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Research Article

Recent origin of low trabecular bone density in modern humans

Habiba Chirchir, Tracy L. Kivell, Christopher B. Ruff, Jean-Jacques Hublin, Kristian J. Carlson, Bernhard Zipfel, and Brian G. Richmond
  1. aCenter for the Advanced Study of Hominid Paleobiology, Department of Anthropology, The George Washington University, Washington, DC 20052;
  2. bHuman Origins Program, Department of Anthropology, National Museum of Natural History, Smithsonian Institution, Washington, DC 20560;
  3. cAnimal Postcranial Evolution Laboratory, School of Anthropology and Conservation, University of Kent, Canterbury, Kent, CT2 7NR, United Kingdom;
  4. dDepartment of Human Evolution, Max Planck Institute for Evolutionary Anthropology, D-04103 Leipzig, Germany;
  5. eCenter for Functional Anatomy and Evolution, Johns Hopkins University School of Medicine, Baltimore, MD 21205;
  6. fEvolutionary Studies Institute, The University of the Witwatersrand, Braamfontein 2000 Johannesburg, South Africa;
  7. gDepartment of Anthropology, Indiana University, Bloomington, IN 47405; and
  8. hDivision of Anthropology, American Museum of Natural History, New York, NY 10024

See allHide authors and affiliations

PNAS first published December 22, 2014; https://doi.org/10.1073/pnas.1411696112
Habiba Chirchir
aCenter for the Advanced Study of Hominid Paleobiology, Department of Anthropology, The George Washington University, Washington, DC 20052;
bHuman Origins Program, Department of Anthropology, National Museum of Natural History, Smithsonian Institution, Washington, DC 20560;
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  • For correspondence: habibachirchir@gmail.com brichmond@amnh.org
Tracy L. Kivell
cAnimal Postcranial Evolution Laboratory, School of Anthropology and Conservation, University of Kent, Canterbury, Kent, CT2 7NR, United Kingdom;
dDepartment of Human Evolution, Max Planck Institute for Evolutionary Anthropology, D-04103 Leipzig, Germany;
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Christopher B. Ruff
eCenter for Functional Anatomy and Evolution, Johns Hopkins University School of Medicine, Baltimore, MD 21205;
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Jean-Jacques Hublin
dDepartment of Human Evolution, Max Planck Institute for Evolutionary Anthropology, D-04103 Leipzig, Germany;
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Kristian J. Carlson
fEvolutionary Studies Institute, The University of the Witwatersrand, Braamfontein 2000 Johannesburg, South Africa;
gDepartment of Anthropology, Indiana University, Bloomington, IN 47405; and
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Bernhard Zipfel
fEvolutionary Studies Institute, The University of the Witwatersrand, Braamfontein 2000 Johannesburg, South Africa;
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Brian G. Richmond
aCenter for the Advanced Study of Hominid Paleobiology, Department of Anthropology, The George Washington University, Washington, DC 20052;
bHuman Origins Program, Department of Anthropology, National Museum of Natural History, Smithsonian Institution, Washington, DC 20560;
hDivision of Anthropology, American Museum of Natural History, New York, NY 10024
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  • For correspondence: habibachirchir@gmail.com brichmond@amnh.org
  1. Edited by Erik Trinkaus, Washington University, St. Louis, MO, and approved November 26, 2014 (received for review June 23, 2014)

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Significance

The human skeleton is unique in having low trabecular density representing a lightly built human body form. However, it remains unknown when during human evolution this unique characteristic first appeared. To our knowledge, this study is the first to examine trabecular bone density throughout the skeleton of fossil hominins spanning several million years. The results show that trabecular density remained high throughout human evolution until it decreased significantly in recent modern humans, suggesting a possible link between changes in our skeleton and increased sedentism.

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

Footnotes

  • ↵1To whom correspondence may be addressed. Email: habibachirchir{at}gmail.com or brichmond{at}amnh.org.
  • Author contributions: H.C. and B.G.R. designed research; H.C. performed research; T.L.K., C.B.R., J.-J.H., K.J.C., and B.Z. contributed new reagents/analytic tools; H.C. analyzed data; H.C. wrote the paper; and T.L.K., C.B.R., and B.G.R. contributed to writing the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1411696112/-/DCSupplemental.

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Recent origin of low trabecular bone density
Habiba Chirchir, Tracy L. Kivell, Christopher B. Ruff, Jean-Jacques Hublin, Kristian J. Carlson, Bernhard Zipfel, Brian G. Richmond
Proceedings of the National Academy of Sciences Dec 2014, 201411696; DOI: 10.1073/pnas.1411696112

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Recent origin of low trabecular bone density
Habiba Chirchir, Tracy L. Kivell, Christopher B. Ruff, Jean-Jacques Hublin, Kristian J. Carlson, Bernhard Zipfel, Brian G. Richmond
Proceedings of the National Academy of Sciences Dec 2014, 201411696; DOI: 10.1073/pnas.1411696112
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