Growth and development of trabecular structure in the calcaneus of Japanese macaques (Macaca fuscata) reflects locomotor behavior, life history, and neuromuscular development.

Abstract

Bone structure dynamically adapts to its mechanical environment throughout ontogeny by altering the structure of trabecular bone, the three-dimensional mesh-like structure found underneath joint surfaces. Trabecular structure, then, can provide a record of variation in loading directions and magnitude; and in ontogenetic samples, it can potentially be used to track developmental shifts in limb posture. We aim to broaden the analysis of trabecular bone ontogeny by incorporating interactions between ontogenetic variation in locomotor repertoire, neuromuscular maturation, and life history. We examine the associations between these variables and age-related variation in trabecular structure in the calcaneus of Japanese macaques (Macaca fuscata). We used high-resolution micro-computed tomography scanning to image the calcaneus in a cross-sectional sample of 34 juvenile M. fuscata aged between 0 and 7 years old at the Primate Research Institute, Japan. We calculated whole bone averages of standard trabecular properties and generated whole-bone morphometric maps of bone volume fraction and Young's modulus. Trabecular structure becomes increasingly heterogeneous in older individuals. Bone volume fraction (BV/total volume [TV]) decreases during the first month of life and increases afterward, coinciding with the onset of independent locomotion in M. fuscata. At birth, primary Young's modulus is oriented orthogonal to the ossification center, but after locomotor onset bone structure becomes stiffest in the direction of joint surfaces and muscle attachments. Age-related variation in bone volume fraction is best predicted by an interaction between the estimated percentage of adult brain size, body mass, and locomotor onset. To explain our findings, we propose a model where interactions between age-related increases in body weight and maturation of the neuromuscular system alter the loading environment of the calcaneus, to which the internal trabecular structure dynamically adapts. This model cannot be directly tested based on our cross-sectional data. However, confirmation of the model by longitudinal experiments and in multiple species would show that trabecular structure can be used both to infer behavior from fossil morphology and serve as a valuable proxy for neuromuscular maturation and life history events like locomotor onset and the achievement of an adult-like gait. This approach could significantly expand our knowledge of the biology and behavior of fossil species.