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Biology subjects

Conlin, P. L.

Publications and source records attributed to Conlin, P. L..

5 recordsLinked to original sources

Emergence of coordinated cell division during the evolution of multicellularity

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.

evolutionary biology↗

Whole-genome duplication in the Multicellularity Long Term Evolution Experiment

Whole-genome duplication (WGD) is widespread across eukaryotes and can promote adaptive evolution1-4. However, given the instability of newly-formed polyploid genomes5-7, understanding how WGDs arise in a population, persist, and underpin adaptations remains a challenge. Using our ongoing Multicellularity Long Term Evolution Experiment (MuLTEE)8, we show that diploid snowflake yeast (Saccharomyces cerevisiae) under selection for larger multicellular size rapidly undergo spontaneous WGD. From its origin within the first 50 days of the experiment, tetraploids persist for the next 950 days (nearly 5,000 generations, the current leading edge of our experiment) in ten replicate populations, despite being genomically unstable. Using synthetic reconstruction, biophysical modeling, and counter-selection experiments, we found that tetraploidy evolved because it confers immediate fitness benefits in this environment, by producing larger, longer cells that yield larger clusters. The same selective benefit also maintained tetraploidy over long evolutionary timescales, inhibiting the reversion to diploidy that is typically seen in laboratory evolution experiments. Once established, tetraploidy facilitated novel genetic routes for adaptation, playing a key role in the evolution of macroscopic multicellular size via the origin of evolutionarily conserved aneuploidy. These results provide unique empirical insights into the evolutionary dynamics and impacts of WGD, showing how it can initially arise due to its immediate adaptive benefits, be maintained by selection, and fuel long-term innovations by creating additional dimensions of heritable genetic variation.

evolutionary biology↗

Entanglement in living systems

Many organisms exhibit branching morphologies that twist around each other and become entangled. Entanglement occurs when different objects interlock with each other, creating complex and often irreversible configurations. This physical phenomenon is well-studied in non-living materials, such as granular matter, polymers, and wires, where it has been shown that entanglement is highly sensitive to the geometry of the component parts. However, entanglement is not yet well understood in living systems, despite its presence in many organisms. In fact, recent work has shown that entanglement can evolve rapidly, and play a crucial role in the evolution of tough, macroscopic multicellular groups. Here, through a combination of experiments, simulations, and numerical analyses, we show that growth generically facilitates entanglement for a broad range of geometries. We find that experimentally grown entangled branches can be difficult or even impossible to disassemble through translation and rotation of rigid components, suggesting that there are many configurations of branches that growth can access that agitation cannot. We use simulations to show that branching trees readily grow into entangled configurations. In contrast to non-growing entangled materials, these trees entangle for a broad range of branch geometries. We thus propose that entanglement via growth is largely insensitive to the geometry of branched-trees, but instead will depend sensitively on time scales, ultimately achieving an entangled state once sufficient growth has occurred. We test this hypothesis in experiments with snowflake yeast, a model system of undifferentiated, branched multicellularity, showing that lengthening the time of growth leads to entanglement, and that entanglement via growth can occur for a wide range of geometries. Taken together, our work demonstrates that entanglement is more readily achieved in living systems than in their non-living counterparts, providing a widely-accessible and powerful mechanism for the evolution of novel biological material properties.

biophysics↗

Division of labor promotes the entrenchment of multicellularity

Simple multicellularity evolves readily in diverse unicellular species, but nascent multicellular groups are prone to reversion to unicellularity. Successful transitions to multicellularity therefore require subsequent mutations that promote the entrenchment of the higher-level unit, stabilizing it through time. Here we explore the causes of entrenchment using digital evolution. When faced with a trade-off between cellular metabolic productivity and information fidelity, digital "multicells" often evolve reproductive division of labor. Because digital "unicells" cannot circumvent this trade-off, unicellular revertants tend to exhibit low fitness relative to their differentiated multicellular ancestors. Thus, division of labor can drive the entrenchment of multicellularity. More generally, division of labor may play a crucial role in major transitions, enriching the complexity and functionality of higher-level units while enhancing their evolutionary stability.

evolutionary biology↗

Clonal development, not aggregation, drives the transition to multicellularity in an isogenic model system

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, though this hypothesis has never been tested in a single model system. We evolved 20 replicate populations of otherwise isogenic clonally-reproducing snowflake yeast ({Delta}ace2/{Delta}ace2) and aggregative floc yeast (GAL1p::FLO1/ GAL1p::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 of 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 biological 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.

evolutionary biology↗