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      A universal power law for modelling the growth and form of teeth, claws, horns, thorns, beaks, and shells

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          Abstract

          Background

          A major goal of evolutionary developmental biology is to discover general models and mechanisms that create the phenotypes of organisms. However, universal models of such fundamental growth and form are rare, presumably due to the limited number of physical laws and biological processes that influence growth. One such model is the logarithmic spiral, which has been purported to explain the growth of biological structures such as teeth, claws, horns, and beaks. However, the logarithmic spiral only describes the path of the structure through space, and cannot generate these shapes.

          Results

          Here we show a new universal model based on a power law between the radius of the structure and its length, which generates a shape called a ‘power cone’. We describe the underlying ‘power cascade’ model that explains the extreme diversity of tooth shapes in vertebrates, including humans, mammoths, sabre-toothed cats, tyrannosaurs and giant megalodon sharks. This model can be used to predict the age of mammals with ever-growing teeth, including elephants and rodents. We view this as the third general model of tooth development, along with the patterning cascade model for cusp number and spacing, and the inhibitory cascade model that predicts relative tooth size. Beyond the dentition, this new model also describes the growth of claws, horns, antlers and beaks of vertebrates, as well as the fangs and shells of invertebrates, and thorns and prickles of plants.

          Conclusions

          The power cone is generated when the radial power growth rate is unequal to the length power growth rate. The power cascade model operates independently of the logarithmic spiral and is present throughout diverse biological systems. The power cascade provides a mechanistic basis for the generation of these pointed structures across the tree of life.

          Supplementary Information

          The online version contains supplementary material available at 10.1186/s12915-021-00990-w.

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          Most cited references57

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          Reiterative signaling and patterning during mammalian tooth morphogenesis.

          Mammalian dentition consists of teeth that develop as discrete organs. From anterior to posterior, the dentition is divided into regions of incisor, canine, premolar and molar tooth types. Particularly teeth in the molar region are very diverse in shape. The development of individual teeth involves epithelial-mesenchymal interactions that are mediated by signals shared with other organs. Parts of the molecular details of signaling networks have been established, particularly in the signal families BMP, FGF, Hh and Wnt, mostly by the analysis of gene expression and signaling responses in knockout mice with arrested tooth development. Recent evidence suggests that largely the same signaling cascade is used reiteratively throughout tooth development. The successional determination of tooth region, tooth type, tooth crown base and individual cusps involves signals that regulate tissue growth and differentiation. Tooth type appears to be determined by epithelial signals and to involve differential activation of homeobox genes in the mesenchyme. This differential signaling could have allowed the evolutionary divergence of tooth shapes among the four tooth types. The advancing tooth morphogenesis is punctuated by transient signaling centers in the epithelium corresponding to the initiation of tooth buds, tooth crowns and individual cusps. The latter two signaling centers, the primary enamel knot and the secondary enamel knot, have been well characterized and are thought to direct the differential growth and subsequent folding of the dental epithelium. Several members of the FGF signal family have been implicated in the control of cell proliferation around the non-dividing enamel knots. Spatiotemporal induction of the secondary enamel knots determines the cusp patterns of individual teeth and is likely to involve repeated activation and inhibition of signaling as suggested for patterning of other epithelial organs.
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            The cutting-edge of mammalian development; how the embryo makes teeth.

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              Predicting evolutionary patterns of mammalian teeth from development.

              One motivation in the study of development is the discovery of mechanisms that may guide evolutionary change. Here we report how development governs relative size and number of cheek teeth, or molars, in the mouse. We constructed an inhibitory cascade model by experimentally uncovering the activator-inhibitor logic of sequential tooth development. The inhibitory cascade acts as a ratchet that determines molar size differences along the jaw, one effect being that the second molar always makes up one-third of total molar area. By using a macroevolutionary test, we demonstrate the success of the model in predicting dentition patterns found among murine rodent species with various diets, thereby providing an example of ecologically driven evolution along a developmentally favoured trajectory. In general, our work demonstrates how to construct and test developmental rules with evolutionary predictability in natural systems.
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                Author and article information

                Contributors
                alistair.evans@monash.edu
                Journal
                BMC Biol
                BMC Biol
                BMC Biology
                BioMed Central (London )
                1741-7007
                30 March 2021
                30 March 2021
                2021
                : 19
                : 58
                Affiliations
                [1 ]GRID grid.1002.3, ISNI 0000 0004 1936 7857, School of Biological Sciences, , Monash University, ; Melbourne, Victoria 3800 Australia
                [2 ]GRID grid.436717.0, ISNI 0000 0004 0500 6540, Geosciences, Museums Victoria, ; Melbourne, Victoria 3001 Australia
                [3 ]GRID grid.1002.3, ISNI 0000 0004 1936 7857, School of Mathematical Sciences, , Monash University, ; Melbourne, Victoria 3800 Australia
                [4 ]GRID grid.1002.3, ISNI 0000 0004 1936 7857, Biomedicine Discovery Institute, , Monash University, ; Melbourne, Victoria 3800 Australia
                Author information
                http://orcid.org/0000-0002-4078-4693
                https://orcid.org/0000-0001-5605-9069
                https://orcid.org/0000-0001-7458-8925
                https://orcid.org/0000-0001-9289-5646
                https://orcid.org/0000-0002-9272-6815
                https://orcid.org/0000-0002-8990-6348
                https://orcid.org/0000-0002-8252-3133
                https://orcid.org/0000-0001-6848-1208
                https://orcid.org/0000-0002-6214-9850
                Article
                990
                10.1186/s12915-021-00990-w
                8008625
                33781258
                cd5e4b95-35f8-4c88-bee4-e37e9cfd6a49
                © The Author(s) 2021

                Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

                History
                : 14 September 2020
                : 22 February 2021
                Funding
                Funded by: Australian Research Council
                Award ID: FT130100968
                Award ID: LP150100403
                Award ID: DP180101797
                Funded by: FundRef http://dx.doi.org/10.13039/501100001779, Monash University;
                Categories
                Research Article
                Custom metadata
                © The Author(s) 2021

                Life sciences
                shape generation,morphogenesis,differential growth,vertebrates,teeth,logarithmic spiral,evo-devo,power law,power cascade,power cone

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