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      The evolution of mammalian brain size

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          Abstract

          An in-depth look at mammalian brain size evolution prompts a reevaluation of a traditional paradigm.

          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.

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          Most cited references105

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          Linked regularities in the development and evolution of mammalian brains.

          Analysis of data collected on 131 species of primates, bats, and insectivores showed that the sizes of brain components, from medulla to forebrain, are highly predictable from absolute brain size by a nonlinear function. The order of neurogenesis was found to be highly conserved across a wide range of mammals and to correlate with the relative enlargement of structures as brain size increases, with disproportionately large growth occurring in late-generated structures. Because the order of neurogenesis is conserved, the most likely brain alteration resulting from selection for any behavioral ability may be a coordinated enlargement of the entire nonolfactory brain.
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            Evolution in the social brain.

            The evolution of unusually large brains in some groups of animals, notably primates, has long been a puzzle. Although early explanations tended to emphasize the brain's role in sensory or technical competence (foraging skills, innovations, and way-finding), the balance of evidence now clearly favors the suggestion that it was the computational demands of living in large, complex societies that selected for large brains. However, recent analyses suggest that it may have been the particular demands of the more intense forms of pairbonding that was the critical factor that triggered this evolutionary development. This may explain why primate sociality seems to be so different from that found in most other birds and mammals: Primate sociality is based on bonded relationships of a kind that are found only in pairbonds in other taxa.
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              Big brains, enhanced cognition, and response of birds to novel environments.

              The widely held hypothesis that enlarged brains have evolved as an adaptation to cope with novel or altered environmental conditions lacks firm empirical support. Here, we test this hypothesis for a major animal group (birds) by examining whether large-brained species show higher survival than small-brained species when introduced to nonnative locations. Using a global database documenting the outcome of >600 introduction events, we confirm that avian species with larger brains, relative to their body mass, tend to be more successful at establishing themselves in novel environments. Moreover, we provide evidence that larger brains help birds respond to novel conditions by enhancing their innovation propensity rather than indirectly through noncognitive mechanisms. These findings provide strong evidence for the hypothesis that enlarged brains function, and hence may have evolved, to deal with changes in the environment.
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                Author and article information

                Journal
                Sci Adv
                Sci Adv
                SciAdv
                advances
                Science Advances
                American Association for the Advancement of Science
                2375-2548
                April 2021
                28 April 2021
                : 7
                : 18
                : eabe2101
                Affiliations
                [1 ]Department of Anthropology, Stony Brook University, Stony Brook, NY 11794, USA.
                [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 ]Campbell Geology Museum, Clemson University, Clemson, SC 29634, USA.
                [28 ]Department of Anthropology, University College London, London WC1H 0BW, UK.
                [29 ]College of Science and Engineering, Flinders University, Bedford Park, SA 5042, Australia.
                Author notes
                [* ]Corresponding author. Email: jeroen.smaers@ 123456stonybrook.edu
                Author information
                http://orcid.org/0000-0003-1741-9839
                http://orcid.org/0000-0002-8985-6168
                http://orcid.org/0000-0003-3813-1412
                http://orcid.org/0000-0003-4030-3818
                http://orcid.org/0000-0002-5464-0041
                http://orcid.org/0000-0003-0043-8267
                http://orcid.org/0000-0002-6809-0052
                http://orcid.org/0000-0003-3487-6513
                http://orcid.org/0000-0003-3162-808X
                http://orcid.org/0000-0001-8768-3171
                http://orcid.org/0000-0001-9273-3655
                http://orcid.org/0000-0003-4996-3839
                http://orcid.org/0000-0003-3020-6803
                http://orcid.org/0000-0002-1881-2854
                http://orcid.org/0000-0003-0522-3679
                http://orcid.org/0000-0002-0990-3594
                http://orcid.org/0000-0001-5448-9612
                http://orcid.org/0000-0003-2370-4046
                http://orcid.org/0000-0002-8418-6759
                Article
                abe2101
                10.1126/sciadv.abe2101
                8081360
                33910907
                9ffd0930-f3d3-4504-8bc5-0a89d6dbf6ad
                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).

                This is an open-access article distributed under the terms of the Creative Commons Attribution-NonCommercial license, which permits use, distribution, and reproduction in any medium, so long as the resultant use is not for commercial advantage and provided the original work is properly cited.

                History
                : 06 August 2020
                : 10 March 2021
                Funding
                Funded by: doi http://dx.doi.org/10.13039/100000001, National Science Foundation;
                Award ID: 80692
                Funded by: doi http://dx.doi.org/10.13039/100010663, H2020 European Research Council;
                Award ID: ERC-Stg-637171
                Funded by: doi http://dx.doi.org/10.13039/100012292, Gerstner Family Foundation;
                Funded by: doi http://dx.doi.org/10.13039/501100000923, Australian Research Council;
                Award ID: DP170103227
                Categories
                Research Article
                Research Articles
                SciAdv r-articles
                Evolutionary Biology
                Paleontology
                Evolutionary Biology
                Custom metadata
                Mariane Belen

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