Vein fate determined by flow-based but time-delayed integration of network architecture

  1. Sophie Marbach
  2. Noah Ziethen
  3. Leonie Bastin
  4. Felix K Bäuerle
  5. Karen Alim  Is a corresponding author
  1. New York University, United States
  2. Max Planck Institute for Dynamics and Self-Organization, Germany
  3. Technical University of Munich, Germany

Abstract

Veins in vascular networks, such as in blood vasculature or leaf networks, continuously reorganize, grow or shrink, to minimize energy dissipation. Flow shear stress on vein walls has been set forth as the local driver for a vein's continuous adaptation. Yet, shear feedback alone cannot account for the observed diversity of vein dynamics - a puzzle made harder by scarce spatiotemporal data. Here, we resolve network-wide vein dynamics and shear rate during spontaneous reorganization in the prototypical vascular networks of Physarum polycephalum. Our experiments reveal a plethora of vein dynamics (stable, growing, shrinking) where the role of shear is ambiguous. Quantitative analysis of our data reveals that (a) shear rate indeed feeds back on vein radius, yet, with a time delay of 1-3 min. Further, we reconcile the experimentally observed disparate vein fates by developing a model for vein adaptation within a network and accounting for the observed time delay. The model reveals that (b) vein fate is determined by parameters - local pressure or relative vein resistance - which integrate the entire network's architecture, as they result from global conservation of fluid volume. Finally, we observe avalanches of network reorganization events that cause entire clusters of veins to vanish. Such avalanches are consistent with network architecture integrating parameters governing vein fate as vein connections continuously change. As the network architecture integrating parameters intrinsically arise from laminar fluid flow in veins, we expect our findings to play a role across ow-based vascular networks.

Data availability

Original microscopic images of all the specimens used for this study are available as movies in MP4 format.Data sharing plan:All data used to generate the figures and the custom written matlab codes will be available on the open access data repository platform mediaTUM if the paper is accepted and which will correspond to the final versions of the figures.

Article and author information

Author details

  1. Sophie Marbach

    Courant Institute of Mathematical Sciences, New York University, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2427-2065
  2. Noah Ziethen

    Max Planck Institute for Dynamics and Self-Organization, Goettingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  3. Leonie Bastin

    Max Planck Institute for Dynamics and Self-Organization, Goettingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  4. Felix K Bäuerle

    Max Planck Institute for Dynamics and Self-Organization, Goettingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  5. Karen Alim

    Department of Bioscience, Technical University of Munich, Garching, Germany
    For correspondence
    k.alim@tum.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2527-5831

Funding

MRSEC Program of the National Science Foundation (Award Number DMR- 1420073)

  • Sophie Marbach

Max Planck Society

  • Karen Alim

European Research Council under the European Union's Horizon 2020 research and innovation programme (grant agreement No. 947630,FlowMem)

  • Karen Alim

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Agnese Seminara, University of Genoa, Italy

Version history

  1. Preprint posted: December 30, 2021 (view preprint)
  2. Received: February 23, 2022
  3. Accepted: March 13, 2023
  4. Accepted Manuscript published: March 14, 2023 (version 1)
  5. Version of Record published: June 1, 2023 (version 2)

Copyright

© 2023, Marbach et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

Metrics

  • 594
    views
  • 135
    downloads
  • 7
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Sophie Marbach
  2. Noah Ziethen
  3. Leonie Bastin
  4. Felix K Bäuerle
  5. Karen Alim
(2023)
Vein fate determined by flow-based but time-delayed integration of network architecture
eLife 12:e78100.
https://doi.org/10.7554/eLife.78100

Share this article

https://doi.org/10.7554/eLife.78100

Further reading

    1. Computational and Systems Biology
    2. Physics of Living Systems
    Taegon Chung, Iksoo Chang, Sangyeol Kim
    Research Article

    Locomotion is a fundamental behavior of Caenorhabditis elegans (C. elegans). Previous works on kinetic simulations of animals helped researchers understand the physical mechanisms of locomotion and the muscle-controlling principles of neuronal circuits as an actuator part. It has yet to be understood how C. elegans utilizes the frictional forces caused by the tension of its muscles to perform sequenced locomotive behaviors. Here, we present a two-dimensional rigid body chain model for the locomotion of C. elegans by developing Newtonian equations of motion for each body segment of C. elegans. Having accounted for friction-coefficients of the surrounding environment, elastic constants of C. elegans, and its kymogram from experiments, our kinetic model (ElegansBot) reproduced various locomotion of C. elegans such as, but not limited to, forward-backward-(omega turn)-forward locomotion constituting escaping behavior and delta-turn navigation. Additionally, ElegansBot precisely quantified the forces acting on each body segment of C. elegans to allow investigation of the force distribution. This model will facilitate our understanding of the detailed mechanism of various locomotive behaviors at any given friction-coefficients of the surrounding environment. Furthermore, as the model ensures the performance of realistic behavior, it can be used to research actuator-controller interaction between muscles and neuronal circuits.

    1. Physics of Living Systems
    Giulio Facchini, Alann Rathery ... Andrea Perna
    Research Article

    Termites build complex nests which are an impressive example of self-organization. We know that the coordinated actions involved in the construction of these nests by multiple individuals are primarily mediated by signals and cues embedded in the structure of the nest itself. However, to date there is still no scientific consensus about the nature of the stimuli that guide termite construction, and how they are sensed by termites. In order to address these questions, we studied the early building behavior of Coptotermes gestroi termites in artificial arenas, decorated with topographic cues to stimulate construction. Pellet collections were evenly distributed across the experimental setup, compatible with a collection mechanism that is not affected by local topography, but only by the distribution of termite occupancy (termites pick pellets at the positions where they are). Conversely, pellet depositions were concentrated at locations of high surface curvature and at the boundaries between different types of substrate. The single feature shared by all pellet deposition regions was that they correspond to local maxima in the evaporation flux. We can show analytically and we confirm experimentally that evaporation flux is directly proportional to the local curvature of nest surfaces. Taken together, our results indicate that surface curvature is sufficient to organize termite building activity and that termites likely sense curvature indirectly through substrate evaporation. Our findings reconcile the apparently discordant results of previous studies.