Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Energetics and the evolution of human brain size

Nature volume 480, pages 91–93 (2011)Cite this article

Subjects

Abstract

The human brain stands out among mammals by being unusually large. The expensive-tissue hypothesis1 explains its evolution by proposing a trade-off between the size of the brain and that of the digestive tract, which is smaller than expected for a primate of our body size. Although this hypothesis is widely accepted, empirical support so far has been equivocal. Here we test it in a sample of 100 mammalian species, including 23 primates, by analysing brain size and organ mass data. We found that, controlling for fat-free body mass, brain size is not negatively correlated with the mass of the digestive tract or any other expensive organ, thus refuting the expensive-tissue hypothesis. Nonetheless, consistent with the existence of energy trade-offs with brain size, we find that the size of brains and adipose depots are negatively correlated in mammals, indicating that encephalization and fat storage are compensatory strategies to buffer against starvation. However, these two strategies can be combined if fat storage does not unduly hamper locomotor efficiency. We propose that human encephalization was made possible by a combination of stabilization of energy inputs and a redirection of energy from locomotion, growth and reproduction.

This is a preview of subscription content, access via your institution

Relevant articles

Open Access articles citing this article.

Access options

Rent or buy this article

Get just this article for as long as you need it

$39.95

Learn more

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Correlations between the masses of visceral organs, brains and adipose depots in mammals.
Figure 2: Correlation between residual brain mass and residual adipose depots mass in wild-caught female mammals, controlling for fat-free body mass.
Figure 3: The expensive-brain framework 19 proposes complementary pathways for an adaptive increase in relative brain size.

References

  1. 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 

  2. Mink, J. W., Blumenschine, R. J. & Adams, D. B. Ratio of central nervous system to body metabolism in vertebrates—its constancy and functional basis. Am. J. Physiol. 241, R203–R212 (1981)

    CAS  PubMed  Google Scholar 

  3. Bruhn, J. M. & Benedict, F. G. The respiratory metabolism of the chimpanzee. Proc. Am. Acad. Arts Sci. 71, 259–326 (1936)

    Article  Google Scholar 

  4. Wrangham, R. Catching Fire: How Cooking Made Us Human (Basic Books, 2009)

    Google Scholar 

  5. Aiello, L. C., Bates, N. & Joffe, T. in Evolutionary Anatomy of the Primate Cerebral Cortex (eds Dean, F. & Gibson, K. ) 57–78 (Cambridge Univ. Press, 2001)

    Book  Google Scholar 

  6. Kaufman, J. A., Hladik, C. M. & Pasquet, P. On the expensive-tissue hypothesis: independent support from highly encephalized fish. Curr. Anthropol. 44, 705–707 (2003)

    Article  Google Scholar 

  7. Isler, K. & van Schaik, C. P. Costs of encephalisation: the energy trade-off hypothesis tested on birds. J. Hum. Evol. 51, 228–243 (2006)

    Article  Google Scholar 

  8. Jones, K. E. & MacLarnon, A. M. Affording larger brains: testing hypotheses of mammalian brain evolution on bats. Am. Nat. 164, E20–E31 (2004)

    Article  Google Scholar 

  9. Potts, R. Environmental hypotheses of hominin evolution. Yearb. Phys. Anthropol. 107, 93–136 (1998)

    Article  Google Scholar 

  10. Mau, M., Südekum, K.-H. & Kaiser, T. M. Why cattle feed much and humans think much—new approach to confirm the expensive tissue hypothesis by molecular data. Biosci. Hypotheses 2, 205–208 (2009)

    Article  CAS  Google Scholar 

  11. Pfefferle, A. D. et al. Comparative expression analysis of the phosphocreatine circuit in extant primates: implications for human brain evolution. J. Hum. Evol. 60, 205–212 (2011)

    Article  Google Scholar 

  12. Santoro, S. et al. Preliminary results from digestive adaptation: a new surgical proposal for treating obesity, based on physiology and evolution. Sao Paulo Med. J. 124, 192–197 (2006)

    Article  Google Scholar 

  13. Pond, C. M. The Fats of Life (Cambridge Univ. Press, 1998)

    Book  Google Scholar 

  14. Sol, D. Revisiting the cognitive buffer hypothesis for the evolution of large brains. Biol. Lett. 5, 130–133 (2009)

    Article  Google Scholar 

  15. van Woerden, J. T., van Schaik, C. P. & Isler, K. Effects of seasonality on brain size evolution: evidence from strepsirrhine primates. Am. Nat. 176, 758–767 (2010)

    Article  Google Scholar 

  16. Garland, T. Scaling the ecological cost of transport to body mass in terrestrial mammals. Am. Nat. 121, 571–587 (1983)

    Article  Google Scholar 

  17. Reader, S. M., Hager, Y. & Laland, K. N. The evolution of primate general and cultural intelligence. Philos. Trans. R. Soc. B 366, 1017–1027 (2011)

