Response to Hansen Wheat et al.: Additional analysis further supports the early emergence of cooperative communication in dogs compared to wolves raised with more human exposure.

Here, we address Hansen Wheat et al.'s commentary in this journal in response to Salomons et al. Current Biology, 31(14), 3137-3144.E11, (2021). We conduct additional analyses in response to Hansen Wheat et al.'s two main questions. First, we examine the claim that it was the move to a human home environment which enabled the dog puppies to outperform the wolf puppies in gesture comprehension tasks. We show that the youngest dog puppies who had not yet been individually placed in raisers' homes were still highly skilled, and outperformed similar-aged wolf puppies who had higher levels of human interaction. Second, we address the claim that willingness to approach a stranger can explain the difference between dog and wolf pups' ability to succeed in gesture comprehension tasks. We explain the various controls in the original study that render this explanation insufficient, and demonstrate via model comparison that the covariance of species and temperament also make this parsing impossible. Overall, our additional analyses and considerations support the domestication hypothesis as laid out by Salomons et al. Current Biology, 31(14), 3137-3144.E11, (2021).

Motivating children's cooperation to conserve forests.

Forests are essential common-pool resources. Understanding children's and adolescents' motivations for conservation is critical to improving conservation education. In 2 experiments, we investigated 1086 school-aged children and adolescents (6-16 years old) from China, the Democratic Republic of Congo, and the United States. testING participants in groups, we assessed their motivation for conservation based on collective-risk common-pool goods games in which they are threatened with losing their endowment unless the group donation exceeds a threshold needed to maintain the forest.eExtrinsic motivations, rather than intrinsic , tended to lead to successful cooperation to maintain a forest. Certainty of losing individual payoffs significantly boosted successful cooperative conservation efforts across cultures (success rates were 90.63 % and 74.19% in the 2 risk-extrinsic conditions and 43.75% in the control condition). In U.S. participants, 2 extrinsic incentives, priming discussions of the value of forests and delay of payoffs as punishment , also increased success of cooperative conservation (success rates were 97.22% and 76.92% in the 2 extrinsic-incentive conditions and 29.19% and 30.77% in the 2 control conditions). Conservation simulations, like those we used, may allow educators to encourage forest protection by leading groups to experience successful cooperation and the extrinsic incentives needed to motivate forest conservation. This article is protected by copyright. All rights reserved.

Cooperative Communication with Humans Evolved to Emerge Early in Domestic Dogs.

Although we know that dogs evolved from wolves, it remains unclear how domestication affected dog cognition. One hypothesis suggests dog domestication altered social maturation by a process of selecting for an attraction to humans.1-3 Under this account, dogs became more flexible in using inherited skills to cooperatively communicate with a new social partner that was previously feared and expressed these unusual social skills early in development.4-6 Here, we comparedog (n = 44) and wolf (n = 37) puppies, 5-18 weeks old, on a battery of temperament and cognition tasks. We find that dog puppies are more attracted to humans, read human gestures more skillfully, and make more eye contact with humans than wolf puppies. The two species are similarly attracted to familiar objects and perform similarly on non-social measures of memory and inhibitory control. These results are consistent with the idea that domestication enhanced the cooperative-communicative abilities of dogs as selection for attraction to humans altered social maturation.

How environmental unpredictability and harshness affect chimpanzees (Pan troglodytes) in risk-choice and temporal discounting tasks.

Animals need to adjust their decision-making strategies to the ecological challenges of their environment. Variation in ecological unpredictability and harshness thus seem to affect their decisions in the wild. In our study, we combine methods from human life history theory and previous comparative work with chimpanzees to investigate whether current variability in ecological factors such as reward unpredictability and harshness affect chimpanzees' decision-making strategies in two value-based scenarios. We presented chimpanzees with choices varying in the probability of obtaining food rewards (risk-choice task) and in their temporal availability (temporal discounting task). These scenarios were preceded by different sets of priming phases mimicking variability in resource unpredictability (predictable or unpredictable rewards) and harshness (abundant or scarce rewards). In addition, we implemented a social manipulation to explore whether variations in unpredictable gains and losses affected chimpanzees' performance in both tasks. We found that chimpanzees were only affected by the social manipulation in the risk-choice scenario. Specifically, after a period of constant food losses chimpanzees became less risk prone. We discuss how different types of negative experiences affect chimpanzees' decisions. (PsycInfo Database Record (c) 2021 APA, all rights reserved).

Gibbons exploit information about what a competitor can see.

