Predictions about reward outcomes in rhesus monkeys.

Human infants and nonhuman animals respond to surprising events by looking longer at unexpected than expected situations. These looking responses provide core cognitive evidence that nonverbal minds make predictions about possible outcomes and detect when these predictions fail to match reality. We propose that this phenomenon has crucial parallels with the processes of reward prediction error, indexing the difference between expected and actual reward outcomes. Most work on reward prediction errors to date involves neurobiological techniques that cannot be implemented in many relevant populations, so we developed a novel behavioral task to assess monkeys' predictions about reward outcomes using looking time responses. In Study 1, we tested how semi-free-ranging monkeys (n = 210) responded to positive error (more rewards than expected), negative error (less rewards than expected), and a number control. We found that monkeys looked longer at a given reward when it was unexpectedly large or small, compared to when the same quantity was expected. In Study 2, we compared responses in the positive error condition in monkeys ranging from infancy to old age (n = 363), to assess lifespan changes in sensitivity to reward predictions. We found that adolescent monkeys showed heightened responses to unexpected rewards, similar to patterns seen in humans, but showed no changes during aging. These results suggest that monkeys' looking responses can be used to track their predictions about rewards, and that monkeys share some developmental signatures of reward sensitivity with humans, providing a new approach to access cognitive processes underlying reward-based decision making. (PsycInfo Database Record (c) 2024 APA, all rights reserved).

Advancing methods for the biodemography of aging within social contexts.

Several social dimensions including social integration, status, early-life adversity, and their interactions across the life course can predict health, reproduction, and mortality in humans. Accordingly, the social environment plays a fundamental role in the emergence of phenotypes driving the evolution of aging. Recent work placing human social gradients on a biological continuum with other species provides a useful evolutionary context for aging questions, but there is still a need for a unified evolutionary framework linking health and aging within social contexts. Here, we summarize current challenges to understand the role of the social environment in human life courses. Next, we review recent advances in comparative biodemography and propose a biodemographic perspective to address socially driven health phenotype distributions and their evolutionary consequences using a nonhuman primate population. This new comparative approach uses evolutionary demography to address the joint dynamics of populations, social dimensions, phenotypes, and life history parameters. The long-term goal is to advance our understanding of the link between individual social environments, population-level outcomes, and the evolution of aging.

Observational approaches to chimpanzee behavior in an African sanctuary: Implications for research, welfare, and capacity-building.

Research in African ape sanctuaries has emerged as an important context for our understanding of comparative cognition and behavior. While much of this work has focused on experimental studies of cognition, these animals semi-free-range in forest habitats and therefore can also provide important information about the behavior of primates in socioecologically-relevant naturalistic contexts. In this "New Approaches" article, we describe a project where we implemented a synthetic program of observational data collection at Ngamba Island Chimpanzee Sanctuary in Uganda, directly modeled after long-term data collection protocols at the Kibale Chimpanzee Project in Uganda, a wild chimpanzee field site. The foundation for this project was a strong partnership between sanctuary staff, field site staff, and external researchers. We describe how we developed a data-collection protocol through discussion and collaboration among these groups, and trained sanctuary caregivers to collect novel observational data using these protocols. We use these data as a case study to examine: (1) how behavioral observations in sanctuaries can inform primate welfare and care practices, such as by understanding aggression within the group; (2) how matched observational protocols across sites can inform our understanding of primate behavior across different contexts, including sex differences in social relationships; and (3) how more robust collaborations between foreign researchers and local partners can support capacity-building in primate range countries, along with mentoring and training students more broadly.

Viruses in saliva from sanctuary chimpanzees (Pan troglodytes) in Republic of Congo and Uganda.

