Skip to main content
SpringerLink
Log in

Physical Determinants in the Emergence and Inheritance of Multicellular Form

  • Thematic Issue Article: Emergence of Shape
  • Published:
Biological Theory Aims and scope Submit manuscript

Abstract

We argue that the physics of complex materials and self-organizing processes should be made central to the biology of form. Rather than being encoded in genes, form emerges when cells and certain of their molecules mobilize physical forces, effects, and processes in a multicellular context. What is inherited from one generation to the next are not genetic programs for constructing organisms, but generative mechanisms of morphogenesis and pattern formation and the initial and boundary conditions for reproducing the specific traits of a taxon. There is no inherent antagonism between this “physicalist” perspective and genetics, since physics acts on matter, and gene products are essential material components of living systems whose variability affects the systems’ parameters. We make this notion concrete by summarizing the concept of “dynamical patterning modules” (DPMs; Newman and Bhat, Phys Biol 5:1–14, 2008; Int J Dev Biol 53:693–705, 2009), an explicit physico-genetic framework for the origin and evolution of multicellular form in animals, as well as (when differences in interaction toolkit genes and applicable physical processes are taken into account) in multicellular plants (Hernández-Hernández et al., Int J Dev Biol 56:661–674, 2012). DPMs provide the missing link between development and evolution by revealing how genes acting in concert with physics can generate and transform morphology in a heritable fashion.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • Abedin M, King N (2008) The premetazoan ancestry of cadherins. Science 319:946–948

    Article  Google Scholar 

  • Allen GE (1986) T. H. Morgan and the split between embryology and genetics, 1910–35. In: Horder TJ, Witkowski JA, Wylie CC (eds) A history of embryology. Cambridge University Press, Cambridge, pp 113–146

    Google Scholar 

  • Amundson R (2007) The changing role of the embryo in evolutionary thought. Cambridge University Press, Cambridge

    Google Scholar 

  • Bateson W, Bateson B (1928) William Bateson, F. R. S., naturalist; his essays & addresses, together with a short account of his life. Cambridge University Press, Cambridge

  • Brodland GW (2002) The differential interfacial tension hypothesis (DITH): a comprehensive theory for the self-rearrangement of embryonic cells and tissues. J Biomech Eng 124:188–197

    Article  Google Scholar 

  • Carroll S, Grenier J, Weatherbee S (2005) From DNA to diversity: molecular genetics and the evolution of animal design. Blackwell, Malden

    Google Scholar 

  • Christley S, Alber MS, Newman SA (2007) Patterns of mesenchymal condensation in a multiscale, discrete stochastic model. PLoS Comput Biol 3:e76

    Article  Google Scholar 

  • Cobb M (2013) 1953: when genes became "information". Cell 153:503–506

    Google Scholar 

  • Conway Morris S (2006) Darwin’s dilemma: the realities of the Cambrian “explosion”. Philos Trans R Soc Lond B 361:1069–1083

    Article  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

    Article  Google Scholar 

  • Damon BJ, Mezentseva NV, Kumaratilake JS, Forgacs G, Newman SA (2008) Limb bud and flank mesoderm have distinct “physical phenotypes” that may contribute to limb budding. Dev Biol 321:319–330

    Article  Google Scholar 

  • Darwin C (1868) The variation of animals and plants under domestication. J. Murray, London de Gennes PG (1992) Soft matter. Science 256:495–497

    Google Scholar 

  • Delbrück M (1976) How Aristotle discovered DNA. In: Huang K (ed) Physics and our world: a symposium in honor of Victor E. Weisskopf. American Institute of Physics, New York, pp 123–130

    Google Scholar 

  • Depew DJ, Weber BH (1996) Darwinism evolving: systems dynamics and the genealogy of natural selection. MIT Press, Cambridge, MA

    Google Scholar 

  • Dequéant ML, Glynn E, Gaudenz K, Wahl M, Chen J, Mushegian A, Pourquié O (2006) A complex oscillating network of signaling genes underlies the mouse segmentation clock. Science 314:1595–1598

    Article  Google Scholar 

  • Droser ML, Gehling JG (2008) Synchronous aggregate growth in an abundant new Ediacaran tubular organism. Science 319:1660–1662

