Serotonin Receptor 1A Variation Is Associated with Anxiety and Agonistic Behavior in Chimpanzees.

Serotonin is a neurotransmitter that plays an important role in regulating behavior and personality in humans and other mammals. Polymorphisms in genes coding for the serotonin receptor subtype 1A (HTR1A), the serotonin transporter (SLC6A4), and the serotonin degrading enzyme monoamine oxidase A (MAOA) are associated with anxiety, impulsivity, and neurotic personality in humans. In primates, previous research has largely focused on SLC6A4 and MAOA, with few studies investigating the role of HTR1A polymorphic variation on behavior. Here, we examined variation in the coding region of HTR1A across apes, and genotyped polymorphic coding variation in a sample of 214 chimpanzees with matched measures of personality and behavior. We found evidence for positive selection at three amino acid substitution sites, one in chimpanzees-bonobos (Thr26Ser), one in humans (Phe33Val), and one in orangutans (Ala274Gly). Investigation of the HTR1A coding region in chimpanzees revealed a polymorphic site, where a C/A single nucleotide polymorphism changes a proline to a glutamine in the amino acid sequence (Pro248Gln). The substitution is located in the third intracellular loop of the receptor, a region important for serotonin signal transduction. The derived variant is the major allele in this population (frequency 0.67), and is associated with a reduction in anxiety, decreased rates of male agonistic behavior, and an increase in socio-positive behavior. These results are the first evidence that the HTR1A gene may be involved in regulating social behavior in chimpanzees and encourage further systematic investigation of polymorphic variation in other primate populations with corresponding data on behavior.

Seasonal dynamics of agonistic behavior and hormones in an ex situ all-male colony of large flying foxes.

Large flying foxes (Pteropus vampyrus) are a socially complex species. In situ colonies typically comprise thousands of individuals in small harems of one male to many females. In ex situ environments, all-male colonies are becoming more common due to a surplus of males in the population. There is limited information describing the hormonal and behavioral patterns of all-male colonies during the breeding season. We assessed seasonal changes in hormones and behavior in an all-male colony of 12 large flying foxes at Disney's Animal Kingdom® . We validated hormone assays using morning urine and fecal samples to assess seasonal changes in excreted immunoreactive testosterone and glucocorticoid metabolites. We collected behavior data using an all-occurrence method, recording agonistic behaviors related to territorial defense (hooking, biting, wing flexing, vocalizing, and wrestling), and sexual behavior (mounting and frontal grabbing). Results indicated that (i) we could reliably measure testosterone and glucocorticoid metabolites concentrations from fecal and urine samples collected from individual bats; (ii) there were distinct relationships between changes in levels of agonism and hormone concentrations throughout the year; and (iii) three agonistic behaviors (chasing, wrestling, and open-mouth threat) peaked prior to the increase in testosterone and glucocorticoid hormones measured during the breeding season. These three behaviors could potentially be used as early indicators to signal the onset of the breeding season and allow time to implement ex situ management changes to reduce the incidence of agonism between individuals.

Atypical early histories predict lower extraversion in captive chimpanzees.

Although much research has been conducted to understand personality development in humans, there remain substantial gaps in our understanding of these processes, particularly in relation to social influences. As such, investigations into personality development in our closest living relative, the chimpanzee, may provide useful insight. We evaluated the impact of early social exposure (to both humans and conspecifics) on personality development by studying 88 chimpanzees, including former pets and entertainers, living in accredited zoos and sanctuaries. During infancy, subjects varied in the amount of time spent with conspecifics compared with humans. Caregivers familiar with the chimpanzees rated them using a modified version of the Hominoid Personality Questionnaire (HPQ) and the ratings were found to have strong inter-rater reliability. We used the published structure of the HPQ to evaluate our results in relation to differences in early life experience. Chimpanzees who as infants spent less time with conspecifics were rated as lower in Extraversion later in life in comparison with chimpanzees who as infants spent more time with conspecifics. These results suggest that a broad range of social influences should be considered when evaluating the impact of early social environment on later personality expression.

