The development and use of elastic resonators to study biomechanics in soft-bodied locomotion

Abstract

Locomotion is a vital behaviour, near-ubiquitous across the Animal Kingdom, forming the ethological fundament for many behaviours critical for survival. Universally among terrestrial animals, these behaviours involve the production and translation of forces into a substrate to produce movement. For rigid-bodied animals, the biophysics of this substrate interaction is very well-studied; however, for soft-bodied animals, this process is comparably poorly understood. To address this aspect of biomechanics, I adapt and apply the novel substrate imaging technique, Wavelength Alternating Resonant Pressure Microscopy (WARP), allowing for the widefield recording of substrate-directed forces using changes in local resonance within a deformable Fabry-Perot elastic resonator. To allow this, I developed a versatile repertoire of force-tuneable elastic resonators, each sensitive to varying degrees of stress.

This allowed the recording of substrate interaction in Drosophila melanogaster larvae with micron-scale spatial resolution, millisecond-scale temporal resolution and nanonewton precision. Using this approach, I uncover novel locomotor appendages and otherwise invisible spatiotemporal force dynamics suited for anchoring to mitigate reaction forces as described by the laws of motion, while also engaging in a strategy of selective sequestration of previously undescribed locomotor appendages to optimise locomotor efficiency.

Utilising the genetic tractability of our model, I was also able to study biomechanics in optogenetically-induced behaviours, specifically the hitherto poorly characterised escape rolling behaviours. It was discovered that these animals exhibit otherwise undetectable preparatory behaviours akin to the loading of an archer’s bow immediately prior to rolling. Furthermore, I found that the substrate interaction of rolling involves a frictional rotation strategy directed parallel to the substrate.

In all, this thesis expands and develops the technique of WARP to allow for the mechanobiology of more than just cell cultures, advances our understanding of and establishes a platform to shine a light on a new dimension in the field of biomechanics.

Date of Award	10 Jun 2024
Original language	English
Awarding Institution	University of St Andrews
Supervisor	Malte Christian Gather (Supervisor) & Stefan Robert Pulver (Supervisor)