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Complexity: the organizing principle at the interface of biological (dis)order

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Abstract

The term complexity means several things to biologists. When qualifying morphological phenotype, on the one hand, it is used to signify the sheer complicatedness of living systems, especially as a result of the multicomponent aspect of biological form. On the other hand, it has been used to represent the intricate nature of the connections between constituents that make up form: a more process-based explanation. In the context of evolutionary arguments, complexity has been defined, in a quantifiable fashion, as the amount of information, an informatic template such as a sequence of nucleotides or amino acids stores about its environment. In this perspective, we begin with a brief review of the history of complexity theory. We then introduce a developmental and an evolutionary understanding of what it means for biological systems to be complex. We propose that the complexity of living systems can be understood through two interdependent structural properties: multiscalarity of interconstituent mechanisms and excitability of the biological materials. The answer to whether a system becomes more or less complex over time depends on the potential for its constituents to interact in novel ways and combinations to give rise to new structures and functions, as well as on the evolution of excitable properties that would facilitate the exploration of interconstituent organization in the context of their microenvironments and macroenvironments.

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References

  • Abraham R. and Shaw C. D. 1982 Dynamics - the geometry of behavior. Aerial Press, Santa Cruz, USA.

    Google Scholar 

  • Abraham R. and Ueda Y. 2000 The chaos avant-garde memories of the early days of chaos theory, Series A, Vol. 39. World Scientific Publishing, Singapore.

  • Abraham R. H. 2011 The genesis of complexity, world futures. J. Glob. Educ. 67, 380–394.

    Google Scholar 

  • Aceto N., Bardia A., Miyamoto D. T., Donaldson M. C., Wittner B. S., Spencer J. A. et al. 2014 Circulating tumor cell clusters are oligoclonal precursors of breast cancer metastasis. Cell 158, 1110–1122.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Adami C. 2002 What is complexity? BioEssays 24, 1085–1094.

    Article  PubMed  Google Scholar 

  • Adami C., Ofria C. and Collier T. C. 2000 Evolution of biological complexity. Proc. Natl. Acad. Sci. USA 97, 4463–4468.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Akam M. 1989 Drosophila development: making stripes inelegantly. Nature 341, 282–283.

    Article  CAS  PubMed  Google Scholar 

  • Alcaraz J., Xu R., Mori H., Nelson C. M., Mroue R., Spencer V. A. et al. 2008 Laminin and biomimetic extracellular elasticity enhance functional differentiation in mammary epithelia. EMBO J. 27, 2829–2838.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Alderson D., Li L., Willinger W. and Doyle J. C. 2005 Understanding internet topology: principles, models, and validation. IEEE/ACM Trans. Netw. 13, 1205–1218.

    Article  Google Scholar 

  • Alexander C. 2002 The nature of order: an essay on the art of building and the nature of the universe. Center for Environmental Structure, Berkeley, USA.

  • Alexander C. 2004 The luminous ground: an essay on the art of building and the nature of the universe. Center for Environmental Structure, Berkeley, USA.

  • Allen B., Stacey B. C. and Bar-Yam Y. 2014 An information-theoretic formalism for multiscale structure in complex systems. arXiv: 1409.4708.

  • Aragona M., Panciera T., Manfrin A., Giulitti S., Michielin F., Elvassore N. et al. 2013 A mechanical checkpoint controls multicellular growth through YAP/TAZ regulation by actin-processing factors. Cell 154, 1047–1059.

    Article  CAS  PubMed  Google Scholar 

  • Aulehla A. and Pourquie O. 2006 On periodicity and directionality of somitogenesis. Anat. Embryo.  211, 3–8.

    Article  Google Scholar 

  • Axelrod J. D. and Tomlin C. J. 2011 Modeling the control of planar cell polarity. Wiley interdisciplinary reviews. Syst. Biol. Med. 3, 588–605.

    CAS  Google Scholar 

  • Bak P. and Paczuski M. 1995 Complexity, contingency, and criticality. Proc. Natl. Acad. Sci. USA 92, 6689–6696.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baker R. E., Schnell S. and Maini P. K. 2006 A clock and wavefront mechanism for somite formation. Dev. Biol. 293, 116–126.

