Bone Health from an Evolutionary Perspective: Development in Early Human Populations

  • Dorothy A. NelsonEmail author
  • Sabrina C. Agarwal
  • Linda L. Darga
Part of the Nutrition and Health book series (NH)


Skeletal characteristics, bone health, and the risk of osteoporosis differ within and between modern day populations, and almost certainly reflect our evolutionary past. In this chapter, we review the major evolutionary events among the hominins, the human sub-family of primates, and provide an overview of evolutionary mechanisms resulting in the genetic changes that helped our ancestors to adapt to diverse environments. The skeleton can also be affected by a number of environmental and cultural factors, including diet, physical activity, work patterns, health and disease. For the purposes of examining evolutionary aspects of bone health, it is fortunate that bones can be preserved in the fossil record, and certain artifacts of cultural adaptation may also be present in hominin fossil sites. Anthropological techniques have been developed that allow us to create reasonable models of life in past human populations, thereby providing some insight into modern-day bone health. The major biocultural shifts during hominin evolution include the following: expansion from the tropics to a wide range of environments; transition from hunting and gathering to food production; change from physically active lifestyles to relative sedentism; and increase in life expectancy, with changes in reproductive behaviors. These four areas form the focal points for an examination of human bone health from an evolutionary perspective.


Hominin evolution Bone health Osteoporosis Dietary calcium Vitamin D 


  1. 1.
    Shubin NH, Daeschler EB, Jenkins Jr FA. The pectoral fin of Tiktaalik roseae and the origin of the tetrapod limb. Nature. 2006;440:764–71.PubMedCrossRefGoogle Scholar
  2. 2.
    Nelson DA. An anthropological perspective on optimizing calcium consumption for the prevention of osteoporosis. Osteoporos Int. 1996;6:325–8.PubMedCrossRefGoogle Scholar
  3. 3.
    Darwin CR. On the origin of species by on the origin of species by means of natural selection, or the preservation of races in the struggle for life. 1st ed. London: John Murray; 1859; 6th ed. London: John Murray; 1872.Google Scholar
  4. 4.
    Woese CR, Magrum LJ, Fox GE. Archaebacteria. J Mol Biol. 1978;11:245–52.Google Scholar
  5. 5.
    Puffenberger EG. Genetic heritage of the Old Order Mennonites of southeastern Pennsylvania. Am J Med Genet. 2003;121:18–31.CrossRefGoogle Scholar
  6. 6.
    Jaenisch R, Bird A. Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nature Genet. 2003;33(Suppl):245–54.PubMedCrossRefGoogle Scholar
  7. 7.
    Niculescu MD, Zeisel SH. Diet, methyl donors and DNA methylation: interactions between dietary folate, methionine and choline. J Nutr. 2002;132:2333S–5.PubMedGoogle Scholar
  8. 8.
    Roth TL, Lubin FD, Funk AJ, Sweatt JD. Lasting epigenetic influence of early-life adversity on the BDNF gene. Biol Psychiatry. 2009;65:760–9.PubMedCentralPubMedCrossRefGoogle Scholar
  9. 9.
    Waters E. DNA is not destiny. Discovery. 2006;27:33–37, 75.Google Scholar
  10. 10.
    Kau AL, Ahern PP, Griffin NW, Goodman AL, Gordon JI. Human nutrition, the gut microbiome and the immune system. Nature. 2011;474:327–36.PubMedCentralPubMedCrossRefGoogle Scholar
  11. 11.
    Semaw S. The world’s oldest stone artefacts from Gona, Ethiopia: their implications for understanding stone technology and patterns of human evolution between 2.6–1.5 million years ago. J Archaeol Sci. 2000;27:1197–214.CrossRefGoogle Scholar
  12. 12.
    Stanford C, Allen JS, Anton SC. Exploring biological anthropology. 3rd ed. Boston, MA: Pearson; 2013.Google Scholar
  13. 13.
