Non-human Great Apes Research Articles

Orangutans and chimpanzees produce morphologically varied laugh faces in response to the age and sex of their social partners

Laugh faces of humans play a key role in everyday social interactions as a pervasive tool of communication across contexts. Humans often vary the degree of mouth opening and teeth exposure when producing these facial expressions, which may depend on who their social partner is (e.g., their gender and age as well as their social relationship), serving this way different functions. Although it was found that laugh faces show evolutionary continuity across humans and non-human great apes according to the Principle of Maximum Parsimony, little is known about the function of laugh face variations from an evolutionary perspective. Hence, the present work examined the morphology of laugh faces in orangutan and chimpanzee dyadic play to test if they are modified with dependence on the playmate’s characteristics (sex, age and social relationship). In total, we analysed over 600 facial expressions of 14 orangutans and 17 chimpanzees by coding the specific muscle activations (Action Units, i.e. AUs) contributing to these expressions, using OrangFACS and ChimpFACS, respectively. Our results suggest that age difference and, to a lesser extent, playmate sex influence laugh face morphology in both taxa, but in opposite ways. While the orangutans of our study seem to expose their upper teeth (with AU10) and to pull the mouth corners (with AU12) more towards weaker partners (younger and female), possibly to communicate non-hostility, the chimpanzees showed both upper and lower teeth exposure (with AU10 and AU16) more often when interacting with the stronger partners (older individuals), possibly to communicate submissiveness. These findings suggest that the ability of humans to modify laugh faces with dependence on social partner characteristics has most likely evolved from pre-existing traits, going back at least to the last common ancestor of today’s great apes, including humans.

Scoping review of general anaesthesia in non-human great apes

Scoping review of general anaesthesia in non-human great apes

The origin of great ape gestural forms.

Two views claim to account for the origins of great ape gestural forms. On the Leipzig view, gestural forms are ontogenetically ritualised from action sequences between pairs of individuals. On the St Andrews view, gestures are the product of natural selection for shared gestural forms. The Leipzig view predicts within- and between-group differences between gestural forms that arise as a product of learning in ontogeny. The St Andrews view predicts universal gestural forms comprehensible within and between species that arise because gestural forms were a target of natural selection. We reject both accounts and propose an alternative "recruitment view" of the origins of great ape gestures. According to the recruitment view, great ape gestures recruit features of their existing behavioural repertoire for communicative purposes. Their gestures inherit their communicative functions from visual (and sometimes tactile) presentations of familiar and easily recognisable action schemas and states and parts of the body. To the extent that great ape species possess similar bodies, this predicts mutual comprehensibility within and between species - but without supposing that gestural forms were themselves targets of natural selection. Additionally, we locate great ape gestural communication within a pragmatic framework that is continuous with human communication, and make testable predications for adjudicating between the three alternative views. We propose that the recruitment view best explains existing data, and does so within a mechanistic framework that emphasises continuity between human and non-human great ape communication.

Chimpanzee utterances refute purported missing links for novel vocalizations and syllabic speech

Nonhuman great apes have been claimed to be unable to learn human words due to a lack of the necessary neural circuitry. We recovered original footage of two enculturated chimpanzees uttering the word “mama” and subjected recordings to phonetic analysis. Our analyses demonstrate that chimpanzees are capable of syllabic production, achieving consonant-to-vowel phonetic contrasts via the simultaneous recruitment and coupling of voice, jaw and lips. In an online experiment, human listeners naive to the recordings’ origins reliably perceived chimpanzee utterances as syllabic utterances, primarily as “ma-ma”, among foil syllables. Our findings demonstrate that in the absence of direct data-driven examination, great ape vocal production capacities have been underestimated. Chimpanzees possess the neural building blocks necessary for speech.

Local genetic adaptation to habitat in wild chimpanzees.

