Understanding the human brain: insights from comparative biology.

Human brains are exceptionally large, support distinctive cognitive processes, and evolved by natural selection to mediate adaptive behavior. Comparative biology situates the human brain within an evolutionary context to illuminate how it has been shaped by selection and how its structure relates to evolutionary function, while identifying the developmental and molecular changes that were involved. Recent applications of powerful phylogenetic methods have uncovered new findings, some of which overturn conventional wisdom about how and why brains evolve. Here, we focus on four long-standing claims about brain evolution and discuss how new work has either contradicted these claims or shown the relevant phenomena to be more complicated than previously appreciated. Throughout, we emphasize studies of non-human primates and hominins, our close relatives and recent ancestors.

Experts in action: why we need an embodied social brain hypothesis.

The anthropoid primates are known for their intense sociality and large brain size. The idea that these might be causally related has given rise to a large body of work testing the 'social brain hypothesis'. Here, the emphasis has been placed on the political demands of social life, and the cognitive skills that would enable animals to track the machinations of other minds in metarepresentational ways. It seems to us that this position risks losing touch with the fact that brains primarily evolved to enable the control of action, which in turn leads us to downplay or neglect the importance of the physical body in a material world full of bodies and other objects. As an alternative, we offer a view of primate brain and social evolution that is grounded in the body and action, rather than minds and metarepresentation. This article is part of the theme issue 'Systems neuroscience through the lens of evolutionary theory'.

Television consumption drives perceptions of female body attractiveness in a population undergoing technological transition.

Perceptions of physical attractiveness vary across cultural groups, particularly for female body size and shape. It has been hypothesized that visual media propagates Western "thin ideals." However, because cross-cultural studies typically consider groups highly differentiated on a number of factors, identifying the causal factors has thus far been impossible. In the present research, we conducted "naturalistic" and controlled experiments to test the influence of media access on female body ideals in a remote region of Nicaragua by sampling from villages with and without regular TV access. We found that greater TV consumption remained a significant predictor of preferences for slimmer, curvier female figures after controlling for a range of other factors in an ethnically balanced sample of 299 individuals (150 female, aged 15-79) across 7 villages. Within-individual analyses in 1 village over 3 years also showed an association between increased TV consumption and preferences for slimmer figures among some participants. Finally, an experimental study in 2 low-media locations demonstrates that exposure to media images of fashion models can directly impact participants' body size ideals. We provide the first converging cross-sectional, longitudinal, and experimental evidence from field-based research, that media exposure can drive changes in perceptions of female attractiveness. (PsycInfo Database Record (c) 2020 APA, all rights reserved).

Maternal investment, life histories and the evolution of brain structure in primates.

Life history is a robust correlate of relative brain size: larger-brained mammals and birds have slower life histories and longer lifespans than smaller-brained species. The cognitive buffer hypothesis (CBH) proposes an adaptive explanation for this relationship: large brains may permit greater behavioural flexibility and thereby buffer the animal from unpredictable environmental challenges, allowing for reduced mortality and increased lifespan. By contrast, the developmental costs hypothesis (DCH) suggests that life-history correlates of brain size reflect the extension of maturational processes needed to accommodate the evolution of large brains, predicting correlations with pre-adult life-history phases. Here, we test novel predictions of the hypotheses in primates applied to the neocortex and cerebellum, two major brain structures with distinct developmental trajectories. While neocortical growth is allocated primarily to pre-natal development, the cerebellum exhibits relatively substantial post-natal growth. Consistent with the DCH, neocortical expansion is related primarily to extended gestation while cerebellar expansion to extended post-natal development, particularly the juvenile period. Contrary to the CBH, adult lifespan explains relatively little variance in the whole brain or neocortex volume once pre-adult life-history phases are accounted for. Only the cerebellum shows a relationship with lifespan after accounting for developmental periods. Our results substantiate and elaborate on the role of maternal investment and offspring development in brain evolution, suggest that brain components can evolve partly independently through modifications of distinct developmental phases, and imply that environmental input during post-natal maturation may be particularly crucial for the development of cerebellar function. They also suggest that relatively extended post-natal maturation times provide a developmental mechanism for the marked expansion of the cerebellum in the apes.

Quantitative uniqueness of human brain evolution revealed through phylogenetic comparative analysis.

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.

Re-evaluating the link between brain size and behavioural ecology in primates.

Comparative studies have identified a wide range of behavioural and ecological correlates of relative brain size, with results differing between taxonomic groups, and even within them. In primates for example, recent studies contradict one another over whether social or ecological factors are critical. A basic assumption of such studies is that with sufficiently large samples and appropriate analysis, robust correlations indicative of selection pressures on cognition will emerge. We carried out a comprehensive re-examination of correlates of primate brain size using two large comparative datasets and phylogenetic comparative methods. We found evidence in both datasets for associations between brain size and ecological variables (home range size, diet and activity period), but little evidence for an effect of social group size, a correlation which has previously formed the empirical basis of the Social Brain Hypothesis. However, reflecting divergent results in the literature, our results exhibited instability across datasets, even when they were matched for species composition and predictor variables. We identify several potential empirical and theoretical difficulties underlying this instability and suggest that these issues raise doubts about inferring cognitive selection pressures from behavioural correlates of brain size.

