Dunbar's number: group size and brain physiology in humans reexamined

Popular academic ideas linking physiological adaptations to social behaviors are spreading disconcertingly into wider societal contexts. In this article, we note our skepticism with one particularly popular—in our view, problematic—supposed causal correlation between neocortex size and social group size. The resulting Dunbar's Number, as it has come to be called, has been statistically tested against observed group size in different primate species. Although there may be reason to doubt the Dunbar's Number hypothesis among nonhuman primate species, we restrict ourselves here to the application of such an explanatory hypothesis to human, culture-manipulating populations. Human information process management, we argue, cannot be understood as a simple product of brain physiology. Cross-cultural comparison of not only group size but also relationship-reckoning systems like kinship terminologies suggests that although neocortices are undoubtedly crucial to human behavior, they cannot be given such primacy in explaining complex group composition, formation, or management.     

The evolution of the social brain: anthropoid primates contrast with other vertebrates

The social brain hypothesis argues that large brains have arisen over evolutionary time as a response to the social and ecological conflicts inherent in group living. We test predictions arising from the hypothesis using comparative data from birds and four mammalian orders (Carnivora, Artiodactyla, Chiroptera and Primates) and show that, across all non-primate taxa, relative brain size is principally related to pairbonding, but with enduring stable relationships in primates. We argue that this reflects the cognitive demands of the behavioural coordination and synchrony that is necessary to maintain stable pairbonded relationships. However, primates differ from the other taxa in that they also exhibit a strong effect of group size on brain size. We use data from two behavioural indices of social intensity (enduring bonds between group members and time devoted to social activities) to show that primate relationships differ significantly from those of other taxa. We suggest that, among vertebrates in general, pairbonding represents a qualitative shift from loose aggregations of individuals to complex negotiated relationships, and that these bonded relationships have been generalized to all social partners in only a few taxa (such as anthropoid primates).     

Asymmetry and Dimensions of Relationship Quality in the Japanese Macaque (<Emphasis Type="Italic">Macaca fuscata yakui</Emphasis>)

Cords and Aureli (2000) proposed that relationship quality can be described by three components, i.e., value, security, and compatibility, based on the benefits social partners receive from their relationship and on how likely it is for them to maintain a stable friendly relationship over time. We aimed to examine whether this 3-components structure can describe social relationships and to investigate the degree of asymmetry of social relationships. We used the Japanese macaque as our model species, as group members may form strong social relationships with one another. We collected 359.2 h of focal samples, on 21 monkeys, and ran a principal component analysis (PCA) on dyadic scores for 9 variables measuring social relationships, e.g., grooming or aggression. This PCA gave 3 components. However, a second PCA run on scores per individual, i.e. for each variable and dyad we obtained 1 score for the actor and 1 for the receiver of behavior, gave a 5-component structure. We interpreted this result as evidence of the asymmetric nature of social relationships, in terms of the frequency and type of behavior exchanged between social partners, in the Japanese macaque. This interpretation was confirmed by the low correlation coefficients between behaviors given and received within a dyad. Overall these results provide mixed support for the 3-components structure predicted by Cords and Aureli (2000). They also show that social relationships may be largely asymmetric and that this asymmetry should be considered in studies on social behavior.     

Allometry of human fertility and energy use

The flux of energy and materials constrains all organisms, and allometric relationships between rates of energy consumption and other biological rates are manifest at many levels of biological organization. Although human ecology is unusual in many respects, human populations also face energetic constraints. Here we present a model relating fertility rates to per capita energy consumption rates in contemporary human nations. Fertility declines as energy consumption increases with a scaling exponent of ?1/3 as predicted by allometric theory. The decline may be explained by parental trade‐offs between the number of children and the energetic investment in each child. We hypothesize that the ?1/3 exponent results from the scaling properties of the networked infrastructure that delivers energy to consumers. This allometric analysis of human fertility offers a framework for understanding the demographic transition to smaller family sizes, with implications for human population growth, resource use and sustainability.     

Neuropeptidergic regulation of affiliative behavior and social bonding in animals

Social relationships are essential for maintaining human mental health, yet little is known about the brain mechanisms involved in the development and maintenance of social bonds. Animal models are powerful tools for investigating the neurobiological mechanisms regulating the cognitive processes leading to the development of social relationships and for potentially extending our understanding of the human condition. In this review, we discuss the roles of the neuropeptides oxytocin and vasopressin in the regulation of social bonding as well as related social behaviors which culminate in the formation of social relationships in animal models. The formation of social bonds is a hierarchical process involving social motivation and approach, the processing of social stimuli and formation of social memories, and the social attachment itself. Oxytocin and vasopressin have been implicated in each of these processes. Specifically, these peptides facilitate social affiliation and parental nurturing behavior, are essential for social recognition in rodents, and are involved in the formation of selective mother-infant bonds in sheep and pair bonds in monogamous voles. The convergence of evidence from these animal studies makes oxytocin and vasopressin attractive candidates for the neural modulation of human social relationships as well as potential therapeutic targets for the treatment of psychiatric disorders associated with disruptions in social behavior, including autism.     

