Peptides and primate personality: Central and peripheral oxytocin and vasopressin levels and social behavior in two baboon species (Papio hamadryas and Papio anubis).

The neurohormones oxytocin (OT) and arginine vasopressin (AVP) are involved in social behaviors and psychiatric conditions. However, more research on nonhuman primates with complex social behaviors is needed. We studied two closely-related primate species with divergent social and mating systems; hamadryas baboons (Papio hamadryas, n=38 individuals) and anubis baboons (Papio anubis, n=46). We measured OT in cerebrospinal fluid (CSF, n=75), plasma (n=81) and urine (n=77), and AVP in CSF (n=45), and we collected over 250 hours of focal behavioral observations. Using Bayesian multivariate models, we found no clear species difference in hormone levels; the strongest support was for hamadryas having higher CSF OT levels than anubis (posterior probability [PP] for females = 0.75, males = 0.84). Looking at nine specific behaviors, OT was associated with affiliative behaviors (approach, proximity, grooming, PP ∼ 0.85 - 1.00), albeit inconsistently across sources of measurement (CSF, plasma, and urine, which were uncorrelated with each other). Most behaviors had low repeatability (R ∼ 0 - 0.2), i.e. they did not exhibit stable between-individual differences (or "personality"), and different behaviors did not neatly coalesce into higher-order factors (or "behavioral syndromes"), which cautions against the use of aggregate behavioral measures and highlights the need to establish stable behavioral profiles when testing associations with baseline hormone levels. In sum, we found some associations between peptides and social behavior, but also many null results, OT levels from different sources were uncorrelated, and our behavioral measures did not indicate clear individual differences in sociability.

Primate social organization evolved from a flexible pair-living ancestor.

Explaining the evolution of primate social organization has been fundamental to understand human sociality and social evolution more broadly. It has often been suggested that the ancestor of all primates was solitary and that other forms of social organization evolved later, with transitions being driven by various life history traits and ecological factors. However, recent research showed that many understudied primate species previously assumed to be solitary actually live in pairs, and intraspecific variation in social organization is common. We built a detailed database from primary field studies quantifying the number of social units expressing different social organizations in each population. We used Bayesian phylogenetic models to infer the probability of each social organization, conditional on several socioecological and life history predictors. Here, we show that when intraspecific variation is accounted for, the ancestral social organization of primates was inferred to be variable, with the most common social organization being pair-living but with approximately 10 to 20% of social units of the ancestral population deviating from this pattern by being solitary living. Body size and activity patterns had large effects on transitions between types of social organizations. As in other mammalian clades, pair-living is closely linked to small body size and likely more common in ancestral species. Our results challenge the assumption that ancestral primates were solitary and that pair-living evolved afterward emphasizing the importance of focusing on field data and accounting for intraspecific variation, providing a flexible statistical framework for doing so.

The social evolution of individual differences: Future directions for a comparative science of personality in social behavior.

Personality is essential for understanding the evolution of cooperation and conflict in behavior. However, personality science remains disconnected from the field of social evolution, limiting our ability to explain how personality and plasticity shape phenotypic adaptation in social behavior. Researchers also lack an integrative framework for comparing personality in the contextualized and multifaceted behaviors central to social interactions among humans and other animals. Here we address these challenges by developing a social evolutionary approach to personality, synthesizing theory, methods, and organizing questions in the study of individuality and sociality in behavior. We critically review current measurement practices and introduce social reaction norm models for comparative research on the evolution of personality in social environments. These models demonstrate that social plasticity affects the heritable variance of personality, and that individual differences in social plasticity can further modify the rate and direction of adaptive social evolution. Future empirical studies of frequency- and density-dependent social selection on personality are crucial for further developing this framework and testing adaptive theory of social niche specialization.

Life-history tradeoffs in a historical population (1896-1939) undergoing rapid fertility decline: Costs of reproduction?

Evolutionary demographers often invoke tradeoffs between reproduction and survival to explain reductions in fertility during demographic transitions. The evidence for such tradeoffs in humans has been mixed, partly because tradeoffs may be masked by individual differences in quality or access to resources. Unmasking tradeoffs despite such phenotypic correlations requires sophisticated statistical analyses that account for endogeneity among variables and individual differences in access to resources. Here we tested for costs of reproduction using N=13,663 birth records from the maternity hospital in Basel, Switzerland, 1896-1939, a period characterized by rapid fertility declines. We predicted that higher parity is associated with worse maternal and offspring condition at the time of birth, adjusting for age and a variety of covariates. We used Bayesian multivariate, multilevel models to simultaneously analyze multiple related outcomes while accounting for endogeneity, appropriately modeling non-linear effects, dealing with hierarchical data structures, and effectively imputing missing data. Despite all these efforts, we found virtually no evidence for costs of reproduction. Instead, women with better access to resources had fewer children. Barring limitations of the data, these results are consistent with demographic transitions reflecting women's investment in their own embodied capital and/or the adoption of maladaptive low-fertility norms by elites.

