Impact of meat and Lower Palaeolithic food processing techniques on chewing in humans

Abstract

The origins of the genus Homo are murky, but by H. erectus, bigger brains and bodies had evolved that, along with larger foraging ranges, would have increased the daily energetic requirements of hominins1,2. Yet H. erectus differs from earlier hominins in having relatively smaller teeth, reduced chewing muscles, weaker maximum bite force capabilities, and a relatively smaller gut3,4,5. This paradoxical combination of increased energy demands along with decreased masticatory and digestive capacities is hypothesized to have been made possible by adding meat to the diet6,7,8, by mechanically processing food using stone tools7,9,10, or by cooking11,12. Cooking, however, was apparently uncommon until 500,000 years ago13,14, and the effects of carnivory and Palaeolithic processing techniques on mastication are unknown. Here we report experiments that tested how Lower Palaeolithic processing technologies affect chewing force production and efficacy in humans consuming meat and underground storage organs (USOs). We find that if meat comprised one-third of the diet, the number of chewing cycles per year would have declined by nearly 2 million (a 13% reduction) and total masticatory force required would have declined by 15%. Furthermore, by simply slicing meat and pounding USOs, hominins would have improved their ability to chew meat into smaller particles by 41%, reduced the number of chews per year by another 5%, and decreased masticatory force requirements by an additional 12%. Although cooking has important benefits, it appears that selection for smaller masticatory features in Homo would have been initially made possible by the combination of using stone tools and eating meat.

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Figure 1: Representative samples of chewed meat and USO (beetroot) boli before swallowing.
Figure 2: Modelled effects of meat and food processing on mastication.

References

  1. 1

    Aiello, L. C. & Wells, J. C. K. Energetics and the evolution of the genus Homo . Annu. Rev. Anthropol. 31, 323–338 (2002)

    Article  Google Scholar 

  2. 2

    Pontzer, H. Ecological energetics in early Homo . Curr. Anthropol. 53, S346–S358 (2012)

    Article  Google Scholar 

  3. 3

    Eng, C. M., Lieberman, D. E., Zink, K. D. & Peters, M. A. Bite force and occlusal stress production in hominin evolution. Am. J. Phys. Anthropol. 151, 544–557 (2013)

    Article  Google Scholar 

  4. 4

    McHenry, H. M. Tempo and mode in human evolution. Proc. Natl Acad. Sci. USA 91, 6780–6786 (1994)

    CAS  ADS  Article  Google Scholar 

  5. 5

    Aiello, L. C. & Wheeler, P. The expensive-tissue hypothesis: the brain and the digestive-system in human and primate evolution. Curr. Anthropol. 36, 199–221 (1995)

    Article  Google Scholar 

  6. 6

    Bunn, H. T. in Evolution of the Human Diet: The Known, the Unknown, and the Unknowable (ed. Ungar, P. ) 191–211 (Oxford Univ. Press, 2007)

  7. 7

    Domínguez-Rodrigo, M., Pickering, T. R., Semaw, S. & Rogers, M. J. Cutmarked bones from Pliocene archaeological sites at Gona, Afar, Ethiopia: implications for the function of the world’s oldest stone tools. J. Hum. Evol. 48, 109–121 (2005)

    Article  Google Scholar 

  8. 8

    Milton, K. A hypothesis to explain the role of meat-eating in human evolution. Evol. Anthropol. 8, 11–21 (1999)

    Article  Google Scholar 

  9. 9

    Keeley, L. H. & Toth, N. Microwear polishes on early stone tools from Koobi-Fora, Kenya. Nature 293, 464–465 (1981)

    ADS  Article  Google Scholar 

  10. 10

    Harmand, S. et al. 3.3-million-year-old stone tools from Lomekwi 3, West Turkana, Kenya. Nature 521, 310–315 (2015)

    CAS  ADS  Article  Google Scholar 

  11. 11

    Lucas, P. Dental Functional Morphology: How Teeth Work (Cambridge Univ. Press, 2004)

  12. 12

    Wrangham, R. W., Jones, J. H., Laden, G., Pilbeam, D. & Conklin-Brittain, N. The raw and the stolen: cooking and the ecology of human origins. Curr. Anthropol. 40, 567–594 (1999)

    CAS  Article  Google Scholar 

  13. 13

    Gowlett, J. & Wrangham, R. W. Earliest fire in Africa: towards the convergence of archaeological evidence and the cooking hypothesis. Azania Arch. Res. Africa 48, 5–30 (2013)

    Google Scholar 

  14. 14

    Shimelmitz, R. et al. ‘Fire at will’: the emergence of habitual fire use 350,000 years ago. J. Hum. Evol. 77, 196–203 (2014)

    Article  Google Scholar 

  15. 15

    Larsen, C. S. Animal source foods and human health during evolution. J. Nutr. 133 (suppl. 2), 3893S–3897S (2003)

    CAS  Article  Google Scholar 

  16. 16

    Lieberman, D. The Evolution of the Human Head (Harvard Press, 2011)

  17. 17

    Organ, C., Nunn, C. L., Machanda, Z. & Wrangham, R. W. Phylogenetic rate shifts in feeding time during the evolution of Homo. Proc. Natl Acad. Sci. USA 108, 14555–14559 (2011)

  18. 18

    Bramble, D. M. & Lieberman, D. E. Endurance running and the evolution of Homo . Nature 432, 345–352 (2004)

