A biomechanical perspective on molar emergence and primate life history

Abstract

The strong relationship between M1 emergence age and life history across primates provides a means of reconstructing fossil life history. The underlying process that leads to varying molar emergence schedules, however, remains elusive. Using three-dimensional data to quantify masticatory form in ontogenetic samples representing 21 primate species, we test the hypothesis that the location and timing of molar emergence are constrained to avoid potentially dangerous distractive forces at the temporomandibular joint (TMJ) throughout growth. We show that (i) molars emerge in a predictable position to safeguard the TMJ, (ii) the rate and duration of jaw growth determine the timing of molar emergence, and (iii) the rate and cessation age of jaw growth is related to life history. Thus, orofacial development is constrained by biomechanics throughout ontogeny. This integrative perspective on primate skull growth is consistent with a long sought-after causal explanation underlying the correlation between molar emergence and life history.

Fig. 1.. Macaque skull indicating study landmarks and masticatory muscle mechanics.

(A) Lateral view of skull (left), basal view of cranium (center), and occlusal view of mandible (right) illustrating the 38 landmarks (see table S8) used to capture the position of the three principal masticatory adductor muscles and overall masticatory configuration. (B) Lateral view of the position and orientation of muscle lines of action (MLAs) for the masseter (left), temporalis (center), and medial pterygoid (right) muscles, as well as the point (blue colored circle) where each MLA intersects the TOS plane (dashed line). Checkered circles indicate landmarks that are out of view. See text and the Supplementary Materials for details. Photo credit: H. Glowacka, University of Arizona.

Fig. 2.. Macaque skull indicating overall masticatory configuration and biomechanical variables.

(A) Intersection points of each MLA from Fig. 1 were projected onto the occlusal plane, and their average position was used to represent the point at which the AMRV (red arrow) crosses the TOS plane, projected onto the occlusal plane (red square). (B) Occlusal view of mandible illustrating (left half of image): the position of the AMRV at the level of the occlusal plane (red square), extended laterally by the red dashed line, and the main masticatory regions where the CLM predicts bite points could be (regions I and II) and should not be (region III) located; (right half of image) the measurement resultant molar taken from the position of the AMRV to the distalmost border of each successively emerging mandibular molar (dp₄, M_1-3) and MAL (gray dashed arrow), comprising the summed linear distance from the AMRV, through the last emerged molar and each interproximal space along the entire mandibular arch, terminating anteriorly at infraoral (point no. 29, the midline point at apex of the septum between the mandibular central incisors; see Fig. 1A and table S8). (C) Occlusal view of juvenile mandible mapping out the regions of the CLM and the location of the measurements, resultant molar, and MAL [colored regions and arrows indicate the same as in (B)]. Checkered circles in (B) and (C) indicate landmarks that are out of view. See text and the Supplementary Materials for details. Photo credit: H. Glowacka, University of Arizona.

Fig. 3.. Position of molar emergence throughout growth.

Boxplots of resultant molar for dp4 (top) to M3 (bottom) dental emergence categories for all included primate species. Red dashed line represents the position at which the AMRV crosses the TOS plane, projected onto the occlusal plane (see Fig. 2). Positive resultant molar values indicate that the distalmost molar (i.e., the most recently emerged molar) is positioned anterior to the AMRV.

Fig. 4.. Growth of MAL.

MAL growth for ontogenetic series of known-age individuals representing a subset of five primate species. Breakpoints (indicated by vertical dashed lines) indicate ages at growth cessation and are determined by segmented regression (see text for details).

Fig. 5.. Relationship between life history and MAL growth rate/cessation.

PGLS results for the relationships between PC1 and MAL growth rate (left) and MAL growth cessation (right). PC1 scores derived from a PCA of five primate species and includes brain size and the following life history variables: age at first reproduction, IBI, and gestation length.