Rank Differences in Ecological Behavior: A Comparative Study of Patas Monkeys (Erythrocebus patas) and Vervets (Cercopithecus aethiops)

One of the central dichotomies in primate behavior is between species in which there are relationships among females that include stable dominance relationships, and those in which the relationships include weak or unstable dominance relationships. This dichotomy has been attributed to differences in food resources, with stable dominance hierarchies occurring in species that feed on usurpable foods. We compared rank-related differences in nonagonistic behaviors considered to be tightly linked to ecology in broadly sympatric vervets (Cercopithecus aethiops) and patas monkeys (Erythrocebus patas), two closely related cercopithecines that are exemplars of this dichotomy, with the expectation that vervets would exhibit stronger rank differences than patas monkeys in these behaviors. Overall, rank explained more than twice as much variation among vervets as among patas monkeys in ranging behavior, activity budgets, and diet. Vervets did not, however, exhibit stronger rank differences when they used Acacia xanthophloea habitat, in which foods are more usurpable, compared to Acacia drepanolobium habitat, in which foods are less usurpable. In Acacia drepanolobium habitat, to which patas are restricted, higher-ranking vervets converged in behavior with patas monkeys to a greater extent than lower-ranking vervets, suggesting that social constraints interfere with the foraging efficiency of lower-ranking vervets even in habitats in which there are fewer opportunities to usurp foods.     

Clique Size and Network Characteristics in Hyperlink Cinema

Hyperlink cinema is an emergent film genre that seeks to push the boundaries of the medium in order to mirror contemporary life in the globalized community. Films in the genre thus create an interacting network across space and time in such a way as to suggest that people’s lives can intersect on scales that would not have been possible without modern technologies of travel and communication. This allows us to test the hypothesis that new kinds of media might permit us to break through the natural cognitive constraints that limit the number and quality of social relationships we can manage in the conventional face-to-face world. We used network analysis to test this hypothesis with data from 12 hyperlink films, using 10 motion pictures from a more conventional film genre as a control. We found few differences between hyperlink cinema films and the control genre, and few differences between hyperlink cinema films and either the real world or classical drama (e.g., Shakespeare’s plays). Conversation group size seems to be especially resilient to alteration. It seems that, despite many efficiency advantages, modern media are unable to circumvent the constraints imposed by our evolved psychology.     

Social cognition on the Internet: testing constraints on social network size

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.     

Dynamical aspects of behavior generation under constraints

Dynamic adaptation is a key feature of brains helping to maintain the quality of their performance in the face of increasingly difficult constraints. How to achieve high-quality performance under demanding real-time conditions is an important question in the study of cognitive behaviors. Animals and humans are embedded in and constrained by their environments. Our goal is to improve the understanding of the dynamics of the interacting brain–environment system by studying human behaviors when completing constrained tasks and by modeling the observed behavior. In this article we present results of experiments with humans performing tasks on the computer under variable time and resource constraints. We compare various models of behavior generation in order to describe the observed human performance. Finally we speculate on mechanisms how chaotic neurodynamics can contribute to the generation of flexible human behaviors under constraints.     

Social context, stress, and plasticity of aging

Positive social contact is an important factor in healthy aging, but our understanding of how social interactions influence senescence is incomplete. As life expectancy continues to increase because of reduced death rates among elderly, the beneficial role of social relationships is emerging as a cross-cutting theme in research on aging and healthspan. There is a need to improve knowledge on how behavior shapes, and is shaped by, the social environment, as well as needs to identify and study biological mechanisms that can translate differences in the social aspects of behavioral efforts, relationships, and stress reactivity (the general physiological and behavioral response-pattern to harmful, dangerous or unpleasant situations) into variation in aging. Honey bees (Apis mellifera) provide a genetic model in sociobiology, behavioral neuroscience, and gerontology that is uniquely sensitive to social exchange. Different behavioral contact between these social insects can shorten or extend lifespan more than 10-fold, and some aspects of their senescence are reversed by social cues that trigger aged individuals to express youthful repertoires of behavior. Here, I summarize how variation in social interactions contributes to this plasticity of aging and explain how beneficial and detrimental roles of social relationships can be traced from environmental and biological effects on honey bee physiology and behavior, to the expression of recovery-related plasticity, stress reactivity, and survival during old age. This system provides intriguing opportunities for research on aging.     

