Genetic determinants of individual variation in the superior temporal sulcus of chimpanzees (Pan troglodytes).

The superior temporal sulcus (STS) is a conserved fold that divides the middle and superior temporal gyri. In humans, there is considerable variation in the shape, folding pattern, lateralization, and depth of the STS that have been reported to be associated with social cognition and linguistic functions. We examined the role that genetic factors play on individual variation in STS morphology in chimpanzees. The surface area and depth of the STS were quantified in sample of 292 captive chimpanzees comprised of two genetically isolated population of individuals. The chimpanzees had been previously genotyped for AVPR1A and KIAA0319, two genes that play a role in social cognition and communication in humans. Single nucleotide polymorphisms in the KIAA0319 and AVPR1A genes were associated with average depth as well as asymmetries in the STS. By contrast, we found no significant effects of these KIA0319 and AVPR1A polymorphism on surface area and depth measures for the central sulcus. The overall findings indicate that genetic factors account for a small to moderate amount of variation in STS morphology in chimpanzees. These findings are discussed in the context of the role of the STS in social cognition and language in humans and their potential evolutionary origins.

Neutrophil to lymphocyte ratio in captive olive baboons (Papio anubis): The effects of age, sex, rearing, stress, and pregnancy.

In apes and humans, neutrophil to lymphocyte ratio (NLR) can be used as a predictive indicator of a variety of clinical conditions, longevity, and physiological stress. In chimpanzees specifically, NLR systematically varies with age, rearing, sex, and premature death, indicating that NLR may be a useful diagnostic tool in assessing primate health. To date, just one very recent study has investigated NLR in old world monkeys and found lower NLR in males and nursery-reared individuals, as well as a negative relationship between NLR and disease outcomes. Given that baboons are increasingly used as research models, we aimed to characterize NLR in baboons by providing descriptive data and examinations of baboon NLR heritability, and of the relationships between NLR, age, rearing, and sex in 387 olive baboons (Papio anubis) between 6 months and 19 years of age. We found that (1) mother-reared baboons had higher NLRs than nursery-reared baboons; (2) females had higher NLRs than males; and (3) there was a quadratic relationship between NLR and age, such that middle-aged individuals had the highest NLR values. We also examined NLR as a function of transport to a new facility using a subset of the data. Baboons exhibited significantly higher transport NLRs compared to routine exam NLRs. More specifically, adult baboons had higher transport NLRs than routine NLRs, whereas juveniles showed no such difference, suggesting that younger animals may experience transport stress differently than older animals. We also found that transport NLR was heritable, whereas routine NLR was not, possibly suggesting that stress responses (as indicated in NLR) have a strong genetic component. Consistent with research in humans and chimpanzees, these findings suggest that NLR varies with important biological and life history variables and that NLR may be a useful health biomarker in baboons.

The gaze of a social monkey is perceptible to conspecifics and predators but not prey.

Eye gaze is an important source of information for animals, implicated in communication, cooperation, hunting and antipredator behaviour. Gaze perception and its cognitive underpinnings are much studied in primates, but the specific features that are used to estimate gaze can be difficult to isolate behaviourally. We photographed 13 laboratory-housed tufted capuchin monkeys (Sapajus [Cebus] apella) to quantify chromatic and achromatic contrasts between their iris, pupil, sclera and skin. We used colour vision models to quantify the degree to which capuchin eye gaze is discriminable to capuchins, their predators and their prey. We found that capuchins, regardless of their colour vision phenotype, as well as their predators, were capable of effectively discriminating capuchin gaze across ecologically relevant distances. Their prey, in contrast, were not capable of discriminating capuchin gaze, even under relatively ideal conditions. These results suggest that specific features of primate eyes can influence gaze perception, both within and across species.

Sulcal Morphology in Cingulate Cortex is Associated with Voluntary Oro-Facial Motor Control and Gestural Communication in Chimpanzees (Pan troglodytes).

