Abstract
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.
Highlights
Complex life has arisen through a series of ‘major transitions’ in which collectives of formerly autonomous individuals evolve into a single, integrated organism
Of the 10 most downregulated genes (Table 1), seven (CTS1, DSE4, DSE2, SUN4, DSE1, SCW11 and AMN1) are regulated by the trans-acting transcription factor ACE2, suggesting that the native function of ACE2 is disrupted in early snowflake yeast
These seven most downregulated genes are involved in daughter cell separation, many acting directly to degrade the bud neck septum[48,49,50], and prior work has shown that ACE2 knockouts form cellular clusters[48,51,52]
Summary
Complex life has arisen through a series of ‘major transitions’ in which collectives of formerly autonomous individuals evolve into a single, integrated organism. Collectives of like individuals (‘fraternal’ transitions)[27] are thought to be important for the evolution of chromosomes from independent replicators, multicellular organisms from solitary cells and eusocial ‘super organisms’ from asocial multicellular ancestors These collectives faced the classic problems of group selection, namely that clusterlevel adaptation requires that the strength of among-collective selection exceed the strength of within-collective selection[28]. Two widely studied social organisms, the slime mold Dictylostelium discoideium and bacterium Myxococcus xanthus, appear stuck in the transition to multicellularity, despite ample time to evolve multicellular complexity (4400 Myr ago for the Dictyostelid cellular slime molds[32] and 4650 Myr ago for the myxobacteria[33]) While both organisms possess multicellular life histories that include cellular division of labour, neither life cycle includes a single-cell bottleneck, and genetic conflict is rampant[18,34,35]. This conflict can select for adaptations that limit the diversity of cells within collectives (for example, policing[36,37], greenbeards38), but these mechanisms are not as effective or evolutionarily durable as the single-cell bottleneck
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