Abstract
Over 60 years have passed since Alan Turing first postulated a mechanism for biological pattern formation. Although Turing did not have the chance to extend his theories before his unfortunate death two years later, his work has not gone unnoticed. Indeed, many researchers have since taken up the gauntlet and extended his revolutionary and counter-intuitive ideas. Here, we reproduce the basics of his theory as well as review some of the recent generalisations and applications that have led our mathematical models to be closer representations of the biology than ever before. Finally, we take a look to the future and discuss open questions that not only show that there is still much life in the theory, but also that the best may be yet to come.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
C.J. Tomlin, J.D. Axelrod, Biology by numbers: mathematical modelling in developmental biology. Nat. Rev. Genet. 8 (5), 331–340 (2007)
L. Wolpert, Positional information and the spatial pattern of cellular differentiation. J. Theor. Biol. 25 (1), 1–47 (1969)
L. Wolpert, Positional information revisited. Development 107 (Suppl.), 3–12 (1989)
A.M. Turing, The chemical basis of morphogenesis. Philos. Trans. R. Soc. Lond. B 237, 37–72 (1952)
A. Gierer, H. Meinhardt, A theory of biological pattern formation. Biol. Cybern. 12 (1), 30–39 (1972)
R. Kapral, K. Showalter, Chemical Waves and Patterns (Kluwer, Dordrecht, 1995)
P. Borckmans, G. Dewell, A. De wit, D. Walgraef, Turing bifurcations and pattern selection, in Chemical Waves and Patterns, Chap. 10 (Kluwer, Dordrecht, 1995), pp. 325–363
Y.I. Balkarei, A.V. Grigor’yants, Y.A. Rzhanov, M.I. Elinson, Regenerative oscillations, spatial-temporal single pulses and static inhomogeneous structures in optically bistable semiconductors. Opt. Commun. 66 (2–3), 161–166 (1988)
D.B. White, The planforms and onset of convection with a temperature-dependent viscosity. J. Fluid Mech. 191 (1), 247–286 (1988)
T. Nozakura, S. Ikeuchi, Formation of dissipative structures in galaxies. Astrophys. J. 279, 40–52 (1984)
B. Futcher, G.I. Latter, P. Monardo, C.S. McLaughlin, J.I. Garrels, A sampling of the yeast proteome. Mol. Cell. Biol. 19 (11), 7357 (1999)
N.G. van Kampen, Stochastic Processes in Physics and Chemistry, 3rd edn. (North Holland, Amsterdam, 2007)
S. Cornell, M. Droz, B. Chopard, Role of fluctuations for inhomogeneous reaction-diffusion phenomena. Phys. Rev. A 44, 4826–4832 (1991)
A. Fick, On liquid diffusion. Philos. Mag. J. Sci. 10 (1), 31–39 (1855)
J.D. Murray, E.A. Stanley, D.L. Brown, On the spatial spread of rabies among foxes. Proc. R. Soc. Lond. B. Biol. 229 (1255), 111–150 (1986)
A. Okubo, P.K. Maini, M.H. Williamson, J.D. Murray, On the spatial spread of the grey squirrel in Britain. Proc. R. Soc. Lond. B. Biol. 238 (1291), 113 (1989)
T.E. Woolley, R.E. Baker, E.A. Gaffney, P.K. Maini, How long can we survive? in Mathematical Modelling of Zombies, Chap. 6 (University of Ottawa Press, Ottawa, 2014)
J.D. Murray, Mathematical Biology I: An Introduction, vol. 1, 3rd edn. (Springer, Heidelberg, 2003)
R. Erban, S.J. Chapman, Reactive boundary conditions for stochastic simulations of reaction–diffusion processes. Phys. Biol. 4, 16 (2007)
T.E. Woolley, R.E. Baker, P.K. Maini, J.L. Aragón, R.A. Barrio, Analysis of stationary droplets in a generic Turing reaction-diffusion system. Phys. Rev. E 82 (5), 051929 (2010)
T.E. Woolley, Spatiotemporal behaviour of stochastic and continuum models for biological signalling on stationary and growing domains. Ph.D. thesis, University of Oxford, 2011
R.A. Barrio, R.E. Baker, B. Vaughan Jr, K. Tribuzy, M.R. de Carvalho, R. Bassanezi, P.K. Maini, Modeling the skin pattern of fishes. Phys. Rev. E 79 (3), 31908 (2009)
R. Dillon, P.K. Maini, H.G. Othmer, Pattern formation in generalized Turing systems. J. Math. Biol. 32 (4), 345–393 (1994)
J.C.B. Petersen, An identification system for zebra (Equus burchelli, Gray). Afr. J. Ecol. 10 (1), 59–63 (1972)
P.K. Maini, T.E. Woolley, R.E. Baker, E.A. Gaffney, S.S. Lee, Turing’s model for biological pattern formation and the robustness problem. Interface Focus 2 (4), 487–496 (2012)
