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Mosaic convergence of rodent dentitions.

Lazzari V, Charles C, Tafforeau P, Vianey-Liaud M, Aguilar JP, Jaeger JJ, Michaux J, Viriot L - PLoS ONE (2008)

Bottom Line: Based on an abundant fossil record and on a well resolved phylogeny, our results show that the most derived functional condition associates longitudinal chewing and non interlocking of cusps.In the second type however, flattening is subsequent to rotation of the chewing movement which can be associated with certain changes in cusp morphology.Because convergent pathways imply distinct ontogenetic trajectories, new Evo/Devo comparative studies on cusp morphogenesis are necessary.

View Article: PubMed Central - PubMed

Affiliation: Institut des Sciences de l'Evolution, CNRS UMR 5554, Université de Montpellier 2, Montpellier, France.

ABSTRACT

Background: Understanding mechanisms responsible for changes in tooth morphology in the course of evolution is an area of investigation common to both paleontology and developmental biology. Detailed analyses of molar tooth crown shape have shown frequent homoplasia in mammalian evolution, which requires accurate investigation of the evolutionary pathways provided by the fossil record. The necessity of preservation of an effective occlusion has been hypothesized to functionally constrain crown morphological changes and to also facilitate convergent evolution. The Muroidea superfamily constitutes a relevant model for the study of molar crown diversification because it encompasses one third of the extant mammalian biodiversity.

Methodology/principal findings: Combined microwear and 3D-topographic analyses performed on fossil and extant muroid molars allow for a first quantification of the relationships between changes in crown morphology and functionality of occlusion. Based on an abundant fossil record and on a well resolved phylogeny, our results show that the most derived functional condition associates longitudinal chewing and non interlocking of cusps. This condition has been reached at least 7 times within muroids via two main types of evolutionary pathways each respecting functional continuity. In the first type, the flattening of tooth crown which induces the removal of cusp interlocking occurs before the rotation of the chewing movement. In the second type however, flattening is subsequent to rotation of the chewing movement which can be associated with certain changes in cusp morphology.

Conclusion/significance: The reverse orders of the changes involved in these different pathways reveal a mosaic evolution of mammalian dentition in which direction of chewing and crown shape seem to be partly decoupled. Either can change in respect to strong functional constraints affecting occlusion which thereby limit the number of the possible pathways. Because convergent pathways imply distinct ontogenetic trajectories, new Evo/Devo comparative studies on cusp morphogenesis are necessary.

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Topographic investigation of tooth crown planation in mammals.A: Topography of the left first upper molars of Atavocricetodon huberi and Gerbillus dasyurus, and the associated histograms of slope value distribution on the tooth crown, with values of Kurtosis K calculated for both taxa (3D slope map with superimposed contour lines computed with Surfer for Windows). B: Box plots showing K value distribution of Muroidea displaying cusp interlocking (n = 23, mean = −0,415) and Muroidea displaying no cusp interlocking (n = 4, mean = −1,08). Mean K values are significantly different between both groups (Student t test: P<0,001).
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pone-0003607-g003: Topographic investigation of tooth crown planation in mammals.A: Topography of the left first upper molars of Atavocricetodon huberi and Gerbillus dasyurus, and the associated histograms of slope value distribution on the tooth crown, with values of Kurtosis K calculated for both taxa (3D slope map with superimposed contour lines computed with Surfer for Windows). B: Box plots showing K value distribution of Muroidea displaying cusp interlocking (n = 23, mean = −0,415) and Muroidea displaying no cusp interlocking (n = 4, mean = −1,08). Mean K values are significantly different between both groups (Student t test: P<0,001).

Mentions: Occlusion in Muroidea is functionally characterized by the occurrence of cusp interlocking and the direction of chewing movements (CD). Discontinuous wear facets observable on lightly worn teeth testify to the occurrence of cusp interlocking or intercuspation (Fig. 1A and 1B). Continuous wear facets are produced along a unique occlusal plane and correspond to non cusp interlocking. The CD value is the angle between the longitudinal tooth row axis and the orientation of microwear scratches [10]. The morphology of molar crown in mammals can be characterized by numerous topographic parameters [e.g. 7], [11], [17], [18]. The present work is focused on the dental plan, the average cusp lowest slope orientation O, the degree of crown levelling K and the hypsodonty index H (Fig. 2). Molars of studied species were assigned to cricetine, murine or intermediary dental plans depending on the number and the arrangement of cusps and crests found (Fig. 2A). The value of O is hypothesized as being related to chewing direction. This descriptor refers to cusp individual shape and more precisely to the lowest slope average orientation in the four main cusps of muroid molars (protocone, hypocone, paracone and metacone, Fig. 2C). The orientation of the lowest slope of the protocone and hypocone has already been shown to be correlated to the direction of chewing in cuspidate muroid molars [11]. The K parameter refers to the crown surface global shape (Fig. 2D) and is estimated by the kurtosis of the distribution of crown slope values provided by computed slope maps (Fig. 3A). It measures the “peakedness” of this distribution. Distributions with K values around 0 are unimodal and indicate a cuspidate crown with rounded cusps (Fig. 3A). Distributions with K inferior to −1 are bimodal with an abundance of extreme slope values and indicate angular cusps and a crown with a nearly flat occlusal surface delimited by steep slopes (Fig. 3A). The hypsodonty index H refers to the relative crown elevation (crown height/crown length, Fig. 2B) [19]. The occurrence of cusp interlocking, the dental plan and the values of CD, K, O and H for each taxon are presented in Table 2.


Mosaic convergence of rodent dentitions.