Nutritional status and the influence of TV consumption on female body size ideals in populations recently exposed to the media.

Television consumption influences perceptions of attractive female body size. However, cross-cultural research examining media influence on body ideals is typically confounded by differences in the availability of reliable and diverse foodstuffs. 112 participants were recruited from 3 Nicaraguan villages that differed in television consumption and nutritional status, such that the contribution of both factors could be revealed. Participants completed a female figure preference task, reported their television consumption, and responded to several measures assessing nutritional status. Communities with higher television consumption and/or higher nutritional status preferred thinner female bodies than communities with lower television consumption and/or lower nutritional status. Bayesian mixed models estimated the plausible range of effects for television consumption, nutritional status, and other relevant variables on individual preferences. The model explained all meaningful differences between our low-nutrition villages, and television consumption, after sex, was the most likely of these predictors to contribute to variation in preferences (probability mass >95% when modelling only variables with zero-order associations with preferences, but only 90% when modelling all possible predictors). In contrast, we found no likely link with nutritional status. We thus found evidence that where media access and nutritional status are confounded, media is the more likely predictor of body ideals.

General intelligence does not help us understand cognitive evolution.

Burkart et al. conflate the domain-specificity of cognitive processes with the statistical pattern of variance in behavioural measures that partly reflect those processes. General intelligence is a statistical abstraction, not a cognitive trait, and we argue that the former does not warrant inferences about the nature or evolution of the latter.

Transparency, usability, and reproducibility: Guiding principles for improving comparative databases using primates as examples.

Recent decades have seen rapid development of new analytical methods to investigate patterns of interspecific variation. Yet these cutting-edge statistical analyses often rely on data of questionable origin, varying accuracy, and weak comparability, which seem to have reduced the reproducibility of studies. It is time to improve the transparency of comparative data while also making these improved data more widely available. We, the authors, met to discuss how transparency, usability, and reproducibility of comparative data can best be achieved. We propose four guiding principles: 1) data identification with explicit operational definitions and complete descriptions of methods; 2) inclusion of metadata that capture key characteristics of the data, such as sample size, geographic coordinates, and nutrient availability (for example, captive versus wild animals); 3) documentation of the original reference for each datum; and 4) facilitation of effective interactions with the data via user friendly and transparent interfaces. We urge reviewers, editors, publishers, database developers and users, funding agencies, researchers publishing their primary data, and those performing comparative analyses to embrace these standards to increase the transparency, usability, and reproducibility of comparative studies.

Brain evolution and development: adaptation, allometry and constraint.

Phenotypic traits are products of two processes: evolution and development. But how do these processes combine to produce integrated phenotypes? Comparative studies identify consistent patterns of covariation, or allometries, between brain and body size, and between brain components, indicating the presence of significant constraints limiting independent evolution of separate parts. These constraints are poorly understood, but in principle could be either developmental or functional. The developmental constraints hypothesis suggests that individual components (brain and body size, or individual brain components) tend to evolve together because natural selection operates on relatively simple developmental mechanisms that affect the growth of all parts in a concerted manner. The functional constraints hypothesis suggests that correlated change reflects the action of selection on distributed functional systems connecting the different sub-components, predicting more complex patterns of mosaic change at the level of the functional systems and more complex genetic and developmental mechanisms. These hypotheses are not mutually exclusive but make different predictions. We review recent genetic and neurodevelopmental evidence, concluding that functional rather than developmental constraints are the main cause of the observed patterns.

Television exposure predicts body size ideals in rural Nicaragua.

Internalization of a thin ideal has been posited as a key risk factor in the development of pathological eating attitudes. Cross-culturally, studies have found a preference for heavier bodies in populations with reduced access to visual media compared to Western populations. As yet, however, there has been little attempt to control for confounding variables in order to isolate the effects of media exposure from other cultural and ecological factors. Here, we examined preferences for female body size in relation to television consumption in Nicaraguan men and women, while controlling for the potential confounding effects of other aspects of Westernization and hunger. We included an urban sample, a sample from a village with established television access, and a sample from a nearby village with very limited television access. The highest BMI preferences were found in the village with least media access, while the lowest BMI preferences were found in the urban sample. Data from the rural sample with established television access were intermediate between the two. Amongst rural women in particular, greater television consumption was a stronger predictor of body weight preferences than acculturation, education, hunger, or income. We also found some evidence for television consumption increasing the likelihood of women seeking to lose weight, possibly via body shape preferences. Overall, these results strongly implicate television access in establishing risk factors for body image disturbances in populations newly gaining access to Western media.

Microparasites and Placental Invasiveness in Eutherian Mammals.