    Brunet M, Guy F, Pilbeam D, Mackaye HT, Likius A, Djimdoumalbaye A, et al. A new hominid from the Upper Miocene of Chad, Central Africa. Nature. 2002;418:145–51.PubMedCrossRefGoogle Scholar
  14. 14.
    Pickford M, Senut B. “Millenium Ancestor”, a 6-million-year-old-bipedal hominid from Kenya: recent discoveries push back human origins by 1.5 million years. S Afr J Sci. 2001;97:2–22.Google Scholar
  15. 15.
    Pickord M, Senut B, Treil J. Bipedalism in Orrorin tugenensis revealed by its femora. C R Palevol. 2002;1:191–203.CrossRefGoogle Scholar
  16. 16.
    Sankararaman S, Patterson N, Li H, Paabo S, Reich D. The date of interbreeding between Neanderthals and modern humans. PLoS Genet. 2012. doi: 10.1371/1002947.PubMedCentralPubMedGoogle Scholar
  17. 17.
    Reich D, Patterson N, Kircher M, Delfin F, Nandineni MR, Pugach I, et al. Denisova admixture and the first modern human dispersals into Southeast Asia and Oceania. Am J Hum Genet. 2011;89:516–28.PubMedCentralPubMedCrossRefGoogle Scholar
  18. 18.
    Wolpoff MH. Paleoanthropology. 2nd ed. New York: McGraw-Hill; 1999.Google Scholar
  19. 19.
    Cann RL, Stoneking M, Wilson AC. Genetic clues to the dispersal in human populations: retracing the past from the present. Science. 1987;291:1742–8.CrossRefGoogle Scholar
  20. 20.
    Ingman M, Kaessmann H, Paabo S, Gyllensen U. Mitochondrial genome variation and the origin of modern humans. Nature. 2000;408:708–13.PubMedCrossRefGoogle Scholar
  21. 21.
    Pritchard JK, Seielsad MT, Perez-Lezaun A, Feldman MW. Population growth of human y chromosomes: a study of Y chromosome microsatellites. Mol Biol Evol. 1999;16:1791–8.PubMedCrossRefGoogle Scholar
  22. 22.
    Thomson R, Pritchard JK, Shen P, Oefner PJ, Feldman MW. Recent common ancestry of human Y chromosomes: evidence from DNA sequence data. Proc Natl Acad Sci U S A. 2000;97:7360–5.PubMedCentralPubMedCrossRefGoogle Scholar
  23. 23.
    Tang H, Siegmund DO, Shen P, Oefner PJ, Feldman MW. Frequentist estimation of coalescence times from nucleotide sequence data using a tree-based partition. Genetics. 2002;161:447–59.PubMedCentralPubMedGoogle Scholar
  24. 24.
    Poznik GD, Henn BM, Yee M-C, Sliwerska E, Eusdirchen GM, Lin AA, et al. Sequencing Y chromosomes resolves discrepancy in time to common ancestor of males versus females. Science. 2013;341:562–5.PubMedCentralPubMedCrossRefGoogle Scholar
  25. 25.
    Eaton SB, Nelson DA. Calcium in evolutionary perspective. Am J Clin Nutr. 1991;54:281S–7.PubMedGoogle Scholar
  26. 26.
    Mazess RB, Mather W. Bone mineral content of North Alaskan Eskimos. Am J Clin Nutr. 1974;27:916–25.PubMedGoogle Scholar
  27. 27.
    FAO/WHO Expert Group: Joint FAO/WHO expert consultation on human vitamin and mineral requirements, Chapter 11, Calcium. 2002.
  28. 28.
    Schuette SA, Hegsted M, Zemel MB, Linkswiler HM. Renal acid, urinary cyclic AMP, and hydroxyproline excretion as affected by level of protein, sulfur amino acid, and phosphorus intake. J Nutr. 1981;111:2106–16.PubMedGoogle Scholar
  29. 29.
    Orwoll ES. The effects of dietary protein insufficiency and excess on skeletal health. Bone. 1992;13:343–50.PubMedCrossRefGoogle Scholar
  30. 30.
