Geometry, packing, and evolutionary paths to increased multicellular size

The evolutionary transition to multicellularity transformed life on earth, allowing for the evolution of large, complex organisms. While multicellularity can be strongly advantageous, its earliest stages bring unique physical challenges. Nascent multicellular organisms must contend with a novel constraint: intercellular stresses arising from cell-cell interactions that can limit multicellular size. Among the possible evolutionary routes to overcoming this size limit, two appear obvious: multicellular organisms can increase intercellular bond strength, allowing them to tolerate larger stresses, or, they can slow the rate of stress accumulation by altering their internal structure. Recent experiments demonstrated that multicellular 'snowflake yeast' readily find a solution to this problem via the latter route. By evolving more elongated cells, which decreases cellular packing fraction and thus the rate of internal stress accumulation during growth, snowflake yeast evolve to delay fracture and grow larger. However, it is unclear if snowflake yeast evolved large size along an optimal path, or if the observed path to large size was taken due to proximate biological reasons. Here, we examine the geometric efficiency of both strategies using a minimal model that was previously demonstrated to replicate many experimentally observed structural properties of snowflake yeast. 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 at increasing the number of cells in a cluster than increasing bond strength. These results suggest that geometrically-imposed physical constraints may have been a key early selective force guiding the emergence of multicellular complexity.