T.E. Woolley, Mighty morphogenesis, in 50 Visions of Mathematics, Chap. 48 (Oxford University Press, Oxford, 2014)
H. Meinhardt, P. Prusinkiewicz, D.R. Fowler, The Algorithmic Beauty of Sea Shells (Springer, Heidelberg, 2003)
S. Kondo, R. Asai, A reaction-diffusion wave on the skin of the marine angelfish Pomacanthus. Nature 376, 765–768 (1995)
S.W. Cho, S. Kwak, T.E. Woolley, M.J. Lee, E.J. Kim, R.E. Baker, H.J. Kim, J.S. Shin, C. Tickle, P.K. Maini, H.S. Jung, Interactions between Shh, Sostdc1 and Wnt signaling and a new feedback loop for spatial patterning of the teeth. Development 138, 1807–1816 (2011)
R. Sheth, L. Marcon, M.F. Bastida, M. Junco, L. Quintana, R. Dahn, M. Kmita, J. Sharpe, M.A. Ros, How genes regulate digit patterning by controlling the wavelength of a Turing-type mechanism. Science 338 (6113), 1476–1480 (2012)
P. Arcuri, J.D. Murray, Pattern sensitivity to boundary and initial conditions in reaction-diffusion models. J. Math. Biol. 24 (2), 141–165 (1986)
E.J. Crampin, E.A. Gaffney, P.K. Maini, Reaction and diffusion on growing domains: scenarios for robust pattern formation. Bull. Math. Biol. 61 (6), 1093–1120 (1999)
T.E. Woolley, R.E. Baker, E.A. Gaffney, P.K. Maini, Power spectra methods for a stochastic description of diffusion on deterministically growing domains. Phys. Rev. E 84 (2), 021915 (2011)
T.E. Woolley, R.E. Baker, E.A. Gaffney, P.K. Maini, Influence of stochastic domain growth on pattern nucleation for diffusive systems with internal noise. Phys. Rev. E 84 (4), 041905 (2011)
T.E. Woolley, R.E. Baker, E.A. Gaffney, P.K. Maini, Stochastic reaction and diffusion on growing domains: understanding the breakdown of robust pattern formation. Phys. Rev. E 84 (4), 046216 (2011)
J.L. Aragón, R.A. Barrio, T.E. Woolley, R.E. Baker, P.K. Maini, Nonlinear effects on Turing patterns: time oscillations and chaos. Phys. Rev. E 86 (2), 026201 (2012)
C.N. Tennyson, H.J. Klamut, R.G. Worton, The human dystrophin gene requires 16 hours to be transcribed and is cotranscriptionally spliced. Nat. Genet. 9 (2), 184–190 (1995)
T.E. Woolley, R.E. Baker, E.A. Gaffney, P.K. Maini, S. Seirin-Lee, Effects of intrinsic stochasticity on delayed reaction-diffusion patterning systems. Phys. Rev. E 85 (5), 051914 (2012)
E.A. Gaffney, N.A.M. Monk, Gene expression time delays and Turing pattern formation systems. Bull. Math. Biol. 68 (1), 99–130 (2006)
S.S. Lee, E.A. Gaffney, Aberrant behaviours of reaction diffusion self-organisation models on growing domains in the presence of gene expression time delays. Bull. Math. Biol. 72, 2161–2179 (2010)
S.S. Lee, E.A. Gaffney, R.E. Baker, The dynamics of Turing patterns for morphogen-regulated growing domains with cellular response delays. Bull. Math. Biol. 73 (11), 2527–2551 (2011)
R.G. Plaza, F. Sanchez-Garduno, P. Padilla, R.A. Barrio, P.K. Maini, The effect of growth and curvature on pattern formation. J. Dyn. Differ. Equ. 16 (4), 1093–1121 (2004)
K.W. Morton, D.F. Mayers, Numerical Solution of Partial Differential Equations: An Introduction (Cambridge University Press, Cambridge, 2005)
C.B. Macdonald, S.J. Ruuth, The implicit closest point method for the numerical solution of partial differential equations on surfaces. SIAM J. Sci. Comput. 31 (6), 4330–4350 (2009)
S.J. Ruuth, B. Merriman, A simple embedding method for solving partial differential equations on surfaces. J. Comput. Phys. 227 (3), 1943–1961 (2008)
T.K. Callahan, E. Knobloch, Bifurcations on the fcc lattice. Phys. Rev. E 53 (4), 3559–3562 (1996)
T. Leppänen, M. Karttunen, K. Kaski, R.A. Barrio, L. Zhang, A new dimension to Turing patterns. Physica D 168, 35–44 (2002)
E. Dulos, P. Davies, B. Rudovics, P. De Kepper, From quasi-2D to 3D Turing patterns in ramped systems. Physica D 98 (1), 53–66 (1996)
S. Muraki, E.B. Lum, K.-L. Ma, M. Ogata, X. Liu, A PC cluster system for simultaneous interactive volumetric modeling and visualization, in Proceedings of the 2003 IEEE Symposium on Parallel and Large-Data Visualization and Graphics (2003), p. 13