How populations adapt to their environment is a fundamental question in biology. Yet we know surprisingly little about this process, especially for endangered species such as non-human great apes. Chimpanzees, our closest living relatives, are particularly interesting because they inhabit diverse habitats, from rainforest to woodland-savannah. Whether genetic adaptation facilitates such habitat diversity remains unknown, despite having wide implications for evolutionary biology and conservation. Using 828 newly generated exomes from wild chimpanzees, we find evidence of fine-scale genetic adaptation to habitat. Notably, adaptation to malaria in forest chimpanzees is mediated by the same genes underlying adaptation to malaria in humans. This work demonstrates the power of non-invasive samples to reveal genetic adaptations in endangered populations and highlights the importance of adaptive genetic diversity for chimpanzees.

Left ventricular trabeculation in Hominidae: divergence of the human cardiac phenotype

Although the gross morphology of the heart is conserved across mammals, subtle interspecific variations exist in the cardiac phenotype, which may reflect evolutionary divergence among closely-related species. Here, we compare the left ventricle (LV) across all extant members of the Hominidae taxon, using 2D echocardiography, to gain insight into the evolution of the human heart. We present compelling evidence that the human LV has diverged away from a more trabeculated phenotype present in all other great apes, towards a ventricular wall with proportionally greater compact myocardium, which was corroborated by post-mortem chimpanzee (Pan troglodytes) hearts. Speckle-tracking echocardiographic analyses identified a negative curvilinear relationship between the degree of trabeculation and LV systolic twist, revealing lower rotational mechanics in the trabeculated non-human great ape LV. This divergent evolution of the human heart may have facilitated the augmentation of cardiac output to support the metabolic and thermoregulatory demands of the human ecological niche.

Intentionality, pointing, and early symbolic cognition

Concepts such as “symbolism” and “symbolic cognition” often remain unspecified in discussions the symbolic capacities of earlier hominins. In this paper, I use conceptual tools from phenomenology to reflect on the origins of early symbolic cognition. In particular, I discuss the possible early use of pointing gestures around the time of the earliest known stone tool industries. I argue that unlike more basic social acts such as expression, gaze following, and attention-getters, which are used by extant non-human great apes, communicative pointing involves key elements that are characteristic of symbolic cognition. In particular, it involves “third order intentionality” as well as “shared practice horizons”: shared frameworks of understanding which are required for the interpretation of communicative acts whose meaning is not codified indexically or iconically in the signaling behavior. In the final part, I briefly review some indications for the use of pointing gestures around the time of the Lomekwian and Oldowan industries, as a way to sustain cooperation and possibly learning by instruction. It is suggested that pointing is more complex than is standardly acknowledged, and that it may have been an important communicative act for Early Stone Age hominins in transitioning to more fully symbolic speech capacities.

Phase I Trial of Viral Vector-Based Personalized Vaccination Elicits Robust Neoantigen-Specific Antitumor T-Cell Responses.

Personalized vaccines targeting multiple neoantigens (nAgs) are a promising strategy for eliciting a diversified antitumor T-cell response to overcome tumor heterogeneity. NOUS-PEV is a vector-based personalized vaccine, expressing 60 nAgs and consists of priming with a nonhuman Great Ape Adenoviral vector (GAd20) followed by boosts with Modified Vaccinia Ankara. Here, we report data of a phase Ib trial of NOUS-PEV in combination with pembrolizumab in treatment-naïve patients with metastatic melanoma (NCT04990479). The feasibility of this approach was demonstrated by producing, releasing, and administering to 6 patients 11 of 12 vaccines within 8 weeks from biopsy collection to GAd20 administration. The regimen was safe, with no treatment-related serious adverse events observed and mild vaccine-related reactions. Vaccine immunogenicity was demonstrated in all evaluable patients receiving the prime/boost regimen, with detection of robust neoantigen-specific immune responses to multiple neoantigens comprising both CD4 and CD8 T cells. Expansion and diversification of vaccine-induced T-cell receptor (TCR) clonotypes was observed in the posttreatment biopsies of patients with clinical response, providing evidence of tumor infiltration by vaccine-induced neoantigen-specific T cells. These findings indicate the ability of NOUS-PEV to amplify and broaden the repertoire of tumor-reactive T cells to empower a diverse, potent, and durable antitumor immune response. Finally, a gene signature indicative of the reduced presence of activated T cells together with very poor expression of the antigen-processing machinery genes has been identified in pretreatment biopsies as a potential biomarker of resistance to the treatment.

