Positional information and information flows in dynamic tissues

bioRxiv (Cold Spring Harbor Laboratory) · 2026-04-20

Abstract During development, embryos store, transmit, and transform information to generate spatial patterns. Positional information (PI) quantifies how precisely cells form patterns at a given time, but cell motion has limited its application to static tissues. We introduce a framework for PI in dynamic tissues by decomposing mutual information between cells’ positions and properties over time into information flows contributing to PI preservation, loss and generation. These reveal information-theoretic signatures of ubiquitous developmental processes, including instruction, sorting and mixing, directly from data. Applying this framework to whole-embryo cell trajectories in Drosophila , mouse and zebrafish gastrulation, we provide local and global information-theoretic quantification of cell mixing and derive bounds on PI preservation imposed by tissue dynamics. Analyzing tissue flows as dynamical systems, we further show that morphogenesis structures mixing, preferentially preserving specific patterns. Finally, we derive inequality conditions for tracing generated PI to candidate information sources and distinguishing among alternative pattern-formation mechanisms, from programmed extracellular cues to self-organizing intercellular interactions.

Control of Tissue Flows and Embryo Geometry in Avian Gastrulation

2026-01-22

Embryonic tissues undergo coordinated flows during avian gastrulation to establish the body plan. Here, we elucidate how tens of thousands of cells coordinate their behaviors to sculpt the chick embryo's dynamic geometry (size and shape). These two distinct geometric changes are each associated with dynamic curves across which trajectories separate (kinematic repellers). Through physical modeling and experimental manipulations, we selectively eliminate either or both repellers in model and experiments, revealing their mechanistic origins. We find that embryo size is affected by the competition between extraembryonic epiboly and embryonic myosin-driven contraction—which persists when mesoderm induction is blocked. Instead, the characteristic shape change from circular to pear-shaped arises from myosin-driven cell intercalations in the mesendoderm, irrespective of epiboly. These findings elucidate modular mechanisms for the independent control of embryo size and shape during development.

Coherent Structures in Active Flows on Dynamic Surfaces

bioRxiv (Cold Spring Harbor Laboratory) · 2025-05-27 · 1 citations

Abstract Coherent structures—flow features that organize material transport and deformation—are central to analyzing complex flows in fluids, plasmas, and active matter. Yet, identifying such structures on dynamic surfaces remains an open challenge, limiting their application to many living and synthetic systems. Here, we introduce a geometric framework to extract Lagrangian and Eulerian coherent structures from velocity data on arbitrarily shaped, time-evolving surfaces. Our method operates directly on triangulated meshes, avoiding global parametrizations while preserving objectivity and robustness to noise. Applying this framework to active nematic vesicles, collectively migrating epithelial spheroids, and beating zebrafish hearts, we uncover hidden transport barriers and Lagrangian deformation patterns—such as dynamic attractors, repellers, isotropic and anisotropic strain—missed by conventional Eulerian analyses. This approach offers a new perspective on soft and living matter, revealing how geometry and activity can be harnessed to program synthetic materials, and how Lagrangian strain and principal deformation directions can help uncover mechanosensitive processes and directional cues in morphogenesis.

Tissue geometry and mechanochemical feedback initiate rotational migration in <i>Drosophila</i>

bioRxiv (Cold Spring Harbor Laboratory) · 2025-09-04

Abstract Collective migration of epithelial cells drives diverse tissue remodeling processes. In many cases, a free tissue edge polarizes the cells to promote directed motion, but how edge-free or closed epithelia initiate migration remains unclear. Here, we show that the rotational migration of follicular epithelial cells in the Drosophila egg chamber is a self-organizing process. Combining experiments and theoretical modeling, we identify a positive feedback loop in which the mechanosensitive behavior of the atypical cadherin Fat2 synergizes with the rigid-body dynamics of the egg chamber to both initiate and sustain rotation. Mechanical constraints arising from cell–cell interactions and tissue geometry further align this motion around the egg chamber’s anterior–posterior axis. Our findings reveal a biophysical mechanism — combining Fat2-mediated velocity–polarity alignment, rigid-body dynamics, and tissue geometry — by which a closed epithelial tissue self-organizes into persistent, large-scale rotational migration in vivo , expanding current flocking theories.

Extracellular volume expansion drives vertebrate axis elongation

Current Biology · 2025-01-28 · 8 citations

Morphogen Patterning in Dynamic Tissues

PRX Life · 2025-11-06 · 6 citations

Embryogenesis integrates morphogenesis-coordinated cell movements-with morphogen patterning and cell differentiation. While largely studied independently, morphogenesis and patterning often unfold simultaneously in early embryos. Yet, how cell movements affect morphogen transport and cells' exposure over time remains unclear, as most pattern formation models assume static tissues. Here, we develop a theoretical framework for morphogen patterning in dynamic tissues, recasting advection-reaction-diffusion equations in the cells' moving reference frames. This framework (i) elucidates how morphogenesis mediates morphogen transport and compartmentalization: cell-cell diffusive transport is enhanced at multicellular flow attractors, while repellers act as barriers, affecting cell fate induction and bifurcations. (ii) It formalizes cell-cell signaling ranges in dynamic tissues, deconfounding morphogenetic movements to identify which cells could communicate via morphogens. (iii) It provides two new nondimensional numbers to assess when and where morphogenesis affects morphogen transport. We demonstrate this framework by analyzing classical patterning models with common morphogenetic motifs as well as experimental tissue flows. Our work rationalizes dynamic tissue patterning in development, constraining candidate patterning mechanisms and parameters using accessible cell motion data.

