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

Abstract

We aim to broaden the analysis of bone structure by suggesting a new way to incorporate the interactions between behavior, neuromuscular development, 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). If skeletal markers linking these variables can be established, our inferences of the biology and behavior of fossil species would be significantly improved. We μCT scanned the calcaneus in a cross-sectional sample of 36 juveniles aged between 0 and 7 years old and 5 adults 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 Youngs modulus. Trabecular structure is increasingly heterogeneous in older individuals. BV/TV decreases during the first month of life and increases afterwards, coinciding with the onset of independent locomotion. At birth, primary Youngs 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 neuromaturation, body mass, and locomotor independence. Results support the common assumption that trabecular structure dynamically adapts to novel joint loading conditions during ontogeny. The timing of independent locomotion, body size, and neuromuscular development, are all correlated to age-related variation in the trabecular structure of the macaque calcaneus. The causal mechanisms behind the observed patterns cannot be directly inferred from our cross-sectional study. If the model presented in this paper holds up under longitudinal experimental conditions, trabecular structure can be used both to infer behavior from fossil morphology and to serve as a valuable proxy for neuromuscular maturation and life history events like locomotor onset and the achievement of an adult-like gait.

The developing juvenile distal tibia: Radiographic identification of distinct ontogenetic phases and structural trajectories

“…Nonmechanical factors, such as hormones and growth factors, also act to guide this mechanism, as does the regulation by epigenetic, extragenetic and genetic influences (Frost, 1998; Skedros et al, 2007). There is a growing understanding of how the juvenile skeleton responds to changing forces, however, this remains an area of active research with gaps within the knowledge remaining (Ryan et al, 2017; Saers et al, 2022).…”