Bridging the bonding gap: the transition from primates to humans

Primate societies are characterized by bonded social relationships of a kind that are rare in other mammal taxa. These bonded relationships, which provide the basis for coalitions, are underpinned by an endorphin mechanism mediated by social grooming. However, bonded relationships of this kind impose constraints on the size of social groups that are possible. When ecological pressures have demanded larger groups, primates have had to evolve new mechanisms to facilitate bonding. This has involved increasing the size of vocal and visual communication repertoires, increasing the time devoted to social interaction and developing a capacity to manage two-tier social relationships (strong and weak ties). I consider the implications of these constraints for the evolution of human social communities and argue that laughter was an early evolutionary innovation that helped bridge the bonding gap between the group sizes characteristic of chimpanzees and australopithecines and those in later hominins.     

Oxytocin,testosterone, and human social cognition

I describe an integrative social‐evolutionary model for the adaptive significance of the human oxytocinergic system. The model is based on a role for this hormone in the generation and maintenance of social familiarity and affiliation across five homologous, functionally similar, and sequentially co‐opted contexts: mothers with offspring, female and male mates, kin groups, individuals with reciprocity partners, and individuals within cooperating and competing social groups defined by culture. In each situation, oxytocin motivates, mediates and rewards the cognitive and behavioural processes that underlie the formation and dynamics of a more or less stable social group, and promotes a relationship between two or more individuals. Such relationships may be positive (eliciting neurological reward, reducing anxiety and thus indicating fitness‐enhancing effects), or negative (increasing anxiety and distress, and thus motivating attempts to alleviate a problematic, fitness‐reducing social situation). I also present evidence that testosterone exhibits opposite effects from oxytocin on diverse aspects of cognition and behaviour, most generally by favouring self‐oriented, asocial and antisocial behaviours. I apply this model for effects of oxytocin and testosterone to understanding human psychological disorders centrally involving social behaviour. Reduced oxytocin and higher testosterone levels have been associated with under‐developed social cognition, especially in autism. By contrast, some combination of oxytocin increased above normal levels, and lower testosterone, has been reported in a notable number of studies of schizophrenia, bipolar disorder and depression, and, in some cases, higher oxytocin involves maladaptively ‘hyper‐developed’ social cognition in these conditions. This pattern of findings suggests that human social cognition and behaviour are structured, in part, by joint and opposing effects of oxytocin and testosterone, and that extremes of such joint effects partially mediate risks and phenotypes of autism and psychotic‐affective conditions. These considerations have direct implications for the development of therapies for alleviating disorders of social cognition, and for understanding how such disorders are associated with the evolution of human cognitive‐affective architecture.     

Culture,biology, and human behavior

Social scientists have not integrated relevant knowledge from the biological sciences into their explanations of human behavior. This failure is due to a longstanding antireductionistic bias against the natural sciences, which follows on a commitment to the view that social facts must be explained by social laws. This belief has led many social scientists into the error of reifying abstract analytical constructs into entities that possess powers of agency. It has also led to a false nature-culture dichotomy that effectively undermines the place of biology in social scientific explanation. Following the principles of methodological individualism, we show how behavioral explanations supported by data and theory from the neurosciences can be used to correct the errors of reificationist thinking in the social sciences. We outline a mechanistic approach to the explanation of human behavior with the hope that the biological sciences will begin to find greater acceptance among social scientists.     

Loss of estrus in human evolution: Too many answers,too few questions

Models addressing the importance of “loss of estrus” in human evolution assume that, as part of a general trend among higher primates, endogenous hormonal fluctuations have less influence on human female sexuality than cognitive and socioenvironmental factors. The diversity of reproductive patterns among primate species is not satisfactorily explained as the outcome of evolutionary trends along dimensions such as brain enlargement, behavioral flexibility, or relative independence of behavior from physiology. Rather, the role of hormones and other factors must be viewed in the context of species' life history and ecological constraints. Human studies on the relationship between the menstrual cycle and sexual behavior have been limited to Western women in industrialized societies, which may not reveal evolved behavioral-physiological patterns. Furthermore, available studies have yielded inconsistent results. No single pattern emerges that can be said to characterize the human female, and no conclusion can be reached regarding the relationship between cyclic hormonal fluctuations and sexual behavior and, thus, whether human ovulation is concealed. Future studies are needed that are methodologically improved and systematically document the interaction among ecological, subsistence, social, and physiological variables.     

