Skip to main content

Randomness and multilevel interactions in biology

Theory in Biosciences volume 132, pages 139–158 (2013)Cite this article

Abstract

The dynamic instability of living systems and the “superposition” of different forms of randomness are viewed, in this paper, as components of the contingently changing, or even increasing, organization of life through ontogenesis or evolution. To this purpose, we first survey how classical and quantum physics define randomness differently. We then discuss why this requires, in our view, an enriched understanding of the effects of their concurrent presence in biological systems’ dynamics. Biological randomness is then presented not only as an essential component of the heterogeneous determination and intrinsic unpredictability proper to life phenomena, due to the nesting of, and interaction between many levels of organization, but also as a key component of its structural stability. We will note as well that increasing organization, while increasing “order”, induces growing disorder, not only by energy dispersal effects, but also by increasing variability and differentiation. Finally, we discuss the cooperation between diverse components in biological networks; this cooperation implies the presence of constraints due to the particular nature of bio-entanglement and bio-resonance, two notions to be reviewed and defined in the paper.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

Notes

  1. By “far from equilibrium system” we mean a system subject to a flow of energy and/or matter.

  2. This notion of randomness as (relative) unpredictability may be seen as epistemic, since it depends on the theory, on the intended mathematical measure theory (e.g. Lebesgue measure in the mathematical spaces used) and on physical measurement, i.e. on which mathematical ways the theory is specified and relates to the “world”, by measurement. Yet, it becomes intrinsic (ontological, some like to say), when the theory subsumes the issue of measurement as an integral part. This is the case of Quantum Mechanics, typically, where the theoretical frame includes indetermination, from the measurement of the energy spectrum and Planck's h, to the probability density as Schrödinger state function (Schrödinger 1944). We will not insist on this “epistemic vs. intrinsic (or ontological)” issue, which may depend on the reader’s metaphysics. It may help though to better specify the extensive and not enough analyzed use of the words “randomness” and “contingency” in Biology, a specification that is the main purpose of this paper.

  3. Spinoza's notion of randomness, mentioned in the introduction, is a weaker form of epistemic randomness: just ignoring the existence of another deterministic, possibly predictable, chain of events. Yet, if known, two systems can, in principle, always be made into one. Classical measurement instead is, by principle, always an interval (i.e. approximated).

  4. Technically, in astrophysics, two planets are in maximal resonance/gravitational interference when they are on the same line with respect to the Sun. Many other forms of resonance, as a component of “divergence” of possible trajectories and, thus, of unpredictability, have been analyzed in mathematical physics. A rather general one is the Pollicott-Ruelle resonance, which applies also to open systems and is related to various forms of dynamical entropy (Gaspard 2007). Thus, while the first form of instability (Poincaré’s) is analyzed in system at equilibrium, the second form may be extended to systems far from equilibrium.

  5. In physical criticality, several observables or their derivatives diverge, at the transition point, see (Binney et al. 1992); this mathematically infinite complexity is a non-obvious issue, possibly to be further explored, for a better understanding of the biological versus physical notions of complexity: infinity is a useful, precise and robust concept in mathematics.

  6. Under stress, some organisms may survive in a quasi-equilibrium state, see (Minsky et al. 2002).

  7. To give a few examples, mammals lungs have a fractal dimension greater than 2, while the lungs of a frog have a two-dimensional surface. As for organs’ “connected components”, primates may have up to 600 muscles, while a horse or a cow at most 400. But of course, the number of tissue types (differentiations) is the main (epistemic) measure (see “References”).

References

  • Arjun R, van Oudenaarden R (2008) Stochastic gene expression and its consequences. Cell 135(2):216–226

    Article  Google Scholar 

  • Arndt M, Juffmann TH, Vedral V (2009) Quantum physics meets biology. HFSP J 3(6):386–400

    PubMed  Article  CAS  Google Scholar 

  • Aspect A, Grangier P, Roger G (1982) Experimental realization of the Einstein–Podolsky–Rosen–Bohm Gedanken experiment: a new violation of Bell’s inequalities. Phys Rev Lett 49:91

    Article  Google Scholar 

  • Bailly F, Longo G (2007) Randomness and determination in the interplay between the continuum and the discrete. Math Struct Comput Sci 17(2):289–307

    Article  Google Scholar 

  • Bailly F, Longo G (2008) Extended critical situations. J Biol Syst 16(2):309–336

    Article  Google Scholar 

  • Bailly F, Longo G (2009) Biological organization and anti-entropy. J Biol Syst 17(1):63–96