    Article  CAS  PubMed  Google Scholar 

  • Bar-Yam Y. and Epstein I. R. 2004 Response of complex networks to stimuli. Proc. Natl. Acad. Sci. USA 101, 4341–4345.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barabási A.-L. 2002 Linked the new science of networks. Perseus Publisher, Cambridge, USA.

    Google Scholar 

  • Bentley P. J. 2001 Digital biology : how nature is transforming our technology and our lives. Simon and Schuster, New York, USA.

    Google Scholar 

  • Bertalanffy L. V. 1950 The theory of open systems in physics and biology. Science 111, 23–29.

    Article  Google Scholar 

  • Bertalanffy L.V. 1952 On the logical status of the theory of evolution. Laval Théologique et Philosophique 8, 161–168.

    Article  Google Scholar 

  • Bertalanffy L.V. and Laszlo E. 1972 The relevance of general systems theory; papers presented to Ludwig von Bertalanffy on his seventieth birthday. G. Braziller, New York, USA.

  • Bhat R., Belardi B., Mori H., Kuo P., Tam A., Hines W. C. et al. 2016a Nuclear repartitioning of galectin-1 by an extracellular glycan switch regulates mammary morphogenesis. Proc. Natl. Acad. Sci. USA 113, 4820–4827.

    Article  CAS  Google Scholar 

  • Bhat R., Chakraborty M., Glimm T., Stewart T. A. and Newman S. A. 2016b Deep phylogenomics of a tandem-repeat galectin regulating appendicular skeletal pattern formation. BMC Evol. Biol. 16, 162.

    Article  PubMed  PubMed Central  Google Scholar 

  • Bhat R., Lerea K. M., Peng H., Kaltner H., Gabius H. J. and Newman S. A. 2011 A regulatory network of two galectins mediates the earliest steps of avian limb skeletal morphogenesis. BMC Dev. Biol. 11, 6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bollobás B. 1998 Modern graph theory. Springer, New York, USA.

    Book  Google Scholar 

  • Braha D., Bar-Yam Y. and Minai A. A. 2006 Complex engineered systems science meets technology, understanding complex systems. Springer-Verlag GmbH, Berlin Heidelberg, Germany.

  • Briggs T. S. and Rauscher W. C. 1973 An oscillating iodine clock. J. Chem. Educ. 50, 496.

    Article  CAS  Google Scholar 

  • Camazine S. 2001 Self-organization in biological systems. Princeton University Press, Princeton, USA.

  • Chaitin G. J. 1969 On simplicity and speed of programs for computing infinite sets of natural numbers. J. ACM 16, 407–422.

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Cowan G. A. 2010 Manhattan project to the santa Fe institute : the memoirs of George A. cowan. University of New Mexico Press, Albuquerque, USA.

  • Crutchfield J. P., 1989 Inferring the dynamic, quantifying physical complexity. NATO Adv. Sci. Ser. B 208, 327–338.

    Google Scholar 

  • de Gennes P. G. 1975 The physics of liquid crystals. Clarendon Press, Oxford, UK.

  • de Gennes P. G. 1992 Soft matter. Science 256, 495–497.

    Article  PubMed  Google Scholar 

  • Dequeant M. L., Glynn E., Gaudenz K., Wahl M., Chen J., Mushegian A. and Pourquie O. 2006 A complex oscillating network of signaling genes underlies the mouse segmentation clock. Science 314, 1595–1598.

    Article  CAS  PubMed  Google Scholar 

  • Drack M. and Pouvreau D. 2015 On the history of Ludwig von Bertalanffy’s “General Systemology”, and on its relationship to cybernetics - part III: convergences and divergences. Int. J. Gen. Sys. 44, 523–571.

    Article  Google Scholar 

  • Duguay D., Foty R. A. and Steinberg M. S. 2003 Cadherin-mediated cell adhesion and tissue segregation: qualitative and quantitative determinants. Dev. Biol. 253, 309–323.

    Article  CAS  PubMed  Google Scholar 

  • Engler A. J., Humbert P. O., Wehrle-Haller B. and Weaver V. M. 2009 Multiscale modeling of form and function. Science 324, 208–212.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Engler A. J., Sen S., Sweeney H. L. and Discher D. E. 2006 Matrix elasticity directs stem cell lineage specification. Cell 126, 677–689.

