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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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The four morpho-functional grades hypothesized in Muroidea by Butler [9] on first upper and lower molars.First column: grades with cusp interlocking during occlusion. Second column: grades without cusp interlocking during occlusion. First line: grades displaying oblique chewing movements. Second line: grades displaying longitudinal chewing movements. Grey tinted areas on teeth delimitate wear facets while white lines display the orientation of microscratches. Arrows indicate the spatial orientation of the tooth. Full arrows indicate the occurrence of spatial components of the chewing movement in the related direction. Dotted arrows indicate no spatial component of movement in the related direction. Presence of a dorsal component of the chewing movement implies cusp interlocking. Absence of a lingual component of chewing movement implies propalinality. A. Grade B: oblique chewing and cusp interlocking associated with cuspidate tooth crown and cricetine dental plan [9]. B. Grade C: oblique chewing and non cusp interlocking associated with flattened tooth crown and cricetine dental plan [9]. C. Grade M: longitudinal chewing and cusp interlocking associated with cuspidate tooth crown and murine dental plan [9], [11]. Grade O also corresponds to this association. D. Grade D: longitudinal chewing and non cusp interlocking associated with flattened tooth crown and cricetine dental plan [9].
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pone-0003607-g001: The four morpho-functional grades hypothesized in Muroidea by Butler [9] on first upper and lower molars.First column: grades with cusp interlocking during occlusion. Second column: grades without cusp interlocking during occlusion. First line: grades displaying oblique chewing movements. Second line: grades displaying longitudinal chewing movements. Grey tinted areas on teeth delimitate wear facets while white lines display the orientation of microscratches. Arrows indicate the spatial orientation of the tooth. Full arrows indicate the occurrence of spatial components of the chewing movement in the related direction. Dotted arrows indicate no spatial component of movement in the related direction. Presence of a dorsal component of the chewing movement implies cusp interlocking. Absence of a lingual component of chewing movement implies propalinality. A. Grade B: oblique chewing and cusp interlocking associated with cuspidate tooth crown and cricetine dental plan [9]. B. Grade C: oblique chewing and non cusp interlocking associated with flattened tooth crown and cricetine dental plan [9]. C. Grade M: longitudinal chewing and cusp interlocking associated with cuspidate tooth crown and murine dental plan [9], [11]. Grade O also corresponds to this association. D. Grade D: longitudinal chewing and non cusp interlocking associated with flattened tooth crown and cricetine dental plan [9].

