Metabolically-driven flows enable exponential growth in macroscopic multicellular yeast

The ecological and evolutionary success of multicellular lineages stems
substantially from their increased size relative to unicellular ancestors.
However, large size poses biophysical challenges, especially regarding
nutrient transport to all cells: these constraints are typically overcome
through multicellular innovations. Here we show that an emergent
biophysical mechanism --- spontaneous fluid flows arising from
metabolically generated density gradients --- can alleviate constraints on
nutrient transport, enabling exponential growth in nascent multicellular
clusters of yeast lacking any multicellular adaptations for nutrient
transport or fluid flow. Beyond a threshold size, the metabolic activity
of experimentally-evolved snowflake yeast clusters drives large-scale
fluid flows that transport nutrients throughout the cluster at speeds
comparable to those generated by the cilia of extant multicellular
organisms. These flows support exponential growth at macroscopic sizes
that theory predicts should be diffusion limited. This demonstrates how
simple physical mechanisms can act as a `biophysical scaffold' to
support the evolution of multicellularity by opening up phenotypic
possibilities prior to genetically-encoded innovations.