    Article  CAS  PubMed  Google Scholar 

  • Epstein I. R. and Pojman J. A. 1998 An introduction to nonlinear chemical dynamics: oscillations, waves, patterns, and chaos. Oxford University Press, New York, UK.

  • Eungdamrong N. J. and Iyengar R. 2004 Modeling cell signaling networks. Biol.Cell 96, 355–362.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fell H. B. and Robison R. 1929 The growth, development and phosphatase activity of embryonic avian femora and limb-buds cultivated in vitro. Biochem. J. 23, 767–784.5.

    Google Scholar 

  • Forgács G. and Newman S. 2005 Biological physics of the developing embryo. Cambridge University Press, New York, USA.

  • Gamow G. 1955 Information transfer in the living cell. Sci. Am. 193, 70–78.

    Article  Google Scholar 

  • Gazave E., Lapebie P., Richards G. S., Brunet F., Ereskovsky A. V. and Degnan B. M. 2009 Origin and evolution of the notch signalling pathway: an overview from eukaryotic genomes. BMC Evol. Biol. 9, 249.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gell-Mann M. 1994 The quark and the jaguar: adventures in the simple and the complex. W.H. Freeman, New York, USA.

  • Gell-Mann M. 1995 What is complexity? remarks on simplicity and complexity by the nobel prize-winning author of the Quark and the Jaguar. Complexity 1, 16–19.

    Article  Google Scholar 

  • Gilbert S. F. 1991 Developmental biology. Sinauer Associates, Sunderland, USA.

    Google Scholar 

  • Glimm T., Bhat R. and Newman S. A. 2014 Modeling the morphodynamic galectin patterning network of the developing avian limb skeleton. J. Theor. Biol. 346, 86–108.

    Article  CAS  PubMed  Google Scholar 

  • Glimm T., Headon D. and Kiskowski M. A. 2012 Computational and mathematical models of chondrogenesis in vertebrate limbs. Birth Defects Res. C Embryo Today 96, 176–192.

    Article  CAS  PubMed  Google Scholar 

  • Godfrey-Smith P. 2009 Darwinian populations and natural selection. Oxford University Press, New York, UK.

    Book  Google Scholar 

  • Goodwin B. C. 1977 Mechanics, fields and statistical mechanics in developmental biology. Proc. R. Soc. London Ser. B 199, 407–414.

    Article  CAS  Google Scholar 

  • Grassberger P. 1991 Information and complexity-measures in dynamic-systems. Inf. Dyn. 256, 15–33.

    Article  Google Scholar 

  • Hall B. K. and Miyake T. 2000 All for one and one for all: condensations and the initiation of skeletal development. BioEssays 22, 138–147.

    Article  CAS  PubMed  Google Scholar 

  • Hallgrimsson B., Willmore K. and Hall B. K. 2002 Canalization, developmental stability, and morphological integration in primate limbs. Am. J. Phys. Anthropol. 35, 131–158.

    Article  PubMed  Google Scholar 

  • Hamley I. W. 2000 Introduction to soft matter: polymers, colloids, amphiphiles and liquid crystals. Wiley-Blackwell, Chichester, New York, USA.

  • Hamley I. W. 2007 Introduction to soft matter: synthetic and biological self-assembling materials. John Wiley and Sons, Chichester, UK.

  • Hardin P. E., Hall J. C. and Rosbash M. 1990 Feedback of the drosophila period gene product on circadian cycling of its messenger RNA levels. Nature 343, 536–540.

    Article  CAS  PubMed  Google Scholar 

  • Harmon D., Lagi M., de Aguiar M. A., Chinellato D. D., Braha D., Epstein I. R. and Bar-Yam Y. 2015 Anticipating economic market crises using measures of collective panic. PLoS One 10, e0131871.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hayden E. C. 2010 Human genome at ten: Life is complicated. Nature 464, 664–667.

    Article  CAS  Google Scholar 

  • Heims S. J. 1991 The cybernetics group. MIT Press, Cambridge, USA.

