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Energetics and the evolution of human brain size

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.

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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.

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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).

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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.

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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)

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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

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