Mentions: For decades tooth crown morphology in mammals has provided key characters for taxonomy, phylogeny and reconstruction of diet adaptations of past species [1]–[3]. Recent discoveries in the developmental field have hoisted tooth morphology to the rank of privileged model for Evo-Devo studies [4]–[6]. Understanding mechanisms that guided tooth crown morphological changes during evolution therefore constitute a crucial area of investigation common to both paleontology and developmental biology. A first step was achieved when three-dimensional investigations enlightened the adaptive relationships between tooth complexity and diet in mammals [7]. The next step, attained in the present work by combined microwear and topographic analyses, consists of a quantitative study of the relationships between chewing movements and crown morphology as hypothesized in previous analyses [8]–[11]. Due to selection constraints in crown morphological evolution, an effective occlusion has to be maintained in order to ensure functional continuity [9]. Muroid rodents appear as the most relevant model in an investigation of this key point because the superfamily Muroidea (sensu Musser and Carleton [12]) includes about one third of modern mammal biodiversity and their phylogeny is well settled [13]–[15]. Muroid molars also display a huge diversity in terms of cusp arrangement and crown elevation. The cricetine dental plan (e.g. Cricetus) illustrates the primitive cusp arrangement of the superfamily [16] with 6 cusps on the first upper molars (M1). The intermediary (e.g. Dendromus) and murine (e.g. Mus) dental plans show derived conditions which have been reached several times during evolution and display respectively 7 and 8 cusps on M1 [11], [14], [16]. The various functional types of occlusion in muroid molars are characterized by two variables; i) the interlocking of corresponding valleys and summits delimited by cusps rows of opposite teeth [11] and ii) the direction of masticatory movements, which can be oblique or propalinal (longitudinal) within the horizontal plane. Butler [8], [9] used qualitative observations of these variables to define four morpho-functional grades for muroid teeth (Fig. 1). Rodents with grade B (Fig. 1A) display oblique chewing movements, cuspidate crowns and cusp interlocking during occlusion [9]. Their cusps bear distinct wear facets and delimit gutters, which allow cusp interlocking. Rodents with grade C (Fig. 1B) also masticate with oblique movements. Their molar crowns are nearly flat, without any well-individualized wear facets [9] and they occlude without cusp interlocking. Grade D rodents (Fig. 1D) exhibit propalinal movements and flat molar occlusal surfaces with no cusp interlocking [9]. Butler recognized the functional singularity of murine molars, for which the grade M has been recently proposed [11]. This grade (Fig. 1C) associates propalinal chewing [8] with cuspidate molars displaying longitudinal gutters which occlude with cusp interlocking [11]. A few members of the muroidea superfamily display cuspidate molars and propalinal movement without longitudinal gutters which limits the longitudinal amplitude of this movement. We defined this new association as grade O (Fig. 1C). Grade B is taken to be the primitive condition within Muroidea [10] while Grades C, D and M are taken to be derived conditions [9]. Transitions from one grade to another are supposed to follow unique evolutionary pathways because of the high functional integration of mammalian dentitions. Crown planation was suggested to allow for a rotation of chewing movement documented by the transition from grade B to grade D through grade C [9], [10]. Cusp reshaping inducing a rotation of crown gutters was proposed to explain the origination of grade M from grade B [11]. Nevertheless these hypotheses have never been tested by analyses confronting morphological, functional and phylogenetic data, and validity of masticatory grades has to be confirmed. In what order do the functional and morphological transformations take place? Does functional continuity allow more flexibility than expected by previous studies?


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)

The four morpho-functional grades hypothesized in Muroidea by Butler [9] on first upper and lower molars.First column: grades with cusp interlocking during occlusion. Second column: grades without cusp interlocking during occlusion. First line: grades displaying oblique chewing movements. Second line: grades displaying longitudinal chewing movements. Grey tinted areas on teeth delimitate wear facets while white lines display the orientation of microscratches. Arrows indicate the spatial orientation of the tooth. Full arrows indicate the occurrence of spatial components of the chewing movement in the related direction. Dotted arrows indicate no spatial component of movement in the related direction. Presence of a dorsal component of the chewing movement implies cusp interlocking. Absence of a lingual component of chewing movement implies propalinality. A. Grade B: oblique chewing and cusp interlocking associated with cuspidate tooth crown and cricetine dental plan [9]. B. Grade C: oblique chewing and non cusp interlocking associated with flattened tooth crown and cricetine dental plan [9]. C. Grade M: longitudinal chewing and cusp interlocking associated with cuspidate tooth crown and murine dental plan [9], [11]. Grade O also corresponds to this association. D. Grade D: longitudinal chewing and non cusp interlocking associated with flattened tooth crown and cricetine dental plan [9].
© Copyright Policy
Related In: Results  -  Collection