Plumage variation and social partner choice in the greater flamingo (Phoenicopterus roseus).

There is evidence that plumage coloration is related to mate choice in several different bird species. However, the relationship between plumage coloration to mate or other social partner choice has rarely been investigated in flamingos. This is important to study because we know plumage coloration can be an indicator of welfare. We assessed plumage color score in relation to sex, age, and social partner choice over a 9-month period in a flock of 34 adult greater flamingos (Phoenicopterus roseus) living at Disney's Animal Kingdom® . When looking at primary social partners, redder males were more likely to have primary social partners compared to less red males. In addition, primary social partners tended to have similar color scores to each other. These findings provide insight into one factor that might influence social partner choice in greater flamingos living in ex situ situations. Future studies should investigate how these results relate to reproductive success as part of ex situ management. Zoo Biol. 35:409-414, 2016. © 2016 Wiley Periodicals, Inc.

Neuroanatomical correlates of personality in chimpanzees (Pan troglodytes): Associations between personality and frontal cortex.

Converging empirical data suggests that a set of largely consistent personality traits exist in both human and nonhuman primates; despite these similarities, almost nothing is known concerning the neurobiological basis of these traits in nonhuman primates. The current study examined associations between chimpanzee personality traits and the grey matter volume and asymmetry of various frontal cortex regions in 107 captive chimpanzees. Chimpanzees rated as higher on Openness and Extraversion had greater bilateral grey matter volumes in the anterior cingulate cortex. Further, chimpanzee rated as higher on Dominance had larger grey volumes in the left anterior cingulate cortex and right Prefrontal Cortex (PFC). Finally, apes rated higher on Reactivity/Unpredictability had higher grey matter volumes in the right mesial PFC. All associations survived after applying False Discovery Rate (FDR) thresholds. Results are discussed in terms of current neuroscientific models of personality which suggest that the frontal cortex, and asymmetries in this region, play an important role in the neurobiological foundation of broad dispositional traits.

Influence of personality, age, sex, and estrous state on chimpanzee problem-solving success.

Despite the importance of individual problem solvers for group- and individual-level fitness, the correlates of individual problem-solving success are still an open topic of investigation. In addition to demographic factors, such as age or sex, certain personality dimensions have also been revealed as reliable correlates of problem-solving by animals. Such correlates, however, have been little-studied in chimpanzees. To empirically test the influence of age, sex, estrous state, and different personality factors on chimpanzee problem-solving, we individually tested 36 captive chimpanzees with two novel foraging puzzles. We included both female (N=24) and male (N=12) adult chimpanzees (aged 14-47 years) in our sample. We also controlled for the females' estrous state-a potential influence on cognitive reasoning-by testing cycling females both when their sexual swelling was maximally tumescent (associated with the luteinizing hormone surge of a female's estrous cycle) and again when it was detumescent. Although we found no correlation between the chimpanzees' success with either puzzle and their age or sex, the chimpanzees' personality ratings did correlate with responses to the novel foraging puzzles. Specifically, male chimpanzees that were rated highly on the factors Methodical, Openness (to experience), and Dominance spent longer interacting with the puzzles. There was also a positive relationship between the latency of females to begin interacting with the two tasks and their rating on the factor Reactivity/Undependability. No other significant correlations were found, but we report tentative evidence for increased problem-solving success by the females when they had detumescent estrous swellings.

Factors affecting initial training success of blood glucose testing in captive chimpanzees (Pan troglodytes).