    Google Scholar 

  • Hunding A., Kauffman S. A. and Goodwin B. C. 1990 Drosophila segmentation: supercomputer simulation of prepattern hierarchy. J. Theor. Biol. 145, 369–384.

    Article  CAS  PubMed  Google Scholar 

  • Hynes R. O. 2012. The evolution of metazoan extracellular matrix. J. Cell Biol. 196, 671–679.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jeeva J. and Zalik S. E. 1996 Hapten inhibitors of the endogenous galactose binding lectins and anti-lectin antibodies inhibit primitive streak formation in the early chick embryo. GlycoBiology 6, 517–526.

    Article  CAS  PubMed  Google Scholar 

  • Jiang T. X., Widelitz R. B., Shen W. M., Will P., Wu D. Y., Lin C. M. et al. 2004 Integument pattern formation involves genetic and epigenetic controls: feather arrays simulated by digital hormone models. Int. J. Dev. Biol. 48, 117–135.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jorgensen S. E. 1992 Integration of ecosystem theories: a pattern, ecology and environment. Springer Netherlands, Dordrecht, Europe.

    Book  Google Scholar 

  • Kaneko K. 2007 Evolution of robustness to noise and mutation in gene expression dynamics. PLoS One 2, e434.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kaneko K. 2008 Shaping robust system through evolution. Chaos 18, 026112.

    Article  PubMed  CAS  Google Scholar 

  • Kaneko K. and Furusawa C. 2006 An evolutionary relationship between genetic variation and phenotypic fluctuation. J. Theor. Biol. 240, 78–86.

    Article  PubMed  Google Scholar 

  • Kauffman S. A. 1993 The origins of order: self organization and selection in evolution. Oxford University Press, New York, USA.

  • Kauffman S. A. 2001 Prolegomenon to a general biology. Ann. N.Y.Acad. Sci. 935, 18–36.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kirschner M., Gerhart J. and Mitchison T. 2000 Molecular “vitalism”.Cell 100, 79–88.

    Article  CAS  PubMed  Google Scholar 

  • Kolmogorov A. N. 1998 On tables of random numbers (Reprinted from Sankhya, The Indian Journal of Statistics, Series A, vol 25, 1963). Theor. Comput. Sci. 207, 387–395.

    Article  Google Scholar 

  • Lacalli T. C., Wilkinson D. A. and Harrison L. G. 1988 Theoretical aspects of stripe formation in relation to Drosophila segmentation. Development 104, 105–113.

    CAS  PubMed  Google Scholar 

  • Laland K., Uller T., Feldman M., Sterelny K., Muller G. B., Moczek A. et al. 2014 Does evolutionary theory need a rethink? Nature 514, 161–164.

    Article  CAS  PubMed  Google Scholar 

  • Laszlo E. 1979 Ludwig von Bertalanffy. Free Press, New York, USA.

    Google Scholar 

  • Lee D. H., Severin K. and Ghadiri M. R. 1997 Autocatalytic networks: the transition from molecular self-replication to molecular ecosystems. Curr. Opin. Chem. Biol. 1, 491–496.

    Article  CAS  PubMed  Google Scholar 

  • Lengyel E. 2010 Ovarian cancer development and metastasis. Am. J. Pathol. 177, 1053–1064.

    Article  PubMed  PubMed Central  Google Scholar 

  • Li C., Alderson D., Doyle J. C. and Willinger W. 2006 Towards a theory of scale-free graphs: definition, properties, and implications. Internet Math. 2, 431–523.

    Article  Google Scholar 

  • Li N., Cruz J., Chien C. S., Sojoudi S., Recht B., Stone D.et al. 2014 Robust efficiency and actuator saturation explain healthy heart rate control and variability. Proc. Natl. Acad. Sci. USA 111, 3476–3485.

    Article  CAS  Google Scholar 

  • Lorda-Diez C. I., Montero J. A., Diaz-Mendoza M. J., Garcia-Porrero J. A. and Hurle J. M. 2011 Defining the earliest transcriptional steps of chondrogenic progenitor specification during the formation of the digits in the embryonic limb. PLoS One 6, e24546.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lyell C. and Deshayes G. P. 1830 Principles of geology; being an attempt to explain the former changes of the earth’s surface, by reference to causes now in operation. J. Murray, London, England.

