Skip to main content Accessibility help

A thermodynamic limit constrains complexity and primitive social function

  • Philip J Gerrish (a1) (a2) (a3) and Claudia P Ferreira (a4)


The evolutionary trend toward increasing complexity and social function is ultimately the result of natural selection's paradoxical tendency to foster cooperation through competition. Cooperating populations ranging from complex societies to somatic tissue are constantly under attack, however, by non-cooperating mutants or transformants, called ‘cheaters’. Structure in these populations promotes the formation of cooperating clusters whose competitive superiority can alone be sufficient to thwart outgrowths of cheaters and thereby maintain cooperation. But we find that when cheaters appear too frequently – exceeding a threshold mutation or transformation rate – their scattered outgrowths infiltrate and break up cooperating clusters, resulting in a cascading loss of social cohesiveness, a switch to net positive selection for cheaters and ultimately in the loss of cooperation. Our findings imply that a critically low mutation rate had to be achieved (perhaps through the advent of proofreading and repair mechanisms) before complex cooperative functions, such as those required for multicellularity and social behaviour, could have evolved and persisted. When mutation rate in our model is also allowed to evolve, the threshold is crossed spontaneously after thousands of generations, at which point cheaters rapidly invade. Probing extrapolations of these findings suggest: (1) in somatic tissue, it is neither social retro-evolution alone nor mutation rate evolution alone but the interplay between these two that ultimately leads to oncogenic transitions; the rate of this coevolution might thereby provide an indicator of lifespan of species, terrestrial or not; (2) the likelihood that extraterrestrial life can be expected to be multicellular and social should be affected by ultraviolet and other mutagenic factors.


Corresponding author

Author for correspondence: Philip J. Gerrish, E-mail:


