Gracility of the modern Homo sapiens skeleton is the result of decreased biomechanical loading

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 2, 2015, Pages 372-377

  Ryan, Timothy M ^a   Shaw, Colin N ^b  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Biomechanics; Gracilization; Human evolution; Mobility; Trabecular bone

Indexed keywords

ADULT; ARTICLE; BIOMECHANICAL LOADING; BODY MASS; BODY REGIONS; BONE MASS; BONE STRUCTURE; EXERCISE; HIP; HUMAN; MICRO-COMPUTED TOMOGRAPHY; MUSCULOSKELETAL FUNCTION; NONHUMAN; PHYSICAL ACTIVITY; PRIORITY JOURNAL; SKELETON; SURFACE PROPERTY; TRABECULAR BONE; ANATOMY AND HISTOLOGY; ANIMAL; BIOMECHANICS; BODY WEIGHT; BONE; EVOLUTION; FOSSIL; HOMINID; MOTOR ACTIVITY; OSTEOPOROSIS; PHYSICAL ANTHROPOLOGY; PHYSIOLOGY; PRIMATE; RADIOGRAPHY; THREE DIMENSIONAL IMAGING; WEIGHT BEARING; YOUNG ADULT;

HOMO; HOMO SAPIENS; PRIMATES;

ADULT; ANIMALS; ANTHROPOLOGY, PHYSICAL; BIOLOGICAL EVOLUTION; BIOMECHANICAL PHENOMENA; BODY WEIGHT; BONE AND BONES; FOSSILS; HOMINIDAE; HUMANS; IMAGING, THREE-DIMENSIONAL; MOTOR ACTIVITY; OSTEOPOROSIS; PRIMATES; WEIGHT-BEARING; X-RAY MICROTOMOGRAPHY; YOUNG ADULT;

EID: 84920983143     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1418646112     Document Type: Article

References (77)