    Bell NH, Shary J, Stevens J, Garza M, Gordon L, Edwards J. Demonstration that bone mass is greater in black than in white children. J Bone Miner Res. 1991;6:719–23.PubMedCrossRefGoogle Scholar
  31. 31.
    Grynpas M. Age and disease-related changes in the mineral of bone. Calcif Tissue Int. 1993;53 Suppl 1:S57–64.PubMedCrossRefGoogle Scholar
  32. 32.
    Abelow BJ, Holford TR, Insogna KL. Cross-cultural association between dietary animal protein and hip fracture: a hypothesis. Calcif Tissue Int. 1992;50:14–8.PubMedCrossRefGoogle Scholar
  33. 33.
    Jablonski NG, Chaplin G. The evolution of human skin coloration. J Hum Evol. 2000;39:57–106.PubMedCrossRefGoogle Scholar
  34. 34.
    Eriksen EF, Glerup H. Vitamin D deficiency and aging: implications for general health and osteoporosis. Biogerontology. 2002;3:73–7.PubMedCrossRefGoogle Scholar
  35. 35.
    Lalueza-Fox C, Rompler H, Caramelli D, Staubert C, Catalano G, Hughes D, et al. A melanocortin 1 receptor allele suggests varying pigmentation among Neanderthals. Science. 2007;318:1453–6.PubMedCrossRefGoogle Scholar
  36. 36.
    Pfeiffer SK, Lazenby RA. Low bone mass in past and present aboriginal populations. In: Draper HH, editor. Advances in nutritional research, vol. 9. New York: Plenum; 1994. p. 35–51.Google Scholar
  37. 37.
    Agarwal SC, Grynpas MD. Bone quantity and quality in past populations. Anat Rec. 1996;246:423–32.PubMedCrossRefGoogle Scholar
  38. 38.
    Cohen MN. Implications of the neolithic demographic transition for world-wide health and mortality in prehistory. In: Bocquet-Appel J-P, Bar-Yosef O, editors. The neolithic demographic transition and its consequences. New York: Springer; 2008. p. 481–500.CrossRefGoogle Scholar
  39. 39.
    Mummert A, Esche E, Robinson J, Armelagos GJ. Stature and robusticity during the agricultural transition: evidence from the bioarchaeological record. Econ Hum Biol. 2011;9:284–301.PubMedCrossRefGoogle Scholar
  40. 40.
    Armelagos GJ, Mielke JH, Owen KH, Van Gerven DP, Dewey JR, Mahler PE. Bone growth and development in prehistoric populations from Sudanese Nubia. J Hum Evol. 1972;1:89–119.CrossRefGoogle Scholar
  41. 41.
    Cohen MN, Armelagos GJ, editors. Paleopathology at the origins of agriculture. Orlando, FL: Academic; 1984.Google Scholar
  42. 42.
    Steckel R, Rose JC, Larsen CS, Walder PL. Skeletal health in the Western Hemisphere from 4000 B.C. to the present. Evol Anthropol. 2002;11:142–55.CrossRefGoogle Scholar
  43. 43.
    Nelson DA. Bone density in three archaeological populations. Am J Phys Anthropol. 1984;63:198.Google Scholar
  44. 44.
    Martin DL, Armelagos GJ. Morphometrics of compact bone: an example from Sudanese Nubia. Am J Phys Anthropol. 1979;51:571–8.PubMedCrossRefGoogle Scholar
  45. 45.
    Martin DL, Armelagos GJ, Goodman AH, Van Gerven DP. The effects of socioeconomic change in prehistoric Africa: Sudanese Nubia as a case study. In: Cohen MN, Armelagos GJ, editors. Paleopathology at the origins of agriculture. New York: Academic; 1984. p. 193–214.Google Scholar
  46. 46.
    Martin DL, Armelagos GJ. Skeletal remodelling and mineralization as indicators of health: an example from prehistoric Sudanese Nubia. J Hum Evol. 1985;14:527–37.CrossRefGoogle Scholar
  47. 47.
