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The question as to why primates have evolved unusually large brains has received much attention, with many alternative proposals all supported by evidence. We review the main hypotheses, the assumptions they make and the evidence for and against them. Taking as our starting point the fact that every hypothesis has sound empirical evidence to support it, we argue that the hypotheses are best interpreted in terms of a framework of evolutionary causes (selection factors), consequences (evolutionary windows of opportunity) and constraints (usually physiological limitations requiring resolution if large brains are to evolve). Explanations for brain evolution in birds and mammals generally, and primates in particular, have to be seen against the backdrop of the challenges involved with the evolution of coordinated, cohesive, bonded social groups that require novel social behaviours for their resolution, together with the specialized cognition and neural substrates that underpin this. A crucial, but frequently overlooked, issue is that fact that the evolution of large brains required energetic, physiological and time budget constraints to be overcome. In some cases, this was reflected in the evolution of ‘smart foraging’ and technical intelligence, but in many cases required the evolution of behavioural competences (such as coalition formation) that required novel cognitive skills. These may all have been supported by a domain-general form of cognition that can be used in many different contexts. This article is part of the themed issue ‘Physiological determinants of social behaviour in animals’.

The social brain hypothesis proposes that large neocortex size evolved to support cognitively demanding social interactions. Accordingly, previous studies have observed that larger orbitofrontal and amygdala structures predict the size of an individual's social network. However, it remains uncertain how an individual's social connectedness reported by other people is associated with the social brain volume. In this study, we found that a greater in-degree network size, a measure of social ties identified by a subject's social connections rather than by the subject, significantly correlated with a larger regional volume of the orbitofrontal cortex, dorsomedial prefrontal cortex and lingual gyrus. By contrast, out-degree size, which is based on an individual's self-perceived connectedness, showed no associations. Meta-analytic reverse inference further revealed that regional volume pattern of in-degree size was specifically involved in social inference ability. These findings were possible because our dataset contained the social networks of an entire village, i.e. a global network. The results suggest that the in-degree aspect of social network size not only confirms the previously reported brain correlates of the social network but also shows an association in brain regions involved in the ability to infer other people's minds. This study provides insight into understanding how the social brain is uniquely associated with sociocentric measures derived from a global network.

An important element in understanding the evolution of human sociality is to understand the factors that governed the evolution of social organisation in our closest living relatives. The ‘social brain hypothesis’ proposes that the complex social world of primates is especially cognitively demanding, and that this imposed intense selection pressure for increasingly large brains. Group size in primates is strongly correlated with brain size but exactly what makes larger groups more ‘socially complex’ than smaller groups is still poorly understood. Chimpanzees and Gorillas are among our closest living relatives and they exhibit remarkable diversity in various aspects of their social organisation both within and across species. They are thus excellent species in which to investigate patterns of sociality and social complexity in primates, and to inform models of human social evolution. We propose a program of research that will provide the first systematic insight into how social structure differs in small, medium and large groups of Chimpanzees and Gorillas, to explore what makes larger groups more socially complex than smaller groups. Further, we propose to investigate how these variations in social structure in different size groups are affected by the social organisation of the species. Chimpanzees live in a fluid fission-fusion social system, whereas Gorillas have more stable, cohesive groups. To carry out both the within and between species comparisons, we advocate use of social network analysis, which provides a novel way to describe and compare social structure. This program of research will therefore lead to a new, systematic way of comparing social complexity across species, something that is lacking in current comparative studies of social structure. Considering that hominins were likely characterized by a fission-fusion social structure, comparing the social complexity of such systems with that of more stable groups may yield valuable insights into the evolution of human sociality.

The ‘social brain hypothesis' proposes a causal link between social complexity and either brain size or the size of key brain parts known to be involved in cognitive processing and decision-making. While previous work has focused on comparisons between species, how social complexity affects plasticity in brain morphology at the intraspecific level remains mostly unexplored. A suitable study model is the mutualist ‘cleaner’ fish Labroides dimidiatus , a species that removes ectoparasites from a variety of ‘client’ fishes in iterative social interactions. Here, we report a positive relationship between the local density of cleaners, as a proxy of both intra- and interspecific sociality, and the size of the cleaner's brain parts suggested to be associated with cognitive functions, such as the diencephalon and telencephalon (that together form the forebrain). In contrast, the size of the mesencephalon, rhombencephalon, and brain stem, assumed more basal in function, were independent of local fish densities. Selective enlargement of brain parts, that is mosaic brain adjustment, appears to be driven by population density in cleaner fish.

The social brain hypothesis (an explanation for the evolution of brain size in primates) predicts that humans typically cannot maintain more than 150 relationships at any one time. The constraint is partly cognitive (ultimately determined by some aspect of brain volume) and partly one of time. Friendships (but not necessarily kin relationships) are maintained by investing time in them, and failure to do so results in an inexorable deterioration in the quality of a relationship. The Internet, and in particular the rise of social networking sites (SNSs), raises the possibility that digital media might allow us to circumvent some or all of these constraints. This allows us to test the importance of these constraints in limiting human sociality. Although the recency of SNSs means that there have been relatively few studies, those that are available suggest that, in general, the ability to broadcast to many individuals at once, and the possibilities this provides in terms of continuously updating our understanding of network members’ behaviour and thoughts, do not allow larger networks to be maintained. This may be because only relatively weak quality relationships can be maintained without face-to-face interaction.

