Signatures of adaptive evolution in platyrrhine primate genomes.

The platyrrhine family Cebidae (capuchin and squirrel monkeys) exhibit among the largest primate encephalization quotients. Each cebid lineage is also characterized by notable lineage-specific traits, with capuchins showing striking similarities to Hominidae such as high sensorimotor intelligence with tool use, advanced cognitive abilities, and behavioral flexibility. Here, we take a comparative genomics approach, performing genome-wide tests for positive selection across five cebid branches, to gain insight into major periods of cebid adaptive evolution. We uncover candidate targets of selection across cebid evolutionary history that may underlie the emergence of lineage-specific traits. Our analyses highlight shifting and sustained selective pressures on genes related to brain development, longevity, reproduction, and morphology, including evidence for cumulative and diversifying neurobiological adaptations across cebid evolution. In addition to generating a high-quality reference genome assembly for robust capuchins, our results lend to a better understanding of the adaptive diversification of this distinctive primate clade.

Capuchin monkeys' (Sapajus [Cebus] apella) categorization of photos of unknown male conspecifics suggests attention to fWHR and a dominance bias.

The ability to quickly perceive others' rank minimizes costs by helping individuals behave appropriately when interacting with strangers. Indeed, humans and at least some other species can quickly determine strangers' rank or dominance based only on physical features without observing others' interactions or behavior. Nonhuman primates can determine strangers' ranks by observing their interactions, and some evidence suggests that at least some cues to dominance, such as facial width-to-height ratio (fWHR), are also present in other primates. However, it is unknown whether they can determine strangers' rank simply by looking at their faces, rather than observing their interactions. If so, this would suggest selective pressure across the primates on both cues to dominance and the ability to detect those cues accurately. To address this, we examined the ability of male and female tufted capuchin monkeys (Sapajus [Cebus] apella) to categorize images of the faces of unknown conspecifics (Sapajus from different colonies) and humans (computer-generated and real) as dominant or nondominant based only on still images. Capuchins' categorization of unknown conspecific faces was consistent with fWHR, a cue to dominance, although there was a strong tendency to categorize strangers as dominant, particularly for males. This was true despite the continued correct categorization of known individuals. In addition, capuchins did not categorize human strangers in accordance with external pre-ratings of dominance by independent human raters, despite the availability of the same cue, fWHR. We consider these results in the context of capuchin socio-ecology and what they mean for the evolution of rapid decision-making in social contexts.

Dogs take into account the actions of a human partner in a cooperative task.

Humans stand out for their capacity to flexibly cooperate, possibly because they understand their partners' role. Researchers have explored if such understanding is unique to humans by assessing whether non-human species wait to manipulate a cooperative apparatus until a delayed partner arrives. If animals do wait, then it is assumed that they recognize the need for a partner. However, success in these tasks may be the result of social facilitation, while failure may be due to poor inhibitory control. Moreover, this approach does not test if animals take their partners' actions into account. Here we trained dogs to press a button simultaneously with their human partner. Afterwards, we tested them in several conditions to disentangle which elements of their partner's behaviour they take into account. Dogs waited to press the button until the delayed partner arrived, the button was available to the partner and the partner acted (pressed the button). We found no relationship between inhibitory control and success. We conclude that dogs are not merely reacting to the presence of their human partners, but are also taking their actions into account when coordinating with them.

Under pressure: the interaction between high-stakes contexts and individual differences in decision-making in humans and non-human species.

Observed behavior can be the result of complex cognitive processes that are influenced by environmental factors, physiological process, and situational features. Pressure, a feature of a situation in which an individual's outcome is impacted by his or her own ability to perform, has been traditionally treated as a human-specific phenomenon and only recently have pressure-related deficits been considered in relation to other species. However, there are strong similarities in biological and cognitive systems among mammals (and beyond), and high-pressure situations are at least theoretically common in the wild. We hypothesize that other species are sensitive to pressure and that we can learn about the evolutionary trajectory of pressure responses by manipulating pressure experimentally in these other species. Recent literature indicates that, as in humans, pressure influences responses in non-human primates, with either deficits in ability to perform ("choking") or an ability to thrive when the stakes are high. Here, we synthesize the work to date on performance under pressure in humans and how hormones might be related to individual differences in responses. Then, we discuss why we would expect to see similar effects of pressure in non-humans and highlight the existing evidence for how other species respond. We argue that evidence suggests that other species respond to high-pressure contexts in similar ways as humans, and that responses to pressure are a critical missing piece of our understanding of cognition in human and non-human animals. Understanding pressure's effects could provide insight into individual variation in decision-making in comparative cognition and the evolution of human decision-making.

