The evolution of mammalian brain size

J B Smaers^{1

2}, R S Rothman³, D R Hudson³, A M Balanoff^{4

5}, B Beatty^{6

7}, D K N Dechmann^{8

9}, D de Vries¹⁰, J C Dunn^{11

12

13}, J G Fleagle¹⁴, C C Gilbert^{6

15

16

17}, A Goswami¹⁸, A N Iwaniuk¹⁹, W L Jungers^{14

20}, M Kerney¹², D T Ksepka^{21

22

23

24}, P R Manger²⁵, C S Mongle^{2

3

26}, F J Rohlf²⁷, N A Smith^{23

28}, C Soligo²⁹, V Weisbecker³⁰, K Safi^{8

9}

Affiliations

¹ Department of Anthropology, Stony Brook University, Stony Brook, NY 11794, USA. jeroen.smaers@stonybrook.edu.
² Division of Anthropology, American Museum of Natural History, New York, NY 10024, USA.
³ Interdepartmental Doctoral Program in Anthropological Sciences, Stony Brook University, Stony Brook, NY 11794, USA.
⁴ Department of Psychological and Brain Sciences Johns Hopkins University, Baltimore, MD 21218, USA.
⁵ Division of Paleontology, American Museum of Natural History, New York, NY 10024, USA.
⁶ NYIT College of Osteopathic Medicine, Old Westbury, NY 11568, USA.
⁷ United States National Museum, Smithsonian Institution, Washington, DC 20560, USA.
⁸ Department of Migration, Max-Planck Institute of Animal Behavior, 78315 Radolfzell, Germany.
⁹ Department of Biology, University of Konstanz, 78464 Konstanz, Germany.
¹⁰ Ecosystems and Environment Research Centre, School of Science, Engineering and Environment, University of Salford, Manchester M5 4WX, UK.
¹¹ Division of Biological Anthropology, University of Cambridge, Cambridge CB2 3QG, UK.
¹² Behavioral Ecology Research Group, Anglia Ruskin University, Cambridge CB1 1PT, UK.
¹³ Department of Cognitive Biology, University of Vienna, Vienna 1090, Austria.
¹⁴ Department of Anatomical Sciences, Stony Brook University, Stony Brook, NY 11794, USA.
¹⁵ Department of Anthropology, Hunter College, New York, NY 10065, USA.
¹⁶ PhD Program in Anthropology, Graduate Center of the City University of New York, 365 Fifth Avenue, New York, NY 10016, USA.
¹⁷ New York Consortium in Evolutionary Primatology, New York, NY 10065, USA.
¹⁸ Department of Life Sciences, Natural History Museum, London SW7 5BD, UK.
¹⁹ Department of Neuroscience, University of Lethbridge, Lethbridge, AB T1K-3M4, Canada.
²⁰ Association Vahatra, BP 3972, Antananarivo 101, Madagascar.
²¹ Bruce Museum, Greenwich, CT 06830, USA.
²² Department of Ornithology, American Museum of Natural History, New York, NY 10024, USA.
²³ Division of Science and Education, Field Museum of Natural History, Chicago, IL 60605, USA.
²⁴ Department of Paleobiology, Smithsonian Institution, Washington, DC 20013, USA.
²⁵ School of Anatomical Sciences, Faculty of Health Sciences, University of the Witwatersrand, Johannesburg, South Africa.
²⁶ Turkana Basin Institute, Stony Brook University, Stony Brook, NY 11794, USA.
²⁷ Department of Anthropology, Stony Brook University, Stony Brook, NY 11794, USA.
²⁸ Campbell Geology Museum, Clemson University, Clemson, SC 29634, USA.
²⁹ Department of Anthropology, University College London, London WC1H 0BW, UK.
³⁰ College of Science and Engineering, Flinders University, Bedford Park, SA 5042, Australia.

PMID: 33910907
PMCID: PMC8081360
DOI: 10.1126/sciadv.abe2101

The evolution of mammalian brain size

J B Smaers et al. Sci Adv. 2021.

. 2021 Apr 28;7(18):eabe2101.

doi: 10.1126/sciadv.abe2101. Print 2021 Apr.