1. Ruff CB (2005) Mechanical determinants of bone form: Insights from skeletal remains. J Musculoskelet Neuronal Interact 5(3):202-212.
2. Ruff CB, Trinkaus E, Walker A, Larsen CS (1993) Postcranial robusticity in Homo. I: Temporal trends and mechanical interpretation. Am J Phys Anthropol 91(1): 21-53.
3. Nowlan NC, Jepsen KJ, Morgan EF (2011) Smaller, weaker, and less stiff bones evolve from changes in subsistence strategy. Osteoporos Int 22(6):1967-1980.
4. Pearson OM (2000) Activity, climate, and postcranial robusticity: Implications for modern human origins and scenarios of adaptive change. Curr Anthropol 41(4):569-607.
5. Stock JT (2006) Hunter-gatherer postcranial robusticity relative to patterns of mobility, climatic adaptation, and selection for tissue economy. Am J Phys Anthropol 131(2):194-204.
6. Holt BM (2003) Mobility in Upper Paleolithic and Mesolithic Europe: Evidence from the lower limb. Am J Phys Anthropol 122(3):200-215.
7. Holt BM, Formicola V (2008) Hunters of the Ice Age: The biology of Upper Paleolithic people. Am J Phys Anthropol 51(Suppl 47):70-99.
8. Ruff C, Holt B, Trinkaus E (2006) Who's afraid of the big bad Wolff: "Wolff's law" and bone functional adaptation. Am J Phys Anthropol 129(4):484-498.
9. Shackelford LL (2007) Regional variation in the postcranial robusticity of late Upper Paleolithic humans. Am J Phys Anthropol 133(1):655-668.
10. Cooper C, Campion G, Melton LJ, 3rd (1992) Hip fractures in the elderly: A world-wide projection. Osteoporos Int 2(6):285-289.
11. Nelson DA, Sauer NJ, Agarwal SC (2002) Evolutionary aspects of bone health. Clin Rev Bone Miner Metab 1(3):169-179.
12. Cotter MM, Loomis DA, Simpson SW, Latimer B, Hernandez CJ (2011) Human evolution and osteoporosis-related spinal fractures. PLoS ONE 6(10):e26658.
13. Latimer B (2005) The perils of being bipedal. Ann Biomed Eng 33(1):3-6.
14. Hernandez CJ, et al. (2009) Biomechanical allometry in hominoid thoracic vertebrae. J Hum Evol 56(5):462-470.
15. Karasik D (2008) Osteoporosis: An evolutionary perspective. Hum Genet 124(4): 349-356.
16. Griffin NL, et al. (2010) Comparative forefoot trabecular bone architecture in extant hominids. J Hum Evol 59(2):202-213.
17. Maga M, Kappelman J, Ryan TM, Ketcham RA (2006) Preliminary observations on the calcaneal trabecular microarchitecture of extant large-bodied hominoids. Am J Phys Anthropol 129(3):410-417.
18. Shaw CN, Ryan TM (2012) Does skeletal anatomy reflect adaptation to locomotor patterns Cortical and trabecular architecture in human and nonhuman anthropoids. Am J Phys Anthropol 147(2):187-200.
19. Cotter MM, Simpson SW, Latimer BM, Hernandez CJ (2009) Trabecular microarchitecture of hominoid thoracic vertebrae. Anat Rec (Hoboken) 292(8):1098-1106.
20. Johnell O, Kanis JA (2006) An estimate of the worldwide prevalence and disability associated with osteoporotic fractures. Osteoporos Int 17(12):1726-1733.
21. Cui WQ, et al. (2008) Age-and region-dependent changes in three-dimensional microstructural properties of proximal femoral trabeculae. Osteoporos Int 19(11): 1579-1587.
22. Hildebrand T, Laib A, Müller R, Dequeker J, Rüegsegger P (1999) Direct threedimensional morphometric analysis of human cancellous bone: Microstructural data from spine, femur, iliac crest, and calcaneus. J Bone Miner Res 14(7):1167-1174.
23. Ciarelli TE, Fyhrie DP, Schaffler MB, Goldstein SA (2000) Variations in threedimensional cancellous bone architecture of the proximal femur in female hip fractures and in controls. J Bone Miner Res 15(1):32-40.
24. Perilli E, et al. (2008) Dependence of mechanical compressive strength on local variations in microarchitecture in cancellous bone of proximal human femur. J Biomech 41(2):438-446.
25. Rumph PF, et al. (1994) Ground reaction force profiles from force platform gait analyses of clinically normal mesomorphic dogs at the trot. Am J Vet Res 55(6): 756-761.
26. Nilsson J, Thorstensson A (1989) Ground reaction forces at different speeds of human walking and running. Acta Physiol Scand 136(2):217-227.
