Mosaic Convergence of Rodent Dentitions

Lazzari, Vincent; Charles, Cyril; Tafforeau, Paul; Vianey‐Liaud, Monique; Aguilar, Jean-Pierre; Jaeger, Jean‐Jacques; Michaux, Jacques; Viriot, Laurent

doi:10.1371/journal.pone.0003607

Cited by 66 publications

(67 citation statements)

References 28 publications

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“…Thus, progressive decreases in Fgf3 dosage in heterozygous and homozygous mutants mimic the changes seen during mammalian evolution, in which a crest arises before arrival of a new cusp. This series of events has been reported often in the fossil record (10,19,20). Moreover, as loss of function of a single gene (Fgf3) causes changes in the same characters that were altered during evolution, our results provide further evidence that the characters associated with the emergence of the murine dental plan may be nonindependent, as previously reported for other dental features (3).…”

Section: Decreases In Dosage Of Fgf3 Mimic Changes During Evolution Osupporting

confidence: 84%

Modulation of Fgf3 dosage in mouse and men mirrors evolution of mammalian dentition

Charles

Lazzari

Tafforeau

et al. 2009

Proc. Natl. Acad. Sci. U.S.A.

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A central challenge in evolutionary biology is understanding how genetic mutations underlie morphological changes. Because highly calcified enamel enables preservation of detailed dental features, studying tooth morphology enables this question to be addressed in both extinct and extant species. Previous studies have found that mutant mice can have severe abnormalities in tooth morphology, and several authors have explored the evolutionary implications of tooth number modifications in mutants. However, although they can potentially shed much light on evolutionary mechanisms, anomalies in tooth shape remain poorly studied. Here, we report that alterations in dosage of the Fgf3 gene cause morphological changes in both genetically engineered mutant mice and in human patients. By comparing the dental morphologies in mice and humans carrying Fgf3 mutations with primitive rodent and primate fossils, we determined that decreases in dosage of Fgf3 lead to phenotypes that resemble the progressive reappearance of ancestral morphologies. We propose that modifications in the FGF signaling pathway have played an important role in evolution of mammalian dentition by giving rise to new cusps and interconnecting cusps by new crests. We anticipate that our multidisciplinary study will advance the detailed correlation of subtle dental modifications with genetic mutations in a variety of mammalian lineages. dental morphology ͉ Muroidea ͉ primates

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Section: Decreases In Dosage Of Fgf3 Mimic Changes During Evolution Osupporting

confidence: 84%

Modulation of Fgf3 dosage in mouse and men mirrors evolution of mammalian dentition

Charles

Lazzari

Tafforeau

et al. 2009

Proc. Natl. Acad. Sci. U.S.A.

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“…the gutter delimited by the cusp rows of the opposite tooth during antero-posterior chewing motions of the murine rasp 3 . In stephanodont species, the more the tooth is worn, the more the occlusal surface is enlarged without being extremely flat, which permits efficient shearing and grinding of food particles.…”

Section: K14-edamentioning

confidence: 99%

“…Today, murine rodents, the Old World mice and rats, are one of the most successful living examples of mammalian radiation, which can partly be explained by the evolution of novel dental morphologies contributing to the colonization of numerous environments and habitats. Although possessing only one ever-growing incisor and three molars per dental quadrant, murines have one of the most derived mammalian dental patterns, typically characterized by numerous cusps arranged in transverse chevrons 3 . Although most murine rodents have omnivorous feeding habits 4 , less than a quarter of species have developed distinct dental adaptations for plant consumption, such as enlarged, complex or high-crowned teeth [5][6][7] .…”

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confidence: 99%

Roles of dental development and adaptation in rodent evolution

et al. 2013

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In paleontology, many changes affecting morphology, such as tooth shape in mammals, are interpreted as ecological adaptations that reflect important selective events. Despite continuing studies, the identification of the genetic bases and key ecological drivers of specific mammalian dental morphologies remains elusive. Here we focus on the genetic and functional bases of stephanodonty, a pattern characterized by longitudinal crests on molars that arose in parallel during the diversification of murine rodents. We find that overexpression of Eda or Edar is sufficient to produce the longitudinal crests defining stephanodonty in transgenic laboratory mice. Whereas our dental microwear analyses show that stephanodonty likely represents an adaptation to highly fibrous diet, the initial and parallel appearance of stephanodonty may have been facilitated by developmental processes, without being necessarily under positive selection. This study demonstrates how combining development and function can help to evaluate adaptive scenarios in the evolution of new morphologies.

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“…1; Table S1) (23)(24)(25)(26). Functionally, lateral cusp configuration is related to occlusion and to chewing direction in cuspidate teeth (26,27).Developmentally, parallel and alternate cusp configurations are one of the earliest features to appear during crown patterning (28), suggesting a relatively narrow time during which the cusp offset can be influenced. Despite the increasing knowledge about developmental regulation of tooth patterning, none of the known pathways or mutations in the mouse has transformed its parallel cusp configuration to the pattern of alternate cusp configuration (2, 6-8, 10-12, 29-31).…”

mentioning

confidence: 99%

“…1; Table S1) (23)(24)(25)(26). Functionally, lateral cusp configuration is related to occlusion and to chewing direction in cuspidate teeth (26,27).…”

mentioning

confidence: 99%

Mechanical constraint from growing jaw facilitates mammalian dental diversity

Renvoisé

Kavanagh

Lazzari

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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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.T he conservation of gene regulatory networks in the development of homologous organs is well exemplified by dentitions. Teeth in fish, reptiles, and mammals have been found to use largely shared developmental gene networks (1, 2). Furthermore, tooth development, similar to organ development in general, results from sequential events that appear to be relatively independent from the development of other organs. In particular, mammalian teeth have been considered highly selfregulatory, as they form inside the dental follicle buffered from the surrounding environment (3-5). The self-regulatory aspect of teeth is further supported by the reiterative use of the same signaling pathways and signaling centers, called enamel knots, present within each growing tooth (2). Experiments on growing teeth have revealed how an activator-inhibitor balance of signaling molecules within a developing tooth and between adjacent teeth regulate dental patterning (6-12).Despite the evidence from mice indicating self-regulation of teeth, several observations suggest an intriguing link between jaw bone and tooth crown formation (3,13,14). In humans, abnormal crown patterns in patients with congenital syphilis have been ascribed to result from infection of the tooth follicle (3). Likewise, loss of function of parathyroid hormone-related protein (PTHrP) leads to loss of alveolar bone resorption and deformation of the tooth crown in the mouse (15)(16)(17)(18)(19). A lethal human syndrome called Blomstrand chondrodysplasia, which invol...

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Mosaic Convergence of Rodent Dentitions

Cited by 66 publications

References 28 publications

Modulation of Fgf3 dosage in mouse and men mirrors evolution of mammalian dentition

Modulation of Fgf3 dosage in mouse and men mirrors evolution of mammalian dentition

Roles of dental development and adaptation in rodent evolution

Mechanical constraint from growing jaw facilitates mammalian dental diversity

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