    Article  CAS  Google Scholar 

  • Bailly F, Longo G (2011) Mathematics and the natural sciences. Imperial College Press, The Physical Singularity of Life

    Google Scholar 

  • Bak P, Tang C, Wiesenfeld K (1988) Self-organized criticality. Phys Rev A 38:364–374

    PubMed  Article  Google Scholar 

  • Barabasi AL, Oltvai ZN (2004) Network biology: understanding the cell functional organization. Nat Rev Genet 5(2):101–111

    PubMed  Article  CAS  Google Scholar 

  • Bateson G (1979) Mind and nature: a necessary unity. Bantam Books, New York

    Google Scholar 

  • Bell JS (1964) On the Einstein–Podolsky–Rosen paradox. Physics 1:195–200

    Google Scholar 

  • Binney J, Dowrick NJ, Fisher AJ, Newman MEJ (1992) The theory of critical phenomena: an introduction to the renormalization group. Oxford University Press, New York

    Google Scholar 

  • Buiatti M (2011) Plants: individuals or epigenetic cell populations? In: the future of Lamarckism, MIT Press, Cambridge (in press)

  • Buiatti M, Buiatti M (2008) Chance vs. necessity in living systems, a false antinomy. Biol Forum 101:29–66

    Google Scholar 

  • Cai J, Guerreschi GG, Briegel HJ (2010) Quantum control and entanglement in a chemical compass. Phys Rev Lett 104:220502. doi:10.1103/PhysRevLett.104.220502

    PubMed  Article  Google Scholar 

  • Čepl JJ, Patkova I, Blahůškov A, Cvrčkov F, Markoš A (2010) Patterning of mutually interacting bacterial bodies: close contacts and airborne signals. BMC Microbiol 10:139

    PubMed  Article  Google Scholar 

  • Ceron-Carrasco JP, Requena A, Perpete EA, Michaux C, Jacquemin D (2009) Double proton transfer mechanism in the adenine–uracil base pair and spontaneous mutation in RNA duplex. Chem Phys Lett 484:64–68

    Article  CAS  Google Scholar 

  • Cha Y, Murray CJ, Klinman JP (1989) Hydrogen tunneling in enzyme reactions. Science 243:1325–1329

    Google Scholar 

  • Collini E, Wong CY, Wilk KE, Curmi PMG, Brurner P, Scholes GD (2010) Coherently wired light harvesting in photosynthetic marine algae at ambient temperature. Nature 463:644–648

    PubMed  Article  CAS  Google Scholar 

  • Crespi BJ (2001) The evolution of social behaviour in microorganisms. Trends Ecol Evol 16:178–183

    PubMed  Article  Google Scholar 

  • Crick FHC (1958) On Protein Synthesis. Symp Soc Exp Biol, 139–163

  • Crick F (1970) Central dogma of molecular biology. Nature 227(5258):561–563

    PubMed  Article  CAS  Google Scholar 

  • Dao ND, Kessin E, Ennis HL (2000) Developmental cheating and the evolutionary biology of Dictyostelium and Myxococcus. Microbiology 146:1505–1512

    PubMed  CAS  Google Scholar 

  • Darwin CH (1875) The variation of animals and plants under domestication, 2nd edn. John Murray, London

  • de Vries H (1902) Die Mutationstheorie. Veit, Lipsia

    Google Scholar 

  • Del Giudice E, Doglia S, Milani M, Vitiello G (1986) Electromagnetic field and spontaneous symmetry breaking in biological matter. Nucl Phys B 275:185–199

    Article  Google Scholar 

  • Del Giudice E, Preparata G (1998) A new QED picture of water: understanding a few fascinating phenomena. In: Sassaroli et al. (eds), Macroscopic quantum coherence. World Scientific, London, UK, pp 108–129

  • Del Giudice E, Vitiello G (2006) Role of the electromagnetic field in the formation of domains in the process of symmetry-breaking phase transitions. Phys Rev A 74:022105

    Article  Google Scholar 

  • Devaney RL (1989) An introduction to chaotic dynamical systems, Addison-Wesley

  • Dietrich MG (2000) From hopeful monsters to homeotic effects: Richard Goldschmidt’s integration of development, evolution, and genetics. Amer Zool 40:738–747

    Article  Google Scholar 

  • Douhal A, Kim SAH, Zewall AH (1995) Femtosecond molecular dynamics of tautomerization in model base pairs. Nature 378:260–263