    Book  Google Scholar 

  • Maini P. K., Baker R. E. and Chuong C. M. 2006 Developmental biology. The turing model comes of molecular age. Science 314, 1397–1398.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mainzer K. 1997 Thinking in complexity: the complex dynamics of matter, mind, and mankind. Springer, Berlin, Germany.

  • McCulloch W. S. 1989 Collected works of Warren S. McCulloch. Intersystems Publications, Salinas, USA.

    Google Scholar 

  • Meinhardt H. 1982 Models of biological pattern formation. Academic Press, London, UK.

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Merkin J. H., Petrov V. V., Scott S. K. and Showalter K. 1996 Wave-induced chemical chaos. Phys. Rev. Lett. 76, 546–549.

    Article  PubMed  Google Scholar 

  • Mikhailov A. S. 1990 Foundations of synergetics. Springer-Verlag, Berlin, Germany.

    Book  Google Scholar 

  • Moftah M. Z., Downie S. A., Bronstein N. B., Mezentseva N., Pu J., Maher P. A. and Newman S. A. 2002 Ectodermal FGFs induce perinodular inhibition of limb chondrogenesis in vitro and in vivo via FGF receptor 2. Dev. Biol. 249, 270–282.

    Article  CAS  PubMed  Google Scholar 

  • Moses J. 2010 Flexibility and Its Relation to Complexity and Architecture. Springer-Verlag, Berlin, Germany.

  • Muller-Linow M., Hilgetag C. C. and Hutt M. T. 2008 Organization of excitable dynamics in hierarchical biological networks. PLoS Comput. Biol. 4, e1000190.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Müller G. and Pigliucci M. 2010 Evolution, the extended synthesis. MIT Press, Cambridge, USA.

    Google Scholar 

  • Nagorcka B. N. 1988 A pattern formation mechanism to control spatial organization in the embryo of Drosophila melanogaster. J. Theor. Biol. 132, 277–306.

    Article  CAS  PubMed  Google Scholar 

  • Nanjundiah V. 2003 Phenotypic plasticity and evolution by genetic assimilation. In Origination of organismal form: beyond the gene in developmental and evolutionary biology (ed. G. Müller and S. Newman), pp. 245–263. MIT Press, Cambridge, USA.

  • Nelson C. M. and Bissell M. J. 2006 Of extracellular matrix, scaffolds, and signaling: tissue architecture regulates development, homeostasis, and cancer. Annu. Rev. Cell Dev. Biol. 22, 287–309.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Newman M. E. J., Barabási A.-L. and Watts D. J. 2006a The structure and dynamics of networks, Princeton studies in complexity. Princeton University Press, New Jersey, USA.

  • Newman S. A. 1970 Note on complex systems. J. Theor. Biol. 28, 411–413.

    Article  CAS  PubMed  Google Scholar 

  • Newman S. A. 2012 Physico-genetic determinants in the evolution of development. Science 338, 217–219.

    Article  CAS  PubMed  Google Scholar 

  • Newman S. A. and Bhat R. 2007 Activator-inhibitor dynamics of vertebrate limb pattern formation. Birth Defects Res. C Embryo Today 81, 305–319.

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Newman S. A., Forgacs G. and Muller G. B. 2006b Before programs: the physical origination of multicellular forms. Int. J. Dev. Biol. 50, 289–299.

    Article  CAS  PubMed  Google Scholar 

  • Newman S. A. and Frisch H. L. 1979 Dynamics of skeletal pattern formation in developing chick limb. Science 205, 662–668.

    Article  CAS  PubMed  Google Scholar 

  • Nusslein-Volhard C. and Wieschaus E. 1980 Mutations affecting segment number and polarity in Drosophila. Nature 287, 795–801.

    Article  CAS  PubMed  Google Scholar 

  • Ozbek S., Balasubramanian P. G., Chiquet-Ehrismann R., Tucker R. P. and Adams J. C. 2010 The evolution of extracellular matrix. Mol. Biol. Cell 21, 4300–4305.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Palsson E., Lee K. J., Goldstein R. E., Franke J., Kessin R. H. and Cox E. C. 1997 Selection for spiral waves in the social amoebae Dictyostelium. Proc. Natl. Acad. Sci. USA 94, 13719–13723.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Petrov V. V., Mihaliuk E., Scott S. K. and Showalter K. 1995 Stabilizing and characterizing unstable states in high-dimensional systems from time series. Phys. Rev. 51, 3988–3996.

