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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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Convergent morpho-functional evolution revealed by microwear pattern and topographic slopes crown maps in three muroid lineages.Cricetidae (A. Democricetodon sp., B. Rotundomys motisrotundi, C. Microtus duodecimcostatus), Gerbillinae (D. Myocricetodon irhoudi, E. Myocricetodon ouedi and F. Gerbillus dasyurus) and Nesomyidae (G. Mystromys sp., H. Dendromus sp. 2 and I. Cricetomys sp.). The morpho-functional grade (B, C, O, M or D in bold) is inferred from crossed quantitative interpretations of crown topography and microwear pattern on left M1. In the upper left quarter is a picture of a wear facet for each species. The white arrow indicates the mean direction of microscratches corresponding to the direction of chewing. White scale bar: 100 µm. A colour slope map displaying the orientation of the cusps lowest slopes is presented on the right half of the diagram for each species. Black scale bar: 500 µm. The histogram of distribution of crown slopes is presented in the lower left quarter. Unimodal histograms (Kurtosis superior to −1) indicate cuspidate crowns, with predominant intermediary slope values associated with round cusps. Bimodal histograms (Kurtosis inferior to −1) indicate flattened crowns, with predominant extreme slope values associated with angular cusps.
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pone-0003607-g006: Convergent morpho-functional evolution revealed by microwear pattern and topographic slopes crown maps in three muroid lineages.Cricetidae (A. Democricetodon sp., B. Rotundomys motisrotundi, C. Microtus duodecimcostatus), Gerbillinae (D. Myocricetodon irhoudi, E. Myocricetodon ouedi and F. Gerbillus dasyurus) and Nesomyidae (G. Mystromys sp., H. Dendromus sp. 2 and I. Cricetomys sp.). The morpho-functional grade (B, C, O, M or D in bold) is inferred from crossed quantitative interpretations of crown topography and microwear pattern on left M1. In the upper left quarter is a picture of a wear facet for each species. The white arrow indicates the mean direction of microscratches corresponding to the direction of chewing. White scale bar: 100 µm. A colour slope map displaying the orientation of the cusps lowest slopes is presented on the right half of the diagram for each species. Black scale bar: 500 µm. The histogram of distribution of crown slopes is presented in the lower left quarter. Unimodal histograms (Kurtosis superior to −1) indicate cuspidate crowns, with predominant intermediary slope values associated with round cusps. Bimodal histograms (Kurtosis inferior to −1) indicate flattened crowns, with predominant extreme slope values associated with angular cusps.

Mentions: The morpho-functional modifications which accompanied grade-to-grade transitions can be reconstructed using fossil record and replaced in the robust muroid phylogenetic context. Several examples of convergent evolutions leading from grade B to grade D through distinct intermediary grades are illustrated here by the Cricetidae (e.g. Arvicolinae), Gerbillinae (e.g. Gerbillinae), and Nesomyidae (e.g. Cricetomyinae). Among Cricetidae, the subfamily Arvicolinae (e.g. Microtus Grade D, Fig. 6C) emerged during the Late Miocene radiation of “microtoid cricetids” [22] like Rotundomys (Grade C, Fig. 6B), which originated from Cricetodontinae like Democricetodon [23] (Grade B, Fig. 6A). In this case the transition from grade B to grade D is accomplished by a transition through grade C. Such a transition is also observed in Nesomyinae and Spalacidae (Fig. 5). Extant Gerbillinae like Gerbillus (Grade D, Fig. 6F) emerged from Miocene taxa like Myocricetodon irhoudi (Grade B, Fig. 6D) through intermediary forms like M. ouedi [24] (Grade O, Fig. 6E). In this lineage, grade D is reached by a transition through grade O. Among Nesomyidae, the Cricetomyinae (e.g. Cricetomys Grade D, Fig. 6I) display a murine dental plan and constitute the sister group of the Dendromurinae [13]–[15] (e.g. Dendromus, Grade M, Fig. 6H) which are showing an intermediary plan. Cricetomyinae and Dendromurinae share a common ancestor with the genus Mystromys [14] (Grade B, Fig. 6G) which displays a cricetine plan. These phylogenetical relationships suggest that grade D has been reached here by a transition through the grade M and accompanied the transition from cricetine to murine dental plan. A similar transition is also observed in Murinae (Fig. 5). However, the emergence of grade D in rodents appears to be more frequently reached via a transition involving grade C. Indeed, not only does it occur at least 3 times in Muroidea (Fig. 5), but it also appears in other groups of rodents as Dipodoidea [10].