    PubMed  Article  CAS  Google Scholar 

  • Edelman J (1987) Neural Darwinism: the theory of neuronal group selection. Basic Books, New York

    Google Scholar 

  • Eigen M, Schuster P (1979) The hypercycle. A principle of natural self-organization. Springer, Berlin

    Google Scholar 

  • Einstein A, Podolsky B, Rosen N (1935) Can quantum-mechanical description of physical reality be considered complete? Phys Rev 41:777

    Article  Google Scholar 

  • Eldredge N (2008) Hierarchies and the sloshing bucket: toward the unification of evolutionary biology. Outreach 1:10–15

    Article  Google Scholar 

  • Eldredge N, Gould SJ (1972) Punctuated equilibria: an alternative to phyletic gradualism. In: Schopf JM (ed), Models in paleo-biology. WH Freeman, San Francisco 72: 82–115

  • Engel GS, Calhoun TR, Read EL, Ahn T, Mançal T, Cheng Y-C, Blankenship RE (2007) Evidence for wavelike energy transfer through quantum coherence in photosynthetic systems. Nature 446:782-786

    Google Scholar 

  • Fleming GR (2007) Evidence for wavelike energy transfer through quantum coherence in photosynthetic systems. Nature 447:782–786

    Article  Google Scholar 

  • Flowers I, Si IL, Stathos A, Saxer G, Ostrowski EA, Strassman DCJE, Purugganan MD (2010) Variation, sex, and social cooperation: molecular population Genetics of the social amoeba Dictyostelium discoideum. PLoS Genetics 6(7):1–14

    Article  Google Scholar 

  • Fox Keller E (2005) Revisiting “scale free” networks. BioEssays 27:1060–1068

    Article  Google Scholar 

  • Gaspard P (2007) Time asymmetry in non equilibrium statistical mechanics. Adv Chem Phys 135:83–133

    Article  CAS  Google Scholar 

  • Gerhart J, Kirschner M (1999) Cells, embryos and evolution. Blackwell Science, Malden

    Google Scholar 

  • Goldschmidt R (1940) The material basis of evolution. Yale University Press, New Haven

    Google Scholar 

  • Gould SJ (1998) Full house. Harmony Books, New York

    Google Scholar 

  • Gray H, Winkler J (2003) Electron tunneling through proteins. Q Rev Biophys 36:341–372

    PubMed  Article  CAS  Google Scholar 

  • Huxley J (1943) Evolution, the modern synthesis. Harper and Brothers Publishers, New York and London

    Google Scholar 

  • Jaeger G (2009) Entanglement, information, and the interpretation of quantum mechanics. Springer, Heildelberg

    Book  Google Scholar 

  • Jean RV (1994) Phyllotaxis : a systemic study in plant morphogenesis. Cambridge University Press, London

    Book  Google Scholar 

  • Jeong HB, Tombor R, Albert ZN, Ottvai AL, Barabasi J (2000) The large scale organization of metabolic networks. Nature 407:651

    PubMed  Article  CAS  Google Scholar 

  • Karafyllidis IG (2008) Quantum mechanical model for information transfer from DNA to protein. Biosystems 93:191–198

    PubMed  Article  CAS  Google Scholar 

  • Kucharski R, Maleszka R, Foret S, Maleszka A (2008) Nutritional control of reproductive status in Honeybees via DNA methylation. Science 319:1827–1830

    PubMed  Article  CAS  Google Scholar 

  • Kupiec JJ (1997) A Darwinian theory for the origin of cellular differentiation. Mol Gen Genet 255:201–208

    PubMed  Article  CAS  Google Scholar 

  • Laskar J (1990) The chaotic behaviour of the solar system. Icarus 88:266–291

    Article  Google Scholar 

  • Laskar J (1994) Large scale chaos in the solar system. Astron Astrophys 287:9–12

    Google Scholar 

  • Lemke J (2000) Opening up closure. Semiotics across scales. Ann NY Acad Sci 901:100–111

    PubMed  Article  Google Scholar 

  • Lerner I.M., 1950, Population genetics and animal improvement, Cambridge University Press

  • Longo G (2013) Interfaces de l’incomplétude, Les Mathématiques, Editions du CNRS, downloadable (Italian original: Le Matematiche vol. 4, Einaudi, 2010; ongoing translation in English)

  • Longo G, Palamidessi C, Paul T (2010) Some bridging results and challenges in classical, quantum and computational randomness. In: Zenil H (ed) Randomness through computation. World Science, Singapore