Cortical bone architecture of hominid intermediate phalanges reveals functional signals of locomotion and manipulation.

Reconstruction of fossil hominin manual behaviors often relies on comparative analyses of extant hominid hands to understand the relationship between hand use and skeletal morphology. In this context, the intermediate phalanges remain understudied. Thus, here we investigate cortical bone morphology of the intermediate phalanges of extant hominids and compare it to the cortical structure of the proximal phalanges, to investigate the relationship between cortical bone structure and inferred loading during manual behaviors. Using micro-CT data, we analyze cortical bone structure of the intermediate phalangeal shaft of digits 2-5 in Pongo pygmaeus (n = 6 individuals), Gorilla gorilla (n = 22), Pan spp. (n = 23), and Homo sapiens (n = 23). The R package morphomap is used to study cortical bone distribution, cortical thickness and cross-sectional properties within and across taxa. Non-human great apes generally have thick cortical bone on the palmar shaft, with Pongo only having thick cortex on the peaks of the flexor sheath ridges, while African apes have thick cortex along the entire flexor sheath ridge and proximal to the trochlea. Humans are distinct in having thicker dorsal shaft cortex as well as thick cortex at the disto-palmar region of the shaft. Variation in cortical bone distribution and properties of the intermediate phalanges is consistent with differences in locomotor and manipulative behaviors in extant great apes. Comparisons between the intermediate and proximal phalanges reveals similar patterns of cortical bone distribution within each taxon but with potentially greater load experienced by the proximal phalanges, even in knuckle-walking African apes. This study provides a comparative context for the reconstruction of habitual hand use in fossil hominins and hominids.

Understanding others' preferences: A comparison across primate species and human societies.

We investigated children's and non-human great apes' ability to anticipate others' choices from their evident food preferences-regardless of whether these preferences deviate or align with one's own. We assessed children from three culturally-diverse societies (Namibia, Germany, and Samoa; N = 71; age range = 5-11) and four non-human great ape species (chimpanzees (Pan troglodytes), bonobos (Pan paniscus), gorillas (Gorilla gorilla), and orangutans (Pongo abelii); N = 25; age range = 7-29) regarding their choices in a dyadic food-retrieval task. Across conditions, participants' preferences were either aligned (same preference condition) or opposed (opposite preference condition) to those of their competitors. Children across societies altered their choices based on their competitor's preferences, indicating a cross-culturally recurrent capacity to anticipate others' choices relying on preferences-based inferences. In contrast to human children, all non-human great apes chose according to their own preferences but independent of those of their competitors. In sum, these results suggest that the tendency to anticipate others' choices based on their food preferences is cross-culturally robust and, among the great apes, most likely specific to humans.

Evaluating the Presence of Disgust in Animals.

The emotion of disgust in humans is widely considered to represent a continuation of the disease-avoidance behavior ubiquitous in animals. The extent to which analogs of human disgust are evident in nonhuman animals, however, remains unclear. The scant research explicitly investigating disgust in animals has predominantly focused on great apes and suggests that disgust might be present in a highly muted form. In this review, we outline the main approaches to disgust. We then briefly discuss disease-avoidance behavior in nonhuman animals, proposing a set of criteria against which evidence for the presence or absence of disgust in animals can be evaluated. The resultant decision tree takes into account other plausible causes of avoidance and aversion when evaluating whether it is likely that the behavior represents disgust. We apply this decision tree to evaluate evidence of disgust-like behavior (e.g., avoidance of carrion and avoidance of feces-contaminated food) in several examples, including nonhuman great apes. Finally, we consider the large disparity between disgust in humans compared to muted disgust in other great apes, examining the possibility that heightened disgust in humans is a relatively recent cultural acquisition.

