A mechanochemical model recapitulates distinct vertebrate gastrulation modes.

During vertebrate gastrulation, an embryo transforms from a layer of epithelial cells into a multilayered gastrula. This process requires the coordinated movements of hundreds to tens of thousands of cells, depending on the organism. In the chick embryo, patterns of actomyosin cables spanning several cells drive coordinated tissue flows. Here, we derive a minimal theoretical framework that couples actomyosin activity to global tissue flows. Our model predicts the onset and development of gastrulation flows in normal and experimentally perturbed chick embryos, mimicking different gastrulation modes as an active stress instability. Varying initial conditions and a parameter associated with active cell ingression, our model recapitulates distinct vertebrate gastrulation morphologies, consistent with recently published experiments in the chick embryo. Altogether, our results show how changes in the patterning of critical cell behaviors associated with different force-generating mechanisms contribute to distinct vertebrate gastrulation modes via a self-organizing mechanochemical process.

Reconstruction of distinct vertebrate gastrulation modes via modulation of key cell behaviors in the chick embryo.

The morphology of gastrulation driving the internalization of the mesoderm and endoderm differs markedly among vertebrate species. It ranges from involution of epithelial sheets of cells through a circular blastopore in amphibians to ingression of mesenchymal cells through a primitive streak in amniotes. By targeting signaling pathways controlling critical cell behaviors in the chick embryo, we generated crescent- and ring-shaped mesendoderm territories in which cells can or cannot ingress. These alterations subvert the formation of the chick primitive streak into the gastrulation modes seen in amphibians, reptiles, and teleost fish. Our experimental manipulations are supported by a theoretical framework linking cellular behaviors to self-organized multicellular flows outlined in detail in the accompanying paper. Together, this suggests that the evolution of gastrulation movements is largely determined by changes in a few critical cell behaviors in the mesendoderm territory across different species and controlled by a relatively small number of signaling pathways.

Optimal locomotion for limbless crawlers.

Limbless crawling is ubiquitous in biology, from cells to organisms. We develop and analyze a model for the dynamics of one-dimensional elastic crawlers, subject to active stress and deformation-dependent friction with the substrate. We find that the optimal active stress distribution that maximizes the crawler's center-of-mass displacement given a fixed amount of energy input is a traveling wave. This theoretical optimum corresponds to peristalsislike extension-contraction waves observed in biological organisms, possibly explaining the prevalence of peristalsis as a convergent gait across species. Our theory elucidates key observations in biological systems connecting the anchoring phase of a crawler to the retrograde and prograde distinction seen in peristaltic waves among various organisms. Using our optimal gait solution, we derive a scaling relation between the crawling speed and body mass, explaining experiments on earthworms with three orders of magnitude body mass variations. Our results offer insights and tools for optimal bioinspired crawling robots design with finite battery capacity.

Author Correction: Search and rescue at sea aided by hidden flow structures.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

Dynamic morphoskeletons in development.

Morphogenetic flows in developmental biology are characterized by the coordinated motion of thousands of cells that organize into tissues, naturally raising the question of how this collective organization arises. Using only the kinematics of tissue deformation, which naturally integrates local and global mechanisms along cell paths, we identify the dynamic morphoskeletons behind morphogenesis, i.e., the evolving centerpieces of multicellular trajectory patterns. These features are model- and parameter-free, frame-invariant, and robust to measurement errors and can be computed from unfiltered cell-velocity data. We reveal the spatial attractors and repellers of the embryo by quantifying its Lagrangian deformation, information that is inaccessible to simple trajectory inspection or Eulerian methods that are local and typically frame-dependent. Computing these dynamic morphoskeletons in wild-type and mutant chick and fly embryos, we find that they capture the early footprint of known morphogenetic features, reveal new ones, and quantitatively distinguish between different phenotypes.

Search and rescue at sea aided by hidden flow structures.

Every year, hundreds of people die at sea because of vessel and airplane accidents. A key challenge in reducing the number of these fatalities is to make Search and Rescue (SAR) algorithms more efficient. Here, we address this challenge by uncovering hidden TRansient Attracting Profiles (TRAPs) in ocean-surface velocity data. Computable from a single velocity-field snapshot, TRAPs act as short-term attractors for all floating objects. In three different ocean field experiments, we show that TRAPs computed from measured as well as modeled velocities attract deployed drifters and manikins emulating people fallen in the water. TRAPs, which remain hidden to prior flow diagnostics, thus provide critical information for hazard responses, such as SAR and oil spill containment, and hence have the potential to save lives and limit environmental disasters.

Objective Eulerian coherent structures.

We define objective Eulerian Coherent Structures (OECSs) in two-dimensional, non-autonomous dynamical systems as the instantaneously most influential material curves. Specifically, OECSs are stationary curves of the averaged instantaneous material stretching-rate or material shearing-rate functionals. From these objective (frame-invariant) variational principles, we obtain explicit differential equations for hyperbolic, elliptic, and parabolic OECSs. As an illustration, we compute OECSs in an unsteady ocean velocity data set. In comparison to structures suggested by other common Eulerian diagnostic tools, we find OECSs to be the correct short-term cores of observed trajectory deformation patterns.