Motility induced fracture reveals a ductile to brittle crossover in the epithelial tissues of a simple animal

ABSTRACT

Animals are characterized by their movement, and their tissues are continuously subjected to dynamic force loading while they crawl, walk, run or swim¹. Tissue mechanics fundamentally determine the ecological niches that can be endured by a living organism². While epithelial tissues provide an important barrier function in animals, they are subjected to extreme strains during day to day physiological activities, such as breathing¹, feeding³, and defense response⁴. How-ever, failure or inability to withstand to these extreme strains can result in epithelial fractures^{5, 6} and associated diseases^{7, 8}. From a materials science perspective, how properties of living cells and their interactions prescribe larger scale tissue rheology and adaptive response in dynamic force landscapes remains an important frontier⁹. Motivated by pushing tissues to the limits of their integrity, we carry out a multi-modal study of a simple yet highly dynamic organism, the Trichoplax Adhaerens^10–12, across four orders of magnitude in length (1 µm to 10 mm), and six orders in time (0.1 sec to 10 hours). We report the discovery of abrupt, bulk epithelial tissue fractures (∼10 sec) induced by the organism’s own motility. Coupled with rapid healing (∼10 min), this discovery accounts for dramatic shape change and physiological asexual division in this early-divergent metazoan. We generalize our understanding of this phenomena by codifying it in a heuristic model, highlighting the fundamental questions underlying the debonding/bonding criterion in a soft-active-living material by evoking the concept of an ‘epithelial alloy’. Using a suite of quantitative experimental and numerical techniques, we demonstrate a force-driven ductile to brittle material transition governing the morphodynamics of tissues pushed to the edge of rupture. This work contributes to an important discussion at the core of developmental biology^13–17, with important applications to an emerging paradigm in materials and tissue engineering^{5, 18–20}, wound healing and medicine^{8, 21, 22}.