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Abstract Upon making the transition from unicellularity to multicellularity, many previously optimized cellular traits experience the renewed scrutiny of natural selection due to their novel effects on emergent multicellular phenotypes. Yet we lack a comprehensive understanding of how and why specific cellular traits influence multicellular phenotypes and fitness. The snowflake yeast model system provides a tractable entry point for such investigations. The effects of several cell-level traits (cellular aspect ratio, cell volume, bud neck strength) on multicellular cluster size have been characterized, but we found that these properties were insufficient to explain the difference in cluster size between the two strains that serve as the ancestors of the ongoing Multicellularity Long-Term Evolution Experiment (MuLTEE). Using time-lapse microscopy and single cell tracking, we identified the timing of cell division as a cellular trait that strongly influences multicellular morphology and size in snowflake yeast. The “petite” ancestor divides asynchronously, with a 25% longer first division, while the “grande” ancestor divided synchronously. Using network theoretical and biophysical models, we showed that strains exhibiting a first division delay generate more highly-branched network topologies, accelerating the accumulation of crowding-induced mechanical stress, resulting in clusters that fracture at smaller sizes. Conversely, synchronously dividing strains produce more symmetric, larger clusters. Synchronous cell division can provide benefits through both faster growth and larger size, suggesting multiple potential selective pathways for its evolution. Furthermore, we explore how accelerated first division can produce even larger groups and how another unexpected mechanism for modifying cluster size, apoptosis rate, may interfere with these effects. Our results identify cell division timing as a previously underappreciated axis of phenotypic variation that strongly influences multicellular morphology. This suggests that temporal regulation of cell division represents an evolutionarily accessible mechanism for early control of morphogenesis in nascent multicellular organisms with permanent intercellular bonds.
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The cellular substrate of evolutionary novelty
A major challenge in biology is comprehending how complex multicellular novelties evolve. Central to this problem is explaining how qualitatively new phenotypic traits — typically the focus of comparative developmental and macroevolutionary studies above the species level — can become established through population genetic processes. Here, we suggest that a resolution may be found by acknowledging the fundamental entities from which functional organismal phenotypes are constructed. We argue that these are not genes, proteins or cell types, but rather gene expression programs (GEPs): sets of co-expressed transcripts that collectively encode cellular subfunctions. We advance that, because GEPs are the smallest, elemental functional units underlying phenotypes, it follows that they represent the substrate upon which population genetic processes must act to explain the origin of evolutionary novelty at the cellular level and above. Novelty arises through the evolution of novel GEPs, through novel synergisms between GEPs that become co-expressed within the same cell or through interactions between different GEPs juxtaposed in cooperating cells within organs. The revolution in single cell biology offers the chance to trace evolution at the resolution of GEPs in populations and across clades, potentially unifying our view of multicellular phenotypic evolution.
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- Award ID(s):
- 2047472
- PAR ID:
- 10678875
- Publisher / Repository:
- Elsevier
- Date Published:
- Journal Name:
- Current Biology
- Volume:
- 35
- Issue:
- 12
- ISSN:
- 0960-9822
- Page Range / eLocation ID:
- R626 to R637
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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- Free Publicly Accessible Full Text
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Accepted Manuscript
- Journal Article:
- https://doi.org/10.1016/j.cub.2025.04.014