Pathogen surveillance for great ape health monitoring has typically been performed on non-invasive samples, primarily feces, in wild apes and blood in sanctuary-housed apes. However, many important primate pathogens, including known zoonoses, are shed in saliva and transmitted via oral fluids. Using metagenomic methods, we identified viruses in saliva samples from 46 wild-born, sanctuary-housed chimpanzees at two African sanctuaries in Republic of Congo and Uganda. In total, we identified 20 viruses. All but one, an unclassified CRESS DNA virus, are classified in five families: Circoviridae, Herpesviridae, Papillomaviridae, Picobirnaviridae, and Retroviridae. Overall, viral prevalence ranged from 4.2% to 87.5%. Many of these viruses are ubiquitous in primates and known to replicate in the oral cavity (simian foamy viruses, Retroviridae; a cytomegalovirus and lymphocryptovirus; Herpesviridae; and alpha and gamma papillomaviruses, Papillomaviridae). None of the viruses identified have been shown to cause disease in chimpanzees or, to our knowledge, in humans. These data suggest that the risk of zoonotic viral disease from chimpanzee oral fluids in sanctuaries may be lower than commonly assumed.

Distinct developmental trajectories for risky and impulsive decision-making in chimpanzees.

Human adolescence is characterized by a suite of changes in decision-making and emotional regulation that promote risky and impulsive behavior. Accumulating evidence suggests that behavioral and physiological shifts seen in human adolescence are shared by some primates, yet it is unclear if the same cognitive mechanisms are recruited. We examined developmental changes in risky choice, intertemporal choice, and emotional responses to decision outcomes in chimpanzees, our closest-living relatives. We found that adolescent chimpanzees were more risk-seeking than adults, as in humans. However, chimpanzees showed no developmental change in intertemporal choice, unlike humans, although younger chimpanzees did exhibit elevated emotional reactivity to waiting compared to adults. Comparisons of cortisol and testosterone indicated robust age-related variation in these biomarkers, and patterns of individual differences in choices, emotional reactivity, and hormones also supported a developmental dissociation between risk and choice impulsivity. These results show that some but not all core features of human adolescent decision-making are shared with chimpanzees. (PsycInfo Database Record (c) 2023 APA, all rights reserved).

Viruses in sanctuary chimpanzees across Africa.

Infectious disease is a major concern for both wild and captive primate populations. Primate sanctuaries in Africa provide critical protection to thousands of wild-born, orphan primates confiscated from the bushmeat and pet trades. However, uncertainty about the infectious agents these individuals potentially harbor has important implications for their individual care and long-term conservation strategies. We used metagenomic next-generation sequencing to identify viruses in blood samples from chimpanzees (Pan troglodytes) in three sanctuaries in West, Central, and East Africa. Our goal was to evaluate whether viruses of human origin or other "atypical" or unknown viruses might infect these chimpanzees. We identified viruses from eight families: Anelloviridae, Flaviviridae, Genomoviridae, Hepadnaviridae, Parvoviridae, Picobirnaviridae, Picornaviridae, and Rhabdoviridae. The majority (15/26) of viruses identified were members of the family Anelloviridae and represent the genera Alphatorquevirus (torque teno viruses) and Betatorquevirus (torque teno mini viruses), which are common in chimpanzees and apathogenic. Of the remaining 11 viruses, 9 were typical constituents of the chimpanzee virome that have been identified in previous studies and are also thought to be apathogenic. One virus, a novel tibrovirus (Rhabdoviridae: Tibrovirus) is related to Bas-Congo virus, which was originally thought to be a human pathogen but is currently thought to be apathogenic, incidental, and vector-borne. The only virus associated with disease was rhinovirus C (Picornaviridae: Enterovirus) infecting one chimpanzee subsequent to an outbreak of respiratory illness at that sanctuary. Our results suggest that the blood-borne virome of African sanctuary chimpanzees does not differ appreciably from that of their wild counterparts, and that persistent infection with exogenous viruses may be less common than often assumed.

The Evolution of Cognitive Control in Lemurs.