Type 2 diabetes can be a problem for captive chimpanzees. Accurate blood glucose (BG) readings are necessary to monitor and treat this disease. Thus, obtaining voluntary samples from primates through positive reinforcement training (PRT) is critical. The current study assessed the voluntary participation of 123 chimpanzees in BG sampling and investigated factors that may contribute to individual success. All subjects participate in regular PRT sessions as part of a comprehensive behavioral management program. Basic steps involved in obtaining BG values include: voluntarily presenting a finger/toe; allowing digit disinfection; holding for the lancet device; and allowing blood collection onto a glucometer test strip for analysis. We recorded the level of participation (none, partial, or complete) when each chimpanzee was first asked to perform the testing procedure. Nearly 30% of subjects allowed the entire procedure in one session, without any prior specific training for the target behavior. Factors that affected this initial successful BG testing included sex, personality (chimpanzees rated higher on the factor "openness" were more likely to participate with BG testing), and past training performance for "present-for-injection" (chimpanzees that presented for their most recent anesthetic injection were more likely to participate). Neither age, rearing history, time since most recent anesthetic event nor social group size significantly affected initial training success. These results have important implications for captive management and training program success, underlining individual differences in training aptitude and the need for developing individual management plans in order to provide optimal care and treatment for diabetic chimpanzees in captivity.

Developing a comprehensive and comparative questionnaire for measuring personality in chimpanzees using a simultaneous top-down/bottom-up design.

One effective method for measuring personality in primates is to use personality trait ratings to distill the experience of people familiar with the individual animals. Previous rating instruments were created using either top-down or bottom-up approaches. Top-down approaches, which essentially adapt instruments originally designed for use with another species, can unfortunately lead to the inclusion of traits irrelevant to chimpanzees or fail to include all relevant aspects of chimpanzee personality. Conversely, because bottom-up approaches derive traits specifically for chimpanzees, their unique items may impede comparisons with findings in other studies and other species. To address the limitations of each approach, we developed a new personality rating scale using a combined top-down/bottom-up design. Seventeen raters rated 99 chimpanzees on the new 41-item scale, with all but one item being rated reliably. Principal components analysis, using both varimax and direct oblimin rotations, identified six broad factors. Strong evidence was found for five of the factors (Reactivity/Undependability, Dominance, Openness, Extraversion, and Agreeableness). A sixth factor (Methodical) was offered provisionally until more data are collected. We validated the factors against behavioral data collected independently on the chimpanzees. The five factors demonstrated good evidence for convergent and predictive validity, thereby underscoring the robustness of the factors. Our combined top-down/bottom-up approach provides the most extensive data to date to support the universal existence of these five personality factors in chimpanzees. This framework, which facilitates cross-species comparisons, can also play a vital role in understanding the evolution of personality and can assist with husbandry and welfare efforts.

Outcomes from an anti-gonadotropin-releasing hormone immunotherapeutic trial in large flying foxes (Pteropus vampyrus).

OBJECTIVE: The anti-GnRH immunotherapeutic product Improvest was administered to intact male large flying foxes (Pteropus vampyrus) under managed care for androgen mitigation, leading to a decrease in agonistic behaviors, falls, and injuries from conspecific attention. ANIMALS: 12 males were included in this study. PROCEDURES: Eleven bats received subcutaneous (SC) Improvest interscapular, and 1 animal received Improvest SC in its leg. Assessments included clinical presentation, treatment, behavior, and urine and fecal glucocorticoid metabolites and testosterone (T5) concentrations. RESULTS: Eleven of the 12 bats developed reactions, which included facial edema, localized irritation, swelling of the head and neck, and pruritus with varying degrees of skin ulceration and subsequent necrosis. Three of the animals required extensive treatments, and the 1 animal who received the injection in its leg was unaffected. Posttreatment, fecal glucocorticoid metabolite and/or T5 values were at or below the nonbreeding season baseline for 3 successive breeding seasons, and there was a reduction in agonistic interactions, falls, and injuries. CLINICAL RELEVANCE: A behavioral characteristic of this species is to focus on areas of irritation that exacerbated the extent of the skin wounds. Some cases required medical, surgical, and behavioral intervention. Large flying foxes may be particularly sensitive to this immunotherapeutic when given subcutaneously in the interscapular region. Despite this reaction, the positive long-term effects on behavior and multiyear reduction of hormones suggest that the use of this immunotherapeutic warrants further investigation, although the results should be taken into consideration with other factors such as handling, treatments, chronicity of lesions.