    Ericksen MF. Cortical bone loss with age in three Native American populations. Am J Phys Anthropol. 1976;45:443–52.PubMedCrossRefGoogle Scholar
  48. 48.
    Ericksen MF. Patterns of microscopic bone remodelling in three aboriginal American populations. In: Brownman DL, editor. Early native Americans: prehistoric demography, economy, and technology. Houton: The Hague; 1980. p. 239–70.Google Scholar
  49. 49.
    Richman EA, Ortner DJ, Schulter-Ellis FP. Differences in intracortical bone remodeling in three aboriginal American populations: possible dietary factors. Calcif Tissue Int. 1979;28:209–14.PubMedCrossRefGoogle Scholar
  50. 50.
    Mazess RB. Bone density in Sadlermiut Eskimo. Hum Biol. 1966;38:42–8.PubMedGoogle Scholar
  51. 51.
    Mazess RB, Jones R. Weight and density of Sadlermiut Eskimo long bones. Hum Biol. 1972;44:537–48.PubMedGoogle Scholar
  52. 52.
    Thompson DD, Guinness-Hey M. Bone mineral-osteon analysis of Yupik-Inupiaq skeletons. Am J Phys Anthropol. 1981;55:1–7.PubMedCrossRefGoogle Scholar
  53. 53.
    Thompson DD, Posner AS, Laughlin WS, Blumenthal NC. Comparison of bone apatite in osteoporotic and normal Eskimos. Calcif Tissue Int. 1983;35:392–3.PubMedCrossRefGoogle Scholar
  54. 54.
    Thompson DD, Salter EM, Laughlin WS. Bone core analysis of Baffin Island skeletons. Arctic Anthropol. 1981;18:87–96.Google Scholar
  55. 55.
    FAO of the United Nations. Production yearbook, vol. 44. Rome: FAO; 1991.Google Scholar
  56. 56.
    Cooper C, Campion G, Melton III LJ. Hip fractures in the elderly: a worldwide projection. Osteoporos Int. 1992;2:285–9.PubMedCrossRefGoogle Scholar
  57. 57.
    Holbrook TL, Barrett-Connor E. Calcium intake: covariates and confounders. Am J Clin Nutr. 1991;53:741–4.PubMedGoogle Scholar
  58. 58.
    Frost P. Vitamin D, deficiency among northern native peoples: a real or apparent problem? Int J Circumpolar Health. 2012;71:1–5.Google Scholar
  59. 59.
    Kleerekoper M, Nelson DA, Peterson EL, Flynn MJ, Pawluszka AS, Jacobsen G, Wilson P. Reference data for bone mass, calciotropic hormones, and biochemical markers of bone remodeling in older (55–75) postmenopausal white and black women. J Bone Miner Res. 1994;9:1267–76.PubMedCrossRefGoogle Scholar
  60. 60.
    Kiel DP, Myers RH, Cupples LA, Kong XF, Zhu XH, Ordovas J, et al. The BsmI vitamin D receptor restriction fragment length polymorphism (bb) influences the effect of calcium intake on bone mineral density. J Bone Miner Res. 1997;12:1049–57.PubMedCrossRefGoogle Scholar
  61. 61.
    Morrison N, Qi JC, Tokita A, Kelly PJ, Crofts L, Nguyen TV, et al. Prediction of bone density from vitamin D receptor alleles. Nature. 1994;367:284–7.PubMedCrossRefGoogle Scholar
  62. 62.
    Sellers EAC, Sharma A, Rodd C. Adaptation of Inuit children to a low-calcium diet. CMAJ. 2003;168:1141–3.PubMedCentralPubMedGoogle Scholar
  63. 63.
    Ruff CB. Mechanical determinants of bone form: insights from skeletal remains. J Musculoskelet Neuronal Interact. 2005;5:202–12.PubMedGoogle Scholar
  64. 64.
    Larsen CS. Bioarchaeology: interpreting behavior from the human skeleton. Cambridge, UK: Cambridge University Press; 1977.Google Scholar
  65. 65.
