De novo evolution of macroscopic multicellularity

Bozdag, G. Ozan; Zamani-Dahaj, Seyed Alireza; Day, Thomas C.; Kahn, Penelope C.; Burnetti, Anthony; Dung, T; Tong, Khim Leng; Conlin, Peter L.; Balwani, Aishwarya H.; Dyer, Eva L.; Yunker, Peter; Ratcliff, William C.

doi:10.1038/s41586-023-06052-1

Cited by 38 publications

(50 citation statements)

References 56 publications

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“…We begin by investigating an experimental system that is known to grow into entangled configurations, a multicellular Baker's yeast called snowflake yeast [14]. Snowflake yeast form structures that resemble branching trees via continued rounds of cell division.…”

Section: Entangled Growing Branchesmentioning

confidence: 99%

“…Therefore, cells are connected one to another in a tree-like pattern, such that breaking any chitinous bond breaks the group into two pieces [15][16][17]. We used snowflake yeast strains taken from an ongoing long-term evolution experiment [14]. We have previously found that branches of yeast cells can interact sterically with one another, intercalating and entangling within a single yeast tree [14], with entanglement arising de novo in less than 600 days of experimental evolution.…”

Section: Entangled Growing Branchesmentioning

confidence: 99%

“…We used snowflake yeast strains taken from an ongoing long-term evolution experiment [14]. We have previously found that branches of yeast cells can interact sterically with one another, intercalating and entangling within a single yeast tree [14], with entanglement arising de novo in less than 600 days of experimental evolution. Given the precision necessary to create non-living entangled materials, it is surprising that this new morphology evolved so readily in all five independently evolving populations.…”

Section: Entangled Growing Branchesmentioning

confidence: 99%

“…Previous work used scanning electron microscopy to image 3D volumes of a single snowflake yeast group [14]. Here, we segmented each disconnected branch of cells in those 3D image stacks, and generated 3D surface data by approximating their surfaces through alpha shapes (Figure 2b).…”

Section: Entangled Growing Branchesmentioning

confidence: 99%

“…We quantified the degree of confinement by performing simulations in which we translated one yeast branch with respect to others. We identified two separate branches (Figure 2b.i) that were entangled, where entanglement was defined as occurring when one disconnected branch penetrated the convex hull of another, a definition broadly used when studying entanglement [2,3,14]. We constructed alpha shapes of both pieces.…”

Section: Entangled Growing Branchesmentioning

confidence: 99%

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Entanglement in living systems

Day,

Zamani-Dahaj,

Bozdag

et al. 2023

Preprint

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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.

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Section: Entangled Growing Branchesmentioning

confidence: 99%

Section: Entangled Growing Branchesmentioning

confidence: 99%

Section: Entangled Growing Branchesmentioning

confidence: 99%

Section: Entangled Growing Branchesmentioning

confidence: 99%

Section: Entangled Growing Branchesmentioning

confidence: 99%

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Entanglement in living systems

Day,

Zamani-Dahaj,

Bozdag

et al. 2023

Preprint

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Integrating Multicellular Systems: Physiological Control and Degrees of Biological Individuality

Bich

2023

Acta Biotheor

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This paper focuses on physiological integration in multicellular systems, a notion often associated with biological individuality, but which has not received enough attention and needs a thorough theoretical treatment. Broadly speaking, physiological integration consists in how different components come together into a cohesive unit in which they are dependent on one another for their existence and activity. This paper argues that physiological integration can be understood by considering how the components of a biological multicellular system are controlled and coordinated in such a way that their activities can contribute to the maintenance of the system. The main implication of this perspective is that different ways of controlling their parts may give rise to multicellular organizations with different degrees of integration. After defining control, this paper analyses how control is realized in two examples of multicellular systems located at different ends of the spectrum of multicellularity: biofilms and animals. It focuses on differences in control ranges, and it argues that a high degree of integration implies control exerted at both medium and long ranges, and that insofar as biofilms lack long-range control (relative to their size) they can be considered as less integrated than other multicellular systems. It then discusses the implication of this account for the debate on physiological individuality and the idea that degrees of physiological integration imply degrees of individuality.

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