Squirrel monkeys' response to inequitable outcomes indicates a behavioural convergence within the primates.

Although several primates respond negatively to inequity, it is unknown whether this results from homology or convergent processes. Behaviours shared within a taxonomic group are often assumed to be homologous, yet this distinction is important for a better understanding of the function of the behaviour. Previous hypotheses have linked cooperation and inequity responses. Supporting this, all species in which inequity responses have been documented are cooperative. In this study, we tested this hypothesis by investigating the response to inequity in squirrel monkeys, which share a phylogenetic family with capuchin monkeys, but do not cooperate extensively. Subjects exchanged tokens to receive food rewards in conditions in which the level of effort required and reward received varied. Squirrel monkeys did not respond negatively to inequity. However, the monkeys were sensitive to the variation present in the task; male subjects showed a contrast effect and, as in previous studies, subjects were more sensitive to differences in reward in the context of a task than when rewards were given for free. Taken with other results, these results support the hypothesis that a negative response to inequity evolved convergently in primates, probably as a mechanism for evaluating outcomes relative to one's partners in cooperative species.

Personality in nonhuman primates: a review and evaluation of past research.

Scientific reports of personality in nonhuman primates are now appearing with increasing frequency across a wide range of disciplines, including psychology, anthropology, endocrinology, and zoo management. To identify general patterns of research and summarize the major findings to date, we present a comprehensive review of the literature, allowing us to pinpoint the major gaps in knowledge and determine what research challenges lay ahead. An exhaustive search of five scientific databases identified 210 relevant research reports. These articles began to appear in the 1930s, but it was not until the 1980s that research on primate personality began to gather pace, with more than 100 articles published in the last decade. Our analyses of the literature indicate that some domains (e.g., sex, age, rearing conditions) are more evenly represented in the literature than are others (e.g., species, research location). Studies examining personality structure (e.g., with factor analysis) have identified personality dimensions that can be divided into 14 broad categories, with Sociability, Confidence/Aggression, and Fearfulness receiving the most research attention. Analyses of the findings pertaining to inter-rater agreement, internal consistency, test-retest reliability, generally support not only the reliability of primate personality ratings scales but also point to the need for more psychometric studies and greater consistency in how the analyses are reported. When measured at the level of broad dimensions, Extraversion and Dominance generally demonstrated the highest levels of inter-rater reliability, with weaker findings for the dimensions of Agreeableness, Emotionality, and Conscientiousness. Few studies provided data with regard to convergent and discriminant validity; Excitability and Dominance demonstrated the strongest validity coefficients when validated against relevant behavioral criterion measures. Overall, the validity data present a somewhat mixed picture, suggesting that high levels of validity are attainable, but by no means guaranteed. Discussion focuses on delineating major theoretical and empirical questions facing research and practice in primate personality.

Frontal lobe activation mediates the relation between sensation seeking and cortisol increases.

Low sensation seekers are theorized to avoid risk more often because risk is emotionally more costly for them (in comparison to high sensation seekers). Therefore, individual differences in sensation seeking should predict differences in risk task-induced cortisol changes. Furthermore, the neural mediation that accounts for the relation between sensation seeking and cortisol changes has not been studied. The current study tested whether individual differences in sensation seeking predicted cortisol changes in relation to a risk task and whether this relation was mediated by frontal lobe activation. Participants (N=17) who varied in sensation seeking completed an fMRI study in which they rated the likelihood they would take various risks. Cortisol was measured from saliva samples collected prior to and after the fMRI procedure. The findings show that low sensation seekers showed the greatest rise in cortisol after the risk procedure, and this relation was partially mediated by increased orbitofrontal cortex activity.

Sex differences in longitudinal personality stability in chimpanzees.