    Article  Google Scholar 

  • Ehebauer M, Hayward P, Arias AM (2006) Notch, a universal arbiter of cell fate decisions. Science 314:1414–1415

    Article  Google Scholar 

  • Einstein A (1905) Über die von der molekularkinetischen Theorie der Wärme geforderte Bewegung von in ruhenden Flüssigkeiten suspendierten Teilchen. Ann Phys 17:549–560

    Article  Google Scholar 

  • Forgacs G, Newman SA (2005) Biological physics of the developing embryo. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Godt D, Tepass U (1998) Drosophila oocyte localization is mediated by differential cadherin-based adhesion. Nature 395:387–391

    Article  Google Scholar 

  • Gómez C, Pourquié O (2009) Developmental control of segment numbers in vertebrates. J Exp Zool B Mol Dev Evol 312:533–544

    Article  Google Scholar 

  • Goodwin BC (1985) What are the causes of morphogenesis? BioEssays 3:32–36

    Article  Google Scholar 

  • Gould SJ (1982) Darwinism and the expansion of evolutionary theory. Science 216:380–387

    Article  Google Scholar 

  • Gould SJ (2002) The structure of evolutionary theory. Harvard University Press, Cambridge

    Google Scholar 

  • Gould SJ, Vrba ES (1982) Exaptation—a missing term in the science of form. Paleobiology 8:4–15

    Google Scholar 

  • Hernández-Hernández V, Niklas KJ, Newman SA, Benítez M (2012) Dynamical patterning modules in plant development and evolution. Int J Dev Biol 56:661–674

    Article  Google Scholar 

  • Jia D, Dajusta D, Foty RA (2007) Tissue surface tensions guide in vitro self-assembly of rodent pancreatic islet cells. Dev Dyn 236:2039–2049

    Article  Google Scholar 

  • Judson HF (1996) The eighth day of creation: makers of the revolution in biology. Cold Spring Harbor Laboratory Press, New York

    Google Scholar 

  • Kant I (1966) Critique of Judgement 1790 (Bernard JH, trans). Hafner, New York (Original work was published in 1790)

  • Karner C, Wharton KA Jr, Carroll TJ (2006a) Planar cell polarity and vertebrate organogenesis. Semin Cell Dev Biol 17:194–203

    Article  Google Scholar 

  • Karner C, Wharton KA, Carroll TJ (2006b) Apical-basal polarity, Wnt signaling and vertebrate organogenesis. Semin Cell Dev Biol 17:214–222

    Article  Google Scholar 

  • Kay LE (2000) Who wrote the book of life? A history of the genetic code. Stanford University Press, Stanford

    Google Scholar 

  • Keller R (2002) Shaping the vertebrate body plan by polarized embryonic cell movements. Science 298:1950–1954

    Article  Google Scholar 

  • Keller R, Davidson L, Edlund A, Elul T, Ezin M, Shook D, Skoglund P (2000) Mechanisms of convergence and extension by cell intercalation. Philos Trans R Soc Lond B 355:897–922

    Article  Google Scholar 

  • King N, Westbrook MJ, Young SL, Kuo A, Abedin M, Chapman J, Fairclough S et al (2008) The genome of the choanoflagellate Monosiga brevicollis and the origin of metazoans. Nature 451:783–788

    Article  Google Scholar 

  • Kolmogorov A, Petrovsky L, Piskunov N (1937) An investigation of the diffusion equation combined with an increase in mass and its application to a biological problem. Bulletin of the University of Moscow Ser Int A1 6:1–26

    Google Scholar 

  • Krieg M et al (2008) Tensile forces govern germ-layer organization in zebrafish. Nat Cell Biol 10:429–436

    Article  Google Scholar 

  • Lamarck JB (1984) Zoological philosophy: an exposition with regard to the natural history of animals (Elliot H, trans), 1809. University of Chicago Press, Chicago

  • Lang BF, O’Kelly C, Nerad T, Gray MW, Burger G (2002) The closest unicellular relatives of animals. Curr Biol 12:1773–1778