Individual differences in sulcal variation within the anterior and mid-cingulate cortex of the human brain, particularly the presence or absence of a paracingulate sulcus (PCGS), are associated with various motor and cognitive processes. Recently, it has been reported that chimpanzees possess a PCGS, previously thought to be a unique feature of the human brain. Here, we examined whether individual variation in the presence or absence of a PCGS as well as the variability in the intralimbic sulcus (ILS) are associated with oro-facial motor control, handedness for manual gestures, and sex in a sample of MRI scans obtained in 225 chimpanzees. Additionally, we quantified the depth of the cingulate sulcus (CGS) along the anterior-posterior axis and tested for association with oro-facial motor control, handedness, and sex. Chimpanzees with better oro-facial motor control were more likely to have a PCGS, particularly in the left hemisphere compared to those with poorer control. Male chimpanzees with better oro-facial motor control showed increased leftward asymmetries in the depth of the anterior CGS, whereas female chimpanzees showed the opposite pattern. Significantly, more chimpanzees had an ILS in the left compared to the right hemisphere, but variability in this fold was not associated with sex, handedness, or oro-facial motor control. Finally, significant population-level leftward asymmetries were found in the anterior portion of the CGS, whereas significant rightward biases were evident in the posterior regions. The collective results suggest that the emergence of a PCGS and enhanced gyrification within the anterior and mid-cingulate gyrus may have directly or indirectly evolved in response to selection for increasing oro-facial motor control in primates.

Age-related cognitive impairment is associated with low serum concentrations of testosterone and CSF levels of amyloid beta 42 in male cynomolgus monkeys (Macaca fascicularis).

Aged memory-impaired cynomolgus monkeys had significantly lower levels of cerebrospinal amyloid (Aß42 ) and serum testosterone compared with young animals and non-memory-impaired controls. Our findings confirm similar findings in the human and substantiate the usefulness of the cynomolgus monkey as a spontaneous model for aging-associated senile dementia of the Alzheimer type.

Predicting their past: Machine language learning can discriminate the brains of chimpanzees with different early-life social rearing experiences.

Early life experiences, including separation from caregivers, can result in substantial, persistent effects on neural, behavioral, and physiological systems as is evidenced in a long-standing literature and consistent findings across species, populations, and experimental models. In humans and other animals, differential rearing conditions can affect brain structure and function. We tested for whole brain patterns of morphological difference between 108 chimpanzees reared typically with their mothers (MR; N = 54) and those reared decades ago in a nursery with peers, human caregivers, and environmental enrichment (NR; N = 54). We applied support vector machine (SVM) learning to archival MRI images of chimpanzee brains to test whether we could, with any degree of significant probability, retrospectively classify subjects as MR and NR based on variation in gray matter within the entire brain. We could accurately discriminate MR and NR chimpanzee brains with nearly 70% accuracy. The combined brain regions discriminating the two rearing groups were widespread throughout the cortex. We believe this is the first report using machine language learning as an analytic method for discriminating nonhuman primate brains based on early rearing experiences. In this sense, the approach and findings are novel, and we hope they stimulate application of the technique to studies on neural outcomes associated with early experiences. The findings underscore the potential for infant separation from caregivers to leave a long-term mark on the developing brain.

Increased expression of GAPDH in cynomolgus monkeys with spontaneous cognitive decline and amyloidopathy reminiscent of an Alzheimer's-type disease is reflected in the circulation.

