Mechanical constraint from growing jaw facilitates mammalian dental diversity

• Published in: Proceedings of the National Academy of Sciences - PNAS Vol. 114; no. 35; pp. 9403 - 9408
• Main Authors: Renvoisé, Elodie, Kavanagh, Kathryn D., Lazzari, Vincent, Häkkinen, Teemu J., Rice, Ritva, Pantalacci, Sophie, Salazar-Ciudad, Isaac, Jernvall, Jukka
• Format: Journal Article
• Language: English
• Published: United States National Academy of Sciences 29.08.2017
• Subjects: Animals; Arvicolinae - embryology; Biological Evolution; Biological Sciences; Biomechanical Phenomena; Body parts; Comparative studies; Computer applications; Computer Simulation; Dentures; Earth Sciences; Embryo, Mammalian; Embryonic Development; Explants; Genotype & phenotype; Integration; Jaw; Mammals; Maxillofacial Development - physiology; Mice; Models, Biological; Molars; Organogenesis; Organs; Paleontology; Sciences of the Universe; Species; Studies; Taxa; Teeth; Tissue culture; Tissue engineering; Tooth - anatomy & histology; Transplants & implants; Wildlife conservation; diversity; tissue engineering; odontogenesis; evodevo; patterning
• ISSN: 0027-8424; 1091-6490
• DOI: 10.1073/pnas.1707410114

Much of the basic information about individual organ development comes from studies using model species. Whereas conservation of gene regulatory networks across higher taxa supports generalizations made from a limited number of species, generality of mechanistic inferences remains to be tested in tissue culture systems. Here, using mammalian tooth explants cultured in isolation, we investigate self-regulation of patterning by comparing developing molars of the mouse, the model species of mammalian research, and the bank vole. A distinct patterning difference between the vole and the mouse molars is the alternate cusp offset present in the vole. Analyses of both species using 3D reconstructions of developing molars and jaws, computational modeling of cusp patterning, and tooth explants cultured with small braces show that correct cusp offset requires constraints on the lateral expansion of the developing tooth. Vole molars cultured without the braces lose their cusp offset, and mouse molars cultured with the braces develop a cusp offset. Our results suggest that cusp offset, which changes frequently in mammalian evolution, is more dependent on the 3D support of the developing jaw than other aspects of tooth shape. This jaw–tooth integration of a specific aspect of the tooth phenotype indicates that organs may outsource specific aspects of their morphology to be regulated by adjacent body parts or organs. Comparative studies of morphologically different species are needed to infer the principles of organogenesis.