Cooperation becomes more difficult as a group becomes larger, but it is unclear where it will break down. Here, we study group size within well-functioning social-ecological systems. We consider centuries-old evidence from hundreds of communities in the Alps that harvested common property resources. Results show that the average group size remained remarkably stable over about six centuries, in contrast to a general increase in the regional population. The population more than doubled, but although single groups experienced fluctuations over time, the average group size remained stable. Ecological factors, such as managing forest instead of pasture land, played a minor role in determining group size. The evidence instead indicates that factors related to social interactions had a significant role in determining group size. We discuss possible interpretations of the findings based on constraints in individual cognition and obstacles in collective decision making.

Sociality is classified as one of the major transitions in the evolution of complexity and much effort has been dedicated to understanding what traits predispose lineages to sociality. Conversely, studies addressing the role of sociality in brain evolution (e.g., the social brain hypothesis) have not focused on particular traits and instead relied largely on measurements of relative brain composition. Hymenoptera range from solitary to advanced social species, providing enticing comparisons for studying sociality and neural trait evolution. Here we argue that measuring the role of sociality in brain evolution will benefit from attending to recent advances in neuroethology and adopting existing phylogenetic comparative methods employed in analysis of non-neural traits. Such analyses should rely on traits we expect to vary at the taxonomic level used in comparative analyses and include phylogenetic structure. We outline the limits of brain size and volumetric interpretation and advocate closer attention to trait stability and plasticity at different levels of organization. We propose neural traits measured at the cellular, circuit, and molecular levels will serve as more robust variables for evolutionary analyses. We include examples of particular traits and specific clades that are well-suited to answer questions about the role of sociality in nervous system evolution.

Social interactions are mediated by recognition systems, meaning that the cognitive abilities or phenotypic diversity that facilitate recognition may be common targets of social selection. Recognition occurs when a receiver compares the phenotypes produced by a sender with a template. Coevolution between sender and receiver traits has been empirically reported in multiple species and sensory modalities, though the dynamics and relative exaggeration of traits from senders versus receivers have received little attention. Here, we present a coevolutionary dynamic model that examines the conditions under which senders and receivers should invest effort in facilitating individual recognition. The model predicts coevolution of sender and receiver traits, with the equilibrium investment dependent on the relative costs of signal production versus cognition. In order for recognition to evolve, initial sender and receiver trait values must be above a threshold, suggesting that recognition requires some degree of pre-existing diversity and cognitive abilities. The analysis of selection gradients demonstrates that the strength of selection on sender signals and receiver cognition is strongest when the trait values are furthest from the optima. The model provides new insights into the expected strength and dynamics of selection during the origin and elaboration of individual recognition, an important feature of social cognition in many taxa. This article is part of the theme issue ‘Signal detection theory in recognition systems: from evolving models to experimental tests’.

Human language and social cognition are two key disciplines that have traditionally been studied as separate domains. Nonetheless, an emerging view suggests an alternative perspective. Drawing on the theoretical underpinnings of the social brain hypothesis (thesis of the evolution of brain size and intelligence), the social complexity hypothesis (thesis of the evolution of communication), and empirical research from comparative animal behavior, human social behavior, language acquisition in children, social cognitive neuroscience, and the cognitive neuroscience of language, it is argued that social cognition and language are two significantly interconnected capacities of the human species. Here, evidence in support of this view reviews (1) recent developmental studies on language learning in infants and young children, pointing to the important crucial benefits associated with social stimulation for youngsters, including the quality and quantity of incoming linguistic information, dyadic infant/child-to-parent non-verbal and verbal interactions, and other important social cues integral for facilitating language learning and social bonding; (2) studies of the adult human brain, suggesting a high degree of specialization for sociolinguistic information processing, memory retrieval, and comprehension, suggesting that the function of these neural areas may connect social cognition with language and social bonding; (3) developmental deficits in language and social cognition, including autism spectrum disorder (ASD), illustrating a unique developmental profile, further linking language, social cognition, and social bonding; and (4) neural biomarkers that may help to identify early developmental disorders of language and social cognition. In effect, the social brain and social complexity hypotheses may jointly help to describe how neurotypical children and adults acquire language, why autistic children and adults exhibit simultaneous deficits in language and social cognition, and why nonhuman primates and other organisms with significant computational capacities cannot learn language. But perhaps most critically, the following article argues that this and related research will allow scientists to generate a holistic profile and deeper understanding of the healthy adult social brain while developing more innovative and effective diagnoses, prognoses, and treatments for maladies and deficits also associated with the social brain.

Sociality is primarily a coordination problem. However, the social (or communication) complexity hypothesis suggests that the kinds of information that can be acquired and processed may limit the size and/or complexity of social groups that a species can maintain. We use an agent-based model to test the hypothesis that the complexity of information processed influences the computational demands involved. We show that successive increases in the kinds of information processed allow organisms to break through the glass ceilings that otherwise limit the size of social groups: larger groups can only be achieved at the cost of more sophisticated kinds of information processing that are disadvantageous when optimal group size is small. These results simultaneously support both the social brain and the social complexity hypotheses.