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Unique pattern of dietary adaptation in the dentition of Carnivora: its advantage and developmental origin

View Article: PubMed Central

ABSTRACT

Carnivora is a successful taxon in terms of dietary diversity. We investigated the dietary adaptations of carnivoran dentition and the developmental background of their dental diversity, which may have contributed to the success of the lineage. A developmental model was tested and extended to explain the unique variability and exceptional phenotypes observed in carnivoran dentition. Carnivorous mammalian orders exhibited two distinct patterns of dietary adaptation in molars and only Carnivora evolved novel variability, exhibiting a high correlation between relative molar size and the shape of the first molar. Studies of Bmp7-hetero-deficient mice, which may exhibit lower Bmp7 expression, suggested that Bmp7 has pleiotropic effects on these two dental traits. Its effects are consistent with the pattern of dietary adaptation observed in Carnivora, but not that observed in other carnivorous mammals. A molecular evolutionary analysis revealed that Bmp7 sequence evolved by natural selection during ursid evolution, suggesting that it plays an evolutionary role in the variation of carnivoran dentition. Using mouse experiments and a molecular evolutionary analysis, we extrapolated the causal mechanism of the hitherto enigmatic ursid dentition (larger M2 than M1 and M3). Our results demonstrate how carnivorans acquired novel dental variability that benefits their dietary divergence.

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Variation and dietary adaptation pattern of lower molars in three mammalian orders. (a) Plots of M2/M1 versus M3/M1. Each data point indicates one species (electronic supplementary material, table S1); the shape indicates the taxon (circle, Carnivora; diamond, Creodonta; triangle, Dasyuromorphia) and the colour indicates the diet (orange, carnivorous; red, hyper-carnivorous; green, herbivorous; purple, insectivorous; blue, omnivorous). The blue line indicates the original regression line in the IC model [13]. The black line indicates the regression of the species in Carnivora that have three lower molars. The grey areas indicate patterns that cannot be explained by the IC model (M1 < M2 > M3 or M1 > M2 < M3) [14]. Omnivorous and insectivorous species tend to have equal-sized molars. Carnivorous carnivorans tend to have larger M1, but carnivorous creodonts and dasyuromorphians tend to have larger mesial molars (smaller M1). Arrowed lines indicate two types of carnivorous adaptations among three orders. (b) Plots of M2/M1 versus tad/trd. Carnivorous species tend to have relatively larger trigonids relative to omnivorous and insectivorous species in all three orders.
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RSPB20160375F1: Variation and dietary adaptation pattern of lower molars in three mammalian orders. (a) Plots of M2/M1 versus M3/M1. Each data point indicates one species (electronic supplementary material, table S1); the shape indicates the taxon (circle, Carnivora; diamond, Creodonta; triangle, Dasyuromorphia) and the colour indicates the diet (orange, carnivorous; red, hyper-carnivorous; green, herbivorous; purple, insectivorous; blue, omnivorous). The blue line indicates the original regression line in the IC model [13]. The black line indicates the regression of the species in Carnivora that have three lower molars. The grey areas indicate patterns that cannot be explained by the IC model (M1 < M2 > M3 or M1 > M2 < M3) [14]. Omnivorous and insectivorous species tend to have equal-sized molars. Carnivorous carnivorans tend to have larger M1, but carnivorous creodonts and dasyuromorphians tend to have larger mesial molars (smaller M1). Arrowed lines indicate two types of carnivorous adaptations among three orders. (b) Plots of M2/M1 versus tad/trd. Carnivorous species tend to have relatively larger trigonids relative to omnivorous and insectivorous species in all three orders.

Mentions: A developmental model called the inhibitory cascade (IC) model proposes that the relative size of the lower molars is governed by the balance of inhibitory molecules secreted by the M1 tooth germ and activation molecules from the mesenchyme [13]. Accordingly, relative molar sizes vary from M1 > M2 > M3 to M1 = M2 = M3 to M1 < M2 < M3 along a particular regression line in the M2/M1 versus M3/M1 morphospace [13] (figure 1). This model can explain interspecific variation in many mammalian groups except for several bear, horse and vole species [13–21]. However, some taxa, such as canids (i.e. Canidae, Carnivora), exhibit unique patterns with small slopes; the slope of the M2/M1 versus M3/M1 regression in canids (0.45) is smaller than that indicated by the IC model in murines (2.0) [13]. The correlation between M2/M1 and M3/M1 indicates that they basically fit the IC model (the inhibition/activation mechanism affects both M2/M1 and M3/M1) [15]. However, ursids (i.e. Ursidae, Carnivora) exhibit M1 < M2 > M3, which could not be explained by the model [14]. Several members of equines (horses) and arvicolines (voles) also exhibit M1 < M2 > M3 or M1 > M2 < M3, which cannot be explained by the model [14,16,17]. The interspecific slope for other carnivorous mammals, the causes underlying the differences in slopes from the IC model and the exceptional dental pattern observed in ursids remain unclear.Figure 1.