How much nonhuman animals understand about seeing has been the focus of comparative cognition research for decades. Many social primates (and other species) are sensitive to cues about what others can and cannot see. Whether this sensitivity evolved in primates through shared descent or convergent evolution remains unclear. The current study tested gibbons-the apes that are least studied yet most distantly related to humans and one of the less social primates-in two food-competition tasks. Specifically, we presented eastern hoolock gibbons, Hoolock leuconedys, and silvery gibbons, Hylobates moloch, with a choice between a contested piece of food visible to both themselves and a human competitor and an uncontested piece visible only to themselves. Subjects successfully stole the uncontested food when the competitor turned away his body (N = 10, experiment 1) and his head (N = 9, experiment 2). However, when the head of the experimenter was oriented towards the contested piece of food, whether the competitor opened or closed his eyes made no difference. Subjects' sensitivity to body- and head-orientation cues was comparable to that of chimpanzees, rhesus macaques, and ring-tailed lemurs-species living in much larger groups than gibbons. These findings support the continuity hypothesis that sensitivity to body- and head-orientation cues is a product of shared descent among primates.

What influences a pet dog's first impression of a stranger?

Dogs live in the dynamic human social networks full of strangers, yet they form strong and selective bonds with familiar caretakers. Little is known about how a bond is initially formed between a dog and a complete stranger. The first-impression hypothesis suggests that interacting with strangers can present an opportunity to form a mutualistic partnership. It predicts that dogs should respond positively toward a complete stranger to facilitate bonding (Prediction 1) and adjust their preferences in response to the perceived risk and benefit of interacting with strangers (Prediction 2). We examine the social preferences of pet dogs toward a complete stranger whom they have never met before and several other potential partners - the owner with whom subjects have had a positive, long-term bond (Experiment 1), and an exposed stranger with whom they have had a positive short-term interaction (Experiment 2) or a negative one (Experiment 3). In support of Prediction 1, subjects were exceptionally trusting across contexts. Mixed results were found with regard to Prediction 2. Subjects preferred their owner over a stranger when following social cues and (to a lesser degree) when approaching and feeding in close proximity. However, relative to a complete stranger, subjects did not consistently prefer the positively exposed stranger or avoid the negatively exposed one. The lack of clear selectivity might be due to pet dogs' high baseline level of trust of complete strangers or reflect the strength of their existing bonds that negated the need for another positive bond with a new human partner.

Bonobos voluntarily hand food to others but not toys or tools.

A key feature of human prosociality is direct transfers, the most active form of sharing in which donors voluntarily hand over resources in their possession Direct transfers buffer hunter-gatherers against foraging shortfalls. The emergence and elaboration of this behaviour thus likely played a key role in human evolution by promoting cooperative interdependence and ensuring that humans' growing energetic needs (e.g. for increasing brain size) were more reliably met. According to the strong prosociality hypothesis, among great apes only humans exhibit sufficiently strong prosocial motivations to directly transfer food. The versatile prosociality hypothesis suggests instead that while other apes may make transfers in constrained settings, only humans share flexibly across food and non-food contexts. In controlled experiments, chimpanzees typically transfer objects but not food, supporting both hypotheses. In this paper, we show in two experiments that bonobos directly transfer food but not non-food items. These findings show that, in some contexts, bonobos exhibit a human-like motivation for direct food transfer. However, humans share across a far wider range of contexts, lending support to the versatile prosociality hypothesis. Our species' unusual prosocial flexibility is likely built on a prosocial foundation we share through common descent with the other apes.

Bonobos respond prosocially toward members of other groups.

Modern humans live in an "exploded" network with unusually large circles of trust that form due to prosociality toward unfamiliar people (i.e. xenophilia). In a set of experiments we demonstrate that semi-free ranging bonobos (Pan paniscus) - both juveniles and young adults - also show spontaneous responses consistent with xenophilia. Bonobos voluntarily aided an unfamiliar, non-group member in obtaining food even when he/she did not make overt requests for help. Bonobos also showed evidence for involuntary, contagious yawning in response to videos of yawning conspecifics who were complete strangers. These experiments reveal that xenophilia in bonobos can be unselfish, proactive and automatic. They support the first impression hypothesis that suggests xenophilia can evolve through individual selection in social species whenever the benefits of building new bonds outweigh the costs. Xenophilia likely evolved in bonobos as the risk of intergroup aggression dissipated and the benefits of bonding between immigrating members increased. Our findings also mean the human potential for xenophilia is either evolutionarily shared or convergent with bonobos and not unique to our species as previously proposed.

Variation in gaze-following between two Asian colobine monkeys.

Gaze-following is a basic cognitive ability found in numerous primate and nonprimate species. However, little is known about this ability and its variation in colobine monkeys. We compared gaze-following of two Asian colobines-François' langurs (Trachypithecus francoisi) and golden snub-nosed monkeys (Rhinopithecus roxellana). Although both species live in small polygynous family units, units of the latter form multilevel societies with up to hundreds of individuals. François' langurs (N = 15) were less sensitive to the gaze of a human experimenter than were golden snub-nosed monkeys (N = 12). We then tested the two species using two classic inhibitory control tasks-the cylinder test and the A-not-B test. We found no difference between species in inhibitory control, which called into question the nonsocial explanation for François' langur's weaker sensitivity to human gaze. These findings are consistent with the social intelligence hypothesis, which predicted that golden snub-nosed monkeys would outperform François' langurs in gaze-following because of the greater size and complexity of their social groups. Furthermore, our results underscore the need for more comparative studies of cognition in colobines, which should provide valuable opportunities to test hypotheses of cognitive evolution.