Placental invasiveness-the number of maternal tissue layers separating fetal tissues from maternal blood-is variable across mammalian species. Although this diversity is likely to be functionally important, variation in placental invasiveness remains unexplained. Here we test the hypothesis that increased risk of transplacental transmission of pathogens from the mother to the fetus promotes the evolution of non-invasive placentation, the most likely derived condition in eutherian mammals. Specifically, we predict that non-invasive placentation is associated with increased microparasite species richness relative to more invasive placental types, based on the assumption that higher numbers of microparasites in a population reflects greater risk of transplacental transmission to fetuses. As predicted, higher bacteria species richness is associated with non-invasive placentation. Protozoa species richness, however, shows the opposite pattern. Because invasive placentae facilitate the transfer of maternal antibodies to the fetus, we propose that the ancestral condition of invasive placentation is retained under selection for protection of newborns from higher risk of postnatal protozoan infection. Hence, our findings suggest that a tradeoff exists between protection against bacterial infection prenatally and protozoan infection postnatally. Future studies are needed to investigate how maternal prevalence of infection and the relative pre- versus postnatal risk of fetal infection by different microparasite groups vary among mammalian hosts in relation to placental invasiveness.

Red clothing increases perceived dominance, aggression and anger.

The presence and intensity of red coloration correlate with male dominance and testosterone in a variety of animal species, and even artificial red stimuli can influence dominance interactions. In humans, red stimuli are perceived as more threatening and dominant than other colours, and wearing red increases the probability of winning sporting contests. We investigated whether red clothing biases the perception of aggression and dominance outside of competitive settings, and whether red influences decoding of emotional expressions. Participants rated digitally manipulated images of men for aggression and dominance and categorized the emotional state of these stimuli. Men were rated as more aggressive and more dominant when presented in red than when presented in either blue or grey. The effect on perceived aggression was found for male and female raters, but only male raters were sensitive to red as a signal of dominance. In a categorization test, images were significantly more often categorized as 'angry' when presented in the red condition, demonstrating that colour stimuli affect perceptions of emotions. This suggests that the colour red may be a cue used to predict propensity for dominance and aggression in human males.

Clean graphene electrodes on organic thin-film devices via orthogonal fluorinated chemistry.

Graphene is a promising flexible, highly transparent, and elementally abundant electrode for organic electronics. Typical methods utilized to transfer large-area films of graphene synthesized by chemical vapor deposition on metal catalysts are not compatible with organic thin-films, limiting the integration of graphene into organic optoelectronic devices. This article describes a graphene transfer process onto chemically sensitive organic semiconductor thin-films. The process incorporates an elastomeric stamp with a fluorinated polymer release layer that can be removed, post-transfer, via a fluorinated solvent; neither fluorinated material adversely affects the organic semiconductor materials. We used Raman spectroscopy, atomic force microscopy, and scanning electron microscopy to show that chemical vapor deposition graphene can be successfully transferred without inducing defects in the graphene film. To demonstrate our transfer method's compatibility with organic semiconductors, we fabricate three classes of organic thin-film devices: graphene field effect transistors without additional cleaning processes, transparent organic light-emitting diodes, and transparent small-molecule organic photovoltaic devices. These experiments demonstrate the potential of hybrid graphene/organic devices in which graphene is deposited directly onto underlying organic thin-film structures.

Primate comparative neuroscience using magnetic resonance imaging: promises and challenges.

Primate comparative anatomy is an established field that has made rich and substantial contributions to neuroscience. However, the labor-intensive techniques employed mean that most comparisons are often based on a small number of species, which limits the conclusions that can be drawn. In this review we explore how new developments in magnetic resonance imaging have the potential to apply comparative neuroscience to a much wider range of species, allowing it to realize an even greater potential. We discuss (1) new advances in the types of data that can be acquired, (2) novel methods for extracting meaningful measures from such data that can be compared between species, and (3) methods to analyse these measures within a phylogenetic framework. Together these developments will allow researchers to characterize the relationship between different brains, the ecological niche they occupy, and the behavior they produce in more detail than ever before.

Rapid evolution of the cerebellum in humans and other great apes.

Humans' unique cognitive abilities are usually attributed to a greatly expanded neocortex, which has been described as "the crowning achievement of evolution and the biological substrate of human mental prowess". The human cerebellum, however, contains four times more neurons than the neocortex and is attracting increasing attention for its wide range of cognitive functions. Using a method for detecting evolutionary rate changes along the branches of phylogenetic trees, we show that the cerebellum underwent rapid size increase throughout the evolution of apes, including humans, expanding significantly faster than predicted by the change in neocortex size. As a result, humans and other apes deviated significantly from the general evolutionary trend for neocortex and cerebellum to change in tandem, having significantly larger cerebella relative to neocortex size than other anthropoid primates. These results suggest that cerebellar specialization was a far more important component of human brain evolution than hitherto recognized and that technical intelligence was likely to have been at least as important as social intelligence in human cognitive evolution. Given the role of the cerebellum in sensory-motor control and in learning complex action sequences, cerebellar specialization is likely to have underpinned the evolution of humans' advanced technological capacities, which in turn may have been a preadaptation for language.