Cognitive control, or executive function, is a key feature of human cognition, allowing individuals to plan, acquire new information, or adopt new strategies when the circumstances change. Yet it is unclear which factors promote the evolution of more sophisticated executive-function abilities such as those possessed by humans. Examining cognitive control in nonhuman primates, our closest relatives, can help to identify these evolutionary processes. Here, we developed a novel battery to experimentally measure multiple aspects of cognitive control in primates: temporal discounting, motor inhibition, short-term memory, reversal learning, novelty responses, and persistence. We tested lemur species with targeted, independent variation in both ecological and social features (ruffed lemurs, Coquerel's sifakas, ring-tailed lemurs, and mongoose lemurs; N = 39) and found that ecological rather than social characteristics best predicted patterns of cognitive control across these species. This highlights the importance of integrating cognitive data with species' natural history to understand the origins of complex cognition.

The origins of cognitive flexibility in chimpanzees.

Cognitive flexibility is a core component of executive function, a suite of cognitive capacities that enables individuals to update their behavior in dynamic environments. Human executive functions are proposed to be enhanced compared to other species, but this inference is based primarily on neuroanatomical studies. To address this, we examined the nature and origins of cognitive flexibility in chimpanzees, our closest living relatives. Across three studies, we examined different components of cognitive flexibility using reversal learning tasks where individuals first learned one contingency and then had to shift responses when contingencies flipped. In Study 1, we tested n = 82 chimpanzees ranging from juvenility to adulthood on a spatial reversal task, to characterize the development of basic shifting skills. In Study 2, we tested how n = 24 chimpanzees use spatial versus arbitrary perceptual information to shift, a proposed difference between human and nonhuman cognition. In Study 3, we tested n = 40 chimpanzees on a probabilistic reversal task. We found an extended developmental trajectory for basic shifting and shifting in response to probabilistic feedback-chimpanzees did not reach mature performance until late in ontogeny. Additionally, females were faster to shift than males were. We also found that chimpanzees were much more successful when using spatial versus perceptual cues, and highly perseverative when faced with probabilistic versus consistent outcomes. These results identify both core features of chimpanzee cognitive flexibility that are shared with humans, as well as constraints on chimpanzee cognitive flexibility that may represent evolutionary changes in human cognitive development.

Sensitivity to line-of-sight in tolerant versus despotic macaques (Macaca sylvanus and Macaca mulatta).

Complex social life is considered important to the evolution of cognition in primates. One key aspect of primate social interactions concerns the degree of competition that individuals face in their social group. To examine how social tolerance versus competition shapes social cognition, we experimentally assessed capacities for flexible gaze-following in more tolerant Barbary macaques (Macaca sylvanus) and compared to previous data from despotic rhesus macaques (Macaca mulatta). Monkeys experienced one of two possible conditions. In the barrier condition, they observed an actor look upwards into an overheard barrier, so they could not directly see the target of the actor's gaze without reorienting. In the no barrier condition, they observed an actor look upwards without a barrier blocking her line-of-sight, so they could observe the target of the actor's gaze by also looking upwards. Both species (N = 58 Barbary macaques, 64 rhesus macaques) could flexibly modulate their gaze responses to account for the demonstrator's line of sight, looking up more often when no barrier was present, and this flexible modulation declined with age in both species. However, neither species preferentially approached to look inside the barrier when their view of the target location was obscured, although rhesus macaques approached more overall. This pattern suggests that both tolerant and despotic macaques exhibit similar capacities to track other's line of sight and do not preferentially reorient their bodies to observe what an actor looks at in this situation. This contrasts with other work indicating that competitive primates are especially adept at some aspects of theory of mind. Thus, it is important to understand both the similarities and differences in the social-cognitive abilities of primates with different social styles. (PsycInfo Database Record (c) 2022 APA, all rights reserved).

Variation in primate decision-making under uncertainty and the roots of human economic behaviour.

Uncertainty is a ubiquitous component of human economic behaviour, yet people can vary in their preferences for risk across populations, individuals and different points in time. As uncertainty also characterizes many aspects of animal decision-making, comparative research can help evaluate different potential mechanisms that generate this variation, including the role of biological differences or maturational change versus cultural learning, as well as identify human-unique components of economic decision-making. Here, we examine decision-making under risk across non-human primates, our closest relatives. We first review theoretical approaches and current methods for understanding decision-making in animals. We then assess the current evidence for variation in animal preferences between species and populations, between individuals based on personality, sex and age, and finally, between different contexts and individual states. We then use these primate data to evaluate the processes that can shape human decision-making strategies and identify the primate foundations of human economic behaviour. This article is part of the theme issue 'Existence and prevalence of economic behaviours among non-human primates'.