    Article  Google Scholar 

  18. Martin, R. D. Relative brain size and basal metabolic rate in terrestrial vertebrates. Nature 293, 57–60 (1981)

    Article  ADS  CAS  Google Scholar 

  19. Isler, K. & van Schaik, C. P. The expensive brain: a framework for explaining evolutionary changes in brain size. J. Hum. Evol. 57, 392–400 (2009)

    Article  Google Scholar 

  20. Isler, K. & van Schaik, C. P. Metabolic costs of brain size evolution. Biol. Lett. 2, 557–560 (2006)

    Article  Google Scholar 

  21. Isler, K. Energetic trade-offs between brain size and offspring production: marsupials confirm a general mammalian pattern. Bioessays 33, 173–179 (2011)

    Article  Google Scholar 

  22. Wells, J. C. K. The Evolutionary Biology of Human Body Fatness (Cambridge Univ. Press, 2009)

    Book  Google Scholar 

  23. Zihlman, A. L. in The Pygmy Chimpanzee (ed. Susman, R. L. ) 179–200 (Plenum Press, 1984)

    Book  Google Scholar 

  24. 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 

  25. 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 

  26. Burkart, J. M., Hrdy, S. B. & van Schaik, C. P. Cooperative breeding and human cognitive evolution. Evol. Anthropol. 18, 175–186 (2009)

    Article  Google Scholar 

  27. Pontzer, H. et al. Locomotor anatomy and biomechanics of the Dmanisi hominins. J. Hum. Evol. 58, 492–504 (2010)

    Article  Google Scholar 

  28. Pontzer, H., Raichlen, D. A. & Sockol, M. D. The metabolic cost of walking in humans, chimpanzees, and early hominins. J. Hum. Evol. 56, 43–54 (2009)

    Article  Google Scholar 

  29. Isler, K. & van Schaik, C. P. Why are there so few smart mammals (but so many smart birds)? Biol. Lett. 5, 125–129 (2009)

    Article  Google Scholar 

  30. Dean, C. et al. Growth processes in teeth distinguish modern humans from Homo erectus and earlier hominins. Nature 414, 628–631 (2001)

    Article  ADS  CAS  Google Scholar 

  31. Pitts, G. & Bullard, T. in Body Composition in Animals and Man (ed. Reit, J. T. ) 45–70 (National Academy of Science Pub No. 1598, 1968)

    Google Scholar 

  32. Isler, K. et al. Endocranial volumes of primate species: scaling analyses using a comprehensive and reliable data set. J. Hum. Evol. 55, 967–978 (2008)

    Article  Google Scholar 

  33. Rehkämper, G., Frahm, H. D. & Zilles, K. Quantitative development of brain and brain structures in birds (Galliformes and Passeriformes) compared to that in mammals (Insectivores and Primates). Brain Behav. Evol. 37, 125–143 (1991)

    Article  Google Scholar 

  34. Orme, D., Freckleton, R. P., Thomas, G., Petzoldt, T. & Fritz, S. CAIC: Comparative Analyses Using Independent Contrasts 〈http://r-forge.r-project.org/projects/caic〉 (2009)

    Google Scholar 

  35. R Development Core Team . R: a language and environment for statistical computing (R Foundation for Statistical Computing, 2010)

Download references

Acknowledgements

We thank R. D. Martin and J. Wermuth for sharing the Chivers data set, J. van Woerden for sharing her endocranial volume data, and M. Genoud for sharing his revised compilation of mammalian BMR values. Specimens were provided by numerous institutions, museums and colleagues (Supplementary Information 2). We acknowledge valuable comments by L. Aiello and R. D. Martin. Financial support was provided by the Swiss National Science Foundation (grant number 3100A0-117789), the A.H. Schultz-Stiftung and the European Integrated Activities grant SYNTHESYS (grant application number HU-TAF-4916).

Author information

Authors and Affiliations

  1. Anthropological Institute and Museum, University of Zurich, Winterthurerstrasse 190, 8057 Zurich, Switzerland

    Ana Navarrete, Carel P. van Schaik & Karin Isler

Authors
  1. Ana Navarrete
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Carel P. van Schaik
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Karin Isler
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

K.I. and C.P.v.S. designed the project. A.N. performed the pilot study and collected the data. A.N. and K.I. performed the analyses and all three authors wrote the manuscript.

Corresponding authors

Correspondence to Ana Navarrete or Karin Isler.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Information

This file contains Supplementary Text comprising Supplementary Data, Supplementary Methods, Supplementary Results and Discussion (see Content list for more details); Supplementary Figures 1-3 with legends; Supplementary Tables 1-11 and additional references. (PDF 1377 kb)

Supplementary Data (Navarette_SupplData)

This file displays the compiled dataset of organ mass and metabolic data for 100 mammal species. (XLS 70 kb)

PowerPoint slides

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Navarrete, A., van Schaik, C. & Isler, K. Energetics and the evolution of human brain size. Nature 480, 91–93 (2011). https://doi.org/10.1038/nature10629

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature10629

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing