Abstract

The allometric relationship between brain and body size among vertebrates is often considered a manifestation of evolutionary constraints. However, birds and mammals have undergone remarkable encephalization, in which brain size has increased without corresponding changes in body size. Here, we explore the hypothesis that a reduction of phenotypic integration between brain and body size has facilitated encephalization in birds and mammals. Using a large dataset comprising 20,213 specimens across 4,587 species of jawed vertebrates, we show that the among-species (evolutionary) brain–body allometries are remarkably constant, both across vertebrate classes and across taxonomic levels. Birds and mammals, however, are exceptional in that their within-species (static) allometries are shallower and more variable than in other vertebrates. These patterns are consistent with the idea that birds and mammals have reduced allometric constraints that are otherwise ubiquitous across jawed vertebrates. Further exploration of ontogenetic allometries in selected taxa of birds, fishes and mammals reveals that birds and mammals have extended the period of fetal brain growth compared to fishes. Based on these findings, we propose that avian and mammalian encephalization has been contingent on increased variability in brain growth patterns.

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Acknowledgements

We thank C. Pélabon and J. Fitzpatrick for helping us with data collection and T. Hansen for insightful advice in the comparative analysis and treatment on measurement errors. This study was funded by the Japanese Society for Promotion of Science (JSPS) Postdoctoral Fellowship for Young Scientist (2016-3238) and the Norwegian Research Council Norway–Japan researcher mobility grant (258580/H30) to M.T., Swedish Research Council grants (2009-5157, 2012-03624) to N.K., Canada Research Chairs Program to A.N.I. and the Australian Research Council to S.P.C.

Author information

Affiliations

  1. Centre for Ecological and Evolutionary Synthesis (CEES), Department of Biology, University of Oslo, Oslo, Norway

    • Masahito Tsuboi
    • , Bjørn Tore Kopperud
    •  & Kjetil L. Voje
  2. Department of Zoology/Ethology, Stockholm University, Stockholm, Sweden

    • Masahito Tsuboi
    • , Wouter van der Bijl
    • , Alexander Kotrschal
    •  & Niclas Kolm
  3. Department of Evolutionary Studies of Biosystems, The Graduate University of Advanced Studies, Hayama, Kanagawa, Japan

    • Masahito Tsuboi
  4. House of Bird Research, Taps, Christiansfeld, Denmark

    • Johannes Erritzøe
  5. Department of Biology and Marine Biology, UNCW Center for Marine Science, University of North Carolina Wilmington, Wilmington, NC, USA

    • Kara E. Yopak
  6. Oceans Graduate School and the Oceans Institute, The University of Western Australia, Crawley, Western Australia, Australia

    • Kara E. Yopak
    •  & Shaun P. Collin
  7. Department of Neuroscience, University of Lethbridge, Lethbridge, Alberta, Canada

    • Andrew N. Iwaniuk

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Contributions

M.T., A.N.I. and N.K. conceived the study and wrote the manuscript. M.T., B.T.K., J.E., A.K., K.E.Y., S.P.C., A.N.I. and N.K. collected the data. M.T., W.v.d.B., B.T.K., K.L.V. and N.K. designed analytical protocols, and M.T., W.v.d.B. and B.T.K. analysed the data. All authors provided input to the manuscript.

Competing interests

The authors declare no competing interests.

Corresponding author

Correspondence to Masahito Tsuboi.

Supplementary information

  1. Supplementary Information

    Supplementary Figures 1–3, Supplementary Tables 1–7

  2. Reporting Summary

  3. Supplementary Data 1

    Summary of fossil taxa and node age used to calibrate supertrees of Amphibia and Chondrichthyes

  4. Supplementary Data 2

    Dataset of static allometric slopes and conditional variance of brain size

  5. Supplementary Data 3

    Description: Dataset of brain mass (g) and body mass (g) used for assessing ontogenetic allometry and static allometry of guppies

  6. Supplementary Code

    Description: Computer code to run SLOUCH version 2.0.0

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https://doi.org/10.1038/s41559-018-0632-1