Lazzari V, Charles C, Tafforeau P, Vianey-Liaud M, Aguilar JP, Jaeger JJ, Michaux J, Viriot L - PLoS ONE (2008)

Topographic investigation of tooth crown planation in mammals.A: Topography of the left first upper molars of Atavocricetodon huberi and Gerbillus dasyurus, and the associated histograms of slope value distribution on the tooth crown, with values of Kurtosis K calculated for both taxa (3D slope map with superimposed contour lines computed with Surfer for Windows). B: Box plots showing K value distribution of Muroidea displaying cusp interlocking (n = 23, mean = −0,415) and Muroidea displaying no cusp interlocking (n = 4, mean = −1,08). Mean K values are significantly different between both groups (Student t test: P<0,001).
© Copyright Policy
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2572836&req=5

pone-0003607-g003: Topographic investigation of tooth crown planation in mammals.A: Topography of the left first upper molars of Atavocricetodon huberi and Gerbillus dasyurus, and the associated histograms of slope value distribution on the tooth crown, with values of Kurtosis K calculated for both taxa (3D slope map with superimposed contour lines computed with Surfer for Windows). B: Box plots showing K value distribution of Muroidea displaying cusp interlocking (n = 23, mean = −0,415) and Muroidea displaying no cusp interlocking (n = 4, mean = −1,08). Mean K values are significantly different between both groups (Student t test: P<0,001).
Mentions: Occlusion in Muroidea is functionally characterized by the occurrence of cusp interlocking and the direction of chewing movements (CD). Discontinuous wear facets observable on lightly worn teeth testify to the occurrence of cusp interlocking or intercuspation (Fig. 1A and 1B). Continuous wear facets are produced along a unique occlusal plane and correspond to non cusp interlocking. The CD value is the angle between the longitudinal tooth row axis and the orientation of microwear scratches [10]. The morphology of molar crown in mammals can be characterized by numerous topographic parameters [e.g. 7], [11], [17], [18]. The present work is focused on the dental plan, the average cusp lowest slope orientation O, the degree of crown levelling K and the hypsodonty index H (Fig. 2). Molars of studied species were assigned to cricetine, murine or intermediary dental plans depending on the number and the arrangement of cusps and crests found (Fig. 2A). The value of O is hypothesized as being related to chewing direction. This descriptor refers to cusp individual shape and more precisely to the lowest slope average orientation in the four main cusps of muroid molars (protocone, hypocone, paracone and metacone, Fig. 2C). The orientation of the lowest slope of the protocone and hypocone has already been shown to be correlated to the direction of chewing in cuspidate muroid molars [11]. The K parameter refers to the crown surface global shape (Fig. 2D) and is estimated by the kurtosis of the distribution of crown slope values provided by computed slope maps (Fig. 3A). It measures the “peakedness” of this distribution. Distributions with K values around 0 are unimodal and indicate a cuspidate crown with rounded cusps (Fig. 3A). Distributions with K inferior to −1 are bimodal with an abundance of extreme slope values and indicate angular cusps and a crown with a nearly flat occlusal surface delimited by steep slopes (Fig. 3A). The hypsodonty index H refers to the relative crown elevation (crown height/crown length, Fig. 2B) [19]. The occurrence of cusp interlocking, the dental plan and the values of CD, K, O and H for each taxon are presented in Table 2.

Bottom Line: Based on an abundant fossil record and on a well resolved phylogeny, our results show that the most derived functional condition associates longitudinal chewing and non interlocking of cusps.In the second type however, flattening is subsequent to rotation of the chewing movement which can be associated with certain changes in cusp morphology.Because convergent pathways imply distinct ontogenetic trajectories, new Evo/Devo comparative studies on cusp morphogenesis are necessary.

View Article: PubMed Central - PubMed

Affiliation: Institut des Sciences de l'Evolution, CNRS UMR 5554, Université de Montpellier 2, Montpellier, France.

ABSTRACT

Background: Understanding mechanisms responsible for changes in tooth morphology in the course of evolution is an area of investigation common to both paleontology and developmental biology. Detailed analyses of molar tooth crown shape have shown frequent homoplasia in mammalian evolution, which requires accurate investigation of the evolutionary pathways provided by the fossil record. The necessity of preservation of an effective occlusion has been hypothesized to functionally constrain crown morphological changes and to also facilitate convergent evolution. The Muroidea superfamily constitutes a relevant model for the study of molar crown diversification because it encompasses one third of the extant mammalian biodiversity.

Methodology/principal findings: Combined microwear and 3D-topographic analyses performed on fossil and extant muroid molars allow for a first quantification of the relationships between changes in crown morphology and functionality of occlusion. Based on an abundant fossil record and on a well resolved phylogeny, our results show that the most derived functional condition associates longitudinal chewing and non interlocking of cusps. This condition has been reached at least 7 times within muroids via two main types of evolutionary pathways each respecting functional continuity. In the first type, the flattening of tooth crown which induces the removal of cusp interlocking occurs before the rotation of the chewing movement. In the second type however, flattening is subsequent to rotation of the chewing movement which can be associated with certain changes in cusp morphology.

Conclusion/significance: The reverse orders of the changes involved in these different pathways reveal a mosaic evolution of mammalian dentition in which direction of chewing and crown shape seem to be partly decoupled. Either can change in respect to strong functional constraints affecting occlusion which thereby limit the number of the possible pathways. Because convergent pathways imply distinct ontogenetic trajectories, new Evo/Devo comparative studies on cusp morphogenesis are necessary.

Show MeSH
Related in: MedlinePlus