    Google Scholar 

  • Longo G, Montévil M (2011) From physics to biology by extending criticality and symmetry breakings. Prog Biophys Mol Biol 106(2):340–347

    PubMed  Article  CAS  Google Scholar 

  • Longo G, Montévil M (2012) Randomness increases order in biological evolution. Invited paper, conference on “Computations, Physics and Beyond”. 21–24 Feb 2012; LNCS vol. 7318 (Dinneen et al. eds). Springer, Auckland, pp 289–308

  • Longo G, Montévil M, Kauffman S (2012) No entailing laws, but enablement in the evolution of the biosphere.In: Invited Paper, ACM Proceedings of the genetic and evolutionary computation conference, GECCO’12, Philadelphia, 7–11 July 2012

  • Luisi PL (2006) The emergence of life: from chemical origin to synthetic biology. Cambridge University Press, London

    Book  Google Scholar 

  • Lush JL (1945) Animal breeding plans. Iowa D State College Press, Ames

    Google Scholar 

  • Mather K (1949) Biometrical genetics. Methuen and Co, London

    Google Scholar 

  • Maffini MV, Calabro JM, Soto AM, Sonnenschein C (2005) Stromal regulation of neoplastic development: age-dependent normalization of neoplastic mammary cells by mammary stroma. Am J Pathol 167:1405–1410

    PubMed  Article  Google Scholar 

  • Mehdiabadi NJ, Kronforst MR, Queller DC, Strassmann J (2008) Phylogeny, reproductive isolation and kin recognition in the social amoeba Dictyostelium Purpureum. Evolution 63(2):542–548

    Article  Google Scholar 

  • Michael JC (1992) Bacterial differentiation within Maraxella bovis colonies growing at the interface of the agar medium with the petri dish. J Gen Microbiol 138:2687–2695

    Article  Google Scholar 

  • Minsky A, Shimoni E, Frenkiel-Krispin D (2002) Stress, order and survival. Nat Rev Mol Cell Biol 3:50–60

    PubMed  Article  CAS  Google Scholar 

  • Moeller AP, Swaddle JP (1997) Asymmetry, developmental stability and evolution Oxford series in ecology and evolution. Oxford University Press, NY

    Google Scholar 

  • Monod J (1970) L’hasard et la nécessité. Seuil, Paris

    Google Scholar 

  • Nielsen MA, Chuang IL (2000) Quantum computation and quantum information. Cambridge University Press, Cambridge

    Google Scholar 

  • Nilsson-Ehle (1909) Kreuzunguntersuchungen an Hafer und Weizen. Academic Dissertation, Lund, p 122

  • Noble D (2010) Biophysics and systems biology. Phil Trans R Soc Math Phys Eng Sci 368(1914):1125–1139

    Article  CAS  Google Scholar 

  • Noguera M, Bertran J, Sodupe M (2004) A quantum chemical study of Cu2 + iteracting with guanine cytosine base pair. Electrostatic and oxidative effects on intermolecular proton-transfer processes. J Phys Chem 108:333–341

    Article  CAS  Google Scholar 

  • Perez A, Tuckerman ME, Hjalmarson HP, von Lilienfeld OA (2010) Enol tautomers of Watson–Crick base pair models are metastable because of nuclear quantum effects. J Am Chem Soc 132:11510–11515

    PubMed  Article  CAS  Google Scholar 

  • Ostrowski EA, Katoh M, Shaulsky G, Queller DC, Strassmann JE (2008) Kin discrimination increases with genetic distance in a social amoeba. PLoS Biol 6:2377–2382

    Article  Google Scholar 

  • Poincaré H (1892) Les méthodes nouvelles de la mécanique celeste, Paris

  • Queller JE, Strassmann MD, Purugganan MD (2010) Variation, sex, and social cooperation: molecular population genetics of the social amoeba Dictyostelium discoideum. PLoS Genetics 6:1–14

    Google Scholar 

  • Reece StY, Nogera DG (2009) Proto-coupled electron transfer in Biology: results from synergistic studies in natural and model systems. Annu Rev Biochem 78:673–699

    PubMed  Article  CAS  Google Scholar 

  • Ricard J (2008) Pourquoi le tout est plus que la somme de ses parties. Hermann, Paris

    Google Scholar 

  • Rieger T, Neubauer Z, Blahůško A, Cvrčkov F, Markoš A (2008) Bacterial body plans: colony ontogeny in Serratia marcescens. Commun Integr Biol 1:78–87

