Functional integration of skeletal traits: an intraskeletal assessment of bone size, mineralization, and volume covariance

Abstract

Understanding the functional integration of skeletal traits and how they naturally vary within and across populations will benefit assessments of functional adaptation directed towards interpreting bone stiffness in contemporary and past humans. Moreover, investigating how these traits intraskeletally vary will guide us closer towards predicting fragility from a single skeletal site. Using an osteological collection of 115 young adult male and female African-Americans, we assessed the functional relationship between bone robustness (i.e. total area/length), cortical tissue mineral density (Ct.TMD), and cortical area (Ct.Ar) for the upper and lower limbs. All long bones demonstrated significant trait covariance (p < 0.005) independent of body size, with slender bones having 25-50% less Ct.Ar and 5-8% higher Ct.TMD compared to robust bones. Robustness statistically explained 10.2-28% of Ct.TMD and 26.6-64.6% of Ct.Ar within male and female skeletal elements. This covariance is systemic throughout the skeleton, with either the slender or robust phenotype consistently represented within all long bones for each individual. These findings suggest that each person attains a unique trait set by adulthood that is both predictable by robustness and partially independent of environmental influences. The variation in these functionally integrated traits allows for the maximization of tissue stiffness and minimization of mass so that regardless of which phenotype is present, a given bone is reasonably stiff and strong, and sufficiently adapted to perform routine, habitual loading activities. Covariation intrinsic to functional adaptation suggests that whole bone stiffness depends upon particular sets of traits acquired during growth, presumably through differing levels of cellular activity, resulting in differing tissue morphology and composition. The outcomes of this intraskeletal examination of robustness and its correlates may have significant value in our progression towards improved clinical assessments of bone strength and fragility.

Keywords: Bone; Cortical area; Functional morphology; Mineralization; Robustness.

Fig. 1.

Intraskeletal regression plots between robustness and Ct.TMD. a) plotted values unadjusted for body size; b) plotted values adjusted for body size. Note the 6 females with very low Ct.TMD values in comparison to the population for both the unadjusted and adjusted values. Corresponding r² values for each bone, both unadjusted and adjusted for body size, are provided in Table 2a.

Fig. 2.

Intraskeletal regression plots between robustness and Ct.Ar. a) plotted values unadjusted for body size; b) plotted values adjusted for body size. Note the drastically different linear relationship of the 2nd and 3rd metacarpals in comparison to the long bones. Corresponding r² values for each bone, both unadjusted and adjusted for body size, are provided in Table 2b.

Fig. 3.

Example of intraskeletal covariance of traits for four individuals within the study population. Femora and radii for two females and males demonstrating maximum slenderness and robustness are presented. For individuals within each sexual cohort, body mass and bone length are similar. Note the range of variation between individuals with similar body size, the intraskeletal consistency in robustness within the same individuals, and the gray value differences between femora and radii, indicating higher mineralization in the radii compared to the femora.

Fig. 4.

Schematic showing trait covariance of robustness, Ct.TMD, and Ct.Ar. a) expected relationship between traits for a given robustness; b) populational variance of trait sets demonstrating a narrow range that is predictable in relation to robustness. The solid line indicates the range of males within the study population, and the dashed line indicates the range of females. The overlap of the two ellipsoids represents the population average. Gray value differences in a) and b) represent the variation in mineralization, with lighter shades reflecting lower Ct.TMD and darker shades reflecting higher Ct.TMD.