The evolution of multicellularity set the stage for sustained increases in organismal complexity [1][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 clusters 6-8 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 clusters [1][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 multicellularity 2,3 . 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.Direct experimental investigation of the early steps in the transition to multicellularity has been challenging, largely because these transitions occurred long ago, and the evolutionary path to multicellularity has been obscured by extinction in most extant lineages 9,10 . Recently, however, this constraint has been circumvented through experimental evolution of novel multicellular organisms [6][7][8]11 , genetic reconstruction of early events 12 and experiments comparing extant multicellular taxa with their unicellular relatives 13,14 . To examine the biophysical basis of the evolution of increased size in a nascent multicellular organism, we employed the tractable 'snowflake' yeast model system [6][7][8] . Multicellular snowflake clusters evolved from the unicellular baker's yeast Saccharomyces cerevisiae under daily selection for rapid settling speed in liquid media 6 . The resulting snowflake growth form is the consequence of a single mutation in the ACE2 gene . This mutation prevents cell separation after ...
The evolutionary transition to multicellularity transformed life on earth, heralding the evolution of large, complex organisms. Recent experiments demonstrated that laboratory-evolved multicellular "snowflake yeast" readily overcome the physical barriers that limit cluster size by modifying cellular geometry [Jacobeen et al., Nat. Phys. 14, 286 (2018)10.1038/s41567-017-0002-y]. However, it is unclear why this route to large size is observed, rather than an evolved increase in intercellular bond strength. Here, we use a geometric model of the snowflake yeast growth form to examine the geometric efficiency of increasing size by modifying geometry and bond strength. We find that changing geometry is a far more efficient route to large size than evolving increased intercellular adhesion. In fact, increasing cellular aspect ratio is on average ∼13 times more effective than increasing bond strength at increasing the number of cells in a cluster. Modifying other geometric parameters, such as the geometric arrangement of mother and daughter cells, also had larger effects on cluster size than increasing bond strength. Simulations reveal that as cells reproduce, internal stress in the cluster increases rapidly; thus, increasing bond strength provides diminishing returns in cluster size. Conversely, as cells become more elongated, cellular packing density within the cluster decreases, which substantially decreases the rate of internal stress accumulation. This suggests that geometrically imposed physical constraints may have been a key early selective force guiding the emergence of multicellular complexity.
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