The evolutionary origins of natural pedagogy: Rhesus monkeys show sustained attention following nonsocial cues versus social communicative signals.

The natural pedagogy hypothesis proposes that human infants preferentially attend to communicative signals from others, facilitating rapid cultural learning. In this view, sensitivity to such signals is a uniquely human adaptation and as such nonhuman animals should not produce or utilize these communicative signals. We test these evolutionary predictions by examining sensitivity to communicative cues in 206 rhesus monkeys (Macaca mulatta) using an expectancy looking time task modeled on prior work with infants. Monkeys observed a human actor who either made eye contact and vocalized to the monkey (social cue), or waved a fruit in front of her face and produced a tapping sound (nonsocial cue). The actor then either looked at an object (referential look) or looked toward empty space (look away). We found that, unlike human infants in analogous situations, rhesus monkeys looked longer at events following nonsocial cues, regardless of the demonstrator's subsequent looking behavior. Moreover younger and older monkeys showed similar patterns of responses across development. These results provide support for the natural pedagogy hypothesis, while also highlighting evolutionary changes in human sensitivity to communicative signals.

Social selectivity in aging wild chimpanzees.

Humans prioritize close, positive relationships during aging, and socioemotional selectivity theory proposes that this shift causally depends on capacities for thinking about personal future time horizons. To examine this theory, we tested for key elements of human social aging in longitudinal data on wild chimpanzees. Aging male chimpanzees have more mutual friendships characterized by high, equitable investment, whereas younger males have more one-sided relationships. Older males are more likely to be alone, but they also socialize more with important social partners. Further, males show a relative shift from more agonistic interactions to more positive, affiliative interactions over their life span. Our findings indicate that social selectivity can emerge in the absence of complex future-oriented cognition, and they provide an evolutionary context for patterns of social aging in humans.

Healthy cardiovascular biomarkers across the lifespan in wild-born chimpanzees (Pan troglodytes).

Chimpanzees (Pan troglodytes) are a crucial model for understanding the evolution of human health and longevity. Cardiovascular disease is a major source of mortality during ageing in humans and therefore a key issue for comparative research. Current data indicate that compared to humans, chimpanzees have proatherogenic blood lipid profiles, an important risk factor for cardiovascular disease in humans. However, most work to date on chimpanzee lipids come from laboratory-living populations where lifestyles diverge from a wild context. Here, we examined cardiovascular profiles in chimpanzees living in African sanctuaries, who range semi-free in large forested enclosures, consume a naturalistic diet, and generally experience conditions more similar to a wild chimpanzee lifestyle. We measured blood lipids, body weight and body fat in 75 sanctuary chimpanzees and compared them to publicly available data from laboratory-living chimpanzees from the Primate Aging Database. We found that semi-free-ranging chimpanzees exhibited lower body weight and lower levels of lipids that are risk factors for human cardiovascular disease, and that some of these disparities increased with age. Our findings support the hypothesis that lifestyle can shape health indices in chimpanzees, similar to effects observed across human populations, and contribute to an emerging understanding of human cardiovascular health in an evolutionary context. This article is part of the theme issue 'Evolution of the primate ageing process'.

Insights from evolutionarily relevant models for human ageing.

As the world confronts the health challenges of an ageing population, there has been dramatically increased interest in the science of ageing. This research has overwhelmingly focused on age-related disease, particularly in industrialized human populations and short-lived laboratory animal models. However, it has become clear that humans and long-lived primates age differently than many typical model organisms, and that many of the diseases causing death and disability in the developed world are greatly exacerbated by modern lifestyles. As such, research on how the human ageing process evolved is vital to understanding the origins of prolonged human lifespan and factors increasing vulnerability to degenerative disease. In this issue, we highlight emerging comparative research on primates, highlighting the physical, physiological, behavioural and cognitive processes of ageing. This work comprises data and theory on non-human primates, as well as under-represented data on humans living in small-scale societies, which help elucidate how environment shapes senescence. Component papers address (i) the critical processes that comprise senescence in long-lived primates; (ii) the social, ecological or individual characteristics that predict variation in the pace of ageing; and (iii) the complicated relationship between ageing trajectories and disease outcomes. Collectively, this work provides essential comparative, evolutionary data on ageing and demonstrates its unique potential to inform our understanding of the human ageing process. This article is part of the theme issue 'Evolution of the primate ageing process'.