    Bridges PS. Bone cortical area in the evaluation of nutrition and activity levels. Am J Hum Biol. 1989;1:785–92.CrossRefGoogle Scholar
  66. 66.
    Larsen CS. Animal source foods and human health during evolution. J Nutr. 2003;11 Suppl 2:3893–7.Google Scholar
  67. 67.
    Ruff C, Holt B, Trinkaus E. Who’s afraid of the big bad Wolff?: “Wolff’s law” and bone functional adaptation. Am J Phys Anthropol. 2006;129(4):484–98.PubMedCrossRefGoogle Scholar
  68. 68.
    Ruff CB, Hayes CS, Larsen WC. Structural changes in the femur with the transition to agriculture on the Georgia coast. Am J Phys Anthropol. 1984;64:125–36.PubMedCrossRefGoogle Scholar
  69. 69.
    Bridges PS. Skeletal evidence of changes in subsistence activities between the Archaic and Mississippian time periods in northwestern Alabama. In: Powell ML, Bridges PS, Mires AMW, editors. What mean these bones: studies in southeastern bioarchaeology. Tuscaloosa, AL: University of Alabama Press; 1991. p. 89–101.Google Scholar
  70. 70.
    Larsen CS. Bioarchaeology of Spanish Florida: the impact of colonialism. Gainesville: University Press of Florida; 2001.Google Scholar
  71. 71.
    Burr DB, Ruff CB, Thompson DD. Patterns of skeletal histological change through time: comparison of an archaic native American population with modern populations. Anat Rec. 1990;226:307–13.PubMedCrossRefGoogle Scholar
  72. 72.
    Kanis JA. Osteoporosis. Oxford, UK: Blackwell Science; 1994.Google Scholar
  73. 73.
    Mosekilde L. Osteoporosis and exercise. Bone. 1995;17:193–5.PubMedCrossRefGoogle Scholar
  74. 74.
    Lees B, Molleson T, Arnett TR, Stevenson JC. Differences in proximal femur bone density over two centuries. Lancet. 1993;341:673–5.PubMedCrossRefGoogle Scholar
  75. 75.
    Ekenman I, Eriksson SA, Lindgren JU. Bone density in medieval skeletons. Calcif Tissue Int. 1995;56:355–8.PubMedCrossRefGoogle Scholar
  76. 76.
    Mays SA, Lees B, Stevenson JC. Age-dependent bone loss in the femur in a medieval population. Int J Osteoarchaeol. 1998;8:97–106.CrossRefGoogle Scholar
  77. 77.
    McEwan JM, Mays S, Blake GM. Measurements of bone mineral density of the radius in a medieval population. Calcif Tissue Int. 2004;2:157–61.CrossRefGoogle Scholar
  78. 78.
    Mays SA. Age-dependent cortical bone loss in a medieval population. Int J Osteoarcheol. 1996;6:144–54.CrossRefGoogle Scholar
  79. 79.
    Agarwal SC, Grynpas MD. Measuring and interpreting age-related loss of vertebral bone mineral density in a medieval population. Am J Phys Anthropol. 2009;139:244–52.PubMedCrossRefGoogle Scholar
  80. 80.
    Agarwal SC, Dumitriu M, Tomlinson GA, Grynpas MD. Medieval trabecular bone architecture: the influence of age, sex, and lifestyle. Am J Phys Anthropol. 2004;124:33–44.PubMedCrossRefGoogle Scholar
  81. 81.
    Bogin B. Modern life history: the evolution of human childhood and fertility. In: Hawkes K, Paine RR, editors. The evolution of human life history. Santa Fe, NM: School of Advanced Research Press; 2006. p. 197–230.Google Scholar
  82. 82.
    Cohen MN. Health and the rise of civilization. New Haven, CT: Yale University Press; 1989.Google Scholar
  83. 83.
    Larsen CS. Biological changes in human populations with agriculture. Annu Rev Anthropol. 1995;24:185–213.CrossRefGoogle Scholar
  84. 84.
    Wilmoth JR. Demography of longevity: past, present, and future trends. Exp Gerontol. 2000;35:1111–29.PubMedCrossRefGoogle Scholar
  85. 85.