Oxytocin increases during fur-rubbing regardless of level of social contact in tufted capuchin monkeys.

Social interactions induce oxytocin release in many social species, suggesting that oxytocin is a critical part of social bonding among individuals. However, oxytocin also increases as a result of physical contact and stimulation, making it unclear which features of affiliative behaviors (for instance, social interaction or physical contact with a conspecific) drive the oxytocin increase observed after engaging in these behaviors. We attempted to tease this apart by studying the differential effect of social interaction, visual coordination with a conspecific, and physical stimulation during the fur-rubbing behavior of tufted capuchin monkeys (Sapajus [Cebus] apella), which often involves social contact with groupmates but is in some cases performed alone. We induced fur-rubbing by providing onions under three conditions: when capuchins had physical access to their social group and fur-rubbed in contact with groupmates (social condition), when capuchins were separated from their social group but could still see them fur-rub (visual coordination), and when capuchins were physically and visually separated from their groupmates (physical stimulation only). We assessed urinary oxytocin in these three conditions and compared them to a control condition in which apples were provided and no fur-rubbing was observed. Capuchins fur-rubbed for less time when they could not see their groupmates, but fur-rubbing increased urinary oxytocin above the control condition in all three fur-rubbing conditions equally, suggesting that the physical stimulation derived from fur-rubbing was the most important driver of oxytocin increase. These results support a model in which physical stimulation is an important factor in the relationship between oxytocin and at least some behaviors, suggesting that oxytocin increase alone is not necessarily indicative of a social influence on behavior. Future work is needed to determine the contexts in which social factors do impact oxytocin, and whether the downstream behaviors are the same for socially and nonsocially induced oxytocin release.

Introduction to pioneers in primatology.

As a relatively young discipline, primatology is lucky to still have many of its pioneering researchers active in the field. At the 2019 American Society of Primatology meeting, I convened the inaugural Pioneers in Primatology symposium to bring together a selection of these researchers to reflect on their careers, with a focus on the stories that defined their work and their thoughts on the important future directions for the field. After the symposium, Karen Strier and I decided that these pioneers' contributions merited preservation, and this special issue is our effort to do so.

Comparative performance of orangutans (Pongo spp.), gorillas (Gorilla gorilla gorilla), and drills (Mandrillus leucophaeus), in an ephemeral foraging task.

A goal of the comparative approach is to test a variety of species on the same task. Here, we examined whether the factors that helped capuchin monkeys improve their performance in a dichotomous choice task would generalize to three other primate species: orangutans, gorillas, and drill monkeys. In this task, subjects have access to two options, each resulting in an identical food, but one (the ephemeral option) is only available if it is chosen first, whereas the other one (the permanent option) is always available. Therefore, the food-maximizing solution is to choose the ephemeral option first, followed by the permanent option for an additional reward. On the original version (plate task), the options were discriminated by the color and pattern of the plates holding the food, while on two subsequent versions we used altered cues that we predicted would improve performance: (1) the color of the foods themselves (color task), which we hypothesized was relevant to primates, who choose foods rather than substrates on which foods are found when foraging, and (2) patterned cups covering the foods (cup task), which we hypothesized would help primates avoid the prepotent response associated with visible food. Like capuchins, all three species initially failed to solve the plate task. However, while orangutans improved their performance from the plate to the color task, they did not for the cup task, and only a few gorillas and no drills succeeded in either task. Unfortunately, our ability to interpret these data was obscured by differences in the subjects' level of experience with cognitive testing and practical constraints that precluded the use of completely identical procedures across species. Nonetheless, we consider what these results can tell us, and discuss the value of conducting studies across multiple sites despite unavoidable differences.