Previous studies of aging cynomolgus monkeys from our group identified spontaneous age-associated cognitive declines associated with biomarkers and brain lesions reminiscent of Alzheimer's Disease (AD), in a proportion of aged monkeys. However, the molecular mechanisms that underlie the spontaneous amyloid disorders and cognitive declines observed in these affected monkeys have yet to be investigated in detail. Using reverse transcriptase quantitative real time PCR techniques, normalized to the ACTB housekeeping gene, we analyzed the expression patterns of a number of genes which have been implicated in amyloid and tau abnormalities, in well-characterized aged cynomolgus monkeys with cognitive decline. A significantly increased expression of the genes coding for glyceraldehyde 3-phosphate dehydrogenase (GAPDH), was found in aged-cognitive decline monkeys compared to age-matched healthy controls. GAPDH has been implicated in several neurodegenerative diseases and interacts with beta amyloid precursor proteins. These findings provide support for the utilization of cynomolgus macaques in translational preclinical research as valid spontaneous models in experimental investigations of the relationships among aging, cognitive decline, and the neuropathy of AD.

Age- and cognition-related differences in the gray matter volume of the chimpanzee brain (Pan troglodytes): A voxel-based morphometry and conjunction analysis.

Several primate species have been shown to exhibit age-related changes in cognition, brain, and behavior. However, severe neurodegenerative illnesses, such as Alzheimer's disease (AD), were once thought to be uniquely human. Recently, some chimpanzees naturally were documented to develop both neurofibrillary tangles and amyloid plaques, the main characteristics of AD pathology. In addition, like humans and other primates, chimpanzees show similar declines in cognition and motor function with age. Here, we used voxel-based morphometry to examine the relationships among gray matter volume, age, and cognition using magnetic resonance imaging scans previously acquired from chimpanzees (N = 216). We first determined the relationship between age and gray matter volume, identifying the regions that declined with age. With a subset of our sample (N = 103), we also determined differences in gray matter volume between older chimpanzees with higher cognition scores than expected for their age, and older chimpanzees with lower than expected scores. Finally, we ran a conjunction analysis to determine any overlap in brain regions between these two analyses. We found that as chimpanzees age, they lose gray matter in regions associated with cognition. In addition, cognitively healthy older chimpanzees (those performing better for their age) have greater gray matter volume in many brain regions compared with chimpanzees who underperform for their age. Finally, the conjunction analysis revealed that regions of age-related decline overlap with the regions that differ between cognitively healthy chimpanzees and those who underperform. This study provides further evidence that chimpanzees are an important model for research on the neurobiology of aging. Future studies should investigate the effects of cognitive stimulation on both cognitive performance and brain structure in aging nonhuman primates.

Age-related changes in chimpanzee (Pan troglodytes) cognition: Cross-sectional and longitudinal analyses.

Chimpanzees are the species most closely related to humans, yet age-related changes in brain and cognition remain poorly understood. The lack of studies on age-related changes in cognition in chimpanzees is particularly unfortunate in light of the recent evidence demonstrating that this species naturally develops Alzheimer's disease (AD) neuropathology. Here, we tested 213 young, middle-aged, and elderly captive chimpanzees on the primate cognitive test battery (PCTB), a set of 13 tasks that assess physical and social cognition in nonhuman primates. A subset of these chimpanzees (n = 146) was tested a second time on a portion of the PCTB tasks as a means of evaluating longitudinal changes in cognition. Cross-sectional analyses revealed a significant quadratic association between age and cognition with younger and older chimpanzees performing more poorly than middle-aged individuals. Longitudinal analyses showed that the oldest chimpanzees at the time of the first test showed the greatest decline in cognition, although the effect was mild. The collective data show that chimpanzees, like other nonhuman primates, show age-related decline in cognition. Further investigations into whether the observed cognitive decline is associated with AD pathologies in chimpanzees would be invaluable in understanding the comparative biology of aging and neuropathology in primates.

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.

Reproducibility of leftward planum temporale asymmetries in two genetically isolated populations of chimpanzees (Pan troglodytes).