    CAS  Google Scholar 

  • Poincaré H. J. 1899 Les méthodes nouvelles de la mécanique céleste. Gauthiers-Villars, Paris.

    Google Scholar 

  • Ranga A., Girgin M., Meinhardt A., Eberle D., Caiazzo M., Tanaka E. M. and Lutolf M. P. 2016 Neural tube morphogenesis in synthetic 3D microenvironments. Proc. Natl. Acad. Sci. USA 113, E6831–E6839.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Raspopovic J., Marcon L., Russo L. and Sharpe J. 2014 Modeling digits. Digit patterning is controlled by a Bmp-Sox9-Wnt Turing network modulated by morphogen gradients. Science 345, 566–570.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rickles D., Hawe P. and Shiell A. 2007 A simple guide to chaos and complexity. J. Epidemiol. Community Health 61, 933–937.

    Article  PubMed  PubMed Central  Google Scholar 

  • Ros M. A., Lyons G. E., Mackem S. and Fallon J. F. 1994 Recombinant limbs as a model to study homeobox gene regulation during limb development. Dev. Biol. 166, 59–72.

    Article  CAS  PubMed  Google Scholar 

  • Rosenblueth A., Norbert W. and Bigelow J. 1943 Behavior, Purpose and Teleology. Philos. Sci. 10, 18–24.

    Article  Google Scholar 

  • Saunders Jr. J. W. 1948 The proximo-distal sequence of origin of the parts of the chick wing and the role of the ectoderm. J. Exp. Zool. 108, 363–403.

    Article  Google Scholar 

  • Shannon C. E. and Weaver W. 1964 The mathematical theory of communication. University of Illinois Press, Urbana, India.

    Google Scholar 

  • Sheth R., Marcon L., Bastida M. F., Junco M., Quintana L., Dahn R. et al. 2012 Hox genes regulate digit patterning by controlling the wavelength of a turing-type mechanism. Science 338, 1476–1480.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sick S., Reinker S., Timmer J. and Schlake T. 2006 WNT and DKK determine hair follicle spacing through a reaction-diffusion mechanism. Science 314, 1447–1450.

    Article  CAS  PubMed  Google Scholar 

  • Siegert F. and Weijer C. J. 1995 Spiral and concentric waves organize multicellular Dictyostelium mounds. Curr. Biol. 5, 937–943.

    Article  CAS  PubMed  Google Scholar 

  • Simpson P. 1997 Notch signalling in development: on equivalence groups and asymmetric developmental potential. Curr. opin. genet. dev. 7, 537–542.

    Article  CAS  PubMed  Google Scholar 

  • Solé R. V. and Goodwin B. C. 2000 Signs of life: how complexity pervades biology. Basic Books, New York, USA.

  • Solomonoff R. J. 1964a Formal theory of inductive inference Part II. Inform. Control 7, 224–254.

    Article  Google Scholar 

  • Solomonoff R. J. 1964b Formal theory of inductive inference Part I. Inform. Control 7, 1–22.

    Article  Google Scholar 

  • Spencer V. A., Xu R. and Bissell M. J. 2010 Gene expression in the third dimension: the ECM-nucleus connection. J. Mammary Gland Biol. Neoplasia 15, 65–71.

    Article  PubMed  PubMed Central  Google Scholar 

  • Sturkie P. D. 1943 Suppression of polydactyly in the domestic fowl by low temperature. J. Exp. Zool. 93, 325–346.

    Article  Google Scholar 

  • Thom R. 1975 Structural stability and morphogenesis; an outline of a general theory of models. W. A. Benjamin, San Franscisco, USA.

    Google Scholar 

  • Turing A. M. 1952 The chemical basis of morphogenesis. Philos. Trans. R. Soc. London Ser. B 237, 37–72.

    Article  Google Scholar 

  • Tyson J. J. 1976 The belousov-zhabotinskii reaction. Springer-Verlag, Berlin, Germany.

