{"title":"Simulating irregular symmetry breaking in gut cross sections using a novel energy-optimization approach in growth-elasticity","authors":"Min Wu","doi":"10.1016/j.jtbi.2024.111971","DOIUrl":null,"url":null,"abstract":"<div><div>Growth-elasticity (also known as morphoelasticity) is a powerful model framework for understanding complex shape development in soft biological tissues. At each instant, by mapping how continuum building blocks have grown geometrically and how they respond elastically to the push-and-pull from their neighbors, the shape of the growing structure is determined from a state of mechanical equilibrium. As mechanical loads continue to be added to the system through growth, many interesting shapes, such as smooth wavy wrinkles, sharp creases, and deep folds, can form on the tissue surface from a relatively flatter geometry.</div><div>Previous numerical simulations of growth-elasticity have reproduced many interesting shapes resembling those observed in reality, such as the foldings on mammalian brains and guts. In the case of mammalian guts, it has been shown that wavy wrinkles, deep folds, and sharp creases on the interior organ surface can be simulated even under a simple assumption of isotropic uniform growth in the interior layer of the organ. Interestingly, the simulated patterns are all regular along the tube’s circumference, with either all smooth or all sharp indentations, whereas some undulation patterns in reality exhibit irregular patterns and a mixture of sharp creases and smooth indentations along the circumference. Can we simulate irregular indentation patterns without further complicating the growth patterning?</div><div>In this paper, we have discovered abundant shape solutions with irregular indentation patterns by developing a Rayleigh–Ritz finite-element method (FEM). In contrast to previous Galerkin FEMs, which solve the weak formulation of the mechanical-equilibrium equations, the new method formulates an optimization problem for the discretized energy functional, whose critical points are equivalent to solutions obtained by solving the mechanical-equilibrium equations. This new method is more robust than previous methods. Specifically, it does not require the initial guess to be near a solution to achieve convergence, and it allows control over the direction of numerical iterates across the energy landscape. This approach enables the capture of more solutions that cannot be easily reached by previous methods. In addition to the previously found regular smooth and non-smooth configurations, we have identified a new transitional irregular smooth shape, new shapes with a mixture of smooth and non-smooth surface indentations, and a variety of irregular patterns with different numbers of creases. Our numerical results demonstrate that growth-elasticity modeling can match more shape patterns observed in reality than previously thought.</div></div>","PeriodicalId":54763,"journal":{"name":"Journal of Theoretical Biology","volume":"595 ","pages":"Article 111971"},"PeriodicalIF":1.9000,"publicationDate":"2024-10-22","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Journal of Theoretical Biology","FirstCategoryId":"99","ListUrlMain":"https://www.sciencedirect.com/science/article/pii/S002251932400256X","RegionNum":4,"RegionCategory":"数学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q2","JCRName":"BIOLOGY","Score":null,"Total":0}
引用次数: 0
Abstract
Growth-elasticity (also known as morphoelasticity) is a powerful model framework for understanding complex shape development in soft biological tissues. At each instant, by mapping how continuum building blocks have grown geometrically and how they respond elastically to the push-and-pull from their neighbors, the shape of the growing structure is determined from a state of mechanical equilibrium. As mechanical loads continue to be added to the system through growth, many interesting shapes, such as smooth wavy wrinkles, sharp creases, and deep folds, can form on the tissue surface from a relatively flatter geometry.
Previous numerical simulations of growth-elasticity have reproduced many interesting shapes resembling those observed in reality, such as the foldings on mammalian brains and guts. In the case of mammalian guts, it has been shown that wavy wrinkles, deep folds, and sharp creases on the interior organ surface can be simulated even under a simple assumption of isotropic uniform growth in the interior layer of the organ. Interestingly, the simulated patterns are all regular along the tube’s circumference, with either all smooth or all sharp indentations, whereas some undulation patterns in reality exhibit irregular patterns and a mixture of sharp creases and smooth indentations along the circumference. Can we simulate irregular indentation patterns without further complicating the growth patterning?
In this paper, we have discovered abundant shape solutions with irregular indentation patterns by developing a Rayleigh–Ritz finite-element method (FEM). In contrast to previous Galerkin FEMs, which solve the weak formulation of the mechanical-equilibrium equations, the new method formulates an optimization problem for the discretized energy functional, whose critical points are equivalent to solutions obtained by solving the mechanical-equilibrium equations. This new method is more robust than previous methods. Specifically, it does not require the initial guess to be near a solution to achieve convergence, and it allows control over the direction of numerical iterates across the energy landscape. This approach enables the capture of more solutions that cannot be easily reached by previous methods. In addition to the previously found regular smooth and non-smooth configurations, we have identified a new transitional irregular smooth shape, new shapes with a mixture of smooth and non-smooth surface indentations, and a variety of irregular patterns with different numbers of creases. Our numerical results demonstrate that growth-elasticity modeling can match more shape patterns observed in reality than previously thought.
期刊介绍:
The Journal of Theoretical Biology is the leading forum for theoretical perspectives that give insight into biological processes. It covers a very wide range of topics and is of interest to biologists in many areas of research, including:
• Brain and Neuroscience
• Cancer Growth and Treatment
• Cell Biology
• Developmental Biology
• Ecology
• Evolution
• Immunology,
• Infectious and non-infectious Diseases,
• Mathematical, Computational, Biophysical and Statistical Modeling
• Microbiology, Molecular Biology, and Biochemistry
• Networks and Complex Systems
• Physiology
• Pharmacodynamics
• Animal Behavior and Game Theory
Acceptable papers are those that bear significant importance on the biology per se being presented, and not on the mathematical analysis. Papers that include some data or experimental material bearing on theory will be considered, including those that contain comparative study, statistical data analysis, mathematical proof, computer simulations, experiments, field observations, or even philosophical arguments, which are all methods to support or reject theoretical ideas. However, there should be a concerted effort to make papers intelligible to biologists in the chosen field.