Personality factors analogous to the Big Five observed in humans are present in the great apes. However, few studies have examined the long-term stability of great ape personality, particularly using factor-based personality instruments. Here, we assessed overall group, and individual-level, stability of chimpanzee personality by collecting ratings for chimpanzees (N = 50) and comparing them with ratings collected approximately 10 years previously, using the same personality scale. The overall mean scores of three of the six factors differed across the two time points. Sex differences in personality were also observed, with overall sex differences found for three traits, and males and females showing different trajectories for two further traits over the 10 year period. Regardless of sex, rank-order stability analysis revealed strong stability for dominance; individuals who were dominant at the first time point were also dominant 10 years later. The other personality factors exhibited poor to moderate rank-order stability, indicating that individuals were variable in their rank-position consistency over time. As many studies assessing chimpanzee cognition rely on personality data collected several years prior to testing, these data highlight the importance of collecting current personality data when correlating them with cognitive performance.

Handedness for tool use correlates with cerebellar asymmetries in chimpanzees (Pan troglodytes).

Recent studies have shown that great ape species possess patterns of macrostructural neocortical asymmetries that are similar to those found in humans. However, little is known about the asymmetry of subcortical structures in great apes. To address this lack of data, the authors assessed left-right asymmetry of the anterior and posterior aspects of cerebellum from MRI brain scans of 53 chimpanzees (Pan troglodytes). No population-level bias was found for either the anterior or the posterior region of the cerebellum. However, a significant inverse association was found in the asymmetry quotients of the anterior and posterior regions, indicating that the cerebellum was torqued at the individual level. Additionally, handedness for tool use but not other measures was associated with variation in cerebellar asymmetries. Last, older chimpanzees had a smaller cerebellum after brain volume was adjusted for. The results are discussed in the context of brain changes in primate evolution related to tool use.

Etiology of Triarchic Psychopathy Dimensions in Chimpanzees (Pan troglodytes).

The current study undertook analyses of genealogical data from a sample of 178 socially-housed chimpanzees (Pan troglodytes) with well-documented pedigrees, to clarify the etiologic bases of triarchic psychopathy dimensions and the influence of early social rearing experiences. Whereas biometric analyses for the full sample indicated significant heritability for the boldness dimension of psychopathy only, heritability estimates varied by early rearing, with all three triarchic dimensions showing significant heritabilities among mother-reared but not nursery-reared apes. For mother-reared apes, both genes and environment contributed to covariance between meanness and disinhibition, whereas environment contributed mainly to covariation between these dimensions and boldness. Results indicate contributions of both genes and environment to psychopathic tendencies, with an important role for early-rearing in their relative contributions to distinct phenotypic subdimensions. In conjunction with findings from human studies, results provide valuable insights into core biobehavioral processes relevant to psychological illness and health.

Lateralized scratching in chimpanzees (Pan troglodytes): Evidence of a functional asymmetry during arousal.

This study evaluated laterality in scratching by chimpanzees (n = 89) during socially arousing circumstances. Hand use and the side of the body scratched was recorded during a baseline and experimental condition. In the experimental condition, chimpanzees were shown a video of other conspecifics sharing, fighting over, and consuming a watermelon. Self-touches were categorized as either rubs or scratches. The chimpanzees showed a significant right hand bias for rubbing and also significantly directed the rubs to the right side of the body. For scratching, the chimpanzees showed no hand preference but a significant bias for scratching on the left side of the body. These results support the view that the right hemisphere regulates the autonomic nervous system during arousal.

A Chimpanzee (Pan troglodytes) Model of Triarchic Psychopathy Constructs: Development and Initial Validation.