Performance of Deaf Participants in an Abstract Visual Grammar Learning Task at Multiple Formal Levels: Evaluating the Auditory Scaffolding Hypothesis.

Previous research has hypothesized that human sequential processing may be dependent upon hearing experience (the "auditory scaffolding hypothesis"), predicting that sequential rule learning abilities should be hindered by congenital deafness. To test this hypothesis, we compared deaf signer and hearing individuals' ability to acquire rules of different computational complexity in a visual artificial grammar learning task using sequential stimuli. As a group, deaf participants succeeded at all levels of the task; Bayesian analysis indicates that they successfully acquired each of several target grammars at ascending levels of the formal language hierarchy. Overall, these results do not support the auditory scaffolding hypothesis. However, age- and education-matched hearing participants did outperform deaf participants in two out of three tested grammars. We suggest that this difference may be related to verbal recoding strategies in the two groups. Any verbal recoding strategies used by the deaf signers would be less effective because they would have to use the same visual channel required for the experimental task.

Social animal models for quantifying plasticity, assortment, and selection on interacting phenotypes.

Both assortment and plasticity can facilitate social evolution, as each may generate heritable associations between the phenotypes and fitness of individuals and their social partners. However, it currently remains difficult to empirically disentangle these distinct mechanisms in the wild, particularly for complex and environmentally responsive phenotypes subject to measurement error. To address this challenge, we extend the widely used animal model to facilitate unbiased estimation of plasticity, assortment and selection on social traits, for both phenotypic and quantitative genetic (QG) analysis. Our social animal models (SAMs) estimate key evolutionary parameters for the latent reaction norms underlying repeatable patterns of phenotypic interaction across social environments. As a consequence of this approach, SAMs avoid inferential biases caused by various forms of measurement error in the raw phenotypic associations between social partners. We conducted a simulation study to demonstrate the application of SAMs and investigate their performance for both phenotypic and QG analyses. With sufficient repeated measurements, we found desirably high power, low bias and low uncertainty across model parameters using modest sample and effect sizes, leading to robust predictions of selection and adaptation. Our results suggest that SAMs will readily enhance social evolutionary research on a variety of phenotypes in the wild. We provide detailed coding tutorials and worked examples for implementing SAMs in the Stan statistical programming language.

Brain size and neuron numbers drive differences in yawn duration across mammals and birds.

Recent studies indicate that yawning evolved as a brain cooling mechanism. Given that larger brains have greater thermolytic needs and brain temperature is determined in part by heat production from neuronal activity, it was hypothesized that animals with larger brains and more neurons would yawn longer to produce comparable cooling effects. To test this, we performed the largest study on yawning ever conducted, analyzing 1291 yawns from 101 species (55 mammals; 46 birds). Phylogenetically controlled analyses revealed robust positive correlations between yawn duration and (1) brain mass, (2) total neuron number, and (3) cortical/pallial neuron number in both mammals and birds, which cannot be attributed solely to allometric scaling rules. These relationships were similar across clades, though mammals exhibited considerably longer yawns than birds of comparable brain and body mass. These findings provide further evidence suggesting that yawning is a thermoregulatory adaptation that has been conserved across amniote evolution.

A comparative approach to affect and cooperation.

A central premise of the science of comparative affect is that we can best learn about the causes and consequences of affect by comparing affective phenomena across a variety of species, including humans. We take as a given that affect is widely shared across animals, but a key challenge is to accurately represent each species' affective experience. A common approach in the comparative study of behavior and cognition is to develop standardized experimental paradigms that can be used across species, with the assumption that if the same task is being used, we can directly compare behavioral responses. This experimental approach rests on two underlying assumptions: first, that different species' perception of and affective response to these paradigms are the same; and second, that behavioral and physiological (including endocrine and neural) responses to these paradigms are homologous; if either of these assumptions is not true, then the comparison becomes much less straightforward. Our goal in the present paper is to summarize the dominant paradigms that have been used for such comparative research, with a particular focus on paradigms common in the cooperation literature, and to critically discuss dominant assumptions about what affective states these tasks can or should measure. We then consider the advantages and drawbacks of this experimental method, and consider alternatives that may improve our understanding. We hope that this will help scholars recognize and avoid pitfalls inherent in studying affect, and stimulate them to create novel, ecologically relevant paradigms for examining affect across the animal kingdom.