    Article  Google Scholar 

  • Larroux C, Luke GN, Koopman P, Rokhsar DS, Shimeld SM, Degnan BM (2008) Genesis and expansion of metazoan transcription factor gene classes. Mol Biol Evol 25:980–996

    Article  Google Scholar 

  • Lenoir T (1982) The strategy of life: teleology and mechanics in nineteenth century German biology. Reidel, Dordrecht

    Google Scholar 

  • Lenoir T (1987) The eternal laws of form: morphotypes and the conditions of existence in Goethe’s biological thought. In: Amrine F, Zucker F, Wheeler H (eds) Goethe and the sciences: a re-appraisal. Reidel, Dordrecht, pp 17–28

  • Levine H, Ben-Jacob E (2004) Physical schemata underlying biological pattern formation-examples, issues and strategies. Phys Biol 1:P14–P22

    Article  Google Scholar 

  • Lewis J (2003) Autoinhibition with transcriptional delay: a simple mechanism for the zebrafish somitogenesis oscillator. Curr Biol 13:1398–1408

    Article  Google Scholar 

  • Linde-Medina M (2010) Natural selection and self-organization: a deep dichotomy in the study of organic form. Ludus Vitalis 18:25–56

    Google Scholar 

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

    Article  Google Scholar 

  • Mendoza M, Redemann S, Brunner D (2005) The fission yeast MO25 protein functions in polar growth and cell separation. Eur J Cell Biol 84:915–926

    Article  Google Scholar 

  • Miura T, Shiota K, Morriss-Kay G, Maini PK (2006) Mixed-mode pattern in Doublefoot mutant mouse limb—Turing reaction-diffusion model on a growing domain during limb development. J Theor Biol 240:562–573

    Article  Google Scholar 

  • Monk NA (2003) Oscillatory expression of Hes1, p53, and NF-kappaB driven by transcriptional time delays. Curr Biol 13:1409–1413

    Article  Google Scholar 

  • Müller GB, Newman SA (2005) The innovation triad: an EvoDevo agenda. J Exp Zool B Mol Dev Evol 304:487–503

    Article  Google Scholar 

  • Newman SA (1994) Generic physical mechanisms of tissue morphogenesis: a common basis for development and evolution. J Evol Biol 7:467–488

    Article  Google Scholar 

  • Newman SA (1998) Epithelial morphogenesis: a physico-evolutionary interpretation. In: Chuong C-M (ed) Molecular basis of epithelial appendage morphogenesis. R. G. Landes, Austin, pp 341–358

    Google Scholar 

  • Newman SA (2002) Developmental mechanisms: putting genes in their place. J Biosci 27:97–104

    Article  Google Scholar 

  • Newman SA (2007) William Bateson’s physicalist ideas. In: Laubichler M, Maienschein J (eds) From embryology to evo-devo: a history of developmental evolution. MIT Press, Cambridge, MA, pp 83–108

    Google Scholar 

  • Newman SA (2010) Dynamical patterning modules. In: Pigliucci M, Müller GB (eds) Evolution: an extended synthesis. MIT Press, Cambridge, MA, pp 281–306

    Google Scholar 

  • Newman SA (2011) Animal egg as evolutionary innovation: a solution to the “embryonic hourglass” puzzle. J Exp Zool B Mol Dev Evol 316:467–483

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Newman SA, Bhat R (2007) Activator-inhibitor dynamics of vertebrate limb pattern formation. Birth Defects Res C Embryo Today 81:305–319

    Article  Google Scholar 

  • Newman SA, Bhat R (2008) Dynamical patterning modules: physico-genetic determinants of morphological development and evolution. Phys Biol 5:1–14

    Article  Google Scholar 

  • Newman SA, Bhat R (2009) Dynamical patterning modules: a “pattern language” for development and evolution of multicellular form. Int J Dev Biol 53:693–705

    Article  Google Scholar 

  • Newman SA, Bhat R (2011) Lamarck’s dangerous idea. In: Gissis SB, Jablonka E (eds) Transformations of Lamarckism: from subtle fluids to molecular biology. MIT Press, Cambridge, MA, pp 157–169

    Google Scholar 

  • Newman SA, Comper WD (1990) “Generic” physical mechanisms of morphogenesis and pattern formation. Development 110:1–18