27. Cavanagh PR, Lafortune MA (1980) Ground reaction forces in distance running. J Biomech 13(5):397-406.
28. Hodgskinson R, Currey JD (1990) Effects of structural variation on Young's modulus of non-human cancellous bone. Proc Inst Mech Eng H 204(1):43-52.
29. Hodgskinson R, Currey JD (1990) The effect of variation in structure on the Young's modulus of cancellous bone: A comparison of human and non-human material. Proc Inst Mech Eng H 204(2):115-121.
30. Mittra E, Rubin C, Qin Y-X (2005) Interrelationship of trabecular mechanical and microstructural properties in sheep trabecular bone. J Biomech 38(6):1229-1237.
31. Kabel J, van Rietbergen B, Odgaard A, Huiskes R (1999) Constitutive relationships of fabric, density, and elastic properties in cancellous bone architecture. Bone 25(4): 481-486.
32. Ulrich D, van Rietbergen B, Laib A, Rüegsegger P (1999) The ability of threedimensional structural indices to reflect mechanical aspects of trabecular bone. Bone 25(1):55-60.
33. Alexander RM (1998) Symmorphosis and safety factors. Principles of Animal Design: The Optimization and Symmorphosis Debate, eds Weibel E, Taylor C, Bolis L (Cambridge Univ Press, New York).
34. Hallgrímsson B, Willmore K, Hall BK (2002) Canalization, developmental stability, and morphological integration in primate limbs. Am J Phys Anthropol 45(Suppl 35): 131-158.
35. Lieberman DE, Crompton A (1998) Responses to stress: Constraints on symmorphosis. Principles of Animal Design: The Optimization and Symmorphosis Debate, eds Weibel E, Taylor C, Bolis L (Cambridge Univ Press, New York), pp 78-86.
36. WHO (1994) Assessment of Fracture Risk and Its Application to Screening for Post-Menopausal Osteoporosis: Report of a World Health Organization Study Group. WHO Technical Report Series No. 843, (WHO, Geneva).
37. Robling AG, Castillo AB, Turner CH (2006) Biomechanical and molecular regulation of bone remodeling. Annu Rev Biomed Eng 8:455-498.
38. Brandi ML (2009) Microarchitecture, the key to bone quality. Rheumatology (Oxford) 48(Suppl 4):iv3-iv8.
39. Seeman E, Delmas PD (2006) Bone quality-The material and structural basis of bone strength and fragility. N Engl J Med 354(21):2250-2261.
40. Stauber M, Müller R (2006) Age-related changes in trabecular bone microstructures: Global and local morphometry. Osteoporos Int 17(4):616-626.
41. Larsen CS (2015) Bioarchaeology: Interpreting Behavior from the Human Skeleton (Cambridge Univ Press, Cambridge, UK).
42. Cho H, Stout SD, Bishop TA (2006) Cortical bone remodeling rates in a sample of African American and European American descent groups from the American Midwest: Comparisons of age and sex in ribs. Am J Phys Anthropol 130(2):214-226.
43. Eaton SB, Nelson DA (1991) Calcium in evolutionary perspective. Am J Clin Nutr 54(1, Suppl):281S-287S.
44. Heaney RP (2003) Is the paradigm shifting? Bone 33(4):457-465.
45. Buikstra JE, Milner GR (1991) Isotopic and archaeological interpretations of diet in the Central Mississippi Valley. J Archaeol Sci 18(3):319-329.
46. Jefferies RW, Lynch BM (1983) Dimensions of Middle Archaic cultural adaptation at the Black Earth Site, Saline County, Illinois. Archaic Hunters and Gatherers in the American Midwest, eds Phillips JL, Brown JA (Academic, New York), pp 299-322.
47. Styles BW, Ahler SR, Fowler ML (1983) Modoc Rock Shelter revisited. Archaic Hunters and Gatherers in the American Midwest, eds Phillips JL, Brown JA (Academic, New York), pp 261-297.
48. Bridges PS (1989) Bone cortical area in the evaluation of nutrition and activity levels. Am J Hum Biol 1(6):785-792.
49. Ruff CB, Larsen CS, Hayes WC (1984) Structural changes in the femur with the transition to agriculture on the Georgia coast. Am J Phys Anthropol 64(2):125-136.
50. Ruff C (2003) Ontogenetic adaptation to bipedalism: Age changes in femoral to humeral length and strength proportions in humans, with a comparison to baboons. J Hum Evol 45(4):317-349.
51. MacLatchy LM (1996) Another look at the australopithecine hip. J Hum Evol 31(5): 455-476.
