4.8 Article

A shark-inspired general model of tooth morphogenesis unveils developmental asymmetries in phenotype transitions

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NATL ACAD SCIENCES
DOI: 10.1073/pnas.2216959120

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tooth development; mathematical modeling; phenotypic diversity; morphospace; evo-devo

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Developmental complexity resulting from the interplay between genetic and biomechanic factors shapes the ways in which genotypes and phenotypes change in evolution. In this study, we investigate the developmental factors underlying typical tooth shape transitions by studying tooth diversity in sharks. Using a realistic mathematical model of odontogenesis, we successfully reproduce key features of tooth development and real tooth shape variation in small-spotted catsharks through in vivo experiments. Interestingly, we find that developmental transitions between tooth shapes tend to be highly degenerate and asymmetrically dependent on the direction of transition. These findings contribute to our understanding of how developmental changes drive adaptive phenotypic change and trait convergence in complex, highly diverse structures.
Developmental complexity stemming from the dynamic interplay between genetic and biomechanic factors canalizes the ways genotypes and phenotypes can change in evolution. As a paradigmatic system, we explore how changes in developmental factors generate typical tooth shape transitions. Since tooth development has mainly been researched in mammals, we contribute to a more general understanding by studying the development of tooth diversity in sharks. To this end, we build a general, but realistic, mathematical model of odontogenesis. We show that it reproduces key shark-specific features of tooth development as well as real tooth shape variation in small-spotted catsharks Scyliorhinus canicula. We validate our model by comparison with experiments in vivo. Strikingly, we observe that developmental transitions between tooth shapes tend to be highly degenerate, even for complex phenotypes. We also discover that the sets of developmental parameters involved in tooth shape transitions tend to depend asymmetrically on the direction of that transition. Together, our findings provide a valuable base for furthering our understanding of how developmental changes can lead to both adaptive phenotypic change and trait convergence in complex, phenotypically highly diverse, structures.

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