The human brain stands out among mammals by being unusually large. The expensive-tissue hypothesis 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. DOI: https://doi.org/10.1038/nature10629Posted at the Zurich Open Repository and Archive, University of Zurich ZORA URL: https://doi.org/10.5167/uzh-57326 Accepted Version Originally published at: Navarrete, A; van Schaik, C P; Isler, K (2011). Energetics and the evolution of human brain size. Nature, 480 (7375) across a broad array of taxa was urgently needed, but has so far not been conducted due to lack of 37 morphological data, nor has there been an examination of the broader trade-offs amongst other 38 expensive organs predicted by an extension of this hypothesis 7 . 39Here, we examine the presence of correlated evolution of organ sizes in a new dataset of the 40 mass of various visceral organs (heart, lungs, stomach, intestines, kidneys, spleen and liver) and 41 associated brain size for 100 mammal species, including 23 primate species (see Suppl. Data). 42Dissections followed a strict protocol and were all conducted by one of the authors (A.N.). We 45In this analysis, it is crucial to control for body size. The usual measure taken for this, body 46 mass, is highly affected by variation in the size of adipose depots, which may confound or even 47 reverse the direction of correlations among organs (Suppl. Fig. 2, Suppl. Table 4b). Here, we 48 therefore used fat-free body mass as the best proxy for body size. All analyses took phylogenetic 49 relatedness into account (Suppl. Fig. 3). The sample size of 100 species yields a power of 0.8 for 50 these analyses, which was determined a priori using a published dataset of 39 mammal species (see 51 Methods). 52Contrary to the predictions of the Expensive Tissue Hypothesis, we found no negative 53 correlations between the relative size of the brain and the digestive tract, other expensive organs or 54 their combined sum among mamm...

Explanations for primate brain expansion and the evolution of human cognition and culture remain contentious despite extensive research. While multiple comparative analyses have investigated variation in brain size across primate species, very few have addressed why primates vary in how much they use social learning. Here, we evaluate the hypothesis that the enhanced reliance on socially transmitted behavior observed in some primates has coevolved with enlarged brains, complex sociality, and extended lifespans. Using recently developed phylogenetic comparative methods we show that, across primate species, a measure of social learning proclivity increases with absolute and relative brain volume, longevity (specifically reproductive lifespan), and social group size, correcting for research effort. We also confirm relationships of absolute and relative brain volume with longevity (both juvenile period and reproductive lifespan) and social group size, although longevity is generally the stronger predictor. Relationships between social learning, brain volume, and longevity remain when controlling for maternal investment and are therefore not simply explained as a by-product of the generally slower life history expected for larger brained species. Our findings suggest that both brain expansion and high reliance on culturally transmitted behavior coevolved with sociality and extended lifespan in primates. This coevolution is consistent with the hypothesis that the evolution of large brains, sociality, and long lifespans has promoted reliance on culture, with reliance on culture in turn driving further increases in brain volume, cognitive abilities, and lifespans in some primate lineages. cultural evolution | social learning | brain evolution | primates | phylogenetic comparative analysis

Despite prolonged interest in comparing brain size and behavioral proxies of "intelligence" across taxa, the adaptive and cognitive significance of brain size variation remains elusive. Central to this problem is the continued focus on hominid cognition as a benchmark and the assumption that behavioral complexity has a simple relationship with brain size. Although comparative studies of brain size have been criticized for not reflecting how evolution actually operates, and for producing spurious, inconsistent results, the causes of these limitations have received little discussion. We show how these issues arise from implicit assumptions about what brain size measures and how it correlates with behavioral and cognitive traits. We explore how inconsistencies can arise through heterogeneity in evolutionary trajectories and selection pressures on neuroanatomy or neurophysiology across taxa. We examine how interference from ecological and life history variables complicates interpretations of brain-behavior correlations and point out how this problem is exacerbated by the limitations of brain and cognitive measures. These considerations, and the diversity of brain morphologies and behavioral capacities, suggest that comparative brain-behavior research can make greater progress by focusing on specific neuroanatomical and behavioral traits within relevant ecological and evolutionary contexts. We suggest that a synergistic combination of the "bottom-up" approach of classical neuroethology and the "top-down" approach of comparative biology/psychology within closely related but behaviorally diverse clades can limit the effects of heterogeneity, interference, and noise. We argue that this shift away from broad-scale analyses of superficial phenotypes will provide deeper, more robust insights into brain evolution.

One contribution of 15 to a theme issue 'Innovation in animals and humans: understanding the origins and development of novel and creative behaviour'.

Since the publication of the primate brain volumetric dataset of Stephan and colleagues in the early 1980s, no major new comparative datasets covering multiple brain regions and a large number of primate species have become available. However, technological and other advances in the last two decades, particularly magnetic resonance imaging (MRI) and the creation of institutions devoted to the collection and preservation of rare brain specimens, provide opportunities to rectify this situation. Here, we present a new dataset including brain region volumetric measurements of 39 species, including 20 species not previously available in the literature, with measurements of 16 brain areas. These volumes were extracted from MRI of 46 brains of 38 species from the Netherlands Institute of Neuroscience Primate Brain Bank, scanned at high resolution with a 9.4-T scanner, plus a further 7 donated MRI of 4 primate species. Partial measurements were made on an additional 8 brains of 5 species. We make the dataset and MRI scans available online in the hope that they will be of value to researchers conducting comparative studies of primate evolution.

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While some descriptions of ruminants' dietary adaptations suggest that the length of the intestinal tract reflects the proportion of grass or browse in the diet, this assumption has been questioned. We collated data on body mass (BM), as well as small intestine, caecum, colon/rectum, large and total intestine length in 68 ruminant species, and, while accounting for the phylogenetic structure of the dataset, evaluated both allometric scaling and the potential influence of diet, digestive physiology or climate proxies on measures of intestine length. Intestinal length generally scaled to BM at an exponent higher than the 0.33 expected due to geometry. Diet or digestive physiology proxies did not have an influence on any intestinal length measures, though some proxies indicating more arid natural habitats were positively correlated with measures of the large intestine. The relative size of a forestomach compartment, the omasum, was negatively correlated with intestine length. The results indicate that intestine length measures provide little indication of feeding type or digestive physiology, but rather indicate adaptations to aridity. Higher-than-geometry scaling of intestinal length may be related to the necessity of maintaining geometric (or metabolic) scaling of intestinal surface area while keeping gut diameter, and hence the diffusion distances, small. The way in which space trade-offs determine the macroanatomy of different organs in the abdominal cavity, such as the omasum and the intestine, deserves further investigation. K E Y W O R D S digestion, feeding type, fluid throughput, omasum, ruminant