Cellular packing, mechanical stress and the evolution of multicellularity

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.

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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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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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