Western lowland gorillas (Gorilla gorilla gorilla) do not show an aversion to inequity in a token exchange task.

Although individuals in some species refuse foods they normally accept if their partner receives a more preferred one, this is not true across all species. The cooperation hypothesis proposes that this species-level variability evolved because inequity aversion is a mechanism to identify situations in which cooperation is not paying off, and that species regularly observed cooperating should be more likely to be averse to inequity. To rule out other potential explanations of inequity aversion, we need to test the converse as well: species rarely observed cooperating, especially those phylogenetically close to more cooperative species, should be less likely to be inequity averse. To this end, we tested eight zoo-housed Western lowland gorillas (Gorilla gorilla gorilla) on a token exchange task in which subjects received either the same food reward or a less-preferred reward for the same or more effort than their partner, recording both refusals to participate in the exchange and refusals to accept the reward. Supporting the cooperation hypothesis, even with procedural differences across sessions, gorillas were significantly more likely to refuse in all conditions in which they received a low-value food reward after completing an exchange, regardless of what their partner received, suggesting that gorillas were not inequity averse, but instead would not work for a low-value reward. Additionally, gorillas were more likely to refuse later in the session; while the pattern of refusals remained unchanged after accounting for this, this suggests that species should be tested on as many trials as is practical.

Anything for a cheerio: Brown capuchins (Sapajus [Cebus] apella) consistently coordinate in an Assurance Game for unequal payoffs.

Unequal outcomes disrupt cooperation in some situations, but this has not been tested in the context of coordination in economic games. To explore this, we tested brown capuchins (Sapajus [Cebus] apella) on a manual version of the Stag Hunt (or Assurance) Game, in which individuals sequentially chose between two options, Stag or Hare, and were rewarded according to their choices and that of their partner. Typically, coordination on Stag results in an equal highest payout, whereas coordinating on Hare results in a guaranteed equal but lower payoff and uncoordinated play results in the lowest payoff when playing Stag. We varied this structure such that one capuchin received double the rewards for the coordinated Stag outcome; thus, it was still both animals' best option, but no longer equally rewarding. Despite the inequality, capuchins coordinated on Stag in 78% of trials, and neither payoff structure nor their partner's choice impacted their decision. Additionally, there was no relationship between self-scratching, a measure of stress in capuchins, and choices. After completing the study, we discovered our reward, cheerios, was sufficiently valuable that in another study, capuchins never refused it, so post hoc we repeated the study using a lower value reward, banana flavored pellets. Capuchins completed only 26% of the pellet trials (compared to 98% with cheerios), constraining our ability to interpret the results, but nonetheless the monkeys showed a decrease in preference for Stag, particularly when they received fewer rewards for the coordinated Stag outcome. These results reinforce capuchins' ability to find coordinated outcomes in the Stag Hunt game, but more work is needed to determine whether the monkeys did not mind the inequality or were unwilling to sacrifice a highly preferred food to rectify it. In either case, researchers should carefully consider the impact of their chosen rewards on subjects' choices.

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.

With a little help from my (Psittacidae) friends.

Understanding the distribution of and mechanisms underlying prosocial behavior in other species has been hampered by methodological differences among studies, questions about animals' interpretations of the designs, and low phylogenetic diversity. Brucks and von Bayern's recent report that African gray parrots are proactively prosocial reiterates the importance of social tolerance and suggests a role for perspective taking, but additional work using identical procedures across taxa is needed to verify the cognitive mechanisms underpinning prosocial behavior.

Capuchin monkeys (Sapajus [Cebus] apella) play Nash equilibria in dynamic games, but their decisions are likely not influenced by oxytocin.