The current work sought to operationalize constructs of the triarchic model of psychopathy in chimpanzees (Pan troglodytes), a species well-suited for investigations of basic biobehavioral dispositions relevant to psychopathology. Across three studies, we generated validity evidence for scale measures of the triarchic model constructs in a large sample (N=238) of socially-housed chimpanzees. Using a consensus-based rating approach, we first identified candidate items for the chimpanzee triarchic (CHMP-Tri) scales from an existing primate personality instrument and refined these into scales. In Study 2, we collected data for these scales from human informants (N=301), and examined their convergent and divergent relations with scales from another triarchic inventory developed for human use. In Study 3, we undertook validation work examining associations between CHMP-Tri scales and task measures of approach-avoidance behavior (N=73) and ability to delay gratification (N=55). Current findings provide support for a chimpanzee model of core dispositions relevant to psychopathy and other forms of psychopathology.

Factors influencing the prevalence and handedness for throwing in captive chimpanzees (Pan troglodytes).

Humans throw right-handed, and it has been suggested that the neurophysiological demands of aimed throwing may have served as a precursor to the evolution of left hemisphere specialization for linguistic functions. Although there are descriptions of throwing by wild and captive chimpanzees (Pan troglodytes), systematic observations of aimed throwing and handedness have not been reported. In this article, evidence of population-level right-handedness for throwing is reported in 2 samples of captive chimpanzees. It is further reported that right-handed throwing is more pronounced than other measures of handedness in captive chimpanzees. The implications of these findings are discussed in the context of theories relating throwing to the evolution of lateralization for language functions.

The contribution of genetics and early rearing experiences to hierarchical personality dimensions in chimpanzees (Pan troglodytes).

A reliable literature finds that traits are related to each other in an organized hierarchy encompassing various conceptualizations of personality (e.g., Big Three, five-factor model). Recent work suggests the potential of a similar organization among our closest nonhuman relative, chimpanzees (Pan troglodytes), with significant links to neurobiology suggesting an evolutionarily and neurobiologically based hierarchical structure of personality. The current study investigated this hierarchical structure, the heritability of the various personality dimensions across levels of the hierarchy, and associations with early social rearing experience in a large sample (N = 238) of socially housed, captive chimpanzees residing in 2 independent colonies of apes. Results provide support for a hierarchical structure of personality in chimpanzees with significant associations with early rearing experiences. Further, heritabilities of the various dimensions varied by early rearing, with affective dimensions found to be significantly heritable among mother-reared apes, whereas personality dimensions were largely independent of relatedness among the nursery-reared apes. Taken together, these findings provide evidence for the influence of both genetic and environmental factors on personality profiles across levels of the hierarchy, supporting the importance of considering environmental variation in models of quantitative trait evolution.

Personality influences responses to inequity and contrast in chimpanzees.

Several species besides humans respond negatively to inequity (i.e. receiving a less preferred outcome as compared to a social partner). Among primates, the taxon for which inequity responses have been most comprehensively studied, there are large individual differences in responses that have, thus far, not been well explained by demographic features such as sex, rank and age. Recent evidence shows that individuals' personalities are important in explaining differences in behavioural outcomes in other contexts. Thus, in the current study, we explored whether personality was associated with chimpanzees' responses to both inequity and contrast (i.e. receiving less than anticipated). Chimpanzees were paired with multiple members of their social groups. These pairs alternated trading a token to receive food rewards that either differed from what their partner received (inequity condition) or from what was initially offered (contrast condition) and we compared their responses to a control in which both subjects were offered and received the same reward for trading the token. We predicted that both personality and the quality and length of the pairs' relationship would influence subjects' reactions to unequal outcomes, as measured by their refusal to exchange tokens. The quality of subjects' relationships, based on a weighted average of grooming, contact and proximity, did not correlate with refusals to exchange, whereas pairs that had lived together longer were less likely to refuse in the contrast condition than were pairs that had lived together for less time. Considering personality, some of the dimensions influenced responses to both inequity and contrast similarly, but the more 'social' personality dimensions ('extraversion' and 'agreeableness') were more strongly correlated with sensitivity to inequity. These results highlight the importance of considering individual differences, including personality, when evaluating responses in cognitive and behavioural tests.