Extensive evidence exists from experimental and observational research showing that trabecular bone is labile and thus responds to varying levels of activity i.e., mechanical loading (Rubin and Lanyon, 1982; Hou et al., 1990; Sakata et al., 1999; Huiskes, 2000; Rubin et al., 2001; MacLatchy and Müller, 2002; Mori et al., 2003; Pontzer et al., 2006; Griffin et al., 2010; Barak et al., 2011; Ryan and Shaw, 2015; Saers et al., 2016; Scherf et al., 2016; Ryan et al., 2018; Dunmore et al., 2019; Ragni, 2020; but see Fajardo et al., 2007; Havill et al., 2010; Judex et al., 2004; Ryan and Walker, 2010; Ryan and Shaw, 2012). Specifically, trabecular bone responds to maximum stress, direction of force and frequency of strain (Barak et al., 2011; Hou et al., 1990; Pontzer et al., 2006; Robling et al., 2006; Rubin et al., 2001; Rubin and Lanyon, 1982; Sakata et al., 1999). In contrast with cortical bone, trabecular bone models in a more dynamic manner to adjust its size and shape in response to loading, partially due to differences in molecular signaling pathways (Park et al., 2021). Trabecular bone has a low elastic modulus, an average of 10.4 GPa compared to 18.6 GPa in cortical bone (Rho et al., 1993). In fact, a correlation exists between elastic modulus and trabecular bone volume fraction and density such that the denser the trabecular bone, the stronger and stiffer it becomes (Keaveny and Hayes, 1993). Elastic modulus of trabecular bone thus makes it critical in absorbing energy conveyed to joints and reducing joint reaction forces (Radin et al., 1982).

The premise of the relationship between mechanical loading and bone alteration relies on the biomechanical understanding that bone adapts to loads, in what is referred to as ‘bone functional adaptation’ (Ruff et al., 2006). Bone functional adaptation posits that mechanical loading on bones from, for instance, locomotion and other in vivo habitual activities, results in bone modeling which alters bone morphology (Ruff et al., 2006; Barak, 2020). These changes occur due to the complex remodeling and modeling of bone stimulated by an increase or decrease in strain (Ruff et al., 2006). Comparative studies of bone volume fraction (the ratio of bone volume to total volume in a region of interest, BV/TV) in recent human populations from the Holocene (last 10,000 years) engaging in different subsistence strategies found that although there were differences in skeletal elements studied and among groups, overall, populations that were predominantly foraging had greater BV/TV than farming and industrial populations (Ryan and Shaw, 2015; Scherf et al., 2016; Saers et al., 2016; Chirchir et al., 2017, Doershuk et al., 2019; Stephens et al., 2018). Based on these findings, the authors concluded that active populations (i.e., hunter-gatherers and foragers) who are highly mobile have greater BV/TV than more sedentary populations, supporting the observation that trabecular bone adapts to increased mechanical loading.

Ryan and Shaw (2015) found that the femoral heads of agricultural groups from North America had lower trabecular BV/TV and thickness compared to their foraging counterparts, thus concluding that reduced activity levels due to reduced mobility contributed to a decline in bone volume. Another study by Scherf et al. (2013) found that humeral head trabecular BV/TV in Neolithic farmers was greater compared to recent modern humans, which the authors attributed to the more strenuous activities of the upper limbs in Neolithic populations compared to the recent modern human populations. Saers et al. (2016) reported higher BV/TV in the lower limbs of populations that had greater mobility (i.e., traveled longer distances) in North American and North African Nubian populations. Chirchir et al. (2017) also investigated BV/TV in upper and lower limb elements of modern human populations who were foragers, farmers, urban industrial dwellers, and those who were transitioning from foraging to farming (transitional). They concluded that the active groups (foragers and the transitional) had greater BV/TV compared with the sedentary farming and industrial populations. Likewise, Doershuk et al. (2019) investigated BV/TV among agricultural and hunter-gather groups and found that the active hunter-gatherers had greater BV/TV than the agricultural groups in both the femoral and humeral heads. Lastly, Stephens et al.’s (2018) work on trabecular bone in the hand including third metacarpal heads of foragers and farming groups showed that although other trabecular bone properties were similar, BV/TV was greater among foragers. Thus, these studies suggest a relationship between increased activity linked to subsistence activity and higher BV/TV.

Differences observed in the lower limb have been linked to greater mobility among hunter-gatherer/forager populations. They travel long distances to acquire food resources and use weapons to pursue and kill game (Holt, 2003; Marchi et al., 2011). For instance, Holt (2003) examined three populations from different periods in the Upper Paleolithic and found that cross-sectional bone strength decreased steadily through time as a population's mobility decreased, leading the authors to conclude that changes in mobility led to changes in diaphyseal robusticity and bone shape. By contrast, although farmers and industrialized modern populations may work longer hours than hunter-gatherers, they are relatively sedentary and travel to and from a ‘place of work’ such as a farm or a factory (Hunt and Albanese, 2005). Nonetheless, studies showing greater robusticity among hunter-gatherer/forager groups compared to famers are not confined to the lower limb. They are also reflected in upper limb elements involved in resource acquisition and other forms of hand manipulation (Stock and Pfeiffer, 2001; Chirchir et al., 2017; Stephens et al., 2018; Doershuk et al., 2019).

