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

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.

The origin of the lower fourth molar in canids, inferred by individual variation

“…Asahara (2013) and Asahara et al (2016) reported that the relative molar size was reflective of the diet among species of canids. The more carnivorous canid species (such as Canis lupus ) possess low M 2 /M 1 scores and the more omnivorous species (such as N. procyonoides or U. cinereoargenteus ) have higher scores (Asahara, 2013; Asahara et al, 2016).…”

“…The more carnivorous canid species (such as Canis lupus ) possess low M 2 /M 1 scores and the more omnivorous species (such as N. procyonoides or U. cinereoargenteus ) have higher scores (Asahara, 2013; Asahara et al, 2016). In addition, the insectivorous hoary fox Lycalopex vetulus has higher M 2 /M 1 and M 3 /M 1 scores than almost all other omnivorous species, and the insectivorous bat-eared fox O. megalotis has higher M 2 /M 1 and M 3 /M 1 scores than all other canids, indicating very low inhibition and high activation during molar development (Asahara, 2013).…”

“…Bat-eared foxes are primarily insectivorous (Sillero-Zubiri, 2009), with a molar morphology comprising an undeveloped carnassial blade, equally sized molars (in relation to the other canids) and increased number of molars, which are attributable to an adaptation to an insectivorous diet (Wang & Tedford, 2008; Asahara, 2013; Asahara et al, 2016). It has been proposed that this dentition is suitable to a diet of insects that are small relative to the body size of the bat-eared fox, with a larger molar row grinding surface that enables greater chewing efficiency (Asahara, 2013; Asahara et al, 2016).…”

“…It has been proposed that this dentition is suitable to a diet of insects that are small relative to the body size of the bat-eared fox, with a larger molar row grinding surface that enables greater chewing efficiency (Asahara, 2013; Asahara et al, 2016). However, this does not explain the presence of the fourth molar, the developmental origin of which remains unclear.…”

“…According to the balance of these two factors, the relative size of M 1 , M 2 , and M 3 (typically shown numerically as M 2 /M 1 and M 3 /M 1 size ratios; the size is defined as projected tooth area from occlusal view) result in a pattern of M 1 > M 2 > M 3 , M 1 = M 2 = M 3 , or M 1 < M 2 < M 3 (Kavanagh, Evans & Jernvall, 2007). This model has previously been applied to explain dental variation in Carnivora (Polly, 2007; Halliday & Goswami, 2013; Asahara, 2013; Asahara et al, 2016). …”