    Jackes M. Building the bases for paleodemographic analyses: adult age determination. In: Katzenberg MA, Saunders SR, editors. Biological anthropology of the human skeleton. New York: Wiley Liss; 2000. p. 417–66.Google Scholar
  86. 86.
    Russell JC. The control of late ancient and medieval populations. Philadelphia, PA: American Philosophical Society; 1985.Google Scholar
  87. 87.
    Sjovold T. Inference concerning the age distribution of skeletal populations and some consequences for paleodemography. Anthrop Kozl. 1978;22:99–114.Google Scholar
  88. 88.
    Saunders SR, Hoppa RD. Growth deficit in survivors and non-survivors: biological mortality bias in subadult skeletal samples. Yearb Phys Anthropol. 1993;36:127–51.CrossRefGoogle Scholar
  89. 89.
    Milner GR, Wood JW, Boldsen JL. Paleodemography. In: Katzenberg MA, Saunders SR, editors. Biological anthropology of the human skeleton. New York: Wiley Liss; 2000. p. 467–97.Google Scholar
  90. 90.
    Hawkes K, O’Connell JF, Blurton-Jones NG. Hadza women’s time allocation, offspring provisioning, and the evolution of long postmenopausal life spans. Curr Anthropol. 1997;38:551–77.CrossRefGoogle Scholar
  91. 91.
    Martin RB. Functional adaptation and fragility of the skeleton. In: Agarwal SC, Stout SD, editors. Bone loss and osteoporosis: an anthropological perspective. New York: Kluwer Plenum Academic Press; 2003. p. 121–36.CrossRefGoogle Scholar
  92. 92.
    Kent GN, Price RI, Gutteridge DH, Allen JR, Rosman KJ, Smith M, Bhagat CI, Wilson SG, Retallack RW. Effect of pregnancy and lactation on maternal bone mass and calcium metabolism. Osteoporos Int. 1993;3 Suppl 1:44–7.PubMedCrossRefGoogle Scholar
  93. 93.
    Lopez JM, Gonzalez G, Reyes V, Campino C, Diaz S. Bone turnover and density in healthy women during breastfeeding and after weaning. Osteoporos Int. 1996;6:153–9.PubMedCrossRefGoogle Scholar
  94. 94.
    Sowers M. Pregnancy and lactation as risk factors for subsequent bone loss and osteoporosis. J Bone Miner Res. 1996;11:1052–60.PubMedCrossRefGoogle Scholar
  95. 95.
    Sowers M, Corton G, Shapiro B, Jannausch ML, Crutchfield M, Smith ML, Randolph JF, et al. Changes in bone density with lactation. JAMA. 1993;269:3130–5.PubMedCrossRefGoogle Scholar
  96. 96.
    Sowers M, Eyre D, Hollis BW, Randolph JF, Shapiro B, Jannausch ML, et al. Biochemical markers of bone turnover in lactating and nonlactating postpartum women. J Clin Endocrinol Metab. 1995;80:2210–6.PubMedGoogle Scholar
  97. 97.
    Turner-Walker G, Syversen U, Mays S. The archaeology of osteoporosis. J Eur Archaeol. 2001;4:263–8.CrossRefGoogle Scholar
  98. 98.
    Agarwal SC, Stuart-Macadam P. An evolutionary and biocultural approach to understanding the effects of reproductive factors on the female skeleton. In: Agarwal SC, Stout SD, editors. Bone loss and osteoporosis: an anthropological perspective. New York: Kluwer Plenum Academic Press; 2003. p. 105–16.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  • Dorothy A. Nelson
    • 1
    Email author
  • Sabrina C. Agarwal
    • 2
  • Linda L. Darga
    • 3
  1. 1.Office of Research Administration and Department of AnthropologyOakland UniversityRochesterUSA
  2. 2.Department of AnthropologyUniversity of California BerkeleyBerkeleyUSA
  3. 3.Department of AnthropologyOakland UniversityRochesterUSA

Personalised recommendations