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Multicellular organisms utilize thin sheet folding to achieve functional three-dimensional forms. During embryonic development, stereotypical epithelial folds emerge from active cellular and molecular processes including cell shape change and differential cell growth. Active thin sheet folding promises to be a powerful design technique in the fields of active solids, soft robotics, and synthetic biology. However, the general principles of active thin sheet folding remain poorly understood. Here we discover a non-canonical cilia-driven thin sheet folding behavior exhibited by basal animal Trichoplax adhaerens. Through volumetric imaging, we found that, despite having no nervous system, T. adhaerens has the remarkable ability to resolve complex body folding states in a non-stereotypical fashion using a carpet of collectively flocking cilia. Cilia-resolved imaging revealed that folds create crease defects in the animal's ciliary carpet, which act as information bottlenecks to break collective behavior of cilia. In turn, these bottlenecks enable the disjointed locomotion required for fold removal. These findings point to a two-way coupling mechanism, wherein ciliary activity shapes the animal's folding state and vice versa. Our work demonstrates the broad configuration space of non-stereotypical active folding and highlights the power of distributed activity to drive folding and unfolding of a thin multicellular sheet. We anticipate our study to be a starting point for the establishment of a new class of distributed active origami wherein fold lines themselves are dynamic and motile, with implications in engineering of self-folding materials. Additionally, our work reveals a new facet of the Placozoan behavioral repertoire, which extends our understanding of mechanical intelligence in the absence of a nervous system.
Multicellular organisms utilize thin sheet folding to achieve functional three-dimensional forms. During embryonic development, stereotypical epithelial folds emerge from active cellular and molecular processes including cell shape change and differential cell growth. Active thin sheet folding promises to be a powerful design technique in the fields of active solids, soft robotics, and synthetic biology. However, the general principles of active thin sheet folding remain poorly understood. Here we discover a non-canonical cilia-driven thin sheet folding behavior exhibited by basal animal Trichoplax adhaerens. Through volumetric imaging, we found that, despite having no nervous system, T. adhaerens has the remarkable ability to resolve complex body folding states in a non-stereotypical fashion using a carpet of collectively flocking cilia. Cilia-resolved imaging revealed that folds create crease defects in the animal's ciliary carpet, which act as information bottlenecks to break collective behavior of cilia. In turn, these bottlenecks enable the disjointed locomotion required for fold removal. These findings point to a two-way coupling mechanism, wherein ciliary activity shapes the animal's folding state and vice versa. Our work demonstrates the broad configuration space of non-stereotypical active folding and highlights the power of distributed activity to drive folding and unfolding of a thin multicellular sheet. We anticipate our study to be a starting point for the establishment of a new class of distributed active origami wherein fold lines themselves are dynamic and motile, with implications in engineering of self-folding materials. Additionally, our work reveals a new facet of the Placozoan behavioral repertoire, which extends our understanding of mechanical intelligence in the absence of a nervous system.
This special issue on "The physics of evolving matter: connectivity, communication and growth" originated at two recent "Geilo Schools" (GS) [1,2], the twenty-sixth and twenty-seventh GS in a series held every two years since 1971 [3].The nature of evolving matter spanning the areas of biology, physics, and materials science provides a fascinating focus on exploring fundamental processes like connectivity, communication, and growth as discussed below.(A) Connectivity is an important theme in understanding the organization and evolution of matter. In biological systems, connectivity underpins the formation of complex structures from simple units-such as the organization of cells into tissues, or the networking of neurons in the brain. In the physical realm, it pertains to how particles, atoms, and molecules interconnect to form different phases and states of matter.In the paper "An Introduction to Phase Ordering in Scalar Active Matter" [4], Meissner and Yeomans explore how individual particles in a system interact to form ordered structures. Their work provides insight into phase transitions in active matter, where the collective behavior emerges from the interaction rules governing individual units. This study is particularly relevant to understanding phenomena such as flocking in animals, the formation of microbial colonies, and the self-assembly of nanostructures.Pieranski and Godinho, in their work on "Collisions of Monopoles, Disclinations, and Dislocations" [5] delve into the role of topological defects in materials science. These defects are crucial for understanding the mechanical and electrical properties of materials, influencing phenomena ranging from the strength of materials to their optical properties. The study of these defects also finds parallels in biological systems, such as in the arrangement of molecules in biological membranes or the folding patterns of DNA.(B) Communication is another critical aspect of evolving matter, referring to the mechanisms by which components of a system exchange information, coordinate actions, and maintain homeostasis. In biological systems, this can range from hormonal signalling in organisms to the exchange of chemical signals among cells. In physical systems, communication can manifest as the transfer of forces or energy among interacting particles.Christophe Eloy's research on the "Hydrodynamics of Flow Sensing in Plankton" [6] exemplifies biological communication. Plankton use flow sensing to navigate, feed, and avoid predators, illustrating how even simple organisms rely on sophisticated mechanisms to interact with their environment. This study highlights the importance of physical principles in biological processes and could inspire biomimetic designs in engineering.Ryskulova and colleagues investigate "Complete De-wetting of Lipid Membranes on Silicon Carbide" [7], a study that delves into the interactions between biological membranes and substrates. This research has implications for understanding cellular processes like adhesion and migration, and also f...
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