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

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. 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-neighbour mechanical signalling 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.

Mechano-Chemical Coupling in Hydra Regeneration and Patterning.

The freshwater cnidarian Hydra can regenerate from wounds, small tissue fragments and even from aggregated cells. This process requires the de novo development of a body axis and oral-aboral polarity, a fundamental developmental process that involves chemical patterning and mechanical shape changes. Gierer and Meinhardt recognized that Hydra's simple body plan and amenability to in vivo experiments make it an experimentally and mathematically tractable model to study developmental patterning and symmetry breaking. They developed a reaction-diffusion model, involving a short-range activator and a long-range inhibitor, which successfully explained patterning in the adult animal. In 2011, HyWnt3 was identified as a candidate for the activator. However, despite the continued efforts of both physicists and biologists, the predicted inhibitor remains elusive. Furthermore, the Gierer-Meinhardt model cannot explain de novo axis formation in cellular aggregates that lack inherited tissue polarity. The aim of this review is to synthesize the current knowledge on Hydra symmetry breaking and patterning. We summarize the history of patterning studies and insights from recent biomechanical and molecular studies, and highlight the need for continued validation of theoretical assumptions and collaboration across disciplinary boundaries. We conclude by proposing new experiments to test current mechano-chemical coupling models and suggest ideas for expanding the Gierer-Meinhardt model to explain de novo patterning, as observed in Hydra aggregates. The availability of a fully sequenced genome, transgenic fluorescent reporter strains, and modern imaging techniques, that enable unprecedented observation of cellular events in vivo, promise to allow the community to crack Hydra's secret to patterning.