Biomechanical Constraints on Molar Emergence in Primates

Molar-emergence age serves as a skeletal proxy for life history in the fossil record. Knowledge of how variation in molar-emergence age arises and why it is closely associated with life history is lacking, however. Understanding the mechanism that produces variation in molar-emergence age is critical to evaluating why molar emergence tracks life history. Molars are part of an integrated system in which they function to comminute food. Developmental coordination among parts of this system is critical for proper food ingestion throughout life. In adult primates, the biomechanics of masticatory system configuration constrain where molars can be situated to avoid damage to the temporomandibular joint (TMJ) during chewing. This research tested the hypothesis that the location of molar emergence is constrained to avoid damage to the TMJ throughout ontogeny. Two predictions were tested: that molars emerge directly anterior to the adductor resultant and that molars emerge significantly anterior to the adductor resultant. 3D coordinate data were collected from cross-sectional ontogenetic samples of primate skulls (n = 21 species, 1258 specimens). The position of the resultant was estimated using two methods: (1) the average position of the three adductor muscle lines of action (MLAs) and (2) the most anterior MLA. Results indicate that molars emerge significantly anterior to the resultant throughout ontogeny; however, when the most anterior MLA is used to approximate the position of the resultant, the last molar is posterior to the MLA in later ontogenetic stages and adults of some taxa. This latter result contradicts previous 28 findings for adult primates and possible reasons for this are discussed. Overall, the study supports the idea that molar emergence is constrained by the biomechanics of mastication, especially early in ontogeny. Introduction The age at which the permanent first molar (M1) emerges into the oral cavity is strongly correlated with life-history variables across primates (Smith 1989; Smith, Crummett, and Brandt 1994; Kelley and Schwartz 2010), and has been used to reconstruct the life history of fossil primates (e.g., Kelley 1997; Kelley and Smith 2003; Zihlman et al. 2004; Kelley and Schwartz 2012). The underlying mechanism driving this strong correlation remains unknown. Molar emergence should be completely integrated into the growth of the skull and part of an integrated masticatory system (Smith 1989; Spencer and Schwartz 2008). This study therefore examines molar emergence in the context of masticatory ontogeny. The adult masticatory system of mammals is configured to avoid distraction of the temporomandibular joint (TMJ) (i.e., when the mandibular condyle is pulled away from the articular eminence) during biting and chewing (Greaves 1978, 1982, 1983, 1991, 2000; Spencer and Demes 1993; Spencer 1995, 1999; Thompson et al. 2003; Perry, Hartstone-Rose, and Logan 2011). According to the Constrained Lever Model (CLM), three points of resistance occur during unilateral biting (one at each TMJ and one at the bite point), and define the edges of the triangle of support. During unilateral biting, the adductor muscle resultant vector must pass through the triangle of support. If the resultant passes outside of the triangle of support, the bite point and balancing-side TMJ 29 experience rotation while the working-side TMJ experiences tension (i.e., TMJ distraction, Greaves 1978; Spencer 1999). Given this limitation, a key aspect of masticatory system configuration is the position of molars along the maxillary and mandibular arches in relation to the adductor muscle resultant vector. As per the CLM, the distal-most molar’s position is constrained so that it is located anterior to the point at which the jaw adductor muscle resultant crosses the triangle of support because biting posterior to this point produces distractive forces at the working-side TMJ (Greaves 1978; Spencer 1999). Molars should, therefore, always be positioned along the mandibular and maxillary arches such that TMJ distraction is mitigated during mastication. The original CLM, as described by Greaves (1978, 1982, 1983, 1988), predicts that the distal-most molar lies immediately anterior to the muscle resultant (Greaves 1978). Several studies have found, however, that the molar’s position is more anterior than predicted by the original CLM (Spencer 1999; Perry, Hartstone-Rose, and Logan 2011; Lucas, 2012). Extending the CLM model into ontogeny will require a test of these two scenarios. Extending the CLM to ontogenetic stages suggests that molars should emerge anterior to the muscle resultant. The availability of space between the muscle resultant and the distal-most tooth present in the tooth row should be a constraint on where molars emerge. Most tests of the CLM in primates have been performed on adult primates and the utility of the CLM in describing the configuration of the masticatory system in infant and juvenile primates has not been explored systematically across primates, though it would seem logical that the same biomechanical constraint operating in adults should also operate at all stages throughout ontogeny. Indeed, in humans, chimpanzees, and 30 papionins, molars emerge at a constant distance to the TMJ (Spencer and Schwartz 2008; Schwartz 2012; Singleton, 2015), a finding consistent with the expectations of the CLM. Therefore, despite there being substantial variation in craniofacial configuration among these taxa, there appears to be a common constraint on the position of molar emergence that operates during ontogeny.