Whither dominance? An enduring evolutionary legacy of primate sociality.

This article discusses dominance personality dimensions found in primates, particularly in the great apes, and how they compare to dominance in humans. Dominance traits are seen in virtually all primate species, and these dimensions reflect how adept an individual is at ascending within a social hierarchy. Among great apes, dominance is one of the most prominent personality factors but, in humans, dominance is usually modeled as a facet of extraversion. Social, cultural, and cognitive differences between humans and our closest ape relatives are explored, alongside humanity's hierarchical and egalitarian heritage. The basic characteristics of dominance in humans and nonhuman great apes are then described, alongside the similarities and differences between great apes. African apes live in societies each with its own hierarchical organization. Humans were a possible exception for some of our history, but more recently, hierarchies have dominated. The general characteristics of high-dominance humans, particularly those living in industrialized nations, are described. Dominance itself can be subdivided into correlated subfactors: domineering, prestige, and leadership. Various explanations have been posed for why dominance has declined in prominence within human personality factor structures, and several possibilities are evaluated. The value of dominance in personality research is discussed: dominance has links to, for instance, age, sex, aggression, self-esteem, locus of control, stress, health, and multiple socioeconomic status indicators. The piece concludes with recommendations for researchers who wish to assess dominance in personality.

Camera traps unveil demography, social structure, and home range of six unhabituated Western chimpanzee groups in the Moyen Bafing National Park, Guinea.

Precise estimates of population dynamics and social grouping patterns are required for effective conservation of wild animal populations. It is difficult to obtain such information on non-human great apes as they have slow reproductive rates. To gain a better understanding of demography in these populations, previous research has typically involved habituation\, a process that requires years. Here, we collected data continuously over year-long periods to monitor an unhabituated population of critically endangered Western chimpanzees (Pan troglodytes verus) in the Moyen Bafing National Park, Guinea. We used two arrays of 100 camera traps that were placed opportunistically in two distinct 100 km2 sites, named Bakoun and Koukoutamba. We identified 227 individuals in Bakoun and 207 in Koukoutamba through their unique facial features. Our camera trap data make clear that these individuals belong to six and seven closed groups, respectively. Six of those groups were near-completely sampled with an average minimum size of 46.8 individuals (range: 37-58), and a mean adult sex ratio of 1.32 (range: 0.93-2.10). We described the demographic composition of these groups and use Bayesian social network analysis to understand population structure. The network analyses suggested that the social bonds within the two populations were structured by sex homophily, with male chimpanzees being more or equally likely to be observed together than other adult associations. Through estimation of minimum convex polygons, we described the minimum home range for those groups. Compared to other chimpanzee groups living in a similar environment (mosaic savanna-forest), the Moyen Bafing region seems to host a high-density of chimpanzees with small home ranges for their group size. Our research highlights the potential of camera traps for studying the demographic composition of chimpanzee populations with high resolution and obtaining crucial information on several groups in a time-efficient and cost-effective way.

Apes and agriculture

Non-human great apes – chimpanzees, gorillas, bonobos, and orangutans – are threatened by agricultural expansion, particularly from rice, cacao, cassava, maize, and oil palm cultivation. Agriculture replaces and fragments great ape habitats, bringing them closer to humans and often resulting in conflict. Though the impact of agriculture on great apes is well-recognized, there is still a need for a more nuanced understanding of specific contexts and associated negative impacts on habitats and populations. Here we review these contexts and their implications for great apes. We estimate that within their African and South-East Asian ranges, there are about 100 people for each great ape. Given that most apes live outside strictly protected areas and the growing human population and increasing demand for resources in these landscapes, it will be challenging to balance the needs of both humans and great apes. Further habitat loss is expected, particularly in Africa, where compromises must be sought to re-direct agricultural expansion driven by subsistence farmers with small fields (generally <0.64 ha) away from remaining great ape habitats. To promote coexistence between humans and great apes, new approaches and financial models need to be implemented at local scales. Overall, optimized land use planning and effective implementation, along with strategic investments in agriculture and wildlife conservation, can improve the synergies between conservation and food production. Effective governance and conservation financing are crucial for optimal outcomes in both conservation and food security. Enforcing forest conservation laws, engaging in trade policy discussions, and integrating policies on trade, food security, improved agricultural techniques, and sustainable food systems are vital to prevent further decline in great ape populations. Saving great apes requires a thorough consideration of specific agricultural contexts.

