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Title: Nonlinear elasticity and short-range mechanical coupling govern the rate and symmetry of mouth opening in Hydra

Journal Article · · Proceedings of the Royal Society B: Biological Sciences
ORCiD logo [1]; ORCiD logo [2];  [2]; ORCiD logo [3];  [3];  [2];  [2];  [2]; ORCiD logo [3]; ORCiD logo [4]
  1. University of California San Diego, La Jolla, CA (United States); Georgia Institute of Technology, Atlanta, GA (United States); University of Maryland, College Park, MD (United States); UC San Diego
  2. Swarthmore College, PA (United States)
  3. University of California San Diego, La Jolla, CA (United States)
  4. University of California San Diego, La Jolla, CA (United States); Swarthmore College, PA (United States); University of Pennsylvania, Philadelphia, PA (United States)
+ Show Author Affiliations

Hydra has a tubular bilayered epithelial body column with a dome-shaped head on one end and a foot on the other. Hydra lacks a permanent mouth: its head epithelium is sealed. Upon neuronal activation, a mouth opens at the apex of the head which can exceed the body column diameter in seconds, allowing Hydra to ingest prey larger than itself. While the kinematics of mouth opening are well characterized, the underlying mechanism is unknown. We show that Hydra mouth opening is generated by independent local contractions that require tissue-level coordination. We model the head epithelium as an active viscoelastic nonlinear spring network. The model reproduces the size, timescale and symmetry of mouth opening. It shows that radial contractions, travelling inwards from the outer boundary of the head, pull the mouth open. Nonlinear elasticity makes mouth opening larger and faster, contrary to expectations. Here, the model correctly predicts changes in mouth shape in response to external forces. By generating innervated : nerve-free chimera in experiments and simulations, we show that nearest-neighbor mechanical signaling suffices to coordinate mouth opening. Hydra mouth opening shows that in the absence of long-range chemical or neuronal signals, short-range mechanical coupling is sufficient to produce long-range order in tissue deformations.

Research Organization:
University of California San Diego, La Jolla, CA (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Fusion Energy Sciences (FES); National Science Foundation (NSF)
Grant/Contract Number:
FG02-04ER54738
OSTI ID:
2316161
Journal Information:
Proceedings of the Royal Society B: Biological Sciences, Journal Name: Proceedings of the Royal Society B: Biological Sciences Journal Issue: 2017 Vol. 291; ISSN 0962-8452
Publisher:
The Royal Society PublishingCopyright Statement
Country of Publication:
United States
Language:
English

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59 BASIC BIOLOGICAL SCIENCES
chimera
epithelium
nearest-neighbor interaction
strain hardening
viscoelastic