Evolutionary consequences of nascent multicellular life cycles
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eLife assessment
This Pentz et al study potentially provides fundamental insight into the evolution of multicellularity by experimentally demonstrating that yeast strains that form clonal groups evolve stronger group traits than ones that aggregate into non-clonal groups. While the repeatability of their experiments, supported by genomic analyses and models is compelling, the experimental design may be inadequate and would need to be extended to better support the main claims.
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Abstract
A key step in the evolutionary transition to multicellularity is the origin of multicellular groups as biological individuals capable of adaptation. Comparative work, supported by theory, suggests clonal development should facilitate this transition, although this hypothesis has never been tested in a single model system. We evolved 20 replicate populations of otherwise isogenic clonally reproducing ‘snowflake’ yeast (Δ ace2/∆ace2 ) and aggregative ‘floc’ yeast ( GAL1 p ::FLO1 /GAL1 p ::FLO1 ) with daily selection for rapid growth in liquid media, which favors faster cell division, followed by selection for rapid sedimentation, which favors larger multicellular groups. While both genotypes adapted to this regime, growing faster and having higher survival during the group-selection phase, there was a stark difference in evolutionary dynamics. Aggregative floc yeast obtained nearly all their increased fitness from faster growth, not improved group survival; indicating that selection acted primarily at the level of cells. In contrast, clonal snowflake yeast mainly benefited from higher group-dependent fitness, indicating a shift in the level of Darwinian individuality from cells to groups. Through genome sequencing and mathematical modeling, we show that the genetic bottlenecks in a clonal life cycle also drive much higher rates of genetic drift—a result with complex implications for this evolutionary transition. Our results highlight the central role that early multicellular life cycles play in the process of multicellular adaptation.
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eLife assessment
This Pentz et al study potentially provides fundamental insight into the evolution of multicellularity by experimentally demonstrating that yeast strains that form clonal groups evolve stronger group traits than ones that aggregate into non-clonal groups. While the repeatability of their experiments, supported by genomic analyses and models is compelling, the experimental design may be inadequate and would need to be extended to better support the main claims.
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Reviewer #1 (Public Review):
Pentz et al experimentally evolve yeast populations starting from two different strains that each differ in one locus compared to the wild-type. They show that these small differences - which result in one strain forming clonal groups, while the other forms multi-strain aggregates of different genotypes - can change the evolutionary fate of the strain under their selection regime. In their evolutionary experiment, they select for growth (an individual trait) and then sedimentation (a group trait) and show that the strain that makes clonal groups evolves a greater improvement in their group trait, while the strain that forms genetically diverse groups evolves a greater improvement in their individual trait. This provides experimental evidence for the hypothesis that clonality is key to the evolution of group …
Reviewer #1 (Public Review):
Pentz et al experimentally evolve yeast populations starting from two different strains that each differ in one locus compared to the wild-type. They show that these small differences - which result in one strain forming clonal groups, while the other forms multi-strain aggregates of different genotypes - can change the evolutionary fate of the strain under their selection regime. In their evolutionary experiment, they select for growth (an individual trait) and then sedimentation (a group trait) and show that the strain that makes clonal groups evolves a greater improvement in their group trait, while the strain that forms genetically diverse groups evolves a greater improvement in their individual trait. This provides experimental evidence for the hypothesis that clonality is key to the evolution of group traits, and potentially, multicellularity. They support their findings with genomic analysis of the mutants and use a mathematical model to explain some of the interesting observations from this analysis: that selection is stronger in genotypically mixed groups, while clonal groups suffer more from drift and bottlenecking effects. The study presents solid evidence for the findings, the methods are simple and clear, the scale of the experiment is impressive, the data analyses support the conclusions and are very complete and convincing, and the paper is very clearly written and a pleasure to read.
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Reviewer #2 (Public Review):
This study by Pentz et al. aims to understand how cellular attachments and/or development affect the fitness of the transition to undifferentiated multicellularity. This work has the potential to better understand why some types of multicellular development (e.g. clonal development) versus others (e.g. aggregative development) are more or less commonly observed in nature.
