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Cellular packing, mechanical stress and the evolution of multicellularity

Nature Physics volume 14, pages 286–290 (2018)Cite this article

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Abstract

The evolution of multicellularity set the stage for sustained increases in organismal complexity1,2,3,4,5. However, a fundamental aspect of this transition remains largely unknown: how do simple clusters of cells evolve increased size when confronted by forces capable of breaking intracellular bonds? Here we show that multicellular snowflake yeast clusters6,7,8 fracture due to crowding-induced mechanical stress. Over seven weeks (~291 generations) of daily selection for large size, snowflake clusters evolve to increase their radius 1.7-fold by reducing the accumulation of internal stress. During this period, cells within the clusters evolve to be more elongated, concomitant with a decrease in the cellular volume fraction of the clusters. The associated increase in free space reduces the internal stress caused by cellular growth, thus delaying fracture and increasing cluster size. This work demonstrates how readily natural selection finds simple, physical solutions to spatial constraints that limit the evolution of group size—a fundamental step in the evolution of multicellularity.

The first step in the transition to multicellularity—prior to the origin of cellular division of labour, genetically regulated development and complex multicellular forms—was the evolution of simple multicellular clusters1,2,3,4,5. Long before simple clusters of cells can evolve traits characteristic of complex multicellularity, they must contend with physical forces—both internal and external—that are capable of breaking cell–cell bonds and thus limit cluster size. This physical challenge is critical for several reasons. First, large size is a likely prerequisite to the evolution of complex multicellularity2,3. Second, these forces act on long length scales that were probably irrelevant to a single-cell ancestor, and are thus evolutionarily novel. Finally, it is unclear how simple multicellular clusters that do not yet possess genetically regulated developmental systems can evolve novel multicellular morphology.

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Fig. 1: Snowflake yeast evolve larger size.
Fig. 2: Snowflake yeast fracture due to growth-induced mechanical stress.
Fig. 3: Snowflake yeast evolve to mitigate mechanical stresses by increasing volume fraction.

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Acknowledgements

This work was supported by NASA Exobiology grant no. NNX15AR33G to W.C.R., NSF grant no. IOS-1656549 to W.C.R. and P.J.Y., and a Packard Foundation Fellowship for W.C.R. We would like to thank J. Weitz and D. Yanni for helpful comments.

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Authors and Affiliations

  1. School of Physics, Georgia Institute of Technology, Atlanta, Georgia, 30332, USA

    Shane Jacobeen, Elyes C. Graba, Colin G. Brandys & Peter J. Yunker

  2. School of Biological Sciences, Georgia Institute of Technology, Atlanta, Georgia, 30332, USA

    Jennifer T. Pentz & William C. Ratcliff

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Contributions

S.J., W.C.R. and P.J.Y. planned this research. S.J., J.T.P. and C.G.B. performed all experiments. S.J. and C.G.B. analysed the AFM and microscopy data. E.C.G. wrote the geometric simulation; E.C.G., S.J. and P.J.Y. analysed the simulation data. S.J. and P.J.Y. wrote the first draft of the paper; all authors contributed to revision.

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Correspondence to William C. Ratcliff or Peter J. Yunker.

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Jacobeen, S., Pentz, J.T., Graba, E.C. et al. Cellular packing, mechanical stress and the evolution of multicellularity. Nature Phys 14, 286–290 (2018). https://doi.org/10.1038/s41567-017-0002-y

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