The evolution of self-control.

Cognition presents evolutionary research with one of its greatest challenges. Cognitive evolution has been explained at the proximate level by shifts in absolute and relative brain volume and at the ultimate level by differences in social and dietary complexity. However, no study has integrated the experimental and phylogenetic approach at the scale required to rigorously test these explanations. Instead, previous research has largely relied on various measures of brain size as proxies for cognitive abilities. We experimentally evaluated these major evolutionary explanations by quantitatively comparing the cognitive performance of 567 individuals representing 36 species on two problem-solving tasks measuring self-control. Phylogenetic analysis revealed that absolute brain volume best predicted performance across species and accounted for considerably more variance than brain volume controlling for body mass. This result corroborates recent advances in evolutionary neurobiology and illustrates the cognitive consequences of cortical reorganization through increases in brain volume. Within primates, dietary breadth but not social group size was a strong predictor of species differences in self-control. Our results implicate robust evolutionary relationships between dietary breadth, absolute brain volume, and self-control. These findings provide a significant first step toward quantifying the primate cognitive phenome and explaining the process of cognitive evolution.

Bonobos share with strangers.

Humans are thought to possess a unique proclivity to share with others--including strangers. This puzzling phenomenon has led many to suggest that sharing with strangers originates from human-unique language, social norms, warfare and/or cooperative breeding. However, bonobos, our closest living relative, are highly tolerant and, in the wild, are capable of having affiliative interactions with strangers. In four experiments, we therefore examined whether bonobos will voluntarily donate food to strangers. We show that bonobos will forego their own food for the benefit of interacting with a stranger. Their prosociality is in part driven by unselfish motivation, because bonobos will even help strangers acquire out-of-reach food when no desirable social interaction is possible. However, this prosociality has its limitations because bonobos will not donate food in their possession when a social interaction is not possible. These results indicate that other-regarding preferences toward strangers are not uniquely human. Moreover, language, social norms, warfare and cooperative breeding are unnecessary for the evolution of xenophilic sharing. Instead, we propose that prosociality toward strangers initially evolves due to selection for social tolerance, allowing the expansion of individual social networks. Human social norms and language may subsequently extend this ape-like social preference to the most costly contexts.

Assessing the psychological health of captive and wild apes: a response to Ferdowsian et al. (2011).

As many studies of cognition and behavior involve captive animals, assessing any psychological impact of captive conditions is an important goal for comparative researchers. Ferdowsian and colleagues (2011) sought to address whether captive chimpanzees show elevated signs of psychopathology relative to wild apes. They modified a checklist of diagnostic criteria for major depression and posttraumatic stress disorder in humans, and applied these criteria to various captive and wild chimpanzee populations. We argue that measures derived from human diagnostic criteria are not a powerful tool for assessing the psychological health of nonverbal animals. In addition, we highlight certain methodological drawbacks of the specific approach used by Ferdowsian and colleagues (2011). We propose that research should (1) focus on objective behavioral criteria that account for species-typical behaviors and can be reliably identified across populations; (2) account for population differences in rearing history when comparing how current environment impacts psychological health in animals; and (3) focus on how changes in current human practices can improve the well-being of both captive and wild animals.

How does cognition evolve? Phylogenetic comparative psychology.

Now more than ever animal studies have the potential to test hypotheses regarding how cognition evolves. Comparative psychologists have developed new techniques to probe the cognitive mechanisms underlying animal behavior, and they have become increasingly skillful at adapting methodologies to test multiple species. Meanwhile, evolutionary biologists have generated quantitative approaches to investigate the phylogenetic distribution and function of phenotypic traits, including cognition. In particular, phylogenetic methods can quantitatively (1) test whether specific cognitive abilities are correlated with life history (e.g., lifespan), morphology (e.g., brain size), or socio-ecological variables (e.g., social system), (2) measure how strongly phylogenetic relatedness predicts the distribution of cognitive skills across species, and (3) estimate the ancestral state of a given cognitive trait using measures of cognitive performance from extant species. Phylogenetic methods can also be used to guide the selection of species comparisons that offer the strongest tests of a priori predictions of cognitive evolutionary hypotheses (i.e., phylogenetic targeting). Here, we explain how an integration of comparative psychology and evolutionary biology will answer a host of questions regarding the phylogenetic distribution and history of cognitive traits, as well as the evolutionary processes that drove their evolution.