Shifting sociality during primate ageing.

Humans exhibit major age-related shifts in social relationships along with changes in social and emotional psychological processes that underpin these behavioural shifts. Does social ageing in non-human primates follow similar patterns, and if so, what are the ultimate evolutionary consequences of these social shifts? Here we synthesize empirical evidence for shifts in social behaviour and underlying psychological processes across species. Focusing on three elements of social behaviour and cognition that are important for humans-propensities to engage with others, the positive versus negative valence of these interactions, and capabilities to influence others, we find evidence for wide variation in the trajectories of these characteristics across primates. Based on this, we identify potential modulators of the primate social ageing process, including social organization, sex and dominance status. Finally, we discuss how comparative research can contextualize human social ageing. This article is part of the theme issue 'Evolution of the primate ageing process'.

Rhesus macaques use probabilities to predict future events.

Humans can use an intuitive sense of statistics to make predictions about uncertain future events, a cognitive skill that underpins logical and mathematical reasoning. Recent research shows that some of these abilities for statistical inferences can emerge in preverbal infants and non-human primates such as apes and capuchins. An important question is therefore whether animals share the full complement of intuitive reasoning abilities demonstrated by humans, as well as what evolutionary contexts promote the emergence of such skills. Here, we examined whether free-ranging rhesus macaques (Macaca mulatta) can use probability information to infer the most likely outcome of a random lottery, in the first test of whether primates can make such inferences in the absence of direct prior experience. We developed a novel expectancy-violation looking time task, adapted from prior studies of infants, in order to assess the monkeys' expectations. In Study 1, we confirmed that monkeys (n = 20) looked similarly at different sampled items if they had no prior knowledge about the population they were drawn from. In Study 2, monkeys (n = 80) saw a dynamic 'lottery' machine containing a mix of two types of fruit outcomes, and then saw either the more common fruit (expected trial) or the relatively rare fruit (unexpected trial) fall from the machine. We found that monkeys looked longer when they witnessed the unexpected outcome. In Study 3, we confirmed that this effect depended on the causal relationship between the sample and the population, not visual mismatch: monkeys (n = 80) looked equally at both outcomes if the experimenter pulled the sampled item from her pocket. These results reveal that rhesus monkeys spontaneously use information about probability to reason about likely outcomes, and show how comparative studies of nonhumans can disentangle the evolutionary history of logical reasoning capacities.

Economic trust in young children.

Mutually beneficial interactions often require trust that others will reciprocate. Such interpersonal trust is foundational to evolutionarily unique aspects of human social behaviour, such as economic exchange. In adults, interpersonal trust is often assessed using the 'trust game', in which a lender invests resources in a trustee who may or may not repay the loan. This game captures two crucial elements of economic exchange: the potential for greater mutual benefits by trusting in others, and the moral hazard that others may betray that trust. While adults across cultures can trust others, little is known about the developmental origins of this crucial cooperative ability. We developed the first version of the trust game for use with young children that addresses these two components of trust. Across three experiments, we demonstrate that 4- and 6-year-olds recognize opportunities to invest in others, sharing more when reciprocation is possible than in a context measuring pure generosity. Yet, children become better with age at investing in trustworthy over untrustworthy partners, indicating that this cooperative skill emerges later in ontogeny. Together, our results indicate that young children can engage in complex economic exchanges involving judgements about interpersonal trust and show increasing sensitivity to appropriate partners over development.

Flexible gaze-following in rhesus monkeys.

