Presentation Information
[C02-01]Distinct mechanical constraints determine the divergence of inner ear morphogenesis across vertebrates
*Shuhei A. Horiguchi1, Shunya Kuroda1, Satoru Okuda1 (1. Kanazawa Univ. (Japan))
Keywords:
mechanics,evo-devo,morphogenesis,inner ear
The inner ear is a sensory organ for equilibrioception and auditory perception. In addition to the function, the development of its morphological structure is highly conserved across vertebrates. It develops in two phases: a closed monolayer of epithelial cells surrounding a lumen, called the otic vesicle, expands the structure in the first phase, and topological transitions increase the genus (the number of holes) to form semicircular canals in the second phase. However, our cross-species comparison identified two quantitatively distinct morphogenetic processes, which implies the divergence of the underlying mechanism.
Previous studies revealed that mechanical factors, including hydrostatic pressure in the lumen, drive inner ear morphogenesis in zebrafish [1,2]. However, it is unclear whether similar mechanisms underlie morphogenesis in other species. If the mechanism is diverged, how different mechanisms achieve the same outcome and why they evolved are intriguing questions from both developmental and evolutionary perspectives.
To answer these questions, we performed pharmacological perturbations and theoretical modeling on the first otic vesicle expansion phase in model organisms—zebrafish and mice, revealing different mechanical processes underlying the two types of developmental processes. We introduce a simple continuum mechanical model that reproduces the expansion of both types of otic vesicles. The zebrafish-type otic vesicle expands through elastic deformation driven by pressurization while maintaining the tissue volume. The mouse-type otic vesicle expands through plastic deformation driven by tissue growth while maintaining the luminal pressure. Thus, mechanical modeling explains how different mechanisms achieve the same outcome.
On the other hand, our mechanical model demonstrates the existence of infinitely many possible strategies for achieving expansion between the two extreme strategies by zebrafish and mouse. From the perturbation experiment and cross-species observations, we find that low tissue growth ability in zebrafish otic vesicles and the homeostatic in-plane stress in mouse otic vesicles constrain the feasibility of strategies. Strikingly, when incorporating these mechanical constraints, we find that the only feasible developmental strategy mathematically coincides with what we observe in nature. Therefore, distinct mechanical constraints prescribe the evolution of divergent morphogenetic processes.
[1] Mosaliganti et al., Size control of the inner ear via hydraulic feedback, eLife, (2019)
[2] Munjal et al., Extracellular hyaluronate pressure shaped by cellular tethers drives tissue morphogenesis, Cell, (2021)
Previous studies revealed that mechanical factors, including hydrostatic pressure in the lumen, drive inner ear morphogenesis in zebrafish [1,2]. However, it is unclear whether similar mechanisms underlie morphogenesis in other species. If the mechanism is diverged, how different mechanisms achieve the same outcome and why they evolved are intriguing questions from both developmental and evolutionary perspectives.
To answer these questions, we performed pharmacological perturbations and theoretical modeling on the first otic vesicle expansion phase in model organisms—zebrafish and mice, revealing different mechanical processes underlying the two types of developmental processes. We introduce a simple continuum mechanical model that reproduces the expansion of both types of otic vesicles. The zebrafish-type otic vesicle expands through elastic deformation driven by pressurization while maintaining the tissue volume. The mouse-type otic vesicle expands through plastic deformation driven by tissue growth while maintaining the luminal pressure. Thus, mechanical modeling explains how different mechanisms achieve the same outcome.
On the other hand, our mechanical model demonstrates the existence of infinitely many possible strategies for achieving expansion between the two extreme strategies by zebrafish and mouse. From the perturbation experiment and cross-species observations, we find that low tissue growth ability in zebrafish otic vesicles and the homeostatic in-plane stress in mouse otic vesicles constrain the feasibility of strategies. Strikingly, when incorporating these mechanical constraints, we find that the only feasible developmental strategy mathematically coincides with what we observe in nature. Therefore, distinct mechanical constraints prescribe the evolution of divergent morphogenetic processes.
[1] Mosaliganti et al., Size control of the inner ear via hydraulic feedback, eLife, (2019)
[2] Munjal et al., Extracellular hyaluronate pressure shaped by cellular tethers drives tissue morphogenesis, Cell, (2021)