Comparative approaches to experimental economics have shed light on the evolution of social decision-making across a range of primate species, including humans. Here we replicate our previous work looking at six pairs of capuchin monkeys' (Sapajus [Cebus] apella) responses to scenarios requiring both coordination (Assurance Game) and anti-coordination (Hawk-Dove Game). This then provides a foundation for assessing their responses to two additional games, one with a scenario of beneficial cooperation with a temptation to defect (Prisoner's Dilemma) and one with an environment requiring changing strategies within short temporal proximity (Alternating Economic Game). We additionally explored the effects of exogenous oxytocin on decision-making. Oxytocin did not affect decisions in any of our games. Results from the first two games largely replicated our previous findings. Responses to the Prisoner's Dilemma were more varied than was seen in previous games, with pairs respectively cooperating, defecting, and failing to establish stable strategies. Such variability indicates that this game may be a good assay for individual differences in social decision-making. Finally, capuchins were able to flexibly switch between their previously established strategies within each of the different games, even when the games were presented within the same session, requiring strategy adjustments within short temporal proximity. These results build on earlier findings showing that capuchins can alter decision-making strategies as the context demands, which is likely essential for decision-making in naturally occurring contexts.

Justice at any cost? The impact of cost-benefit salience on criminal punishment judgments.

This study investigated the effect of cost-benefit salience on simulated criminal punishment judgments. In two vignette-based survey experiments, we sought to identify how the salience of decision costs influences laypeople's punishment judgments. In both experiments (N1  = 109; N2  = 398), undergraduate participants made sentencing judgments with and without explicit information about the direct, material costs of incarceration. Using a within-subjects design, Experiment 1 revealed that increasing the salience of incarceration costs mitigated punishments. However, when costs were not made salient, punishments were no lower than those made when the costs were externalized (i.e., paid by a third party). Experiment 2 showed the same pattern using a between-subjects design. We conclude that, when laypeople formulate sentencing attitudes without exposure to the costs of the punishment, they are prone to discount those costs, behaving as if punishment is societally cost-free. However, when cost information is salient, they utilize it, suggesting the operation of a genuine, albeit labile, punishment preference. We discuss the implications of these findings for psychological theories of decision making and for sentencing policy, including the degree of transparency about the relevant costs of incarceration during the decision process.

Urinary oxytocin in capuchin monkeys: Validation and the influence of social behavior.

In highly social species, like primates, oxytocin plays an important role in cooperation, and in the formation and maintenance of social relationships. Despite recent interest in the relationship between oxytocin and social behavior in nonhuman primates, relatively little is known about endogenous oxytocin in social New World Monkeys. In this paper, we investigate the relationship between oxytocin and affiliative behaviors in socially-housed captive capuchin monkeys (Sapajus [Cebus] apella) by first validating methods of analysis of urinary oxytocin in this species and, second, examining the effects of grooming and fur-rubbing behavior on oxytocin concentrations and further affiliative behavior. In the validation, we found that intranasal exogenous oxytocin significantly increased urinary oxytocin 15-60 min post-administration. Oxytocin was also implicated in both grooming and fur-rubbing behaviors. We found that oxytocin concentrations increased after subjects engaged in grooming or fur-rubbing. In addition, we found that fur-rubbing influenced affiliative behaviors, both during and after a social fur-rubbing bout. While individuals spent more time in contact and proximity while fur-rubbing, immediately following the fur-rubbing event (15-30 min afterwards) all affiliative behaviors decreased. This supports previous research that oxytocin may, in fact, initially be related to increased social distance in this species. Yet, an increase in all affiliative behaviors 30-45 min after the onset of fur-rubbing suggests that fur-rubbing, like grooming, may ultimately function to strengthen social relationships. Overall, these results support a critical role for oxytocin in affiliative behaviors that maintain and strengthen social relationships in capuchin monkeys, and highlight the complexity of the interactions among oxytocin, affiliative behaviors, and social bonding.

Humans as a model for understanding biological fundamentals.

How special are humans? This question drives scholarly output across both the sciences and the humanities. Whereas some disciplines, and the humanities in particular, aim at gaining a better understanding of humans per se, most biologists ultimately aim to understand life in general. This raises the question of whether and when humans are acceptable, or even desirable, models of biological fundamentals. Especially for basic biological processes, non-human species are generally accepted as a relevant model to study topics for which studying humans is impractical, impossible, or ethically inadvisable, but the reverse is controversial: are humans 'too unique' to be informative with respect to biological fundamentals relevant to other species? Or are there areas where we share key components, or for which our very uniqueness serves to allow novel explorations? In this special feature, authors from disciplines including biology, psychology, anthropology, neuroscience and philosophy tackle this question. Their overall conclusion is a qualified yes: humans do tell us about biological fundamentals, in some contexts. We hope this special feature will spur a discussion that will lead to a more careful delineation of the similarities and the differences between humans and other species, and how these impact the study of biological fundamentals.

