When less means more: evolutionary and developmental hypotheses in rodent molars

Abstract

Tooth number in rodents is an example of reduction in evolution. All rodents have a toothless diastema lacking canine and most premolars present in most other mammals. Whereas some rodent lineages retained one premolar (p4), many others lost it during evolution. Recently, an 'inhibitory cascade' developmental model (IC) has been used to predict how the first molar (m1) influences the number and relative sizes of the following distal molars (m2 and m3). The model does not, however, consider the presence of premolars, and here we examine whether the premolar could influence and constrain molar proportions during development and evolution. By investigating a large data set of both extinct and extant rodent families over more than 40 million years, we show that the basal phenotype is characterized by the presence of premolars together with equally sized molars. More recent rodent families, with and without premolar, show more unequal molar sizes. Analysing molar areas, we demonstrated that (i) rodents harbour almost all the molar proportions known in mammals, and the IC model can explain about 80% of taxa in our data set; (ii) proportions of molars are influenced by the presence or absence of p4; and (iii) the most variable teeth in the dental row are m1 and m3, whether p4 is present or not. Moreover, m1 can represent up to half of the total molar area when p4 is absent. We hypothesize that p4 loss during evolution released the constraint on m1 development, resulting in a more variable size of m1 and thereby having an indirect effect on the evolution of the whole molar row.

Testing the inhibitory cascade model in Mesozoic and Cenozoic mammaliaforms

“…This observation is consistent with, although slightly higher than, other studies, in which 12-20% fall outside the predicted region [10,12]. Of the 46 taxa which fell outside this ‘m2 intermediate’ region, 39 fell in the area in which m2 was the largest lower molar; only 7 displayed an m2 that was the smallest of the three molars.…”

“…Furthermore, this study is wholly consistent with, and resembles closely, the results from a recent study that focused on rodents [12]. While murids made up the majority of the rodents in this study, Labonne et al [12] used a broader phylogenetic sampling of rodent taxa, which spanned the same range of molar ratios as do all mammals. This correspondence strongly suggests that a common developmental mechanism underlies the development of all mammalian teeth, rather than being specific to rodents.…”

“…Labonne et al [12] demonstrated that loss of the lower fourth premolar in some taxa appeared to remove a spatial constraint on the development of the lower first molar. This loss would then affect the development of the first molar to a far greater extent that the more posterior molars, enabling a proportionally larger m1.…”

“…While the approach used here, and in the studies noted above, estimated tooth area as a product of maximum length and width, some other studies [8,11,12,14] have measured tooth occlusal area directly. In order to establish the comparability of these area measurements, we also directly measured molar area in 41 genera (41 specimens) for which specimens were available.…”

“…The predictions of the IC Model have been found to, for the most part, be applicable to Rodentia [12] as a whole, and South American ungulates [13], although in each case, several taxa fell outside of the expected area. Thus far, the largest deviation from the predictions of the IC Model has been found in canids (dogs and their kin) [11], but also in arvicoline rodents (voles and lemmings) [14], leading the latter authors to conclude that the IC Model might not be generalisable even across rodents.…”