Although the hand is used in a ‘multifunctional’ manner such as in hoeing and food pounding among agricultural groups, and when using tools such as bows and arrows, and fishing tools, for food acquisition and processing among hunter-gatherers, previous work found a significant difference between farmers and hunter-gatherers/foragers which the authors attributed to the heterogeneity in elbow and wrist use during these activities (Chirchir et al., 2017). Additionally, there is evidence that hunter-gatherers inhabiting coastal areas who exploit marine resources rely on swimming and watercraft navigation (Stock and Pfeiffer, 2001; Stock, 2006). These activities require strong upper limbs, and therefore marine hunter-gatherers have been shown to exhibit robust upper limbs (Stock and Pfeiffer, 2001). In the current study, one of our aims is to build upon this existing work by comparing hand bones of hunter-gatherers and farmers to evaluate if indeed there are differences among the two activity types as some have reported previously.

In addition to differences in BV/TV attributed to subsistence strategy, other studies have found that recent modern humans from the Holocene are markedly more gracile compared to Pleistocene humans, including those from the Late Pleistocene. For instance, Chirchir et al. (2015) and Chirchir (2019) found that anatomically modern humans from as late as 11,000 ka were significantly more robust, showing higher BV/TV in both upper and lower limb bones when compared with recent modern humans from the Holocene. Others have also shown that modern humans have notably more gracile limb bones than their closest living nonhuman primate relatives, the chimpanzees (Maga et al., 2006; Griffin et al., 2010; Tsegai et al., 2018; Georgiou et al., 2019). Modern humans have also been shown to exhibit gracile cortical bone morphology, as determined from midshaft cross-sectional geometric properties, that has increased over the last 100 kyr, especially with increased sedentism in the Holocene (Churchill et al., 1996; Ruff, 2005; Ruff et al., 2006). Specifically, Ruff (2005) showed that relative femoral strength has decreased since prehistoric times and especially over the past few thousand years (Ruff et al., 2015), although there is some variability, particularly in the Upper Paleolithic (Holt, 2003; Shackelford, 2007, Trinkaus and Ruff, 2012).

Therefore, compared to modern humans, it is reasonable to expect comparatively more robust skeletons (i.e., high BV/TV) in Late Pleistocene modern humans in light of the evidence suggesting that human skeletons became more gracile only during the Holocene. However, previous studies documenting the gracile morphology of recent modern humans were based on a small sample of Late Pleistocene humans. In this study, we add to the existing data by including one individual from Ohalo II in Israel (n = 1), individuals from Dolní Věstonice in the Czech Republic (n = 6), and recent modern humans—hunter/gatherers (n = 6) and farmers (n = 39)—to better understand when gracile morphology in recent modern humans emerged and whether there are differences in BV/TV between subsistence strategies.

A growing body of research over the last decade has focused on understanding BV/TV patterns in different types of subsistence activities (Stewart et al., 1986; Ryan and Shaw, 2015; Saers et al., 2016; Scherf et al., 2016; Chirchir et al., 2017; Doershuk et al., 2019; DeMars et al., 2021). Many of these studies sampled only a few anatomical sites, to compare across populations (Ryan and Shaw, 2015; Scherf et al., 2016; Stewart et al., 1986; Doershuk et al., 2019; DeMars et al., 2021; but see Saers et al., 2016; Chirchir et al., 2017). Different limb elements throughout the skeleton are loaded in diverse ways and research has shown some variation in BV/TV in different anatomical sites that is likely dependent on loading conditions (Amling et al., 1996; Hildebrand et al., 1999; Saers et al., 2016; Stephens et al., 2018; Tsegai et al., 2018; DeMars et al., 2021). Thus, it is important to sample from as diverse skeletal elements as possible to better understand the effect of activity level on trabecular bone. It is necessary to expand existing data sets to improve our understanding of BV/TV regionally and in terms of subsistence strategy by incorporating more geographic locales. Many studies have focused on North America and Europe, and occasionally North Africa. Therefore, in this study, we undertook an analysis of BV/TV in three skeletal elements (femoral head, humeral head, and head of the third metacarpal) used in locomotion as well as food acquisition and processing. We evaluated BV/TV in a sample of Late Pleistocene humans and a sample of recent Holocene human groups from North Africa and South America. We then compared these groups to determine whether there are differences in BV/TV between the two time periods.