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)

Convergent morpho-functional evolution revealed by microwear pattern and topographic slopes crown maps in three muroid lineages.Cricetidae (A. Democricetodon sp., B. Rotundomys motisrotundi, C. Microtus duodecimcostatus), Gerbillinae (D. Myocricetodon irhoudi, E. Myocricetodon ouedi and F. Gerbillus dasyurus) and Nesomyidae (G. Mystromys sp., H. Dendromus sp. 2 and I. Cricetomys sp.). The morpho-functional grade (B, C, O, M or D in bold) is inferred from crossed quantitative interpretations of crown topography and microwear pattern on left M1. In the upper left quarter is a picture of a wear facet for each species. The white arrow indicates the mean direction of microscratches corresponding to the direction of chewing. White scale bar: 100 µm. A colour slope map displaying the orientation of the cusps lowest slopes is presented on the right half of the diagram for each species. Black scale bar: 500 µm. The histogram of distribution of crown slopes is presented in the lower left quarter. Unimodal histograms (Kurtosis superior to −1) indicate cuspidate crowns, with predominant intermediary slope values associated with round cusps. Bimodal histograms (Kurtosis inferior to −1) indicate flattened crowns, with predominant extreme slope values associated with angular cusps.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2572836&req=5

pone-0003607-g006: Convergent morpho-functional evolution revealed by microwear pattern and topographic slopes crown maps in three muroid lineages.Cricetidae (A. Democricetodon sp., B. Rotundomys motisrotundi, C. Microtus duodecimcostatus), Gerbillinae (D. Myocricetodon irhoudi, E. Myocricetodon ouedi and F. Gerbillus dasyurus) and Nesomyidae (G. Mystromys sp., H. Dendromus sp. 2 and I. Cricetomys sp.). The morpho-functional grade (B, C, O, M or D in bold) is inferred from crossed quantitative interpretations of crown topography and microwear pattern on left M1. In the upper left quarter is a picture of a wear facet for each species. The white arrow indicates the mean direction of microscratches corresponding to the direction of chewing. White scale bar: 100 µm. A colour slope map displaying the orientation of the cusps lowest slopes is presented on the right half of the diagram for each species. Black scale bar: 500 µm. The histogram of distribution of crown slopes is presented in the lower left quarter. Unimodal histograms (Kurtosis superior to −1) indicate cuspidate crowns, with predominant intermediary slope values associated with round cusps. Bimodal histograms (Kurtosis inferior to −1) indicate flattened crowns, with predominant extreme slope values associated with angular cusps.
Mentions: The morpho-functional modifications which accompanied grade-to-grade transitions can be reconstructed using fossil record and replaced in the robust muroid phylogenetic context. Several examples of convergent evolutions leading from grade B to grade D through distinct intermediary grades are illustrated here by the Cricetidae (e.g. Arvicolinae), Gerbillinae (e.g. Gerbillinae), and Nesomyidae (e.g. Cricetomyinae). Among Cricetidae, the subfamily Arvicolinae (e.g. Microtus Grade D, Fig. 6C) emerged during the Late Miocene radiation of “microtoid cricetids” [22] like Rotundomys (Grade C, Fig. 6B), which originated from Cricetodontinae like Democricetodon [23] (Grade B, Fig. 6A). In this case the transition from grade B to grade D is accomplished by a transition through grade C. Such a transition is also observed in Nesomyinae and Spalacidae (Fig. 5). Extant Gerbillinae like Gerbillus (Grade D, Fig. 6F) emerged from Miocene taxa like Myocricetodon irhoudi (Grade B, Fig. 6D) through intermediary forms like M. ouedi [24] (Grade O, Fig. 6E). In this lineage, grade D is reached by a transition through grade O. Among Nesomyidae, the Cricetomyinae (e.g. Cricetomys Grade D, Fig. 6I) display a murine dental plan and constitute the sister group of the Dendromurinae [13]–[15] (e.g. Dendromus, Grade M, Fig. 6H) which are showing an intermediary plan. Cricetomyinae and Dendromurinae share a common ancestor with the genus Mystromys [14] (Grade B, Fig. 6G) which displays a cricetine plan. These phylogenetical relationships suggest that grade D has been reached here by a transition through the grade M and accompanied the transition from cricetine to murine dental plan. A similar transition is also observed in Murinae (Fig. 5). However, the emergence of grade D in rodents appears to be more frequently reached via a transition involving grade C. Indeed, not only does it occur at least 3 times in Muroidea (Fig. 5), but it also appears in other groups of rodents as Dipodoidea [10].

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