Title:
Biophysical Constraints of Multicellularity: Building a Darwinian Material
Biophysical Constraints of Multicellularity: Building a Darwinian Material
Author(s)
Day, Thomas Cooper
Advisor(s)
Yunker, Peter J.
Ratcliff, William C.
Ratcliff, William C.
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Abstract
The evolution of multicellularity fundamentally changed life on Earth, resulting in successful and impactful lineages that continue to permeate and change the planet. Yet its origins, usually buried in the deep past, have remained unclear. For example, it is unknown how multicellular traits arise and emerge as repeatable and heritable. It is also unclear how spatial patterns of cell differentiation arise from undifferentiated origins. One camp of study has investigated the emergence of these traits from a genetic point of view. This camp is interested in how group-level genes are created, and then encoded into a multicellular genome. But, there is also a growing understanding that physical considerations play an outstanding role in shaping incipient multicellularity. Here, we use this biophysical viewpoint to investigate how physical constraints arise in freshly multicellular groups, and how these constraints may enable or limit subsequent adaptation and evolution. We show that some properties of multicellularity, that are historically considered difficult to achieve, can freely emerge without needing group-level genes.
First, we review the many ways that cells can physically attach, and introduce a helpful classification scheme based upon their mechanical function: intercellular bonds can either be reformable after breaking, or they can be nonreformable. We investigate some of the downstream consequences of attaching cells from either one of these two classes, arguing that non-reformable bonds may bestow inherent advantages to a biological material, naturally producing some of the key features necessary to partake in evolution by natural selection, without any need for group level genes. Second, we consider one of the consequences of self-assembling cells via cell attachments: how are cells organized absent a developmental program? We find, through a combination of experiments and simulations, that, no matter the starting intercellular bond class, random noise resulting from cell birth and death processes result in a distribution of cell organization that is repeatable and predictable. In other words, there is a universal ``ground state'' of multicellular organization, that not only exists but repeatably reproduces itself, with the potential to effect any multicellular trait that relies upon cell packing. Therefore, heritable group-level traits can be generated simply by attaching cells together, without the need for developmental programs.
After these two chapters, we turn our attention to investigating the evolution of spatially-patterned multicellularity. A fundamental prerequisite to achieving spatial patterning is for nascent multicellular organisms to become large, yet it is currently unknown if organisms can achieve such large size \textit{de novo}. Here, we experimentally show that initially microscopic organisms, without developmental plans, can achieve macroscopic size, on the order of millimeters, by evolving a mechanism that enables large size: material toughness. We uncover a novel biophysical adaptation, the entanglement of separate branches of cells, that evolved \textit{de novo} to achieve this material toughness. Later, we explore (through experiments, simulations, and theory) how entanglement might arise in general for growing systems, finding that entanglement is a relatively easy emergent biophysical phenomenon for any multicellular group with nonreformable, branching cell structures. Since these structures are rampant in both extant and fossil multicellularity, we suggest that physical entanglement may be a hitherto underappreciate mechanism for achieving group toughness, that can evolve without any need for group-level development.
Taken together, we have thus shown that some key characteristics of multicellular life, including characteristics necessary for its origins, may freely emerge from physical considerations. We suggest that by considering more biophysical challenges for nascent multicellularity, we may yet find solutions to problems that were previously considered unsolvable.
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Date Issued
2023-04-27
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Resource Type
Text
Resource Subtype
Dissertation