Unique pattern of dietary adaptation in the dentition of Carnivora: its advantage and developmental origin
Variation and dietary adaptation pattern of lower molars in three mammalian orders. (a) Plots of M2/M1 versus M3/M1. Each data point indicates one species (electronic supplementary material, table S1); the shape indicates the taxon (circle, Carnivora; diamond, Creodonta; triangle, Dasyuromorphia) and the colour indicates the diet (orange, carnivorous; red, hyper-carnivorous; green, herbivorous; purple, insectivorous; blue, omnivorous). The blue line indicates the original regression line in the IC model [13]. The black line indicates the regression of the species in Carnivora that have three lower molars. The grey areas indicate patterns that cannot be explained by the IC model (M1 < M2 > M3 or M1 > M2 < M3) [14]. Omnivorous and insectivorous species tend to have equal-sized molars. Carnivorous carnivorans tend to have larger M1, but carnivorous creodonts and dasyuromorphians tend to have larger mesial molars (smaller M1). Arrowed lines indicate two types of carnivorous adaptations among three orders. (b) Plots of M2/M1 versus tad/trd. Carnivorous species tend to have relatively larger trigonids relative to omnivorous and insectivorous species in all three orders.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4920314&req=5

RSPB20160375F1: Variation and dietary adaptation pattern of lower molars in three mammalian orders. (a) Plots of M2/M1 versus M3/M1. Each data point indicates one species (electronic supplementary material, table S1); the shape indicates the taxon (circle, Carnivora; diamond, Creodonta; triangle, Dasyuromorphia) and the colour indicates the diet (orange, carnivorous; red, hyper-carnivorous; green, herbivorous; purple, insectivorous; blue, omnivorous). The blue line indicates the original regression line in the IC model [13]. The black line indicates the regression of the species in Carnivora that have three lower molars. The grey areas indicate patterns that cannot be explained by the IC model (M1 < M2 > M3 or M1 > M2 < M3) [14]. Omnivorous and insectivorous species tend to have equal-sized molars. Carnivorous carnivorans tend to have larger M1, but carnivorous creodonts and dasyuromorphians tend to have larger mesial molars (smaller M1). Arrowed lines indicate two types of carnivorous adaptations among three orders. (b) Plots of M2/M1 versus tad/trd. Carnivorous species tend to have relatively larger trigonids relative to omnivorous and insectivorous species in all three orders.
Mentions: A developmental model called the inhibitory cascade (IC) model proposes that the relative size of the lower molars is governed by the balance of inhibitory molecules secreted by the M1 tooth germ and activation molecules from the mesenchyme [13]. Accordingly, relative molar sizes vary from M1 > M2 > M3 to M1 = M2 = M3 to M1 < M2 < M3 along a particular regression line in the M2/M1 versus M3/M1 morphospace [13] (figure 1). This model can explain interspecific variation in many mammalian groups except for several bear, horse and vole species [13–21]. However, some taxa, such as canids (i.e. Canidae, Carnivora), exhibit unique patterns with small slopes; the slope of the M2/M1 versus M3/M1 regression in canids (0.45) is smaller than that indicated by the IC model in murines (2.0) [13]. The correlation between M2/M1 and M3/M1 indicates that they basically fit the IC model (the inhibition/activation mechanism affects both M2/M1 and M3/M1) [15]. However, ursids (i.e. Ursidae, Carnivora) exhibit M1 < M2 > M3, which could not be explained by the model [14]. Several members of equines (horses) and arvicolines (voles) also exhibit M1 < M2 > M3 or M1 > M2 < M3, which cannot be explained by the model [14,16,17]. The interspecific slope for other carnivorous mammals, the causes underlying the differences in slopes from the IC model and the exceptional dental pattern observed in ursids remain unclear.Figure 1.

View Article: PubMed Central

ABSTRACT

Carnivora is a successful taxon in terms of dietary diversity. We investigated the dietary adaptations of carnivoran dentition and the developmental background of their dental diversity, which may have contributed to the success of the lineage. A developmental model was tested and extended to explain the unique variability and exceptional phenotypes observed in carnivoran dentition. Carnivorous mammalian orders exhibited two distinct patterns of dietary adaptation in molars and only Carnivora evolved novel variability, exhibiting a high correlation between relative molar size and the shape of the first molar. Studies of Bmp7-hetero-deficient mice, which may exhibit lower Bmp7 expression, suggested that Bmp7 has pleiotropic effects on these two dental traits. Its effects are consistent with the pattern of dietary adaptation observed in Carnivora, but not that observed in other carnivorous mammals. A molecular evolutionary analysis revealed that Bmp7 sequence evolved by natural selection during ursid evolution, suggesting that it plays an evolutionary role in the variation of carnivoran dentition. Using mouse experiments and a molecular evolutionary analysis, we extrapolated the causal mechanism of the hitherto enigmatic ursid dentition (larger M2 than M1 and M3). Our results demonstrate how carnivorans acquired novel dental variability that benefits their dietary divergence.

No MeSH data available.


Related in: MedlinePlus