Presently, much of our understanding of these processes comes from observation and theoretical work. This work aims to bridge this gap by rewiring the evolutionary clock and testing if different selected undifferentiated multicellular developmental strategies are better or worse.
The authors compare the fitness of Snowflake and Floc yeast under settling-based selection. They find that Snowflake is fitter under these conditions than Floc. …
Reviewer #2 (Public Review):
This study by Pentz et al. aims to understand how cellular attachments and/or development affect the fitness of the transition to undifferentiated multicellularity. This work has the potential to better understand why some types of multicellular development (e.g. clonal development) versus others (e.g. aggregative development) are more or less commonly observed in nature.
Presently, much of our understanding of these processes comes from observation and theoretical work. This work aims to bridge this gap by rewiring the evolutionary clock and testing if different selected undifferentiated multicellular developmental strategies are better or worse.
The authors compare the fitness of Snowflake and Floc yeast under settling-based selection. They find that Snowflake is fitter under these conditions than Floc. They augment these findings with a simplified mathematical model that supports these findings.
On their face, the findings seem interesting but have limitations in that the authors did not consider alternate selective conditions and may come to different conclusions, potentially supporting the null hypothesis. In addition, doing experiments in related multicellular model systems that the authors have previously worked in would substantially improve generalizability.
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Reviewer #3 (Public Review):
A big open question in evolutionary biology is how single cells become multicellular organisms, capable of adaptation as a collective. Many cells form groups, but adaptation at the level of the group tends to be inefficient (especially in comparison to cells). Theoretically, it has been proposed that groups formed by clonal development (cells remain attached to each other after division) can more readily lead to group-level adaptation than groups coming together through the aggregation of different cells post-division. To evaluate empirically the plausibility of this hypothesis, the authors compared adaptation in two lines of yeast that differ only in a couple of mutations determining their mechanism of group formation. Ace2 mutants develop through staying together, and Floc mutants through aggregation. They …
Reviewer #3 (Public Review):
A big open question in evolutionary biology is how single cells become multicellular organisms, capable of adaptation as a collective. Many cells form groups, but adaptation at the level of the group tends to be inefficient (especially in comparison to cells). Theoretically, it has been proposed that groups formed by clonal development (cells remain attached to each other after division) can more readily lead to group-level adaptation than groups coming together through the aggregation of different cells post-division. To evaluate empirically the plausibility of this hypothesis, the authors compared adaptation in two lines of yeast that differ only in a couple of mutations determining their mechanism of group formation. Ace2 mutants develop through staying together, and Floc mutants through aggregation. They performed a form of size selection (through settling) as a way to select for multicellularity (this selection regime has been used before to obtain multicellular phenotypes). This selective regime has two components: growing (largely due to differences between cells) and settling (largely due to differences between groups). Thus, the authors assume that increases in fitness through growth are due mostly to adaptation at the single-cell level, whereas increases in fitness through settling are mostly due to adaptation at the multicellular level. They find that adaptation in clonal groups is mostly through settling and that aggregative groups adapt more through growth (despite getting bigger).
Overall this assumption makes sense (especially in a positive way) but growth, in this case, is also selecting against groups in the snowflake case and less strongly so in the floc case in which cells aggregate and disaggregate with some probability, and therefore cells can keep growing. That is, in addition to assortment the result is somewhat expected because there is less of a trade-off between growth and settling in floc: having a higher density in floc probably leads to higher aggregation and indirectly benefits settling, whereas in the clonal case, larger groups mean that a larger proportion of cells is not growing.
The main result of the paper holds true: clonal development favors multicellular adaptation relative to aggregative multicellularity, but the reason is not exclusively a difference in the distribution of variation, but a difference in the trade-off between single cell and multicellular traits.
In the second part of the paper, the authors beautifully show that the mechanisms of group formation affect evolutionary processes. Clonal aggregation leads to a decrease in the effective population size (because the descendants of mutants are likely to be in the same group, and therefore be selected together). This result shows that the mode of development can affect evolution!
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