S.L. Judd, M. Silber, Simple and superlattice Turing patterns in reaction-diffusion systems: bifurcation, bistability, and parameter collapse. Physica D 136 (1–2), 45–65 (2000)
T.K. Callahan, E. Knobloch, Pattern formation in three-dimensional reaction–diffusion systems. Physica D 132 (3), 339–362 (1999)
T.K. Callahan, E. Knobloch, Symmetry-breaking bifurcations on cubic lattices. Nonlinearity 10 (5), 1179–1216 (1997)
T. Leppänen, M. Karttunen, R.A. Barrio, K. Kaski, Morphological transitions and bistability in Turing systems. Phys. Rev. E. 70, 066202 (2004)
D.T. Gillespie, Approximate accelerated stochastic simulation of chemically reacting systems. J. Chem. Phys. 115, 1716 (2001)
M. Rathinam, L.R. Petzold, Y. Cao, D.T. Gillespie, Stiffness in stochastic chemically reacting systems: the implicit tau-leaping method. J. Chem. Phys. 119 (24), 12784–12794 (2003)
Y. Yang, M. Rathinam, Tau leaping of stiff stochastic chemical systems via local central limit approximation. J. Comput. Phys. 242, 581–606 (2013)
G. Klingbeil, R. Erban, M. Giles, P.K. Maini, STOCHSIMGPU: parallel stochastic simulation for the Systems Biology Toolbox 2 for Matlab. Bioinformatics 27 (8), 1170–1171 (2011)
R.A. Satnoianu, M. Menzinger, P.K. Maini, Turing instabilities in general systems. J. Math. Biol. 41 (6), 493–512 (2000)
V. Klika, R.E. Baker, D. Headon, E.A. Gaffney, The influence of receptor-mediated interactions on reaction-diffusion mechanisms of cellular self-organisation. B. Math. Biol. 74 (4), 935–957 (2012)
J. Dean, S. Ghemawat, MapReduce: simplified data processing on large clusters. Commun. ACM 51 (1), 107–113 (2008)
T. Ideker, T. Galitski, L. Hood, A new approach to decoding life: systems biology. Annu. Rev. Genomics Hum. Genet. 2 (1), 343–372 (2001)
M.W. Covert, B.O. Palsson, Constraints-based models: regulation of gene expression reduces the steady-state solution space. J. Theor. Biol. 221 (3), 309–325 (2003)
O. Cominetti, A. Matzavinos, S. Samarasinghe, D. Kulasiri, S. Liu, P.K. Maini, R. Erban, DifFUZZY: a fuzzy clustering algorithm for complex datasets. Int. J. Comput. Intel. Bioinf. Syst. Biol. 1 (4), 402–417 (2010)
H. Conzelmann, J. Saez-Rodriguez, T. Sauter, E. Bullinger, F. Allgöwer, E.D. Gilles, Reduction of mathematical models of signal transduction networks: simulation-based approach applied to EGF receptor signalling. Syst. Biol. 1 (1), 159–169 (2004)
O. Radulescu, A.N. Gorban, A. Zinovyev, A. Lilienbaum, Robust simplifications of multiscale biochemical networks. BMC Syst. Biol. 2 (1), 86 (2008)
L. Marcon, X. Dirego, J. Sharpe, P. Muller, High-throughput mathematical analysis identifies Turing networks for patterning with equally diffusing signals. eLife 5, e14022 (2016)
W. Weber, J. Stelling, M. Rimann, B. Keller, M. Daoud-El Baba, C.C. Weber, D. Aubel, M. Fussenegger, A synthetic time-delay circuit in mammalian cells and mice. Proc. Natl. Acad. Sci. 104 (8), 2643–2648 (2007)
E. Fung, W.W. Wong, J.K. Suen, T. Bulter, S. Lee, J.C. Liao, A synthetic gene–metabolic oscillator. Nature 435 (7038), 118–122 (2005)
Acknowledgements
TEW would like to thank St John’s College Oxford for its financial support. This publication is based on work supported by Award No. KUK-C1-013-04, made by King Abdullah University of Science and Technology (KAUST). The cheetah and lemur photos were used under the Attribution-ShareAlike 2.0 license and were downloaded from http://www.flickr.com/photos/53936799@N05/ and http://www.flickr.com/photos/ekilby/.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2017 Springer International Publishing AG
About this chapter
Cite this chapter
Woolley, T.E., Baker, R.E., Maini, P.K. (2017). Turing’s Theory of Morphogenesis: Where We Started, Where We Are and Where We Want to Go. In: Cooper, S., Soskova, M. (eds) The Incomputable. Theory and Applications of Computability. Springer, Cham. https://doi.org/10.1007/978-3-319-43669-2_13
Download citation
DOI: https://doi.org/10.1007/978-3-319-43669-2_13
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-43667-8
Online ISBN: 978-3-319-43669-2
eBook Packages: Computer ScienceComputer Science (R0)