Recent origin of low trabecular bone density in modern humans

Abstract

Humans are unique, compared with our closest living relatives (chimpanzees) and early fossil hominins, in having an enlarged body size and lower limb joint surfaces in combination with a relatively gracile skeleton (i.e., lower bone mass for our body size). Some analyses have observed that in at least a few anatomical regions modern humans today appear to have relatively low trabecular density, but little is known about how that density varies throughout the human skeleton and across species or how and when the present trabecular patterns emerged over the course of human evolution. Here, we test the hypotheses that (i) recent modern humans have low trabecular density throughout the upper and lower limbs compared with other primate taxa and (ii) the reduction in trabecular density first occurred in early Homo erectus, consistent with the shift toward a modern human locomotor anatomy, or more recently in concert with diaphyseal gracilization in Holocene humans. We used peripheral quantitative CT and microtomography to measure trabecular bone of limb epiphyses (long bone articular ends) in modern humans and chimpanzees and in fossil hominins attributed to Australopithecus africanus, Paranthropus robustus/ early Homo from Swartkrans, Homo neanderthalensis, and early Homo sapiens. Results show that only recent modern humans have low trabecular density throughout the limb joints. Extinct hominins, including pre-Holocene Homo sapiens, retain the high levels seen in nonhuman primates. Thus, the low trabecular density of the recent modern human skeleton evolved late in our evolutionary history, potentially resulting from increased sedentism and reliance on technological and cultural innovations. trabecular bone | human evolution | gracilization | Homo sapiens | sedentism O bligate bipedalism-a defining feature of humans that distinguishes us from our closest living relatives, the African apes-has transformed the human skeleton. Among these unique features are long lower limbs with large joint surfaces. These large joint surfaces help distribute loads over a larger surface area and thus are better at resisting the high forces incurred during locomotion on two limbs instead of four (1-5). Early African Homo erectus at 1.8-1.5 Ma had enlarged lower limb joint surfaces (1, 3) and a larger stature (6) and body mass (7, 8) than many earlier hominins, and this pattern often is considered to reflect the emergence of a more modern human-like body plan (1, 3, 5, 6, 9; but also see ref. 7).Recent modern human (Holocene Homo sapiens) skeletons also appear to be gracile as compared with earlier hominins (10-14). Here, "gracilization" refers to the reduction in strength and bone mass relative to body mass inferred from osseous tissue and overall bone size and has been studied mainly using diaphyseal cortical bone cross-sections (10-16). Although the relationship between mechanical loading during life and bone strength is likely to be complex (17), there is much evidence that increased mechanical loading leads to increases in relative ...

Gradual decline in mobility with the adoption of food production in Europe

“…This finding is consistent with recently reported results based on limb bone trabecular structure (10,26), in which significant differences in bone density were found between Holocene foragers and farmers but not between farmers and a modern industrial sample. Our results for a much more comprehensive Holocene sample indicate that moderate variation in activity level, i.e., between the Iron/Roman period and 20th century, does not affect relative bone strength significantly.…”

“…Earlier studies identified declines in skeletal robusticity (strength relative to body size) in Homo throughout the Pleistocene (24,25), but recent analyses suggest that the major decrease in robusticity occurred later, at the end of the Pleistocene, between early anatomically modern H. sapiens and Holocene populations (26,27). This suggestion in turn strongly implicates increased sedentism as a major driver in producing the more gracile modern human skeleton (10,25,26) and focuses attention on the Holocene as the critical period during which this transformation took place. However, the timing and pace of this change relative to major subsistence and lifestyle transitions cannot be determined from these studies, given their sparse sampling of terminal Pleistocene and Holocene populations.…”

“…Although skeletal morphology is determined by a complex interplay between various genetic and environmental factors (18,19), there is abundant evidence that mechanical loading during life has a strong influence on skeletal structure (20)(21)(22)(23). Earlier studies identified declines in skeletal robusticity (strength relative to body size) in Homo throughout the Pleistocene (24,25), but recent analyses suggest that the major decrease in robusticity occurred later, at the end of the Pleistocene, between early anatomically modern H. sapiens and Holocene populations (26,27). This suggestion in turn strongly implicates increased sedentism as a major driver in producing the more gracile modern human skeleton (10,25,26) and focuses attention on the Holocene as the critical period during which this transformation took place.…”

Inner structural organization of the distal humerus in Paranthropus and Homo

“…It seems nonetheless interesting to note that, besides the ambiguous evidence from TM 1517g because of its low bone-matrix contrast, the two specimens from Swartkrans share the presence of more numerous and thick struts, locally resulting into a more closed network of plate-like structures from the accumulation of more material in the cell wall (Dalstra and Huiskes, 1995;Gibson, 1985;Stauber and Müller, 2006). At any comparable site, struts are invariably thicker in the fossil specimens than in the extant human humeri available to us, which is consistent with the process of skeletal gracilisation and trabecular bone density reduction occurred in recent humans (Chirchir et al, 2015(Chirchir et al, , 2017Ryan and Shaw, 2015). It is also noticeable that the medullary cavity of the OH 80-10 distal humerus fragment from the P. boisei partial skeleton of Olduvai Gorge, Tanzania, is filled by trabecular bone (Domínguez-Rodrigo et al, 2013).…”

Revisiting the peroneal trochlea of the StW 352 calcaneus

“…15 Chimpanzees also exhibit a generally more robust postcranial skeleton than modern humans, who appear to exhibit systemically lower bone mass, particularly with age. 25 Thus, by including the chimpanzee calcaneus, any gross differences in cortical and trabecular bone distribution, particularly those related to potential internal partitioning of the peroneal trochlea from the calcaneal body, generated by differences in the development of this anatomy should be accounted for in the current evaluation.…”