Systemic patterns of trabecular bone across the human and chimpanzee skeleton

Abstract

Aspects of trabecular bone architecture are thought to reflect regional loading of the skeleton, and thus differ between primate taxa with different locomotor and postural modes. However, there are several systemic factors that affect bone structure that could contribute to, or be the primary factor determining, interspecific differences in bone structure. These systemic factors include differences in genetic regulation, sensitivity to loading, hormone levels, diet, and activity levels. Improved understanding of inter-/intraspecific variability, and variability across the skeleton of an individual, is required to interpret properly potential functional signals present within trabecular structure. Using a whole-region method of analysis, we investigated trabecular structure throughout the skeleton of humans and chimpanzees. Trabecular bone volume fraction (BV/TV), degree of anisotropy (DA) and trabecular thickness (Tb.Th) were quantified from high resolution micro-computed tomographic scans of the humeral and femoral head, third metacarpal and third metatarsal head, distal tibia, talus and first thoracic vertebra. We found that BV/TV is, in most anatomical sites, significantly higher in chimpanzees than in humans, suggesting a systemic difference in trabecular structure unrelated to local loading regime. Differences in BV/TV between the forelimb and hindlimb did not clearly reflect differences in locomotor loading in the study taxa. There were no clear systemic differences between the taxa in DA and, as such, this parameter might reflect function and relate to differences in joint loading. This systemic approach reveals both the pattern of variability across the skeleton and between taxa, and helps identify those features of trabecular structure that may relate to joint function.

Palaeobiological inferences based on long bone epiphyseal and diaphyseal structure - the forelimb of xenarthrans (Mammalia)

“…PREPRINT discriminating parameter in extant xenarthrans (Amson et al 2017a). It was also singled out as reflecting joint loading in primates better than other parameters (Tsegai et al 2018), and, more generally, DA was found as functionally informative in several analyses about that clade (e.g. Ryan & Ketcham 2002;Griffin et al 2010;Barak et al 2013;Su et al 2013;Georgiou et al 2018;Ryan et al 2018;Tsegai et al 2018).…”

“…Comparative studies focusing on either trabeculae or cortical structure intend to leverage this great plasticity to associate structural phenotypes to PREPRINT lifestyles or functional uses of a limb. This has been achieved in some analyses (as recently exemplified by Georgiou et al 2018;Ryan et al 2018;Tsegai et al 2018) but not all of them (see review of Kivell 2016), suggesting that some confounding factors are likely to be at play, and more generally that the approach is limited. For trabecular bone in particular, important intraspecific variation has been documented (e.g., in Pongo; Tsegai et al 2013;Georgiou et al 2018).…”

Trabecular variation in the first metacarpal and manipulation in hominids

“…While these results appear consistent with what is known of hominid behavior and anatomy, the function of trabecular bone is not only biomechanical but also physiological, as it is important for mineral homeostasis (Clarke, ). Furthermore, trabecular structure may be affected by systemic factors, including the gut biomes of an animal (Tsegai et al, ) and is determined genetically to some extent (Almécija, Wallace, Judex, Alba, & Moyà‐Solà, ; Havill et al, ; Judex, Zhang, Donahue, & Ozcivici, ; Lovejoy et al, ). Some researchers have also argued that functional adaptation of bone is largely limited to mechanical strains experienced during growth (Bertram & Swartz, ; Lovejoy et al, ; Wallace et al, ).…”

“…This standardization of BV/TV values was performed for several reasons. BV/TV can vary systemically across species (Tsegai, Skinner, Pahr, Hublin, & Kivell, ) and thus may diminish the potential functional signal under investigation here. Further, while BV/TV yields functional information relating to the response of trabecular bone to both magnitude and direction of load, it conflates these signals.…”

Bone modeling or bone remodeling: That is the question

“…However, hand‐in‐hand with the increase in publications relating to bone functional adaptation, which is a bone modeling mechanism, the important distinction between bone modeling and bone remodeling was repeatedly dismissed as a mere terminology issue. This led some authors to address all adjustments of bone morphology related to loading, especially in the case of trabecular bone, as bone remodeling (Dunmore, Kivell, Bardo, & Skinner, ; Hoechel, Schulz, & Müller‐Gerbl, ; Kivell, ; Kivell, Davenport, Hublin, Thackeray, & Skinner, ; Saers, Ryan, & Stock, ; Tsegai, Skinner, Pahr, Hublin, & Kivell, , ; Zeininger, Richmond, & Hartman, ). The aim of this commentary is to elucidate the key differences between bone modeling and bone remodeling and to stress the importance of using the correct term, that is, bone modeling, when referring to trabecular bone structural adaptation in response to loading.…”