    Book  Google Scholar 

  • Ulanowicz R. E. 2003 Some steps toward a central theory of ecosystem dynamics. Comput. Biol. Chem. 27, 523–530.

    Article  CAS  PubMed  Google Scholar 

  • Wagoner Johnson A. and Harley B. A. C. 2011 Mechanobiology of cell-cell and cell-matrix interactions. Springer Science, Business Media, LLC, Boston, USA.

  • Watkins C. 2009 Selective breeding analysed as a communication channel: channel capacity as a fundamental limit on adaptive complexity. In SYNASC 2008, 10th International Symposium on Symbolic and Numeric Algorithms for Scientific Computing, Timisoara, Romania, 26–29 September 2008, pp. 514–518.

  • Webster G. and Goodwin B. 1981 History and structure in biology. Per. Biol. Med. 25, 39–62.

    Article  CAS  Google Scholar 

  • Weigel H. 1981 Eigenschaften der oszillierenden Briggs-Rauscher-Reaktion: spektralphotometrische Untersuchungen mit mikrocomputergesteuerter Photonenzählung. Minerva-Publikation, München, Germany.

  • West-Eberhard M. J. 1989 Phenotypic plasticity and the origins of diversity. Ann. Rev. Ecol. Sys. 20, 249–278.

    Article  Google Scholar 

  • Whyte J., Bergin O., Bianchi A., McNally S. and Martin F. 2009 Key signalling nodes in mammary gland development and cancer. Mitogen-activated protein kinase signalling in experimental models of breast cancer progression and in mammary gland development. Breast Cancer Res11, 209.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wiener N. 1948 Cybernetics. John Wiley publisher, New York, USA.

    Google Scholar 

  • Winfree A. T. 2001 The geometry of biological time. Springer, New York, USA.

    Book  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Wolpert L. 1989 Positional information revisited. Development 107, 3–12.

    PubMed  Google Scholar 

  • Wolpert L. 2011 Positional information and patterning revisited. J. Theor. Biol. 269, 359–365.

    Article  PubMed  Google Scholar 

  • Yagil G. 2000 Complexity and order in chemical and biological systems. In Unifying themes in complex systems (ed. Y. Bar-Yam), pp. 645–654. Perseus Books, New York, USA.

    Google Scholar 

  • Yamaguchi M., Yoshimoto E. and Kondo S. 2007 Pattern regulation in the stripe of zebrafish suggests an underlying dynamic and autonomous mechanism. Proc. Natl. Acad. Sci. USA 104, 4790–4793.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zachary G. P. 1997 Endless frontier: Vannevar Bush, engineer of the American century. Free Press, New York, USA.

  • Zhang D., Gyorgyi L. and Peltier W. R. 1993 Deterministic chaos in the Belousov-Zhabotinsky reaction: Experiments and simulations. Chaos 3, 723–745.

    Article  CAS  PubMed  Google Scholar 

  • Zimmer C. 2007 This man wants to control the internet and you should let him. Discover Magazine, Prescott, USA.

    Google Scholar 

  • Zwilling E. 1964 Development of fragmented and of dissociated limb bud mesoderm. Dev. Biol89, 20–37.

    Article  Google Scholar 

  • Zykov V. S. 1987 Simulation of wave processes in exitable media. Manchester University Press, New York, USA.

    Google Scholar 

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Acknowledgements

R.B. would like to thank the organizers of 3rd Foundations of Biology meeting held at the Indian Institute of Science Education and Research, Pune, where an intense dialogue with the participants on complexity led to several of the ideas proposed in this manuscript. We would also like to thank Stuart A. Newman, Tilmann Glimm, Christopher Rose, I. S. Mian and three anonymous reviewers for providing valuable criticisms on earlier drafts of this manuscript.

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Correspondence to Ramray Bhat.

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Corresponding editor: T. N. C. Vidya

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Bhat, R., Pally, D. Complexity: the organizing principle at the interface of biological (dis)order. J Genet 96, 431–444 (2017). https://doi.org/10.1007/s12041-017-0793-8

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  • DOI: https://doi.org/10.1007/s12041-017-0793-8

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