Energetics and the evolution of human brain size

Journal name:
Nature
Volume:
480,
Pages:
91–93
Date published:
DOI:
doi:10.1038/nature10629
Received
Accepted
Published online

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.

At a glance

Figures

  1. Correlations between the masses of visceral organs, brains and adipose depots in mammals.
    Figure 1: Correlations between the masses of visceral organs, brains and adipose depots in mammals.

    The analysis is based on a sample of 100 mammalian species and controls for phylogenetic relationships and fat-free body mass. Statistical details are listed in the Supplementary Information 3.1.

  2. Correlation between residual brain mass and residual adipose depots mass in wild-caught female mammals, controlling for fat-free body mass.
    Figure 2: Correlation between residual brain mass and residual adipose depots mass in wild-caught female mammals, controlling for fat-free body mass.

    Species-level values: N = 28 species, r2 = 0.258, P = 0.006. PGLS: λ = 1.00, β = −0.12, t value = −3.42, P = 0.002.

  3. The expensive-brain framework proposes complementary pathways for an adaptive increase in relative brain size.
    Figure 3: The expensive-brain framework19 proposes complementary pathways for an adaptive increase in relative brain size.

    First, brains can get larger when energy inputs are stabilized on a higher level (higher total metabolic turnover20) through an increase in mean dietary quality (for example, more animal fat and protein in early Homo4, 22, 24), energy subsidies from other individuals (for example, cooperative breeding, allomaternal care19, 21) or by reducing fluctuations in energy inputs (for example, cognitive solutions15, including culture). Second, at constant total energy intake, energy allocation to other functions may be reduced, such as locomotion (for example, efficient bipedalism27, 28) or production (for example, slower life history pace30).

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, 199221 (1995)
  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, R203R212 (1981)
  3. Bruhn, J. M. & Benedict, F. G. The respiratory metabolism of the chimpanzee. Proc. Am. Acad. Arts Sci. 71, 259326 (1936)
  4. Wrangham, R. Catching Fire: How Cooking Made Us Human (Basic Books, 2009)
  5. Aiello, L. C., Bates, N. & Joffe, T. in Evolutionary Anatomy of the Primate Cerebral Cortex (eds Dean, F. & Gibson, K.) 5778 (Cambridge Univ. Press, 2001)
  6. Kaufman, J. A., Hladik, C. M. & Pasquet, P. On the expensive-tissue hypothesis: independent support from highly encephalized fish. Curr. Anthropol. 44, 705707 (2003)
  7. Isler, K. & van Schaik, C. P. Costs of encephalisation: the energy trade-off hypothesis tested on birds. J. Hum. Evol. 51, 228243 (2006)
  8. Jones, K. E. & MacLarnon, A. M. Affording larger brains: testing hypotheses of mammalian brain evolution on bats. Am. Nat. 164, E20E31 (2004)
  9. Potts, R. Environmental hypotheses of hominin evolution. Yearb. Phys. Anthropol. 107, 93136 (1998)
  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, 205208 (2009)
  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, 205212 (2011)
  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, 192197 (2006)
  13. Pond, C. M. The Fats of Life (Cambridge Univ. Press, 1998)
  14. Sol, D. Revisiting the cognitive buffer hypothesis for the evolution of large brains. Biol. Lett. 5, 130133 (2009)
  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, 758767 (2010)
  16. Garland, T. Scaling the ecological cost of transport to body mass in terrestrial mammals. Am. Nat. 121, 571587 (1983)
  17. Reader, S. M., Hager, Y. & Laland, K. N. The evolution of primate general and cultural intelligence. Philos. Trans. R. Soc. B 366, 10171027 (2011)
  18. Martin, R. D. Relative brain size and basal metabolic rate in terrestrial vertebrates. Nature 293, 5760 (1981)
  19. Isler, K. & van Schaik, C. P. The expensive brain: a framework for explaining evolutionary changes in brain size. J. Hum. Evol. 57, 392400 (2009)
  20. Isler, K. & van Schaik, C. P. Metabolic costs of brain size evolution. Biol. Lett. 2, 557560 (2006)
  21. Isler, K. Energetic trade-offs between brain size and offspring production: marsupials confirm a general mammalian pattern. Bioessays 33, 173179 (2011)
  22. Wells, J. C. K. The Evolutionary Biology of Human Body Fatness (Cambridge Univ. Press, 2009)
  23. Zihlman, A. L. in The Pygmy Chimpanzee (ed. Susman, R. L.) 179200 (Plenum Press, 1984)
  24. Aiello, L. C. & Wells, J. C. K. Energetics and the evolution of the genus Homo. Annu. Rev. Anthropol. 31, 323338 (2002)
  25. Kaplan, H., Hill, K., Lancaster, J. & Hurtado, A. M. A theory of human life history evolution: diet, intelligence, and longevity. Evol. Anthropol. 9, 156185 (2000)
  26. Burkart, J. M., Hrdy, S. B. & van Schaik, C. P. Cooperative breeding and human cognitive evolution. Evol. Anthropol. 18, 175186 (2009)
  27. Pontzer, H. et al. Locomotor anatomy and biomechanics of the Dmanisi hominins. J. Hum. Evol. 58, 492504 (2010)
  28. Pontzer, H., Raichlen, D. A. & Sockol, M. D. The metabolic cost of walking in humans, chimpanzees, and early hominins. J. Hum. Evol. 56, 4354 (2009)
  29. Isler, K. & van Schaik, C. P. Why are there so few smart mammals (but so many smart birds)? Biol. Lett. 5, 125129 (2009)
  30. Dean, C. et al. Growth processes in teeth distinguish modern humans from Homo erectus and earlier hominins. Nature 414, 628631 (2001)
  31. Pitts, G. & Bullard, T. in Body Composition in Animals and Man (ed. Reit, J. T.) 4570 (National Academy of Science Pub No. 1598, 1968)
  32. Isler, K. et al. Endocranial volumes of primate species: scaling analyses using a comprehensive and reliable data set. J. Hum. Evol. 55, 967978 (2008)
  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, 125143 (1991)
  34. Orme, D., Freckleton, R. P., Thomas, G., Petzoldt, T. & Fritz, S. CAIC: Comparative Analyses Using Independent Contrasts left fencehttp://r-forge.r-project.org/projects/caicright fence (2009)
  35. R Development Core Team. R: a language and environment for statistical computing (R Foundation for Statistical Computing, 2010)

Download references

Author information

Affiliations

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

    • Ana Navarrete,
    • Carel P. van Schaik &
    • Karin Isler

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.

Competing financial interests

The authors declare no competing financial interests.

Corresponding authors

Correspondence to:

Author details

Supplementary information

PDF files

  1. Supplementary Information (1.3M)

    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.

Excel files

  1. Supplementary Data (Navarette_SupplData) (70K)

    This file displays the compiled dataset of organ mass and metabolic data for 100 mammal species.

Additional data