Comparing species decisions in a dichotomous choice task: adjusting task parameters improves performance in monkeys.

In comparative psychology, both similarities and differences among species are studied to better understand the evolution of their behavior. To do so, we first test species in tasks using similar procedures, but if differences are found, it is important to determine their underlying cause(s) (e.g., are they due to ecology, cognitive ability, an artifact of the study, and/or some other factor?). In our previous work, primates performed unexpectedly poorly on an apparently simple two-choice discrimination task based on the natural behavior of cleaner fish, while the fish did quite well. In this task, if the subjects first chose one of the options (ephemeral) they received both food items, but if they chose the other (permanent) option first, the ephemeral option disappeared. Here, we test several proposed explanations for primates' relatively poorer performance. In Study 1, we used a computerized paradigm that differed from the previous test by removing interaction with human experimenters, which may be distracting, and providing a more standardized testing environment. In Study 2, we adapted the computerized paradigm from Study 1 to be more relevant to primate ecology. Monkeys' overall performance in these adapted tasks matched the performance of the fish in the original study, showing that with the appropriate modifications they can solve the task. We discuss these results in light of comparative research, which requires balancing procedural similarity with considerations of how the details of the task or the context may influence how different species perceive and solve tasks differently.

Chimpanzees, cooking, and a more comparative psychology.

A recent report suggested that chimpanzees demonstrate the cognitive capacities necessary to understand cooking (Warneken & Rosati, 2015). We offered alternative explanations and mechanisms that could account for the behavioral responses of those chimpanzees, and questioned the manner in which the data were used to examine human evolution (Beran, Hopper, de Waal, Sayers, & Brosnan, 2015). Two commentaries suggested either that we were overly critical of the original report's claims and methodology (Rosati & Warneken, 2016), or that, contrary to our statements, early biological thinkers contributed little to questions concerning the evolutionary importance of cooking (Wrangham, 2016). In addition, both commentaries took issue with our treatment of chimpanzee referential models in human evolutionary studies. Our response offers points of continued disagreement as well as points of conciliation. We view Warneken and Rosati's general conclusions as a case of affirming the consequent-a logical conundrum in which, in this case, a demonstration of a partial list of the underlying abilities required for a cognitive trait/suite (understanding of cooking) are suggested as evidence for that ability. And although we strongly concur with both Warneken and Rosati (2015) and Wrangham (2016) that chimpanzee research is invaluable and essential to understanding humanness, it can only achieve its potential via the holistic inclusion of all available evidence-including that from other animals, evolutionary theory, and the fossil and archaeological records.

Chimpanzee food preferences, associative learning, and the origins of cooking.

A recent report suggested that chimpanzees demonstrate the cognitive capacities necessary to understand cooking (Warneken & Rosati, 2015). We offer alternate explanations and mechanisms that could account for the behavioral responses of those chimpanzees, without invoking the understanding of cooking as a process. We discuss broader issues surrounding the use of chimpanzees in modeling hominid behavior and understanding aspects of human evolution.

Justice- and fairness-related behaviors in nonhuman primates.

A distinctive feature across human societies is our interest in justice and fairness. People will sometimes invest in extremely costly behavior to achieve fair outcomes for themselves and others. Why do people care so much about justice? One way to address this is comparatively, exploring behaviors related to justice and fairness in other species. In this paper, I review work exploring responses to inequity, prosocial behavior, and other relevant behaviors in nonhuman primates in an effort to understand both the potential evolutionary function of these behaviors and the social and ecological reasons for the individual differences in behavior. I also consider how these behaviors relate to human behavior, particularly in the case of experimental studies using games derived from experimental economics to compare nonhuman primates' responses to those of humans in similar experimental conditions. These results emphasize the importance of a comparative approach to better understand the function and diversity of human behavior.