Trabecular Bone Structure Correlates with Hand Posture and Use in Hominoids

Tsegai, Zewdi J.; Kivell, Tracy L.; Groß, Thomas; Nguyễn, Huynh Nhu; Pahr, Dieter H.; Smaers, Jeroen B.; Skinner, Matthew M.

doi:10.1371/journal.pone.0078781

Cited by 101 publications

(214 citation statements)

References 79 publications

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“…Contrary to Almécija et al's (1) claim, our comparative sample does include tool-using Taï chimpanzees [Pan troglodytes verus; original table S1 (2)], and their metacarpals do not show any similarity to the trabecular distribution found in humans, Neandertals, and A. africanus. We agree that examining other nonhuman primates is likely to further elucidate links between hand use and trabecular structure, but the limited trabecular bone in the epiphyses of smaller-bodied hominoids and monkeys (14) suggests caution in applying either our method or traditional volume-of-interest approaches to broad comparative samples. For example, hylobatids have very few trabecular struts in their hand bone epiphyses.…”

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confidence: 65%

Response to Comment on “Human-like hand use in Australopithecus africanus ”

Skinner

Stephens

Tsegai

et al. 2015

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Almécija and colleagues claim that we apply a simplified understanding of bone functional adaptation and that our results of human-like hand use in Australopithecus africanus are not novel. We argue that our results speak to actual behavior, rather than potential behaviors, and our functional interpretation is well supported by our methodological approach, comparative sample, and previous experimental data.A lmécija et al.(1) challenge our conclusions on three points: (i) we do not give sufficient credence to published studies on the external morphology of australopith hand bones that are consistent with precision grip capabilities; (ii) we overstate the evidence for a form-function signal in trabecular bone; and (iii) our comparative sample and analyses do not support differences in trabecular patterning between humans and extant apes. Their critique suffers from a lack of recognition that (i) our study provides evidence for hand postures actually adopted by australopiths, rather than those they were potentially capable of; (ii) we base our conclusions on the three-dimensional distribution of trabecular bone throughout the epiphysis rather than on particular measures of subregions of trabecular structure; and (iii) our comparative sample, which includes stone toolusing Taï chimpanzees, indicates that humans have a distinctive trabecular pattern that is shared with Neandertals and Australopithecus africanus (2).We do not claim that our results "refute the previously existing hypothesis that human-like manipulation preceded systematized stone tool manufacture" (1); to the contrary, we state that our results are consistent with the use of "forceful hand grips for any number of manipulative behaviors" (2). Almécija et al.(1) refer to previous studies (mainly their own) based on the relative lengths and external morphology of hand bones that "have provided compelling evidence for padto-pad precision grasping before the widespread occurrence of flaked stone tools" (1) and that australopiths and earlier hominins "were likely capable of human-like manipulation" (1). We agree; however, Almécija et al.(1) fail to acknowledge that our results are novel because they reflect (i) actual behavior, rather than the capability for particular behaviors and (ii) forceful pad-to-pad precision grasping, which is what separates human dexterity from that of other primates (3). The asymmetric distribution of trabecular bone within the base of the thumb and metacarpal heads in humans, Neandertals, and A. africanus (and the absence of this pattern in apes) provides evidence for habitual, forceful opposition of the thumb to the fingers. We agree that inferences for humanlike hand use among australopiths referred to by Almécija et al. are neither "unprecedented nor unexpected" (1). However, the inferences we can now make, based on the trabecular bone distribution and the well-accepted concept that trabeculae remodel in response to habitual load during an individual's lifetime (4, 5), are much stronger than they and others have been able to...

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Response to Comment on “Human-like hand use in Australopithecus africanus ”

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“…In both these cases, modern human joints are consistently low in TBF (32,36). Therefore, within specific articulations, it is not clear to what extent parameters such as trabecular anisotropy, thickness, and spacing vary systematically among closely related taxa (32,36,44,45). Incorporating additional structural properties across the same or different anatomical regions in future studies could help determine whether architectural changes (if any) paralleled the changes in trabecular density during hominin evolution and whether they were complementary or compensatory during the transition to recent modern humans.…”

Section: Discussionmentioning

confidence: 93%

“…Anisotropy in particular appears to be related to principal loading direction (42). Work to date suggests that in some anatomical regions, such as metatarsal heads, humans are characterized by higher degrees of anisotropy (36), but in others, such as metacarpal heads, humans and apes have comparable degrees of anisotropy (32). In both these cases, modern human joints are consistently low in TBF (32,36).…”

Section: Discussionmentioning

confidence: 99%

“…Work to date suggests that in some anatomical regions, such as metatarsal heads, humans are characterized by higher degrees of anisotropy (36), but in others, such as metacarpal heads, humans and apes have comparable degrees of anisotropy (32). In both these cases, modern human joints are consistently low in TBF (32,36). Therefore, within specific articulations, it is not clear to what extent parameters such as trabecular anisotropy, thickness, and spacing vary systematically among closely related taxa (32,36,44,45).…”

Section: Discussionmentioning

confidence: 99%

“…A few studies examining individual limb elements have reported low trabecular density, as measured by volumetric density (the trabecular bone fraction, TBF, or bone volume relative to total volume), in recent modern human epiphyses. The recent modern human arm (humerus) and hand (metacarpals) have low TBF (31,32) and mineral density (33) compared with chimpanzees and orangutans. This finding might be expected, because humans rarely use their upper limbs for locomotion and therefore do not habitually expose their upper limb bones to the high loads of body-weight support.…”

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Recent origin of low trabecular bone density in modern humans

Chirchir

Kivell

Ruff

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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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 ...

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