Authors

Affiliations

¹ Department of Anthropology, Stony Brook University, Stony Brook, NY 11794, USA. jeroen.smaers@stonybrook.edu.
² Division of Anthropology, American Museum of Natural History, New York, NY 10024, USA.
³ Interdepartmental Doctoral Program in Anthropological Sciences, Stony Brook University, Stony Brook, NY 11794, USA.
⁴ Department of Psychological and Brain Sciences Johns Hopkins University, Baltimore, MD 21218, USA.
⁵ Division of Paleontology, American Museum of Natural History, New York, NY 10024, USA.
⁶ NYIT College of Osteopathic Medicine, Old Westbury, NY 11568, USA.
⁷ United States National Museum, Smithsonian Institution, Washington, DC 20560, USA.
⁸ Department of Migration, Max-Planck Institute of Animal Behavior, 78315 Radolfzell, Germany.
⁹ Department of Biology, University of Konstanz, 78464 Konstanz, Germany.
¹⁰ Ecosystems and Environment Research Centre, School of Science, Engineering and Environment, University of Salford, Manchester M5 4WX, UK.
¹¹ Division of Biological Anthropology, University of Cambridge, Cambridge CB2 3QG, UK.
¹² Behavioral Ecology Research Group, Anglia Ruskin University, Cambridge CB1 1PT, UK.
¹³ Department of Cognitive Biology, University of Vienna, Vienna 1090, Austria.
¹⁴ Department of Anatomical Sciences, Stony Brook University, Stony Brook, NY 11794, USA.
¹⁵ Department of Anthropology, Hunter College, New York, NY 10065, USA.
¹⁶ PhD Program in Anthropology, Graduate Center of the City University of New York, 365 Fifth Avenue, New York, NY 10016, USA.
¹⁷ New York Consortium in Evolutionary Primatology, New York, NY 10065, USA.
¹⁸ Department of Life Sciences, Natural History Museum, London SW7 5BD, UK.
¹⁹ Department of Neuroscience, University of Lethbridge, Lethbridge, AB T1K-3M4, Canada.
²⁰ Association Vahatra, BP 3972, Antananarivo 101, Madagascar.
²¹ Bruce Museum, Greenwich, CT 06830, USA.
²² Department of Ornithology, American Museum of Natural History, New York, NY 10024, USA.
²³ Division of Science and Education, Field Museum of Natural History, Chicago, IL 60605, USA.
²⁴ Department of Paleobiology, Smithsonian Institution, Washington, DC 20013, USA.
²⁵ School of Anatomical Sciences, Faculty of Health Sciences, University of the Witwatersrand, Johannesburg, South Africa.
²⁶ Turkana Basin Institute, Stony Brook University, Stony Brook, NY 11794, USA.
²⁷ Department of Anthropology, Stony Brook University, Stony Brook, NY 11794, USA.
²⁸ Campbell Geology Museum, Clemson University, Clemson, SC 29634, USA.
²⁹ Department of Anthropology, University College London, London WC1H 0BW, UK.
³⁰ College of Science and Engineering, Flinders University, Bedford Park, SA 5042, Australia.

PMID: 33910907
PMCID: PMC8081360
DOI: 10.1126/sciadv.abe2101

Abstract

Relative brain size has long been considered a reflection of cognitive capacities and has played a fundamental role in developing core theories in the life sciences. Yet, the notion that relative brain size validly represents selection on brain size relies on the untested assumptions that brain-body allometry is restrained to a stable scaling relationship across species and that any deviation from this slope is due to selection on brain size. Using the largest fossil and extant dataset yet assembled, we find that shifts in allometric slope underpin major transitions in mammalian evolution and are often primarily characterized by marked changes in body size. Our results reveal that the largest-brained mammals achieved large relative brain sizes by highly divergent paths. These findings prompt a reevaluation of the traditional paradigm of relative brain size and open new opportunities to improve our understanding of the genetic and developmental mechanisms that influence brain size.

Copyright © 2021 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works. Distributed under a Creative Commons Attribution NonCommercial License 4.0 (CC BY-NC).

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Figures

**Fig. 1. Time-calibrated phylogeny of mammals with branch colors corresponding to the 30 significantly different allometric grades identified in this study (Table 1).**
The ancestral mammalian grade is indicated in gray, with warmer colors (green and red) assigned to higher-slope grades, and colder colors (blue and purple) to lower-slope grades. For each grade, a lighter color hue indicates grades with a lower intercept, and a darker hue indicates grades with a higher intercept (Table 1). Arrows indicate changes in mean body size (white arrows) or mean brain size (black arrows) resulting in grade shifts, with double arrows indicating one of these variables is changing faster than the other after considering allometry. Triangles indicate changes in cross-species trait variance in body size (white triangles) or brain size (black triangles), with normal triangles indicating increase in mean variance and inverted triangles indicating decrease in mean variance (tables S3 to S5). The equality sign (=) indicates no discernible change in brain size variance. See data S2 for individual species labels. Illustration by J. Lázaro.

**Fig. 2. pGLS regressions for each of the grades.**
The ancestral mammalian grade is indicated in each display to provide an evolutionary context. Numbers indicate the value of the slope for each grade. Colors and silhouettes are as in Fig. 1.

See this image and copyright information in PMC

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The evolution of mammalian brain size

Affiliations

The evolution of mammalian brain size

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