Negative emotional contagion and cognitive bias in common ravens (Corvus corax).

Emotional contagion is described as an emotional state matching between subjects, and has been suggested to facilitate communication and coordination in complex social groups. Empirical studies typically focus on the measurement of behavioral contagion and emotional arousal, yet, while highly important, such an approach often disregards an additional evaluation of the underlying emotional valence. Here, we studied emotional contagion in ravens by applying a judgment bias paradigm to assess emotional valence. We experimentally manipulated positive and negative affective states in demonstrator ravens, to which they responded with increased attention and interest in the positive condition, as well as increased redirected behavior and a left-eye lateralization in the negative condition. During this emotion manipulation, another raven observed the demonstrator's behavior, and we used a bias paradigm to assess the emotional valence of the observer to determine whether emotional contagion had occurred. Observers showed a pessimism bias toward the presented ambiguous stimuli after perceiving demonstrators in a negative state, indicating emotional state matching based on the demonstrators' behavioral cues and confirming our prediction of negative emotional contagion. We did not find any judgment bias in the positive condition. This result critically expands upon observational studies of contagious play in ravens, providing experimental evidence that emotional contagion is present not only in mammalian but also in avian species. Importantly, this finding also acts as a stepping stone toward understanding the evolution of empathy, as this essential social skill may have emerged across these taxa in response to similar socioecological challenges.

Artificial Grammar Learning Capabilities in an Abstract Visual Task Match Requirements for Linguistic Syntax.

Whether pattern-parsing mechanisms are specific to language or apply across multiple cognitive domains remains unresolved. Formal language theory provides a mathematical framework for classifying pattern-generating rule sets (or "grammars") according to complexity. This framework applies to patterns at any level of complexity, stretching from simple sequences, to highly complex tree-like or net-like structures, to any Turing-computable set of strings. Here, we explored human pattern-processing capabilities in the visual domain by generating abstract visual sequences made up of abstract tiles differing in form and color. We constructed different sets of sequences, using artificial "grammars" (rule sets) at three key complexity levels. Because human linguistic syntax is classed as "mildly context-sensitive," we specifically included a visual grammar at this complexity level. Acquisition of these three grammars was tested in an artificial grammar-learning paradigm: after exposure to a set of well-formed strings, participants were asked to discriminate novel grammatical patterns from non-grammatical patterns. Participants successfully acquired all three grammars after only minutes of exposure, correctly generalizing to novel stimuli and to novel stimulus lengths. A Bayesian analysis excluded multiple alternative hypotheses and shows that the success in rule acquisition applies both at the group level and for most participants analyzed individually. These experimental results demonstrate rapid pattern learning for abstract visual patterns, extending to the mildly context-sensitive level characterizing language. We suggest that a formal equivalence of processing at the mildly context sensitive level in the visual and linguistic domains implies that cognitive mechanisms with the computational power to process linguistic syntax are not specific to the domain of language, but extend to abstract visual patterns with no meaning.

Personality assessment and model comparison with behavioral data: A statistical framework and empirical demonstration with bonobos (Pan paniscus).

Interest in quantifying consistent among-individual variation in primate behavior, also known as personality, has grown rapidly in recent decades. Although behavioral coding is the most frequently utilized method for assessing primate personality, limitations in current statistical practice prevent researchers' from utilizing the full potential of their coding datasets. These limitations include the use of extensive data aggregation, not modeling biologically relevant sources of individual variance during repeatability estimation, not partitioning between-individual (co)variance prior to modeling personality structure, the misuse of principal component analysis, and an over-reliance upon exploratory statistical techniques to compare personality models across populations, species, and data collection methods. In this paper, we propose a statistical framework for primate personality research designed to address these limitations. Our framework synthesizes recently developed mixed-effects modeling approaches for quantifying behavioral variation with an information-theoretic model selection paradigm for confirmatory personality research. After detailing a multi-step analytic procedure for personality assessment and model comparison, we employ this framework to evaluate seven models of personality structure in zoo-housed bonobos (Pan paniscus). We find that differences between sexes, ages, zoos, time of observation, and social group composition contributed to significant behavioral variance. Independently of these factors, however, personality nonetheless accounted for a moderate to high proportion of variance in average behavior across observational periods. A personality structure derived from past rating research receives the strongest support relative to our model set. This model suggests that personality variation across the measured behavioral traits is best described by two correlated but distinct dimensions reflecting individual differences in affiliation and sociability (Agreeableness) as well as activity level, social play, and neophilia toward non-threatening stimuli (Openness). These results underscore the utility of our framework for quantifying personality in primates and facilitating greater integration between the behavioral ecological and comparative psychological approaches to personality research.