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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: 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 ciliary actuation in 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 before genetically encoded innovations. 

The ecological and evolutionary success of multicellular lineages is due in no small part to their increased size relative to unicellular ancestors. However, large size also poses biophysical challenges, especially regarding the transport of nutrients to all cells; these constraints are typically overcome through multicellular innovations (e.g., a circulatory system). 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. Surprisingly, 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 work 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. More broadly, our findings highlight how cooption of conserved physical processes is a crucial but underappreciated facet of evolutionary innovation across scales. 

Abstract The evolution of multicellularity led to the origin of new kinds of organisms and, in several lineages, massive adaptive radiations through the formation of entirely new ecosystems. This paper examines three key mechanisms underpinning parallel adaptive radiations within the five clades of ‘complex’ multicellularity: animals, land plants, fungi, red algae, and brown algae. First, the evolution of key multicellular innovations permitted diversification into new ecological roles. Second, the evolution of large multicellular organisms with strong genetic bottlenecks between generations fundamentally changed the population genetic context of evolution, greatly reducing effective population size and increasing the role of genetic drift. This may be beneficial during adaptive radiations, underpinning nonadaptive expansions of genome size and allowing broader exploration of multicellular trait space. Finally, we explore how evolutionary priority effects provide a first-mover advantage, maintaining ancient adaptive radiations over long time periods by suppressing competition from convergently evolving multicellular taxa. Investigating parallel patterns of diversification across independent origins of complex multicellularity provides insight into the principles underpinning these crucially important adaptive radiations.