Ontogenetic and morphological variation in primate long bones reflects signals of size and behavior

Abstract

Objectives: Many primates change their locomotor behavior as they mature from infancy to adulthood. Here we investigate how long bone cross-sectional geometry in Pan, Gorilla, Pongo, Hylobatidae, and Macaca varies in shape and form over ontogeny, including whether specific diaphyseal cross sections exhibit signals of periosteal adaptation or canalization. Materials and methods: Diaphyseal cross sections were analyzed in an ontogenetic series across infant, juvenile, and adult subgroups. Three-dimensional laser-scanned long bone models were sectioned at midshaft (50% of biomechanical length) and distally (20%) along the humerus and femur. Traditional axis ratios acted as indices of cross-sectional circularity, while geometric morphometric techniques were used to study cross-sectional allometry and ontogenetic trajectory. Results: The humeral midshaft is a strong indicator of posture and locomotor profile in the sample across development, while the mid-femur appears more reflective of shifts in size. By comparison, the distal diaphyses of both limb elements are more ontogenetically constrained, where periosteal shape is largely static across development relative to size, irrespective of a given taxon's behavior or ecology. Discussion: Primate limb shape is not only highly variable between taxa over development, but at discrete humeral and femoral diaphyseal locations. Overall, periosteal shape of the humeral and femoral midshaft cross sections closely reflects ontogenetic transitions in behavior and size, respectively, while distal shape in both bones appears more genetically constrained across intraspecific development, regardless of posture or size. These findings support prior research on tradeoffs between function and safety along the limbs.

Skeletal indicators of developmental changes in arboreality and locomotor maturation in extant apes and their relevance to hominin paleobiology

“…Overall, these results are consistent with the prediction that ratios of Total.BV/TV between anatomical regions corresponds to agerelated variation in locomotor repertoire. These findings support evidence of strong associations between locomotor ontogeny and bone morphology from studies on midshaft diaphyseal cortical bone geometry (Pearson and Lieberman, 2004;Ruff et al, 2018;Nadell et al, 2021;Cosman, 2023). The relationship between trabecular bone ontogeny and age-related variation in locomotion is not as straightforward.…”

“…Reconstructing age-related variation in locomotor behaviour from skeletal remains requires mechanically sensitive traits that are phenotypically plastic throughout ontogeny. Several studies have demonstrated the developmental plasticity in response to locomotor loading in hominoid long bone diaphyseal structure (Carrier, 1983;Cowgill, 2010;Cowgill et al, 2010;Sarringhaus et al, 2016;Cowgill and Robyn, 2018;Morimoto et al, 2018;Ruff et al, 2018;Nadell et al, 2021). Ruff and colleagues (2018) investigated the ontogeny of limb morphology and diaphyseal strength between relatively arboreal western lowland gorillas to more terrestrial Virunga mountain gorillas.…”

Do femoral biomechanical properties follow locomotor changes in primates? An ontogenetic study of olive baboons (Papio anubis)

“…In contrast, African apes which have a locomotor repertoire that also involves parasagittal movements during knuckle‐walking, but whose arboreal locomotion is more important than in adult baboons, present even more mediolaterally oriented bending rigidity and thicker medial and lateral diaphyses (Morimoto et al, 2018; Nadell, 2017; Puymerail, 2011). Additionally, the mediolateral bending rigidity and strength that characterize the distal diaphysis of our adult sample, are observed in the femoral distal diaphysis of several primates with varied locomotor repertoire and body size including hominoids even in large bodied arboreal primates such as orangutans (Nadell et al, 2021; Rodríguez, 2018; Trinkaus & Ruff, 2012). Additionally, asymmetrical load resistance along the longitudinal axis of the diaphysis has been described in hominine (Mongle et al, 2015).…”

Coming to the Caribbean—acclimation of Rhesus macaques (Macaca mulatta) at Cayo Santiago

“…This runs counter to the proposed direction of acclimation, including Weinstein's (2001) findings that warmer‐residing macaque species exhibit greater relative joint diameters than those in colder climates. Given the twofold decrease in female to male macaque body weight, it seems likely that female diaphyseal dimensions exhibited a relative increase either as an allometric constraint (Egi, 2001; Campione & Evans, 2012; Nadell et al, 2021) to facilitate stability or movement, rather than indications of physical activity (Lieberman et al, 2001; Ruff & Runestad, 1992), or locomotion preference (Godfrey et al, 1991).…”