Empirical challenges from the comparative and developmental literature to the Shared Intentionality Theory - a review of alternative data on recursive mind reading, prosociality, imitation and cumulative culture.

Humans have an irresistible inclination to coordinate actions with others, leading to species-unique forms of cooperation. According to the highly influential Shared Intentionality Theory (SITh), human cooperation is made possible by shared intentionality (SI), typically defined as a suite of socio-cognitive and motivational traits for sharing psychological states with others, thereby enabling individuals to engage in joint action in the mutually aware pursuit of shared goals. SITh theorises that SI evolved as late as 400,000 years ago, when our ancestors (in particular, Homo heidelbergensis) turned to a kind of food procurement that obligatorily required joint coordinated action. SI is, thus, hypothesized to be absent in other extant species, including our closest genetic relatives, the nonhuman great apes ("apes"). According to SITh, ape psychology is exclusively driven by individualistic motivations, as opposed to human psychology which is uniquely driven by altruistic motivations. The evolutionary scenario proposed by SITh builds on a series of findings from socio-cognitive research with apes and human children, and on the assumption that abilities expressed early in human development are human universals, unlikely to have been shaped by socio-cultural influences. Drawing on the primatological and developmental literature, we provide a systematic - albeit selective - review of SITh-inconsistent findings concerning psychological and behavioural traits theorised to be constitutive of SI. The findings we review pertain to all three thematic clusters typically addressed in SITh: (i) recursive mind reading; (ii) prosociality; (iii) imitation and cumulative culture. We conclude that such alternative data undermine two core SITh claims: the late evolutionary emergence of SI and the radical divide between ape and human psychology. We also discuss several conceptual and methodological limitations that currently hamper reliable comparative research on SI, in particular those engendered by Western-centric biases in the social sciences, where an overreliance on Western samples has promoted the formulation of Western-centric conceptualisations, operationalisations and methodologies.

Great ape interaction: Ladyginian but not Gricean.

Nonhuman great apes inform one another in ways that can seem very humanlike. Especially in the gestural domain, their behavior exhibits many similarities with human communication, meeting widely used empirical criteria for intentionality. At the same time, there remain some manifest differences, most obviously the enormous range and scope of human expression. How to account for these similarities and differences in a unified way remains a major challenge. Here, we make a key distinction between the expression of intentions (Ladyginian) and the expression of specifically informative intentions (Gricean), and we situate this distinction within a "special case of" framework for classifying different modes of attention manipulation. We hence describe how the attested tendencies of great ape interaction-for instance, to be dyadic rather than triadic, to be about the here-and-now rather than "displaced," and to have a high degree of perceptual resemblance between form and meaning-are products of its Ladyginian but not Gricean character. We also reinterpret video footage of great ape gesture as Ladyginian but not Gricean, and we distinguish several varieties of meaning that are continuous with one another. We conclude that the evolutionary origins of linguistic meaning lie not in gradual changes in communication systems, but rather in gradual changes in social cognition, and specifically in what modes of attention manipulation are enabled by a species' cognitive phenotype: first Ladyginian and in turn Gricean. The second of these shifts rendered humans, and only humans, "language ready."

A test of memory for stimulus sequences in great apes.