    PubMed  Article  Google Scholar 

  • Salthe S (1985) Evolving hierarchical systems. Columbia University Press, New York

    Google Scholar 

  • Sarovar M, Ishizaki A, Fleming GR, Whaley KB (2010) Quantum entanglement in photosynthetic light-harvesting complexes. Nature-Phys 6:462–467

    Article  CAS  Google Scholar 

  • Schrödinger E (1944) What is life? The physical aspect of the living cell. Cambridge University Press, London

    Google Scholar 

  • Sonnenschein C, Soto AM (1999) The society of cells: cancer and control of cell proliferation. Springer, Berlin

    Google Scholar 

  • Sorsa M (1980) Somatic mutation theory. J Toxicol Environ Health 6:5–6

    Google Scholar 

  • Soto AM, Sonnenschein C, Miquel PA (2008) On physicalism and downward causation in developmental and cancer biology. Acta Biotheor 56:257–274

    PubMed  Article  CAS  Google Scholar 

  • Soto AM, Sonnenschein C (2010) Environmental causes of cancer: endocrine disruptors as carcinogens. Nat Rev Endocrinol 6(7):363–370

    PubMed  Article  CAS  Google Scholar 

  • Strassmann JE, Zhu Y, Queller DC (2000) Altruism and social cheating in the social amoeba Dictyostelium discoideum. Nature 408:465–466

    Article  Google Scholar 

  • Theißen G (2010) Saltational evolution: hopeful monsters are here to stay. Theory Biosci 128:43–51

    Article  Google Scholar 

  • Van Driessche N, Shaw C, Katoh M, Morio T, Sucgang R, Ibarra M, Kuwayama H, Saito T, Urushihara H, Maeda M, Takeuchi I, Ochiai H, Eaton W, Tollett J, Halter J, Kuspa A, Tanaka Y, Shaulsky G (2002) A transcriptional profile of multicellular development in Dictyostelium discoideum. Development 129:1543–1552

    PubMed  Google Scholar 

  • Waddington CH (1975) The evolution of an evolutionist. Cornell University Press, Ithaca

    Google Scholar 

  • Watson JD, Crick FHC (1953) Molecular structure of nucleic acids: a structure for deoxyribonucleic acid. Nature 171:737–738

    PubMed  Article  CAS  Google Scholar 

  • West SA, Griffin AS, Gardner A, Diggle SP (2006) Social evolution theory for microorganisms. Nat Rev Microbiol 4:597–607

    PubMed  Article  CAS  Google Scholar 

  • Winkler J, Gray H, Prytkova T, Kurnikov I, Beratan D (2005) Electron transfer through proteins. Bioelectronics, pp 15–33, Wiley-VCH,Weinheim, Germany

  • Wimpenny JWT, Parr JA (1979) Biochemical differentiation in large colonies of Enterobacter cloacae. J Gen Microbiol 114:487–489

    PubMed  Article  CAS  Google Scholar 

  • Wright S (1932) The roles of mutation, inbreeding, crossbreeding ad selection in evolution. In: Proceedings of the Sixth International Congress on Genetics, vol 1. Ithaca, New york, pp 356–366

  • Wright S (1940) Breeding structure of populations in relation to speciation: the American naturalist. The University of Chicago Press for the American society of naturalists, vol 74, pp 232–248

  • Zak M (2007) From quantum entanglement to mirror neurons, Solitons and Fractals, Chaos 34:344–359

    Google Scholar 

  • Zeh DW, Zeh JA, Ishida Y (2009) Transposable elements and an epigenetic basis for punctuated equilibria 31:715–726

    CAS  Google Scholar 

Download references

Acknowledgments

We would like to thank warmly the anonymous referee for his/her close analysis and constructive critique of our paper.

Author information

Affiliations

  1. Department of Evolutionary, Biology Florence University, Florence, Italy

    Marcello Buiatti

  2. Centre Cavaillès, CNRS, Ecole Normale Supérieure, Paris, France

    Giuseppe Longo

Authors
  1. Marcello Buiatti
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Giuseppe Longo
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Marcello Buiatti.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Buiatti, M., Longo, G. Randomness and multilevel interactions in biology. Theory Biosci. 132, 139–158 (2013). https://doi.org/10.1007/s12064-013-0179-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12064-013-0179-2

Keywords

  • Classical/quantum randomness
  • Biological randomness
  • Critical transitions
  • Random complexification
  • Entropy production
  • Network constraints
  • Bio-resonance