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      Quantitative uniqueness of human brain evolution revealed through phylogenetic comparative analysis

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          Abstract

          While the human brain is clearly large relative to body size, less is known about the timing of brain and brain component expansion within primates and the relative magnitude of volumetric increases. Using Bayesian phylogenetic comparative methods and data for both extant and fossil species, we identified that a distinct shift in brain-body scaling occurred as hominins diverged from other primates, and again as humans and Neanderthals diverged from other hominins. Within hominins, we detected a pattern of directional and accelerating evolution towards larger brains, consistent with a positive feedback process in the evolution of the human brain. Contrary to widespread assumptions, we found that the human neocortex is not exceptionally large relative to other brain structures. Instead, our analyses revealed a single increase in relative neocortex volume at the origin of haplorrhines, and an increase in relative cerebellar volume in apes.

          eLife digest

          Humans have much larger brains than other primates, but it is not clear exactly when and how this difference emerged during evolution. Some scientists believe that the expansion of a part of the brain called the neocortex – which handles sight, hearing, conscious decision-making and language – drove the increase in the size of the human brain. Newer studies have challenged that idea.

          One way to learn more about how humans evolved bigger brains is to compare the size of the brain, and specific parts of the brain, between humans and our closest relatives: non-human primates. To make accurate comparisons, scientists must account for many factors. Closely related primates may have more similar traits because they more recently shared a common ancestor. This means the evolutionary relationships between species need to be considered. Larger animals also tend to have larger brains so it is important to consider body size, too.

          Now, Miller at al. show that the human brain is much larger than expected even after accounting for these factors, and that increases in brain size accelerated over the course of early human evolution. In the analyses, the brain and skull sizes of different living primate species, like chimpanzees and gorillas, and fossils of extinct primates, including Neanderthals, were compared using mathematical models.

          These findings suggest that larger brains provided fitness advantages that led to large brain sizes in modern humans and Neanderthals. These increases in brain size were not driven by disproportionate growth in the neocortex alone, but rather by increases in the size of many parts of the brain. Increases in the relative size of the cerebellum, which is essential for balance and movement, were also important.

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          Most cited references63

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          Phylogenetic Comparative Analysis: A Modeling Approach for Adaptive Evolution

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            The evolution of self-control.

            Cognition presents evolutionary research with one of its greatest challenges. Cognitive evolution has been explained at the proximate level by shifts in absolute and relative brain volume and at the ultimate level by differences in social and dietary complexity. However, no study has integrated the experimental and phylogenetic approach at the scale required to rigorously test these explanations. Instead, previous research has largely relied on various measures of brain size as proxies for cognitive abilities. We experimentally evaluated these major evolutionary explanations by quantitatively comparing the cognitive performance of 567 individuals representing 36 species on two problem-solving tasks measuring self-control. Phylogenetic analysis revealed that absolute brain volume best predicted performance across species and accounted for considerably more variance than brain volume controlling for body mass. This result corroborates recent advances in evolutionary neurobiology and illustrates the cognitive consequences of cortical reorganization through increases in brain volume. Within primates, dietary breadth but not social group size was a strong predictor of species differences in self-control. Our results implicate robust evolutionary relationships between dietary breadth, absolute brain volume, and self-control. These findings provide a significant first step toward quantifying the primate cognitive phenome and explaining the process of cognitive evolution.
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              Body mass in comparative primatology.

              Data are presented on adult body mass for 230 of 249 primate species, based on a review of the literature and previously unpublished data. The issues involved in collecting data on adult body mass are discussed, including the definition of adults, the effects of habitat and pregnancy, the strategy for pooling data on single species from multiple studies, and use of an appropriate number of significant figures. An analysis of variability in body mass indicates that the coefficient of variation for body mass increases with increasing species mean mass. Evaluation of several previous body mass reviews reveals a number of shortcomings with data that have been used often in comparative studies.
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                Author and article information

                Contributors
                Role: Senior Editor
                Role: Reviewing Editor
                Journal
                eLife
                Elife
                eLife
                eLife
                eLife Sciences Publications, Ltd
                2050-084X
                31 January 2019
                2019
                : 8
                : e41250
                Affiliations
                [1 ]deptEcology and Evolutionary Biology Princeton University PrincetonUnited States
                [2 ]deptDepartment of Evolutionary Anthropology Duke University DurhamUnited States
                [3 ]deptEvolutionary Anthropology Research Group, Department of Anthropology University of Durham DurhamUnited Kingdom
                [4 ]deptDuke Global Health Institute Duke University DurhamUnited States
                University of Michigan United States
                Yale United States
                Yale United States
                Midwestern University United States
                California State Long Beach United States
                Emory University United States
                Author information
                http://orcid.org/0000-0002-2673-9618
                http://orcid.org/0000-0001-9330-2873
                Article
                41250
                10.7554/eLife.41250
                6379089
                30702428
                98e66d0d-bf87-47b9-b968-cec5db6b755e
                © 2019, Miller et al

                This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.

                History
                : 22 August 2018
                : 29 January 2019
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/100000001, National Science Foundation;
                Award ID: BCS-1355902
                Award Recipient :
                The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
                Categories
                Research Article
                Evolutionary Biology
                Neuroscience
                Custom metadata
                The exceptionally large size of the human brain is the result of accelerating evolution towards larger brains in hominins, but is not the product of neocortical expansion.

                Life sciences
                brain evolution,phylogenetic comparative methods,human evolution,primate,human,other
                Life sciences
                brain evolution, phylogenetic comparative methods, human evolution, primate, human, other

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