The adaptive significance of enamel loss in the mandibular incisors of cercopithecine primates (Mammalia: Cercopithecidae): a finite element modelling study

Abstract

In several primate groups enamel is reduced or absent from the lingual (tongue) side of the mandibular incisor crowns akin to other placental and marsupial mammalian groups such as rodents, lagomorphs and wombats. Here we investigate the presumed adaptation of crowns with unilateral enamel to the incision of tough foods in cercopithecines, an Old World monkey subfamily, using a simulation approach. We developed and validated a finite element model of the lower central incisor of the rhesus macaque (Macaca mulatta) with labial enamel only to compute three-dimensional displacements and maximum principal stresses on the crown subjected to compressive loads varying in orientation. Moreover, we developed a model of a macaque incisor with enamel present on both labial and lingual aspects, thus resembling the ancestral condition found in the sister taxon, the leaf-eating colobines. The results showed that, concomitant with experimental results, the cercopithecine crown with unilateral enamel bends predominantly towards the inside of the mouth, while displacements decreased when both labial and lingual enamel are present. Importantly, the cercopithecine incisor crown experienced lower maximum principal stress on the lingual side compared to the incisor with enamel on the lingual and labial aspects under non-axial loads directed either towards the inside or outside of the mouth. These findings suggest that cercopithecine mandibular incisors are adapted to a wide range of ingestive behaviours compared to colobines. We conclude that the evolutionary loss of lingual enamel in cercopithecines has conferred a safeguard against crown failure under a loading regime assumed for the ingestion (peeling, scraping) of tough-skinned fruits.

Figure 1. Displacements in a mandibular central incisor of a macaque under an axial load (F).

X, Y and Z indicate displacements in the three orthogonal planes (data from Lev-Tov Chattah et al. , their Fig. 2).

Figure 2. 3D models of macaque mandibular central incisor with labial enamel (A, top row) and both labial and lingual enamel (B, top row).

The bottom row shows longitudinal sections through the models and illustrates the dental materials included in analysis. Labial is to the left. PDL  =  periodontal ligament.

Figure 3. Lateral view of incisor model illustrating constraints (thick arrows and black dot) and loads applied (thin arrows) in FEA.

Numbers indicate different load angles in the labio-lingual direction. A load angle of 14° is along the long axis of the tooth and corresponds to the experimental loading regime. Inset shows occlusal view of model and indicates area where forces were applied to.

Figure 4. Maximum principal stress (MPa) maps in model with labial enamel (A, C) and model with both labial and lingual enamel (B, D) under different loading conditions.

A and B are labial views, and C and D lingual views. Boxes show locations on labial (superior and inferior) and lingual surfaces (superior and inferior) from which means were calculated. Sup lab  =  superior labial; Inf lab  =  inferior labial; Sup ling  =  superior lingual; Inf ling  =  inferior lingual.

Figure 5. Maximum principal stress (MPa) mean values at four locations on labial and lingual surface of incisor in model with labial enamel (LAB) and in model with labial and lingual enamel (LING).

Same abbreviation as in Fig. 4.

Figure 6. Longitudinal sections through an unworn (A) and a worn (B) mandibular central incisor crown of Macaca mulatta (collection of Peter Shellis).

The arrows indicate cracks in the enamel (E) which run parallel to the dark and light Hunter-Schreger bands from the enamel-dentine junction to the outer enamel surface. Note the orientation of the crack in B) which is near parallel to the worn incisal plane. D  =  dentine. Images not to scale. Photos courtesy of Chris Dean.