Once considered a hallmark of human uniqueness, brain asymmetry has emerged as a feature shared with several other species, including chimpanzees, one of our closest living relatives. Most notable has been the discovery of asymmetries in homologues of cortical language areas in apes, particularly in the planum temporale (PT), considered a central node of the human language network. Several lines of evidence indicate a role for genetic mechanisms in the emergence of PT asymmetry; however, the genetic determinants of cerebral asymmetries have remained elusive. Studies in humans suggest that there is heritability of brain asymmetries of the PT, but this has not been explored to any extent in chimpanzees. Furthermore, the potential influence of non-genetic factors has raised questions about the reproducibility of earlier observations of PT asymmetry reported in chimpanzees. As such, the present study was aimed at examining both the heritability of phenotypic asymmetries in PT morphology, as well as their reproducibility. Using magnetic resonance imaging, we evaluated morphological asymmetries of PT surface area (mm2) and mean depth (mm) in captive chimpanzees (n = 291) derived from two genetically isolated populations. Our results confirm that chimpanzees exhibit a significant population-level leftward asymmetry for PT surface area, as well as significant heritability in the surface area and mean depth of the PT. These results conclusively demonstrate the existence of a leftward bias in PT asymmetry in chimpanzees and suggest that genetic mechanisms play a key role in the emergence of anatomical asymmetry in this region.

Greater variability in chimpanzee (Pan troglodytes) brain structure among males.

Across the animal kingdom, males tend to exhibit more behavioural and morphological variability than females, consistent with the 'greater male variability hypothesis'. This may reflect multiple mechanisms operating at different levels, including selective mechanisms that produce and maintain variation, extended male development, and X chromosome effects. Interestingly, human neuroanatomy shows greater male variability, but this pattern has not been demonstrated in any other species. To address this issue, we investigated sex-specific neuroanatomical variability in chimpanzees by examining relative and absolute surface areas of 23 cortical sulci across 226 individuals (135F/91M), using permutation tests of the male-to-female variance ratio of residuals from MCMC generalized linear mixed models controlling for relatedness. We used these models to estimate sulcal size heritability, simulations to assess the significance of heritability, and Pearson correlations to examine inter-sulcal correlations. Our results show that: (i) male brain structure is relatively more variable; (ii) sulcal surface areas are heritable and therefore potentially subject to selection; (iii) males exhibit lower heritability values, possibly reflecting longer development; and (iv) males exhibit stronger inter-sulcal correlations, providing indirect support for sex chromosome effects. These results provide evidence that greater male neuroanatomical variability extends beyond humans, and suggest both evolutionary and developmental explanations for this phenomenon.

Heritability of Gray Matter Structural Covariation and Tool Use Skills in Chimpanzees (Pan troglodytes): A Source-Based Morphometry and Quantitative Genetic Analysis.

Nonhuman primates, and great apes in particular, possess a variety of cognitive abilities thought to underlie human brain and cognitive evolution, most notably, the manufacture and use of tools. In a relatively large sample (N = 226) of captive chimpanzees (Pan troglodytes) for whom pedigrees are well known, the overarching aim of the current study was to investigate the source of heritable variation in brain structure underlying tool use skills. Specifically, using source-based morphometry (SBM), a multivariate analysis of naturally occurring patterns of covariation in gray matter across the brain, we investigated (1) the genetic contributions to variation in SBM components, (2) sex and age effects for each component, and (3) phenotypic and genetic associations between SBM components and tool use skill. Results revealed important sex- and age-related differences across largely heritable SBM components and associations between structural covariation and tool use skill. Further, shared genetic mechanisms appear to account for a heritable link between variation in both the capacity to use tools and variation in morphology of the superior limb of the superior temporal sulcus and adjacent parietal cortex. Findings represent the first evidence of heritability of structural covariation in gray matter among nonhuman primates.

Unpacking chimpanzee (Pan troglodytes) patch use: Do individuals respond to food patches as predicted by the marginal value theorem?

