A fundamental problem in biology is the evolutionary transition from single cells to multicellular life forms1,2,3. During this transition the unit of selection shifts from individual cells to groups of cooperating cells1,3,4. Although there is much theory5,6,7,8,9,10,11,12,13,14,15, there are few empirical studies16. Here we describe an evolutionary transition that occurs in experimental populations of Pseudomonas fluorescens propagated in a spatially heterogeneous environment17. Cooperating groups are formed by over-production of an adhesive polymer18, which causes the interests of individuals to align with those of the group. The costs and benefits of cooperation, plus evolutionary susceptibility to defecting genotypes, were analysed to determine conformation to theory1,3,12. Cooperation was costly to individuals, but beneficial to the group. Defecting genotypes evolved in populations founded by the cooperating type and were fitter in the presence of this type than in its absence. In the short term, defectors sabotaged the viability of the group; but these findings nevertheless show that transitions to higher orders of complexity are readily achievable, provide insights into the selective conditions, and facilitate experimental analysis of the evolution of individuality.
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Maynard Smith, J. & Szathmary, E. The Major Transitions in Evolution (Freeman, Oxford, 1995)
Bonner, J. T. First Signals: The Evolution of Multicellular Development, (Princeton Univ. Press, Princeton, 2000)
Buss, L. W. The Evolution of Individuality (Princeton Univ. Press, Princeton, 1987)
Maynard Smith, J. in Evolutionary Progress (ed. Nitecki, M. H.) 219–230 (Univ. Chicago Press, Chicago, 1988)
Hamilton, W. D. The genetical evolution of social behaviour. J. Theor. Biol. 7, 1–52 (1964)
Williams, G. C. Adaptation and Natural Selection (Princeton Univ. Press, Princeton, 1966)
Wilson, D. S. A theory of group selection. Proc. Natl Acad. Sci. USA 72, 143–146 (1975)
Dawkins, R. The Selfish Gene (Oxford Univ. Press, Oxford, 1976)
Axelrod, R. & Hamilton, W. D. The evolution of cooperation. Science 211, 1390–1396 (1981)
Ferriere, R. & Michod, R. E. The evolution of cooperation in spatially heterogeneous populations. Am. Nat. 147, 692–717 (1996)
Sober, E. & Wilson, D. S. Unto Others: The Evolution and Psychology of Unselfish Behaviour (Harvard Univ. Press, Cambridge, MA, 1998)
Michod, R. E. Darwinian Dynamics: Evolutionary Transitions in Fitness and Individuality (Princeton Univ. Press, Princeton, 1999)
Pfeiffer, T., Schuster, S. & Bonhoeffer, S. Cooperation and competition in the evolution of ATP-producing pathways. Science 292, 504–507 (2001)
Smith, J. The social evolution of bacterial pathogenesis. Proc. R. Soc. Lond. B 268, 61–69 (2001)
Pfeiffer, T. & Bonhoeffer, S. An evolutionary scenario for the transition to undifferentiated multicellularity. Proc. Natl Acad. Sci. USA 100, 1095–1098 (2003)
Boraas, M. E., Seale, D. B. & Boxhorn, J. E. Phagotrophy by a flagellate selects for colonial prey: A possible origin of multicellularity. Evol. Ecol. 12, 153–164 (1998)
Rainey, P. B. & Travisano, M. Adaptive radiation in a heterogeneous environment. Nature 394, 69–72 (1998)
Spiers, A. J., Kahn, S. G., Bohannon, J., Travisano, M. & Rainey, P. B. Adaptive divergence in experimental populations of Pseudomonas fluorescens. I. Genetic and phenotypic bases of wrinkly spreader fitness. Genetics 161, 33–46 (2002)
Wolpert, L. The evolution of development. Biol. J. Linn. Soc. 39, 109–124 (1990)
Bell, G. in The Origin and Evolution of Sex (eds Halvorson, H. & Mornoy, A.) 221–256 (Alan R. Liss, New York, 1985)
Koufopanou, V. & Bell, G. Soma and germ - an experimental approach using Volvox. Proc. R. Soc. Lond. B 254, 107–113 (1993)
Kerszberg, M. & Wolpert, L. The origin of metazoa and the egg: a role for cell death. J. Theor. Biol. 193, 535–537 (1998)
Foster, K. R., Fortunato, A., Strassmann, J. E. & Queller, D. C. The costs and benefits of being a chimera. Proc. R. Soc. Lond. B 269, 2357–2362 (2002)
Lenski, R. E., Rose, M. R., Simpson, S. C. & Tadler, S. C. Long-term experimental evolution in Escherichia coli. I. Adaptation and divergence during 2,000 generations. Am. Nat. 138, 1315–1341 (1991)
Buckling, A., Kassen, R., Bell, G. & Rainey, P. B. Disturbance and diversity in experimental microcosms. Nature 408, 961–964 (2000)
Hardin, G. The tragedy of the commons. Science 162, 1243–1248 (1968)
Kassen, R., Buckling, A., Bell, G. & Rainey, P. B. Diversity peaks at intermediate productivity in a laboratory microcosm. Nature 406, 508–512 (2000)
Frank, S. A. Mutual policing and repression of competition in the evolution of cooperative groups. Nature 377, 520–522 (1995)
Queller, D. C., Ponte, E., Bozzaro, S. & Strassmann, J. E. Single-gene greenbeard effects in the social amoeba Dictyostelium discoideum. Science 299, 105–106 (2003)
Wolf, J. B. Genetic architecture and evolutionary constraint when the environment contains genes. Proc. Natl Acad. Sci. USA 100, 4655–4660 (2003)
Velicer, G. J. & Yu, Y. N. Evolution of novel cooperative swarming in the bacterium Myxococcus xanthus. Nature 425 75–78 (2003)
We are grateful to D. S. Wilson and A. Buckling whose comments improved the manuscript. A Biotechnology and Biological Sciences Research Council (UK) Research Fellowship to P.B.R. supported the work.
The authors declare that they have no competing financial interests.
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Rainey, P., Rainey, K. Evolution of cooperation and conflict in experimental bacterial populations. Nature 425, 72–74 (2003). https://doi.org/10.1038/nature01906
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