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

pone-0003607-g001: The four morpho-functional grades hypothesized in Muroidea by Butler [9] on first upper and lower molars.First column: grades with cusp interlocking during occlusion. Second column: grades without cusp interlocking during occlusion. First line: grades displaying oblique chewing movements. Second line: grades displaying longitudinal chewing movements. Grey tinted areas on teeth delimitate wear facets while white lines display the orientation of microscratches. Arrows indicate the spatial orientation of the tooth. Full arrows indicate the occurrence of spatial components of the chewing movement in the related direction. Dotted arrows indicate no spatial component of movement in the related direction. Presence of a dorsal component of the chewing movement implies cusp interlocking. Absence of a lingual component of chewing movement implies propalinality. A. Grade B: oblique chewing and cusp interlocking associated with cuspidate tooth crown and cricetine dental plan [9]. B. Grade C: oblique chewing and non cusp interlocking associated with flattened tooth crown and cricetine dental plan [9]. C. Grade M: longitudinal chewing and cusp interlocking associated with cuspidate tooth crown and murine dental plan [9], [11]. Grade O also corresponds to this association. D. Grade D: longitudinal chewing and non cusp interlocking associated with flattened tooth crown and cricetine dental plan [9].
Mentions: For decades tooth crown morphology in mammals has provided key characters for taxonomy, phylogeny and reconstruction of diet adaptations of past species [1]–[3]. Recent discoveries in the developmental field have hoisted tooth morphology to the rank of privileged model for Evo-Devo studies [4]–[6]. Understanding mechanisms that guided tooth crown morphological changes during evolution therefore constitute a crucial area of investigation common to both paleontology and developmental biology. A first step was achieved when three-dimensional investigations enlightened the adaptive relationships between tooth complexity and diet in mammals [7]. The next step, attained in the present work by combined microwear and topographic analyses, consists of a quantitative study of the relationships between chewing movements and crown morphology as hypothesized in previous analyses [8]–[11]. Due to selection constraints in crown morphological evolution, an effective occlusion has to be maintained in order to ensure functional continuity [9]. Muroid rodents appear as the most relevant model in an investigation of this key point because the superfamily Muroidea (sensu Musser and Carleton [12]) includes about one third of modern mammal biodiversity and their phylogeny is well settled [13]–[15]. Muroid molars also display a huge diversity in terms of cusp arrangement and crown elevation. The cricetine dental plan (e.g. Cricetus) illustrates the primitive cusp arrangement of the superfamily [16] with 6 cusps on the first upper molars (M1). The intermediary (e.g. Dendromus) and murine (e.g. Mus) dental plans show derived conditions which have been reached several times during evolution and display respectively 7 and 8 cusps on M1 [11], [14], [16]. The various functional types of occlusion in muroid molars are characterized by two variables; i) the interlocking of corresponding valleys and summits delimited by cusps rows of opposite teeth [11] and ii) the direction of masticatory movements, which can be oblique or propalinal (longitudinal) within the horizontal plane. Butler [8], [9] used qualitative observations of these variables to define four morpho-functional grades for muroid teeth (Fig. 1). Rodents with grade B (Fig. 1A) display oblique chewing movements, cuspidate crowns and cusp interlocking during occlusion [9]. Their cusps bear distinct wear facets and delimit gutters, which allow cusp interlocking. Rodents with grade C (Fig. 1B) also masticate with oblique movements. Their molar crowns are nearly flat, without any well-individualized wear facets [9] and they occlude without cusp interlocking. Grade D rodents (Fig. 1D) exhibit propalinal movements and flat molar occlusal surfaces with no cusp interlocking [9]. Butler recognized the functional singularity of murine molars, for which the grade M has been recently proposed [11]. This grade (Fig. 1C) associates propalinal chewing [8] with cuspidate molars displaying longitudinal gutters which occlude with cusp interlocking [11]. A few members of the muroidea superfamily display cuspidate molars and propalinal movement without longitudinal gutters which limits the longitudinal amplitude of this movement. We defined this new association as grade O (Fig. 1C). Grade B is taken to be the primitive condition within Muroidea [10] while Grades C, D and M are taken to be derived conditions [9]. Transitions from one grade to another are supposed to follow unique evolutionary pathways because of the high functional integration of mammalian dentitions. Crown planation was suggested to allow for a rotation of chewing movement documented by the transition from grade B to grade D through grade C [9], [10]. Cusp reshaping inducing a rotation of crown gutters was proposed to explain the origination of grade M from grade B [11]. Nevertheless these hypotheses have never been tested by analyses confronting morphological, functional and phylogenetic data, and validity of masticatory grades has to be confirmed. In what order do the functional and morphological transformations take place? Does functional continuity allow more flexibility than expected by previous studies?

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