Complex life has arisen through a series of major transitions'in which collectives of formerly autonomous individuals evolve into a single, integrated organism. A key step in this process is the origin of higher-level evolvability, but little is known about how higher-level entities originate and gain the capacity to evolve as an individual. Here we report a single mutation that not only creates a new level of biological organization, but also potentiates higher-level evolvability. Disrupting the transcription factor ACE2 in Saccharomyces cerevisiae prevents mother-daughter cell separation, generating multicellular snowflake'yeast. Snowflake yeast develop through deterministic rules that produce geometrically defined clusters that preclude genetic conflict and display a high broad-sense heritability for multicellular traits; as a result they are preadapted to multicellular adaptation. This work demonstrates that simple microevolutionary changes can have profound macroevolutionary consequences, and suggests that the formation of clonally developing clusters may often be the first step to multicellularity.
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This paper is dedicated to the memory of Johnathon Fankhauser. JF (as he was called in the lab) was a tremendously talented student and colleague who flung himself whole heartedly into every endeavour. We miss him greatly. We thank Jessica Nguyen, Chelsea Du Fresne and Kristin Jacobsen for lab assistance; Jennifer Pentz, Ruth Shaw and Georgiana May for feedback on the manuscript; and Ben Kerr and Amanda Muehlbauer for mathematical advice. This work was supported by NSF DEB-1051115 (W.C.R., M.T., J.D.F.), NSF GRFP no. 00006595 (J.D.F.) and the Max Planck Institute for Evolutionary Biology (W.C.R., D.W.R., D.G.).