    CAS  ADS  Article  Google Scholar 

  19. 19

    Wrangham, R. & Conklin-Brittain, N. Cooking as a biological trait. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 136, 35–46 (2003)

    Article  Google Scholar 

  20. 20

    Zink, K. D., Lieberman, D. E. & Lucas, P. W. Food material properties and early hominin processing techniques. J. Hum. Evol. 77, 155–166 (2014)

    Article  Google Scholar 

  21. 21

    Lillford, P. J. Mechanisms of fracture in foods. J. Texture Stud. 32, 397–417 (2001)

    Article  Google Scholar 

  22. 22

    Dominy, N. J., Vogel, E. R., Yeakel, J. D., Constantino, P. & Lucas, P. W. Mechanical properties of plant underground storage organs and implications for dietary models of early hominins. Evol. Biol. 35, 159–175 (2008)

    Article  Google Scholar 

  23. 23

    Boback, S. M. et al. Cooking and grinding reduces the cost of meat digestion. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 148, 651–656 (2007)

    Article  Google Scholar 

  24. 24

    Carmody, R. N., Weintraub, G. S. & Wrangham, R. W. Energetic consequences of thermal and nonthermal food processing. Proc. Natl Acad. Sci. USA 108, 19199–19203 (2011)

    CAS  ADS  Article  Google Scholar 

  25. 25

    Boesch, C. & Boesch-Achermann, H. The Chimpanzees of the Tai Forest: Behavioural Ecology and Evolution (Oxford Univ. Press, 2000)

  26. 26

    Laden, G. & Wrangham, R. The rise of the hominids as an adaptive shift in fallback foods: plant underground storage organs (USOs) and australopith origins. J. Hum. Evol. 49, 482–498 (2005)

    Article  Google Scholar 

  27. 27

    Wolpoff, M. H. Posterior tooth size, body size, and diet in South African gracile Australopithecines. Am. J. Phys. Anthropol. 39, 375–393 (1973)

    CAS  Article  Google Scholar 

  28. 28

    Kaplan, H., Hill, K., Lancaster, J. & Hurtado, A. M. A theory of human life history evolution: diet, intelligence, and longevity. Evol. Anthropol. 9, 156–185 (2000)

    Article  Google Scholar 

  29. 29

    Smith, A. R., Carmody, R. N., Dutton, R. J. & Wrangham, R. W. The significance of cooking for early hominin scavenging. J. Hum. Evol. 84, 62–70 (2015)

    Article  Google Scholar 

  30. 30

    Gould, R. A. Living Archaeology (Cambridge Univ. Press, 1980)

  31. 31

    Lagerstedt, A., Enfält, L., Johansson, L. & Lundström, K. Effect of freezing on sensory quality, shear force and water loss in beef M. longissimus dorsi . Meat Sci. 80, 457–461 (2008)

    CAS  Article  Google Scholar 

  32. 32

    Vieira, C., Diaz, M. T., Martínez, B. & García-Cachán, M. D. Effect of frozen storage conditions (temperature and length of storage) on microbiological and sensory quality of rustic crossbred beef at different states of ageing. Meat Sci. 83, 398–404 (2009)

    CAS  Article  Google Scholar 

  33. 33

    Thexton, A. J. A randomisation method for discriminating between signal and noise recordings of rhythmic electromyographic activity. J. Neurosci. Methods 66, 93–98 (1996)

    CAS  Article  Google Scholar 

  34. 34

    Carpenter, J. & Bithell, J. Bootstrap confidence intervals: when, which, what? A practical guide for medical statisticians. Stat. Med. 19, 1141–1164 (2000)

    CAS  Article  Google Scholar 

  35. 35

    R Development Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2014)

  36. 36

    Proeschel, P. A. & Morneburg, T. Task-dependence of activity/bite-force relations and its impact on estimation of chewing force from EMG. J. Dent. Res. 81, 464–468 (2002)

    CAS  Article  Google Scholar 

  37. 37

    Bolker, B. M. et al. Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol. Evol. 24, 127–135 (2009)

    Article  Google Scholar 

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Acknowledgements

We thank R. Carmody, P. Lucas, J. Shea, T. Smith and R. Wrangham for helpful discussions, and E. Castillo and S. Worthington for statistical guidance. This research was funded by the National Science Foundation (#0925688) and by the American School of Prehistoric Research (Peabody Museum, Harvard University).

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Authors

Contributions

K.D.Z. and D.E.L. designed the experiments; K.D.Z. collected and analysed the data, with help from D.E.L.; D.E.L. and K.D.Z. co-wrote the paper.

Corresponding authors

Correspondence to Katherine D. Zink or Daniel E. Lieberman.

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The authors declare no competing financial interests.

Extended data figures and tables

Extended Data Table 1 The number and size of food particles contained within chewed USO (beetroot) and meat boli at ‘swallow’
Extended Data Table 2 Average percentage change of chewing muscle recruitment per chew when masticating size-standardized processed USOs and meat, relative to unprocessed samples
Extended Data Table 3 Average percentage change of chewing muscle recruitment per sample when masticating size-standardized processed USOs and meat, relative to unprocessed samples

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Zink, K., Lieberman, D. Impact of meat and Lower Palaeolithic food processing techniques on chewing in humans. Nature 531, 500–503 (2016). https://doi.org/10.1038/nature16990

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