Identifying cognitive capacities underlying the human evolutionary transition is challenging, and many hypotheses exist for what makes humans capable of, for example, producing and understanding language, preparing meals, and having culture on a grand scale. Instead of describing processes whereby information is processed, recent studies have suggested that there are key differences between humans and other animals in how information is recognized and remembered. Such constraints may act as a bottleneck for subsequent information processing and behavior, proving important for understanding differences between humans and other animals. We briefly discuss different sequential aspects of cognition and behavior and the importance of distinguishing between simultaneous and sequential input, and conclude that explicit tests on non-human great apes have been lacking. Here, we test the memory for stimulus sequences-hypothesis by carrying out three tests on bonobos and one test on humans. Our results show that bonobos' general working memory decays rapidly and that they fail to learn the difference between the order of two stimuli even after more than 2,000 trials, corroborating earlier findings in other animals. However, as expected, humans solve the same sequence discrimination almost immediately. The explicit test on whether bonobos represent stimulus sequences as an unstructured collection of memory traces was not informative as no differences were found between responses to the different probe tests. However, overall, this first empirical study of sequence discrimination on non-human great apes supports the idea that non-human animals, including the closest relatives to humans, lack a memory for stimulus sequences. This may be an ability that sets humans apart from other animals and could be one reason behind the origin of human culture.

Evolution of the human tongue and emergence of speech biomechanics.

The tongue is one of the organs most central to human speech. Here, the evolution and species-unique properties of the human tongue is traced, via reference to the apparent articulatory behavior of extant non-human great apes, and fossil findings from early hominids - from a point of view of articulatory phonetics, the science of human speech production. Increased lingual flexibility provided the possibility of mapping of articulatory targets, possibly via exaptation of manual-gestural mapping capacities evident in extant great apes. The emergence of the human-specific tongue, its properties, and morphology were crucial to the evolution of human articulate speech.

Great apes reach momentary altered mental states by spinning

Among animals, humans stand out in their consummate propensity to self-induce altered states of mind. Archaeology, history and ethnography show these activities have taken place since the beginnings of civilization, yet their role in the emergence and evolution of the human mind itself remains debatable. The means through which modern humans actively alter their experience of self and reality frequently depend on psychoactive substances, but it is uncertain whether psychedelics or other drugs were part of the ecology or culture of pre-human ancestors. Moreover, (nonhuman) great apes in captivity are currently being retired from medical research, rendering comparative approaches thus far impracticable. Here, we circumvent this limitation by harnessing the breadth of publicly available YouTube data to show that apes engage in rope spinning during solitary play. When spinning, the apes achieved speeds sufficient to alter self-perception and situational awareness that were comparable to those tapped for transcendent experiences in humans (e.g. Sufi whirling), and the number of revolutions spun predicted behavioural evidence for dizziness. Thus, spinning serves as a self-sufficient means of changing body-mind responsiveness in hominids. A proclivity for such experiences is shared between humans and great apes, and provides an entry point for the comparative study of the mechanisms, functions, and adaptive value of altered states of mind in human evolution.

The shifting shelf task: a new, non-verbal measure for attentional set shifting.

Attentional set shifting is a core ingredient of cognition, allowing for fast adaptation to changes in the environment. How this skill compares between humans and other primates is not well known. We examined performance of 3- to 5-year-old children and chimpanzees on a new attentional set shifting task. We presented participants with two shelves holding the same set of four boxes. To choose the correct box on each shelf, one has to switch attention depending on which shelf one is currently presented with. Experiment 1 (forty-six 3- to 5-year olds, predominantly European White) established content validity, showing that the majority of errors were specific switching mistakes indicating failure to shift attention. Experiment 2 (one hundred and seventy-eight 3- to 6-year olds, predominantly European White) showed that older children made fewer mistakes, but if mistakes were made, a larger proportion were switching mistakes rather than 'random' errors. Experiment 3 (52 chimpanzees) established suitability of the task for non-human great apes and showed that chimpanzees' performance was comparable to the performance of 3- and 4-year olds, but worse than 5-year olds. These results suggest that chimpanzees and young children share attentional set shifting capacities, but that there are unique changes in the human lineage from 5 years of age.