The marginal value theorem is an optimal foraging model that predicts how efficient foragers should respond to both their ecological and social environments when foraging in food patches, and it has strongly influenced hypotheses for primate behavior. Nevertheless, experimental tests of the marginal value theorem have been rare in primates and observational studies have provided conflicting support. As a step towards filling this gap, we test whether the foraging decisions of captive chimpanzees (Pan troglodytes) adhere to the assumptions and qualitative predictions of the marginal value theorem. We presented 12 adult chimpanzees with a two-patch foraging environment consisting of both low-quality (i.e., low-food density) and high-quality (i.e., high-food density) patches and examined the effect of patch quality on their search behavior, foraging duration, marginal capture rate, and its proxy measures: giving-up density and giving-up time. Chimpanzees foraged longer in high-quality patches, as predicted. In contrast to predictions, they did not depress high-quality patches as thoroughly as low-quality patches. Furthermore, since chimpanzees searched in a manner that fell between systematic and random, their intake rates did not decline at a steady rate over time, especially in high-quality patches, violating an assumption of the marginal value theorem. Our study provides evidence that chimpanzees are sensitive to their rate of energy intake and that their foraging durations correlate with patch quality, supporting many assumptions underlying primate foraging and social behavior. However, our results question whether the marginal value theorem is a constructive model of chimpanzee foraging behavior, and we suggest a Bayesian foraging framework (i.e., combining past foraging experiences with current patch sampling information) as a potential alternative. More work is needed to build an understanding of the proximate mechanisms underlying primate foraging decisions, especially in more complex socioecological environments.

The implementation and initial evaluation of a physical therapy program for captive chimpanzees (Pan troglodytes).

Due to advances in captive nonhuman primate (NHP) medical care, the number of geriatric chimpanzees (≥35-years old) is growing. With old age comes a variety of physical conditions, including arthritis, stroke, and mobility impairments. Programs aimed at enhancing the welfare of geriatric chimpanzees are now quite common, but there are few published empirical evaluations of the efficacy of such programs. The current study aimed to create, implement, and evaluate the effects of participation in a physical therapy (PT) program on physical health, mobility, welfare, and behavior. Nine chimpanzees with mobility impairments participated in personalized PT routines (using positive reinforcement training) twice per week for 5 months. Additionally, nine control chimpanzees (non-mobility-impaired, matched with PT chimpanzees on age and gender) participated in body exam behavior sessions (also using positive reinforcement training) twice per week. All chimpanzees were rated on 14 health, well-being, and behavior items, as well as level of mobility throughout the PT program. Chimpanzees that participated in the PT program showed significant increases in ratings of physical health, well-being, and activity levels across phases of the program. Furthermore, compared to control chimpanzees, PT chimpanzees showed significant increases in ratings of ease of movement. Because raters were not blind to physical therapy treatment, our results represent an initial evaluation of the program that may suggest that participation in the PT program has physical, behavioral, and welfare benefits. Assessments of novel geriatric-focused care strategies and programs are essential to further enhance the welfare of the captive chimpanzee population, which is currently comprised of many geriatric animals, whose proportion of the captive population will only increase.

Validation and utility of a body condition scoring system for chimpanzees (Pan troglodytes).

Obesity is a problem in captive chimpanzee colonies that can lead to increased risk for disease; therefore, implementation of effective weight management strategies is imperative. To properly implement a weight management program, captive managers should be able to noninvasively identify and assess overweight or obese individuals. Traditional means of categorizing obese individuals involve sedating the animals to obtain body weights or skin fold measurements. The current study aimed to validate a noninvasive, subjective body condition score (BCS) system for captive chimpanzees. The system utilizes a 10-point scale, with one rated as "emaciated," five as "normal," and 10 as "extremely obese." Between 2013 and 2014, 158 chimpanzees were weighed and scored using this system (a) while sedated and (b) while awake in their social group within 1-3 days of sedation ("In-group" ratings). We found high inter-rater reliability between In-group raters, as well as between sedated and In-group scores. BCSs, which require observation only, were significantly positively correlated with weight (an objective measure of obesity often requiring anesthetization), supporting the scale's validity. The BCS system identified 36 individuals as "overweight," while the use of weights alone identified only 26 individuals as "overweight." Furthermore, the BCS system was able to classify individuals of the same sex and weight as having different BCSs, ranging from normal to overweight. Lastly, using focal animal behavioral observations from 2016 to 2018 (N = 120), we found that In-group BCS predicted individual levels of inactive behavior more than 2 years later, demonstrating the predictive validity of the scale. These results illustrate the utility of the BCS system as a noninvasive, reliable, and valid technique that may be more sensitive than traditional methods in identifying and quantifying obesity in chimpanzees. This system can be a useful tool for captive managers to monitor and manage the weight of chimpanzees and other nonhuman primates.