Genetic and environmental influences on human psychological differences

Psychological researchers typically distinguish five major domains of individual differences in human behavior: cognitive abilities, personality, social attitudes, psychological interests, and psychopathology (Lubinski, 2000). In this article we: discuss a number of methodological errors commonly found in research on human individual differences; introduce a broad framework for interpreting findings from contemporary behavioral genetic studies; briefly outline the basic quantitative methods used in human behavioral genetic research; review the major criticisms of behavior genetic designs, with particular emphasis on the twin and adoption methods; describe the major or dominant theoretical scheme in each domain; and review behavioral genetic findings in all five domains. We conclude that there is now strong evidence that virtually all individual psychological differences, when reliably measured, are moderately to substantially heritable.     

Advances in Applied Zoo Animal Welfare Science

ABSTRACT

Nonhuman animal welfare science is the scientific study of the welfare state of animals that attempts to make inferences about how animals feel from their behavior, endocrine function, and/or signs of physical health. These welfare measurements are applicable within zoos yet inherently more complex than in farms and laboratories. This complexity is due to the vast number of species housed, lack of fundamental biological information, and relatively lower sample sizes and levels of experimental control. This article summarizes the invited presentations on the topic of “Advances in Applied Animal Welfare Science,” given at the Fourth Global Animal Welfare Congress held jointly by the Detroit Zoological Society and the World Association of Zoos and Aquariums in 2017. The article focuses on current trends in research on zoo animal welfare under the following themes: (a) human–animal interactions and relationships, (b) anticipatory behavior, (c) cognitive enrichment, (d) behavioral biology, and (e) reproductive and population management. It highlights areas in which further advancements in zoo animal welfare science are needed and the challenges that may be faced in doing so.     

Baboon (Papio anubis) social complexity--a network approach

Although many studies have analyzed the causes and consequences of social relationships, few studies have explicitly assessed how measures of social relationships are affected by the choice of behaviors used to quantify them. The use of many behaviors to measure social relationships in primates has long been advocated, but it was analytically difficult to implement this framework into primatological work. However, recent advances in social network analysis (SNA) now allow the comparison of multiple networks created from different behaviors. Here we use our database of baboon social behavior (Papio anubis, Gashaka Gumti National Park, Nigeria) to investigate (i) to what extent social networks created from different behaviors overlap, (ii) to what extent individuals occupy similar social positions in these networks and (iii) how sex affects social network position in this population of baboons. We used data on grooming, aggression, displacement, mounting and presenting, which were collected over a 15-month period. We calculated network parameters separately for each behavior. Networks based on displacement, mounting and presenting were very similar to each other, whereas grooming and aggression networks differed both from each other and from mounting, displacement and presenting networks. Overall, individual network positions were strongly affected by sex. Individuals central in one network tended to be central in most other networks as well, whereas other measures such as clustering coefficient were found to vary depending on the behavior analyzed. Thus, our results suggest that a baboon's social environment is best described by a multiplex network based on affiliative, aggressive and sexual behavior. Modern SNA provides a number of useful tools that will help us to better understand animals' social environment. We also discuss potential caveats related to their use.     

Social cognitive evolution in captive foxes is a correlated by-product of experimental domestication

Dogs have an unusual ability for reading human communicative gestures (e.g., pointing) in comparison to either nonhuman primates (including chimpanzees) or wolves . Although this unusual communicative ability seems to have evolved during domestication , it is unclear whether this evolution occurred as a result of direct selection for this ability, as previously hypothesized , or as a correlated by-product of selection against fear and aggression toward humans--as is the case with a number of morphological and physiological changes associated with domestication . We show here that fox kits from an experimental population selectively bred over 45 years to approach humans fearlessly and nonaggressively (i.e., experimentally domesticated) are not only as skillful as dog puppies in using human gestures but are also more skilled than fox kits from a second, control population not bred for tame behavior (critically, neither population of foxes was ever bred or tested for their ability to use human gestures) . These results suggest that sociocognitive evolution has occurred in the experimental foxes, and possibly domestic dogs, as a correlated by-product of selection on systems mediating fear and aggression, and it is likely the observed social cognitive evolution did not require direct selection for improved social cognitive ability.     

Seasonal Changes in Male Associative Behavior and Subgrouping of Alouatta palliata on an Island

Howler groups are usually spatially cohesive and stable in composition; however, more flexible grouping patterns occur in some social groups. We analyzed the associative and subgrouping patterns of males living in a group with fission-fusion social organization. Based on information from previous studies on Alouatta palliata and other primates and in the current socioecological models, we established initial predictions on the variations in male behavior according to several socioecological factors. We studied associative behavior via scan sampling at 15-min intervals to register the identity of males in the subgroups and the presence and number of receptive females. We calculated an association index that was then transformed into a measure of association strength. We found individual association trends, as well as important seasonal differences in the subgrouping patterns of males. During the dry season the presence of many receptive females resulted in reduced levels of association, and therefore fewer males per subgroup. The scenario changed during the wet season, when males grouped together significantly more and kinship relationships were a major determinant for individual association preferences.