    Google Scholar 

  • Newman SA, Forgacs G, Müller GB (2006) Before programs: the physical origination of multicellular forms. Int J Dev Biol 50:289–299

    Article  Google Scholar 

  • Newman SA, Bhat R, Mezentseva NV (2009) Cell state switching factors and dynamical patterning modules: complementary mediators of plasticity in development and evolution. J Biosci 34:553–572

    Article  Google Scholar 

  • Nichols SA, Dirks W, Pearse JS, King N (2006) Early evolution of animal cell signaling and adhesion genes. Proc Natl Acad Sci USA 103:12451–12456

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Odling-Smee FJ, Laland KN, Feldman MW (2003) Niche construction: the neglected process in evolution. Princeton University Press, Princeton

    Google Scholar 

  • Owen R (1848) On the archetype and homologies of the vertebrate skeleton microform. J. Van Voorst, London

    Google Scholar 

  • Owen R (1849) On the nature of limbs: a discourse delivered on Friday, February 9, at an evening meeting of the Royal Institution of Great Britain. J. Van Voorst, London

    Google Scholar 

  • Palmeirim I, Henrique D, Ish-Horowicz D, Pourquié O (1997) Avian hairy gene expression identifies a molecular clock linked to vertebrate segmentation and somitogenesis. Cell 91:639–648

    Article  Google Scholar 

  • Philippe H, Snell EA, Bapteste E, López P, Holland PW, Casane D (2004) Phylogenomics of eukaryotes: impact of missing data on large alignments. Mol Biol Evol 21:1740–1752

    Article  Google Scholar 

  • Rashevsky N (1948) Mathematical biophysics. University of Chicago Press, Chicago

    Google Scholar 

  • Richards RJ (1992) The meaning of evolution: the morphological construction and ideological reconstruction of Darwin’s theory. University of Chicago Press, Chicago

    Book  Google Scholar 

  • Richardson MK (1999) Vertebrate evolution: the developmental origins of adult variation. BioEssays 21:604–613

    Article  Google Scholar 

  • Robert JS (2004) Embryology, epigenesis and evolution: taking development seriously. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Rokas A, Kruger D, Carroll SB (2005) Animal evolution and the molecular signature of radiations compressed in time. Science 310:1933–1938

    Article  Google Scholar 

  • Ros MA, Lyons GE, Mackem S, Fallon JF (1994) Recombinant limbs as a model to study homeobox gene regulation during limb development. Dev Biol 166:59–72

    Article  Google Scholar 

  • Rose SM (1958) Feedback in the differentiation of cells. Sci Am 199(6):36–41

    Article  Google Scholar 

  • Schrödinger E (1945) What is life? The physical aspect of the living cell. Cambridge University Press, New York

    Google Scholar 

  • Schwartz JH, Maresca B (2006) Do molecular clocks run at all? A critique of molecular systematics. Biol Theory 1:357–371

    Article  Google Scholar 

  • Sebé-Pedrós A, Roger AJ, Lang FB, King N, Ruiz-Trillo I (2010) Ancient origin of the integrin-mediated adhesion and signaling machinery. Proc Natl Acad Sci USA 107:10142–10147

    Article  Google Scholar 

  • Shalchian-Tabrizi K, Minge MA, Espelund M, Orr R, Ruden T, Jakobsen KS, Cavalier-Smith T (2008) Multigene phylogeny of choanozoa and the origin of animals. PLoS One 3:e2098

    Article  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 338:1476–1480

    Article  Google Scholar 

  • Simpson GG (1950) The meaning of evolution. Yale University Press, New Haven

    Google Scholar 

  • Srivastava M, Begovic E, Chapman J, Putnam NH, Hellsten U, Kawashima T, Kuo A, Mitros T, Salamov A, Carpenter ML, Signorovitch AY, Moreno MA, Kamm K, Grimwood J, Schmutz J, Shapiro H, Grigoriev IV, Buss L, Schierwater B, Dellaporta SL, Rokhsar DS (2008) The Trichoplax genome and the nature of placozoans. Nature 454:955–960