Does group size matter? Captive chimpanzee (Pan troglodytes) behavior as a function of group size and composition.

The National Institutes of Health and the Association of Zoos and Aquariums recommend that captive chimpanzees be housed in multi-male, multi-female, age-diverse groups of no less than seven individuals. These recommendations are rooted in the idea that captive chimpanzee groups should be modeled after free-ranging, wild, fission-fusion chimpanzee societies. However, captive chimpanzees do not face the environmental pressures faced by wild chimpanzees, including food scarcity, inter-group competition, and predation. As such, it has been posited that wild, natural conditions may not be the most relevant metric for defining optimal captive chimpanzee group sizes and compositions. Additionally, captive housing poses a set of restrictions on group sizes and compositions, including the need to balance large, multi-male groups with space per animal limitations and intra-group aggression. In the present study, we examined the behavioral effects of group size, within-group age range, and percentage of males in the group. We collected 713 hr of focal animal samples across 120 captive chimpanzees housed in social groups of 4-10 individuals using a 58-behavior ethogram. Chimpanzees housed in groups with a large age range exhibited less inactivity and more locomotion than chimpanzees housed in groups with smaller age ranges. Additionally, chimpanzees in groups of ≥7 with less than half males showed the highest levels of locomotion. Lastly, chimpanzees in groups of ≥7 with at least half males showed the highest levels of affiliation. There were no other significant differences in behavior as a function of these variables or their interactions. These findings lend some support to the existing group size and composition recommendations, providing empirical evidence that there may be certain advantages to housing captive chimpanzees in larger groups with a more diverse age range and/or more males. These results also have practical implications for behavioral management programs across captive settings.

Relationships between captive chimpanzee (Pan troglodytes) welfare and voluntary participation in behavioural studies.

Voluntary participation in behavioural studies offers several scientific, management, and welfare benefits to non-human primates (NHPs). Aside from the scientific benefit of increased understanding of NHP cognition, sociality, and behaviour derived from noninvasive behavioural studies, participation itself has the potential to provide functional simulations of natural behaviours, enrichment opportunities, and increased control over the captive environment, all of which enhance welfare. Despite a developing consensus that voluntary participation offers these welfare enhancements, little research has empirically investigated the ways that participation in behavioural studies may affect welfare. In the current study, we investigated potential relationships between captive chimpanzee welfare and long-term, repeated voluntary participation in noninvasive behavioural studies. We collected behavioural data on 118 chimpanzees at the National Center for Chimpanzee Care (NCCC) in Bastrop, Texas, USA between 2016 and 2018 using 15-minute focal animal samples. Additionally, we collected information on 41 behavioural studies conducted between 2010 and 2018 with the NCCC chimpanzees that involved exposure to a stimulus or manipulation. The total number of behavioural studies in which chimpanzees had participated over the approximately eight-year period was then examined in relation to levels of behavioural diversity, abnormal behaviour, rough scratching, inactivity, and locomotion using a series of regression analyses that controlled for rearing status and age of the chimpanzee at the time of data collection. Analyses revealed significant, positive relationships between the total number of studies in which chimpanzees participated and 1) behavioural diversity scores, R2 adj = .21, F(3,114) = 11.25, p < 0.001; and 2) rough scratching, R2 adj = .11, F(3,114) = 6.01, p = 0.001. The positive relationship between behavioural diversity scores and the total number of studies in which chimpanzees participated seems unsurprising, although we cannot draw conclusions about the directionality of this relationship. The result that rough scratching and the total number of studies in which chimpanzees participated were positively correlated is unexpected. However, rough scratching made up less than 1% of all activity in the current study, and as such, this result may not be biologically meaningful. These findings suggest that participation in behavioural studies is not likely to be detrimental to chimpanzee well-being, and may even be beneficial. Data such as these, which empirically investigate existing recommendations can help inform decisions pertaining to the participation of chimpanzees in behavioural research.