Hide All
Alexander, RD (1987) The Biology of Moral Systems. New York: Aldine de Gruyter.
Allen, BA, Traulsen, A, Tarnita, CE and Nowak, MA (2012) How mutation affects evolutionary games on graphs. Journal of Theoretical Biology 299, 97105.
Axelrod, R and Hamilton, WD (1981) The evolution of cooperation. Science 211, 13901396.
Baalen, V (2000) Pair approximations for different spatial geometries. In Dieckmann, U, Law, R and Metz, JAJ (eds), The Geometry of Ecological Interactions: Simplifying Spatial Complexity. Cambridge University Press, pp. 359387.
Ellner, SP (2001) Pair approximation for lattice models with multiple interaction scales. Journal of Theoretical Biology 210(4), 435447.
Fiegna, F and Velicer, GJ (2003) Competitive fates of bacterial social parasites: persistence and self-induced extinction of Myxococcus xanthus cheaters. Proceedings of the Royal Society of London B 270, 15271534.
Frank, SA (1994) Kin selection and virulence in the evolution of protocells and parasites. Proceedings. Biological Sciences/The Royal Society 258, 153161.
Garcia, J and Traulsen, A (2012) The structure of mutations and the evolution of cooperation. PloS ONE 7(4), e35287.
Gerrish, PJ (2010) Mutation rate and the maintenance of cooperation: a parsimonious model of somatic evolution and oncogenic transitions. Proceedings of Computational and Mathematical Methods in Science and Engineering 2010, 11291132.
Hamilton, WD (1964) The genetical evolution of social behaviour. Journal of Theoretical Biology 7, 116.
Hanahan, D and Weinberg, RA (2000) The hallmarks of cancer. Cell 100(1), 5770.
Hardin, G (1968) The tragedy of the commons. Science 162, 12431248.
Harrison, F and Buckling, A (2005) Hypermutability impedes cooperation in pathogenic bacteria. Current Biology 15, 19681971.
Ichinose, G, Satotani, Y and Sayama, H (2018) How mutation alters the evolutionary dynamics of cooperation on networks. New Journal of Physics.
Lane, N and Martin, W (2010) The energetics of genome complexity. Nature 467, 929.
Levin, SR, Scott, TW, Cooper, HS and West, SA (2017) Darwin's aliens. International Journal of Astrobiology 69, 19.
Maynard Smith, J and Szathmáry, Er (1995) The Major Transitions in Evolution. Oxford: Oxford University Press.
Merlo, LM, Pepper, JW, Reid, BJ and Maley, CC (2006) Cancer as an evolutionary and ecological process. Nature Reviews Cancer 6(12), 924935.
Michod, RE and Roze, D (2001) Cooperation and conflict in the evolution of multicellularity. Nature Heredity 86, 17.
Modrich, P (1994) Mismatch repair, genetic stability and cancer. Science 266(5193), 19591960.
Nelson, GW and Perelson, AS (1995) Modeling defective interfering virus therapy for AIDS: conditions for DIV survival. Mathematical Biosciences 125(2), 127153.
Nowak, MA (2012) Why we help: the evolution of cooperation. Scientific American 307(1), 3439.
Nowak, MA and May, RM (1992) Evolutionary games and spatial chaos. Nature 359, 826829.
Nowak, MA and Sigmund, K (1998) Evolution of indirect reciprocity by image scoring. Nature 393, 573577.
Nowak, MA and Sigmund, K (2004) Evolutionary dynamics of biological games. Science 303(5659), 793799.
Nowak, MA, Bonhoeffer, S and May, RM (1994) Spatial games and the maintenance of cooperation. Proceedings of the National Academy of Sciences of the USA 91, 48774881.
Ohtsuki, H, Hauert, C, Lieberman, E and Nowak, MA (2006) A simple rule for the evolution of cooperation on graphs and social networks. Nature 441(7092), 502505.
Pacheco, JM, Traulsen, A and Nowak, MA (2006) Coevolution of strategy and structure in complex networks with dynamical linking. Physical Review Letters 97(25), 258103.
Price, GR (1972) Extension of covariance selection mathematics. Annals of Human Genetics 35, 485490.
Queller, DC (1997) Cooperators since life began. The Quarterly Review of Biology 72(2), 184188.
Riolo, RL, Cohen, MD and Axelrod, R (2001) Evolution of cooperation without reciprocity. Nature 414, 441443.
Santorelli, LA, Thompson, CRL, Villegas, E, Svetz, J, Dinh, C, Parikh, A, Sucgang, R, Kuspa, A, Strassmann, JE, Queller, DC and Shaulsky, G (2008) Facultative cheater mutants reveal the genetic complexity of cooperation in social amoebae. Nature 451(7182), 11071110.
Sniegowski, PD, Gerrish, PJ and Lenski, RE (1997) Evolution of high mutation rates in experimental populations of E. coli. Nature 387(6634), 703705.
Stewart, AJ and Plotkin, JB (2014) Collapse of cooperation in evolving games. Proceedings of the National Academy of Sciences of the USA 111, 1755817563.
Stewart, AJ and Plotkin, JB (2015) The evolvability of cooperation under local and non-local mutations. Games 6, 213250.
Strassmann, JE, Zhu, Y and Queller, DC (2000) Altruism and social cheating in the social amoeba Dictyostelium discoideum. Nature 408, 965967.
Szathmáry, E (2015) Toward major evolutionary transitions theory 2.0. Proceedings of the National Academy of Sciences 112, 1010410111.
Taylor, PD, Day, T and Wild, G (2007) Evolution of cooperation in a finite homogeneous graph. Nature 447(7143), 469472.
Turner, PE and Chao, L (1999) Prisoner's dilemma in an RNA virus. Nature 398, 441443.
Velicer, GJ (2003) Social strife in the microbial world. TRENDS in Microbiology 11, 330337.
Velicer, G and Vos, M (2009) The evolution of cooperation in the Myxobacteria. Annual Review of Microbiology 63, 599623.
Velicer, GJ, Kroos, L and Lenski, RE (1998) Loss of social behaviors by Myxococcus xanthus during evolution in an unstructured habitat. Proceedings of the National Academy of Sciences of the USA 95, 1237612380.
Velicer, GJ, Kroos, L and Lenski, RE (2000) Developmental cheating in the social bacterium Myxococcus xanthus. Nature 404, 598601.
Ward, PD and Brownlee, D (2000) Rare Earth: Why Complex Life is Uncommon in the Universe. New York: Copernicus Books.
West, SA, Fisher, RM, Gardner, A and Kiers, ET (2015) Major evolutionary transitions in individuality. Proceedings of the National Academy of Sciences of the USA 112(33), 1011210119.
West, SA, Griffin, AS, Gardner, A and Diggle, SP (2006) Social evolution theory for microorganisms. Nature Review Microbiology 4(8), 597607.


Related content

Powered by UNSILO
Type Description Title
Supplementary materials

Gerrish and Ferreira supplementary material 1
Gerrish and Ferreira supplementary material

 Unknown (1.1 MB)
1.1 MB
Supplementary materials

Gerrish and Ferreira supplementary material 2
Gerrish and Ferreira supplementary material

 PDF (579 KB)
579 KB

A thermodynamic limit constrains complexity and primitive social function

  • Philip J Gerrish (a1) (a2) (a3) and Claudia P Ferreira (a4)


Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed.