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.V ertebrates exhibit remarkable diversity in their dentitions, which is a feature of the importance of tooth shape in adaptation to new feeding strategies in evolution. Even quite closely related species of mammals can have different shapes of teeth and thus tooth development provides an excellent model for molecularly based evolutionary developmental biological studies (evo/devo). These tooth evolutional changes took place by the activation or inactivation of gene function, and thus evolutionary lost structures or gene activation/inactivation during evolution are occasionally retained as vestigial structures or latent gene activation/inactivation at embryonic stages.The current view is that all mammalian teeth evolved from simple ancestral teeth with a conical shape not dissimilar to mammalian canines (1). Mammalian heterodont dentitions contain a variety of tooth shapes and most evo/devo studies have focused solely on the molar dentition, with cuspal morphology being used as the main comparative feature between specimens (1). A cusp is a pointed or rounded projection of the tooth that is composed of both enamel and dentin, and the general consensus is that multicuspid teeth (molariform) evolved from conical teeth by progressive addition of extra "cones" (1). Incisors however are a uniquely mammalian tooth type that are neither conical nor multicuspid and their evolutional process is not understood.Among mammalian teeth, murine dentition has been used as a powerful tool for evo/devo studies because of the relative ease of gene manipulation. A major defining feature of R...

Anatomical and histological characteristics of teeth in agouti (Dasyprocta prymnolopha Wagler, 1831)

“…The enamel prisms provide greater mechanical strength and increase in mechanic imbrication are more adapted to act as masticatory dental elements, which features a small enamel prismless layer temporary on the tooth surface, or even mice, which have a thin layer of enamel surface (Bishop 1995, Koussoulakou 2009, Ohazama et al 2010). The underlying dentin enamel tubules showed a pattern in which the tubules are interleaved by a more compacted dentin, called intertubular dentin, and this pattern is found in other mammals, even in humans (Forssell-Ahlberg et al Muylle et al 2001).…”

Development and evolution of the unique cetacean dentition

“…Our understanding of how morphologically-distinct tooth classes and complex tooth crown shapes develop in mammals is largely derived from research on mice (Munne et al, 2010; Ohazama et al, 2010a; Ohazama et al, 2010b). The first morphological sign of tooth development begins with a thickening of oral epithelium along the maxillary and mandibular arches early in the embryonic period before individual teeth can be distinguished (Leche, 1892; Leche, 1895; Orban, 1980; Ruch et al, 1984).…”

Regulation of tooth number by fine-tuning levels of receptor-tyrosine kinase signaling

“…The detailed analysis of one of these mutants (Sostdc1) showed that the supernumerary incisor developed on the lingual side of the normal one, and this tooth was considered to belong to a different tooth generation, corresponding to the revival of either the replacement incisor (Munne et al, 2009) or of a rudimentary lacteal incisor (Murashima-Suginami et al, 2007). The supernumerary incisor of Lrp4-null mice has been considered as having the same origin as the supernumerary incisor of Sostdc1 mutants (Ohazama et al, 2010). In the sprouty mutants reported here, the concomitant developmental origin and the side-by-side organization of the two incisors indicate that they must be considered as the same tooth generation.…”