Genetic Factors and Orofacial Motor Learning Selectively Influence Variability in Central Sulcus Morphology in Chimpanzees (Pan troglodytes).

Captive chimpanzees (Pan troglodytes) have been shown to learn the use of novel attention-getting (AG) sounds to capture the attention of humans as a means of requesting or drawing their attention to a desired object or food. There are significant individual differences in the use of AG sounds by chimpanzees and, here, we examined whether changes in cortical organization of the central sulcus (CS) were associated with AG sound production. MRI scans were collected from 240 chimpanzees, including 122 that reliably produced AG sounds and 118 that did not. For each subject, the depth of CS was quantified along the superior-inferior plane with specific interest in the inferior portion corresponding to the region of the motor cortex where the mouth and orofacial movements are controlled. Results indicated that CS depth in the inferior, but not superior, portion was significantly greater in chimpanzees that reliably produced AG sounds compared with those who did not. Quantitative genetic analyses indicated that overall CS surface area and depth were significantly heritable, particularly in the superior regions, but less so in the inferior and central portions. Further, heritability in CS depth was altered as a function of acquisition of AG sounds. The collective results suggest that learning to produce AG sounds resulted in region-specific cortical reorganization within the inferior portion of the CS, a finding previously undocumented in chimpanzees or any nonhuman primate.SIGNIFICANCE STATEMENT Recent studies in chimpanzees (Pan troglodytes) have shown that some can learn to produce novel sounds by configuring different orofacial movement patterns and these sounds are used in communicatively relevant contexts. Here, we examined the neuromorphological correlates in the production of these sounds in chimpanzees. We show that chimpanzees that have learned to produce these sounds show significant differences in central sulcus (CS) morphology, particularly in the inferior region. We further show that overall CS morphology and regions within the superior portion are significantly heritable, whereas central and inferior portions of the CS are not. The collective findings suggest chimpanzees exhibit cortical plasticity in regions of the brain that were central to the emergence of speech functions in humans.

Chimpanzees prioritise social information over pre-existing behaviours in a group context but not in dyads.

How animal communities arrive at homogeneous behavioural preferences is a central question for studies of cultural evolution. Here, we investigated whether chimpanzees (Pan troglodytes) would relinquish a pre-existing behaviour to adopt an alternative demonstrated by an overwhelming majority of group mates; in other words, whether chimpanzees behave in a conformist manner. In each of five groups of chimpanzees (N = 37), one individual was trained on one method of opening a two-action puzzle box to obtain food, while the remaining individuals learned the alternative method. Over 5 h of open access to the apparatus in a group context, it was found that 4/5 'minority' individuals explored the majority method and three of these used this new method in the majority of trials. Those that switched did so after observing only a small subset of their group, thereby not matching conventional definitions of conformity. In a further 'Dyad' condition, six pairs of chimpanzees were trained on alternative methods and then given access to the task together. Only one of these individuals ever switched method. The number of observations that individuals in the minority and Dyad individuals made of their untrained method was not found to influence whether or not they themselves switched to use it. In a final 'Asocial' condition, individuals (N = 10) did not receive social information and did not deviate from their first-learned method. We argue that these results demonstrate an important influence of social context upon prioritisation of social information over pre-existing methods, which can result in group homogeneity of behaviour.