Humans are characterized by complex social cognitive abilities that emerge early in development. Comparative studies of nonhuman primates can illuminate the evolutionary history of these social capacities. We examined the cognitive skills that rhesus monkeys (Macaca mulatta) use to follow gaze, a foundational skill in human social development. While rhesus monkeys can make inferences about others' gaze when competing, it is unclear how they think about gaze information in other contexts. In study 1, monkeys (n = 64) observed a demonstrator look upwards either in a barrier condition where a box was overhead, so that monkeys could not see the target of her gaze, or a no barrier condition where nothing blocked her view. In study 2, monkeys (n = 59) could approach to observe the target of the demonstrator's gaze when the demonstrator looked behind a barrier on the ground or, in the no barrier condition, behind a window frame in the same location. Monkeys were more likely to directly look up in study 1 if they could initially see the location where the demonstrator was looking, but they did not preferentially reorient their bodies to observe the out-of-view location when they could not see that location. In study 2, monkeys did preferentially reorient, but at low rates. This indicates that rhesus monkeys can use social cognitive processes outside of competitive contexts to model what others can or cannot see, but may not be especially motivated to see what others look at in non-competitive contexts, as they reorient infrequently or in an inconsistent fashion. These similarities and differences between gaze-following in monkeys and children can help to illuminate the evolution of human social cognition.

Ecological rationality: Convergent decision-making in apes and capuchins.

Humans and other animals appear to defy many principles of economic 'rationality' when making decisions. Here, we use an ecological rationality framework to examine patterns of decision-making across species to illuminate the origins of these strategies. We argue that examples of convergent evolution-the independent emergence of similar traits in species facing similar environments-can provide a crucial test for evolutionary theories of decision-making. We first review theoretical work from evolutionary biology proposing that many economically-puzzling patterns of decision-making may be biologically adaptive when considering the environment in which they are made. We then focus on convergence in ecology, behavior, and cognition of apes and capuchin monkeys as an example of how to apply this ecological framework across species. We review evidence that wild chimpanzees and capuchins, despite being distantly related, both exploit ecological niches characterized by costly extractive foraging and risky hunting behaviors. We then synthesize empirical studies comparing these species' decision preferences. In fact, both capuchins and chimpanzees exhibit high tolerance for delays in inter-temporal choice tasks, as well as a preference for risky outcomes when making decisions under uncertainty. Moreover, these species exhibit convergent psychological mechanisms for choices, including emotional responses to decision outcomes and sensitivity to social context. Finally, we argue that identifying the evolutionary pressures driving the emergence of specific decision strategies can shed light into the adaptive nature of human economic preferences.

Heterochrony in chimpanzee and bonobo spatial memory development.

OBJECTIVES: The emergence of human-unique cognitive abilities has been linked to our species' extended juvenile period. Comparisons of cognitive development across species can provide new insights into the evolutionary mechanisms shaping cognition. This study examined the development of different components of spatial memory, cognitive mechanisms that support complex foraging, by comparing two species with similar life history that vary in wild ecology: bonobos (Pan paniscus) and chimpanzees (Pan troglodytes). MATERIALS AND METHODS: Spatial memory development was assessed using a cross-sectional experimental design comparing apes ranging from infancy to adulthood. Study 1 tested 73 sanctuary-living apes on a task examining recall of a single location after a 1-week delay, compared to an earlier session. Study 2 tested their ability to recall multiple locations within a complex environment. Study 3 examined a subset of individuals from Study 2 on a motivational control task. RESULTS: In Study 1, younger bonobos and chimpanzees of all ages exhibited improved performance in the test session compared to their initial learning experience. Older bonobos, in contrast, did not exhibit a memory boost in performance after the delay. In Study 2, older chimpanzees exhibited an improved ability to recall multiple locations, whereas bonobos did not exhibit any age-related differences. In Study 3, both species were similarly motivated to search for food in the absence of memory demands. DISCUSSION: These results indicate that closely related species with similar life history characteristics can exhibit divergent patterns of cognitive development, and suggests a role of socioecological niche in shaping patterns of cognition in Pan.