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A role for suppressed incisor cuspal morphogenesis in the evolution of mammalian heterodont dentition.

ABSTRACT: Changes in tooth shape have played a major role in vertebrate evolution with modification of dentition allowing an organism to adapt to new feeding strategies. The current view is that molar teeth evolved from simple conical teeth, similar to canines, by progressive addition of extra "cones" to form progressively complex multicuspid crowns. Mammalian incisors, however, are neither conical nor multicuspid, and their evolution is unclear. We show that hypomorphic mutation of a cell surface receptor, Lrp4, which modulates multiple signaling pathways, produces incisors with grooved enamel surfaces that exhibit the same molecular characteristics as the tips of molar cusps. Mice with a null mutation of Lrp4 develop extra cusps on molars and have incisors that exhibit clear molar-like cusp and root morphologies. Molecular analysis identifies misregulation of Shh and Bmp signaling in the mutant incisors and suggests an uncoupling of the processes of tooth shape determination and morphogenesis. Incisors thus possess a developmentally suppressed, cuspid crown-like morphogenesis program similar to that in molars that is revealed by loss of Lrp4 activity. Several mammalian species naturally possess multicuspid incisors, suggesting that mammals have the capacity to form multicuspid teeth regardless of location in the oral jaw. Localized loss of enamel may thus have been an intermediary step in the evolution of cusps, both of which use Lrp4-mediated signaling.

SUBMITTER: Ohazama A

PROVIDER: S-EPMC2806730 | biostudies-literature | 2010 Jan

REPOSITORIES: biostudies-literature

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A role for suppressed incisor cuspal morphogenesis in the evolution of mammalian heterodont dentition.

Ohazama Atsushi A Blackburn James J Porntaveetus Thantrira T Ota Masato S MS Choi Hong Y HY Johnson Eric B EB Myers Philip P Oommen Shelly S Eto Kazuhiro K Kessler John A JA Kondo Takashi T Fraser Gareth J GJ Streelman J Todd JT Pardiñas Ulyses F J UF Tucker Abigail S AS Ortiz Pablo E PE Charles Cyril C Viriot Laurent L Herz Joachim J Sharpe Paul T PT

Proceedings of the National Academy of Sciences of the United States of America 20091214 1

Changes in tooth shape have played a major role in vertebrate evolution with modification of dentition allowing an organism to adapt to new feeding strategies. The current view is that molar teeth evolved from simple conical teeth, similar to canines, by progressive addition of extra "cones" to form progressively complex multicuspid crowns. Mammalian incisors, however, are neither conical nor multicuspid, and their evolution is unclear. We show that hypomorphic mutation of a cell surface recepto ...[more]

PMID: 20018657

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Project description:BackgroundThe Mexican tetra (Astyanax mexicanus) has emerged as a good animal model to study the constructive and regressive changes associated with living in cave environments, as both the ancestral sighted morph and the cave dwelling morph are extant. The cave dwelling morphs lack eyes and body pigmentation, but have well developed oral and sensory systems that are essential for survival in dark environments. The cave forms and surface forms are interfertile and give rise to F1 hybrids progeny known as intermediates. In cavefish, degeneration of the lens is one of the key events leading to eye regression. We have previously shown that surgical lens removal in surface fish embryos has an effect on the craniofacial skeleton. Surprisingly, lens removal was also found to have an effect on the caudal teeth in the lower jaw. In order to understand this result, we analyzed the lower jaw and upper jaw dentitions of surface, cavefish and F1 hybrids of surface and cavefish and compared our findings with surface fish that underwent lens removal. We also investigated the upper jaw (premaxillae and maxillae) dentition in these fish.ResultsOur tooth analyses shows that cavefish have the highest numbers of teeth in the mandible and maxillae, surface forms have the lowest numbers and F1 hybrids are between these groups. These differences are not observed in the premaxillae. A wide diversity of cuspal morphology can also be found in these fish. Jaw size also differs amongst the groups, with the mandible exhibiting the greatest differences. Interestingly, tooth number in surgery fish is different only in the caudal region of the mandible; this is the region that is constrained in size in all morphs.ConclusionOur data provides the first detailed description of the jaw dentitions of two morphs of Astyanax mexicanus, as well as in F1 hybrids. Tooth number, patterning and cuspal morphology are enhanced in cavefish in all jaws. This is in contrast to the increase in tooth number previously observed on the lens ablated side of the surgery fish. These findings indicate that the mechanisms which govern the constructive traits in cavefish are different to the mechanisms causing an increase tooth number in surgery fish.

Dataset Information

A role for suppressed incisor cuspal morphogenesis in the evolution of mammalian heterodont dentition.

Publications

A role for suppressed incisor cuspal morphogenesis in the evolution of mammalian heterodont dentition.

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