    Article  Google Scholar 

  • Srivastava M, Simakov O, Chapman J, Fahey B, Gauthier ME, Mitros T, Richards GS, Conaco C, Dacre M, Hellsten U, Larroux C, Putnam NH, Stanke M, Adamska M, Darling A, Degnan SM, Oakley TH, Plachetzki DC, Zhai Y, Adamski M, Calcino A, Cummins SF, Goodstein DM, Harris C, Jackson DJ, Leys SP, Shu S, Woodcroft BJ, Vervoort M, Kosik KS, Manning G, Degnan BM, Rokhsar DS (2010) The Amphimedon queenslandica genome and the evolution of animal complexity. Nature 466:720–726

    Google Scholar 

  • Steinberg MS (1962a) On the mechanism of tissue reconstruction by dissociated cells, I. Population kinetics, differential adhesiveness, and the absence of directed migration. Proc Natl Acad Sci USA 48:1577–1582

    Article  Google Scholar 

  • Steinberg MS (1962b) On the mechanism of tissue reconstruction by dissociated cells, III. Free energy relations and the reorganization of fused, heteronomic tissue fragments. Proc Natl Acad Sci USA 48:1769–1776

    Article  Google Scholar 

  • Steinberg MS (2007) Differential adhesion in morphogenesis: a modern view. Curr Opin Genet Dev 17:281–286

    Article  Google Scholar 

  • Strogatz SH (1994) Nonlinear dynamics and chaos. With applications to physics, biology, chemistry, and engineering. Perseus, Cambridge, MA

  • Thompson DW (1942) On growth and form. Cambridge University Press, Cambridge

    Google Scholar 

  • Tickle C (2003) Patterning systems-from one end of the limb to the other. Dev Cell 4:449–458

    Article  Google Scholar 

  • Tucker RP (2013) Horizontal gene transfer in choanoflagellates. J Exp Zool B Mol Dev Evol 320:1–9

    Article  Google Scholar 

  • Turing A (1952) The chemical basis of morphogenesis. Philos Trans R Soc Lond B 237:37–72

    Article  Google Scholar 

  • Wainright PO, Hinkle G, Sogin ML, Stickel SK (1993) Monophyletic origins of the metazoa: an evolutionary link with fungi. Science 260:340–342

    Article  Google Scholar 

  • Webster G, Goodwin B (1996) Form and transformation. Cambridge University Press, Cambridge

    Google Scholar 

  • Winklbauer R (2012) Cadherin function during Xenopus gastrulation. Subcell Biochem 60:301–320

    Article  Google Scholar 

  • Yin L, Zhu M, Knoll AH, Yuan X, Zhang J, Hu J (2007) Doushantuo embryos preserved inside diapause egg cysts. Nature 446:661–663

    Article  Google Scholar 

  • Zeller R, López-Ríos J, Zúñiga A (2009) Vertebrate limb bud development: moving towards integrative analysis of organogenesis. Nat Rev Genet 10:845–858

    Article  Google Scholar 

  • Zhu J, Zhang Y-T, Alber MS, Newman SA (2010) Bare bones pattern formation: a core regulatory network in varying geometries reproduces major features of vertebrate limb development and evolution. PLoS One 5:e10892

    Article  Google Scholar 

  • Zwilling E (1964) Development of fragmented and of dissociated limb bud mesoderm. Dev Biol 89:20–37

    Article  Google Scholar 

Download references

Acknowledgments

We thank the National Science Foundation (Grant EF-0526854 awarded to SAN) and the European Commission (Marie Curie Fellowship PIOF-GA-2008-219676 awarded to ML-M) for support.

Author information

Authors and Affiliations

  1. Department of Cell Biology and Anatomy, New York Medical College, Valhalla, NY, USA

    Stuart A. Newman & Marta Linde-Medina

  2. Faculty of Life Sciences, University of Manchester, Manchester, UK

    Marta Linde-Medina

Authors
  1. Stuart A. Newman
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Marta Linde-Medina
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Stuart A. Newman.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Newman, S.A., Linde-Medina, M. Physical Determinants in the Emergence and Inheritance of Multicellular Form. Biol Theory 8, 274–285 (2013). https://doi.org/10.1007/s13752-013-0116-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13752-013-0116-0

Keywords

Search

Navigation