

    CAS  PubMed  Google Scholar 

  • Shubin N, Dahn R (2004) Lost and found. Nature 428(6984):703–704

    CAS  PubMed  Google Scholar 

  • Simmons RE, Altwegg R (2010) Necks-for-sex or competing browsers? A critique of ideas on the evolution of giraffe. J Zool 282(1):6–12

    Google Scholar 

  • Stern DL, Orgogozo V (2008) The loci of evolution: how predictable is genetic evolution? Evolution 62(9):2155–2177

    PubMed Central  PubMed  Google Scholar 

  • Struhl K (1993) Yeast transcription factors. Curr Opin Cell Biol 5(3):513–520

    CAS  PubMed  Google Scholar 

  • Sun YH, Chen SP, Wang YP, Hu W, Zhu ZY (2005) Cytoplasmic impact on cross-genus cloned fish derived from transgenic common carp (Cyprinus carpio) nuclei and goldfish (Carassius auratus) enucleated eggs. Biol Reprod 72(3):510–515

    CAS  PubMed  Google Scholar 

  • Thewissen JGM (1999) The emergence of whales. Springer, New York

    Google Scholar 

  • Thom R (1972) Structural stability and morphogenesis. WA Benjamin Reading, Massachusetts

    Google Scholar 

  • Thompson DW (1917) On growth and form. Cambridge University Press, Cambridge

    Google Scholar 

  • Tian NM, Price DJ (2005) Why cavefish are blind. BioEssays 27(3):235–238

    CAS  PubMed  Google Scholar 

  • Tiraihi A, Tiraihi M, Tiraihi T (2011) Self-organization of developing embryo using scale-invariant approach. Theor Biol Med Model 8:17

    PubMed Central  PubMed  Google Scholar 

  • Vandenberg LN, Morrie RD, Adams DS (2011) V-ATPase-dependent ectodermal voltage and pH regionalization are required for craniofacial morphogenesis. Dev Dyn 240(8):1889–1904

    CAS  PubMed  Google Scholar 

  • Vandenberg LN, Adams DS, Levin M (2012) Normalized shape and location of perturbed craniofacial structures in the Xenopus tadpole reveal an innate ability to achieve correct morphology. Dev Dyn 241:863–878

    PubMed Central  PubMed  Google Scholar 

  • Vogel G (2012) Turing pattern fingered for digit formation. Science 338(6113):1406

    CAS  PubMed  Google Scholar 

  • Waddington CH (1957) The strategy of the genes. George Allen & Unwin, Australia

    Google Scholar 

  • Wang IE, Reddien PW, Wagner DE (2011) Clonogenic neoblasts are pluripotent adult stem cells that underlie planarian regeneration. Science 332(6031):811–816

    PubMed Central  PubMed  Google Scholar 

  • Wartlick O, Kicheva A, González-Gaitán M (2009) Morphogen gradient formation. Cold Spring Harb Perspect Biol 1(3):a001255

    PubMed Central  PubMed  Google Scholar 

  • Wei C, Larsen M, Hoffman MP, Yamada KM (2007) Self-organization and branching morphogenesis of primary salivary epithelial cells. Tissue Eng 13(4):721–735

    CAS  PubMed  Google Scholar 

  • Weibel ER (1991) Fractal geometry: a design principle for living organisms. Am J Physiol 261(6 Pt 1):L361–L369

    CAS  PubMed  Google Scholar 

  • Weiss PA (1939) Principles of development; a text in experimental embryology. H. Holt and Company, New York

    Google Scholar 

  • Weissman A (1892) Das Keimplasm (The Germ Plasm). Fischer, Jena

    Google Scholar 

  • Wells J (2011) Gene regulatory networks in embryos depend on pre-existing spatial coordinates. Abstract #347: Society for Developmental Biology Annual Meeting, Chicago

  • Wennekamp S, Mesecke S, Nédélec F, Hiiragi T (2013) A self-organization framework for symmetry breaking in the mammalian embryo. Nat Rev Mol Cell Biol 14(7):454–461

    CAS  Google Scholar 

  • Wittkopp PJ (2006) Evolution of cis-regulatory sequence and function in Diptera. Heredity (Edinb) 97(3):139–147

    CAS  Google Scholar 

  • Wolpert L (1969) Positional information and the spatial pattern of cellular differentiation. J Theor Biol 25:1–47

    CAS  PubMed  Google Scholar 

  • Wolpert L (1989) Positional information revisited. Development 107(Suppl):3–12

    PubMed  Google Scholar 

  • Wolpert L (1991) The triumph of the embryo. Oxford University Press, Oxford

    Google Scholar 

  • Wolpert L (2010) Positional information and patterning revisited. J Theor Biol 269(1):359–365

    PubMed  Google Scholar 

  • Woltering JM, Noordermeer D, Leleu M, Duboule D (2014) Conservation and Divergence of Regulatory Strategies at Hox Loci and the Origin of Tetrapod Digits. PLoS Biol 12(1):e1001773

    PubMed Central  PubMed  Google Scholar 

  • Turing AM (1952) The chemical basis of morphogenesis philosophical transactions of the royal society of London. Series B Biological Sci 237:641

    Google Scholar 

  • Yim HS et al (2014) Minke whale genome and aquatic adaptation in cetaceans. Nat Genet 46(1):88–92

    CAS  PubMed Central  PubMed  Google Scholar 

  • Yoshida H, Kaneko K (2009) Unified description of regeneration by coupled dynamical systems theory: intercalary/segmented regeneration in insect legs. Dev Dyn 238:1974–1983

    PubMed  Google Scholar 

  • Zhang YD, Chen Z, Song YQ, Liu C, Chen YP (2005) Making a tooth: growth factors, transcription factors, and stem cells. Cell Res 15(5):301–316

    CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Joseph E. Hannon Bozorgmehr.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bozorgmehr, J.E.H. The role of self-organization in developmental evolution. Theory Biosci. 133, 145–163 (2014). https://doi.org/10.1007/s12064-014-0200-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12064-014-0200-4

Keywords

Navigation