52. Ryan TM, Shaw CN (2013) Trabecular bone microstructure scales allometrically in the primate humerus and femur. Proc Biol Sci 280(1758):20130172.
53. McHenry HM, Coffing K (2000) Australopithecus to Homo: Transformations in body and mind. Annu Rev Anthropol 29:125-146.
54. Pontzer H (2007) Effective limb length and the scaling of locomotor cost in terrestrial animals. J Exp Biol 210(Pt 10):1752-1761.
55. Braun DR, Harris JWK, Maina DN (2009) Oldowan raw material procurement and use: Evidence from the Koobi Fora formation. Archaeometry 51(1):26-42.
56. Bramble DM, Lieberman DE (2004) Endurance running and the evolution of Homo. Nature 432(7015):345-352.
57. Raichlen DA, Foster AD, Gerdeman GL, Seillier A, Giuffrida A (2012) Wired to run: Exercise-induced endocannabinoid signaling in humans and cursorial mammals with implications for the 'runner's high'. J Exp Biol 215(Pt 8):1331-1336.
58. Lieberman DE (2013) The Story of the Human Body: Evolution, Health, and Disease (Pantheon, New York).
59. Jefferies RW, Avery GE (1982) The Carrier Mills Archaeological Project: Human Adaptation in the Saline Valley, Illinois (Southern Illinois Univ Press, Carbondale, IL).
60. Jefferies RW (2013) The Archaeology of Carrier Mills: 10,000 Years in the Saline Valley of Illinois (Southern Illinois Univ Press, Carbondale, IL).
61. Ahler SR, Bade MJ, King FB, Styles BW, Thorson P, eds (1992) Late Archaic Components at Modoc Rock Shelter, Randolph County, Illinois. Reports of Investigations (Illinois State Museum, Springfield, IL).
62. Milner GR, Humpf DA, Harpending HC (1989) Pattern matching of age-at-death distributions in paleodemographic analysis. Am J Phys Anthropol 80(1):49-58.
63. Lovejoy CO, Meindl RS, Mensforth RP, Barton TJ (1985) Multifactorial determination of skeletal age at death: A method and blind tests of its accuracy. Am J Phys Anthropol 68(1):1-14.
64. Ryan TM, Ketcham RA (2002) The three-dimensional structure of trabecular bone in the femoral head of strepsirrhine primates. J Hum Evol 43(1):1-26.
65. Ryan TM, Ketcham RA (2005) Angular orientation of trabecular bone in the femoral head and its relationship to hip joint loads in leaping primates. J Morphol 265(3): 249-263.
66. Ryan TM, Shaw CN (2012) Unique suites of trabecular bone features characterize locomotor behavior in human and non-human anthropoid primates. PLoS ONE 7(7): e41037.
67. Ryan TM, Walker A (2010) Trabecular bone structure in the humeral and femoral heads of anthropoid primates. Anat Rec (Hoboken) 293(4):719-729.
68. Ridler TW, Calvard S (1978) Picture thresholding using an iterative selection method. IEEE Trans Syst Man Cybern SMC-8(8):630-632.
69. Trussell HJ (1979) Comments on "Picture thresholding using an iterative selection method. " IEEE Trans Syst Man Cybern SMC-9(5):311.
70. Laib A, et al. (2000) 3D micro-computed tomography of trabecular and cortical bone architecture with application to a rat model of immobilisation osteoporosis. Med Biol Eng Comput 38(3):326-332.
71. Payseur BA, Covert HH, Vinyard CJ, Dagosto M (1999) New body mass estimates for Omomys carteri, a middle Eocene primate from North America. Am J Phys Anthropol 109(1):41-52.
72. Ruff CB (2003) Long bone articular and diaphyseal structure in Old World monkeys and apes. II: Estimation of body mass. Am J Phys Anthropol 120(1):16-37.
73. Ruff CB, Trinkaus E, Holliday TW (1997) Body mass and encephalization in Pleistocene Homo. Nature 387(6629):173-176.
74. Ruff C (1988) Hindlimb articular surface allometry in Hominoidea and Macaca, with comparisons to diaphyseal scaling. J Hum Evol 17(7):687-714.
75. Jungers WL (1991) Scaling of postcranial joint size in hominoid primates. Hum Evol 6(5-6):391-399.
76. Ruff CB (2002) Long bone articular and diaphyseal structure in old world monkeys and apes. I: Locomotor effects. Am J Phys Anthropol 119(4):305-342.
77. Doube M, Klosowski MM, Wiktorowicz-Conroy AM, Hutchinson JR, Shefelbine SJ (2011) Trabecular bone scales allometrically in mammals and birds. Proc Biol Sci 278(1721):3067-3073.