Mechanics dictate where and how freshwater planarians fission

Abstract

Asexual freshwater planarians reproduce by tearing themselves into two pieces by a process called binary fission. The resulting head and tail pieces regenerate within about a week forming two new worms. Understanding this process of ripping oneself into two parts poses a challenging biomechanical problem. Since planarians stop "doing it" at the slightest disturbance, this remained a centuries-old puzzle. We focus on Dugesia japonica fission and show that it proceeds in three stages: a local constriction ("waist formation"), pulsationwhich increases waist longitudinal stresses -and transverse rupture. We developed a linear mechanical model with a planarian represented by a thin shell. The model fully captures the pulsation dynamics leading to rupture and reproduces empirical time scales and stresses. It asserts that fission execution is a mechanical process. Furthermore, we show that the location of waist formation, and thus fission, is determined by physical constraints. Together, our results demonstrate that where and how a planarian rips itself apart during asexual reproduction can be fully explained through biomechanics.Keywords: planarians, biomechanics, fission, rupture, traction forces Significance Statement: How planarians reproduce by ripping themselves into a head and a tail piece, which subsequently regenerate into two new worms, is a centuries-old biomechanics problem. Michael Faraday contemplated how this feat can be achieved in the 1800s, but it remained unanswered because it is experimentally difficult to observe planarians "doing it". We recorded Dugesia japonica planarians in the act and developed a physical model which captures pivotal steps of their reproduction dynamics. The model reproduces experimental time scales and rupture stresses without fit parameters. The key to rupture is a local reduction of the animal's cross-sectional area, which greatly amplifies the stresses exerted by the planarian's musculature and enables rupture at substrate stresses in the Pa range. \body Already Michael Faraday and his contemporaries were intrigued by the observation that asexual freshwater planarians, squishy worms a few mm in length, reproduced by tearing themselves into a head and tail offspring, in a process called binary fission (1). How was it possible for these animals to generate the forces necessary to rip themselves using only their

Planarian cholinesterase: molecular and functional characterization of an evolutionarily ancient enzyme to study organophosphorus pesticide toxicity

“…Planarians secrete mucus for self-defense and locomotion, the latter of which is accomplished by cilia beating in a layer of secreted adhesive mucus (Martin 1978). Increased mucus secretion or changes in mucus composition in response to environmental stimuli can increase mucus production (Cochet-Escartin et al 2015) and the worm’s adhesion to its substrate (“stickiness”) (Malinowski et al 2017). To quantify the animals’ stickiness, we dispelled a controlled stream of water at the animal and measured the flow rate necessary to dislodge the worm (Malinowski et al 2017).…”

“…Increased mucus secretion or changes in mucus composition in response to environmental stimuli can increase mucus production (Cochet-Escartin et al 2015) and the worm’s adhesion to its substrate (“stickiness”) (Malinowski et al 2017). To quantify the animals’ stickiness, we dispelled a controlled stream of water at the animal and measured the flow rate necessary to dislodge the worm (Malinowski et al 2017). In agreement with our qualitative assessment of increased stickiness, planarians which had been treated with 1μM diazinon or physostigmine for 5 days required larger flow rates to be dislodged, indicating increased stickiness and adhesion (Fig.…”

“…This suggests that this endpoint may be modulated in part or total by some other mechanism besides decreased ChE activity. We have previously shown that the detergent Triton-X 100 increases mucus secretion and planarian stickiness (Malinowski et al 2017) raising the possibility that increased mucus secretion and subsequent increased stickiness may be a nonspecific defense response to external toxicants. However, subchronic exposure (11–12 days) of regenerating planarians to the same concentrations of these ChE inhibitors did not elicit increased stickiness, compared to control animals (Fig.…”

“…Increased secretions, including increased sweating, lacrimation, and salivation, due to overstimulation of muscarinic receptors are a hallmark of cholinergic toxicity (Pope et al 2005; Eleršek and Filipic 2011; Taylor 2017). We have previously shown that increased planarian stickiness is correlated with an increase in mucus secretion (Malinowski et al 2017). Therefore, we speculate that, while being induced through ChE inhibition, increased worm stickiness may not be correlated directly with decreased ChE activity as compensatory mechanisms may allow planarians to adapt to long-term cholinergic overstimulation by down-regulating muscarinic receptors.…”

“…The stickiness of planarians was determined based on the worms’ ability to adhere to a substrate as described in (Malinowski et al 2017). In brief, an individual planarian was placed into a 3D printed plastic arena filled with 25ml of IO water and allowed to acclimate for approximately 2 mins.…”