Morphogen Patterning in Dynamic Tissues

bioRxiv (Cold Spring Harbor Laboratory) · 2025-01-04 · 6 citations

Abstract Embryogenesis integrates morphogenesis—coordinated cell movements—with morphogen patterning and cell differentiation. While largely studied independently, morphogenesis and patterning often unfold simultaneously in early embryos. Yet, how cell movements affect patterning remains unclear, as most pattern formation models assume static tissues. We address this gap by developing a mathematical framework for morphogen patterning in dynamic tissues, reformulating advection-reaction-diffusion models in cells’ reference frames—the most natural for signal interpretation and fate decisions. This framework (i) elucidates how morphogenesis mediates morphogen transport and compartmentalization: multicellular attractors enhance cell-cell diffusive transport, while repellers act as barriers, affecting cell fate induction and bifurcations. (ii) It formalizes cell-cell signaling ranges in dynamic tissues, deconfounding morphogenetic movements and identifying which cells can communicate. (iii) It provides two nondimensional numbers—typically distinct from the Péclet number—to assess when and where morphogenesis is relevant for patterning. (iv) It elucidates the generative role of cell density dynamics in patterning. We apply this framework to classic patterning models, morphogenetic motifs, and avian gastrulation data. Broadly, our work provides a quantitative perspective to rationalize dynamic tissue patterning in natural and synthetic embryos.

Dynamical systems of fate and form in development

Seminars in Cell and Developmental Biology · 2025-06-03 · 7 citations

Developmental biology has long drawn on dynamical systems to understand the diverging fates and the emerging form of the developing embryo. Cell differentiation and morphogenesis unfold in high-dimensional gene-expression spaces and position spaces. Yet, their stable and reproducible outcomes suggest low-dimensional geometric structures-e.g., fixed points, manifolds, and dynamic attracting and repelling structures-that organize cell trajectories in both spaces. This review surveys the history and recent advances in dynamical systems frameworks for development. We focus on techniques for extracting the organizing geometric structures of cell fate decisions and morphogenetic movements from experiments, as well as their interconnections. This unifying, dynamical systems perspective aids in rationalizing increasingly complex experimental datasets, facilitating principled dimensionality reduction and an integrated understanding of development, bridging typically distinct domains.

Control of tissue flows and embryo geometry in avian gastrulation

Nature Communications · 2025-06-04 · 7 citations

Embryonic tissues undergo coordinated flows during avian gastrulation to establish the body plan. Here, we elucidate how the interplay between embryonic and extraembryonic tissues affects the chick embryo's size and shape. These two distinct geometric changes are each associated with dynamic curves across which trajectories separate (kinematic repellers). Through physical modeling and experimental manipulations of both embryonic and extraembryonic tissues, we selectively eliminate either or both repellers in model and experiments, revealing their mechanistic origins. We find that embryo size is affected by the competition between extraembryonic epiboly and embryonic myosin-driven contraction-which persists when mesoderm induction is blocked. Instead, the characteristic shape change from circular to pear-shaped arises from myosin-driven cell intercalations in the mesendoderm, irrespective of epiboly. These findings elucidate modular mechanisms controlling avian gastrulation flows and provide a mechanistic basis for the independent control of embryo size and shape during development.

Advances in mechanochemical modelling of vertebrate gastrulation

Biochemical Society Transactions · 2025-07-22 · 1 citations

Gastrulation is an essential process in the early embryonic development of all higher animals. During gastrulation, the three embryonic germ layers, the ectoderm, mesoderm and endoderm, form and move to their correct positions in the developing embryo. This process requires the integration of cell division, differentiation and movement of thousands of cells. These cell behaviours are coordinated through shortand long-range signalling and must involve feedback to execute gastrulation in a reproducible and robust manner. Mechanosensitive signalling pathways and processes are being uncovered, revealing that shortand long-range mechanical stresses integrate cell behaviours at the tissue and organism scale. Because the interactions between cell behaviours, signalling and feedback are complex, combining experimental and modelling approaches is necessary to elucidate the regulatory mechanisms that drive development. We highlight how recent experimental and theoretical studies provided key insights into mechanical feedback that coordinates relevant cell behaviours at the organism scale during gastrulation. We outline advances in modelling the mechanochemical processes controlling primitive streak formation in the early avian embryo and discuss future developments.