From temporal network data to the dynamics of social relationships.

Networks are well-established representations of social systems, and temporal networks are widely used to study their dynamics. However, going from temporal network data (i.e. a stream of interactions between individuals) to a representation of the social group's evolution remains a challenge. Indeed, the temporal network at any specific time contains only the interactions taking place at that time and aggregating on successive time-windows also has important limitations. Here, we present a new framework to study the dynamic evolution of social networks based on the idea that social relationships are interdependent: as the time we can invest in social relationships is limited, reinforcing a relationship with someone is done at the expense of our relationships with others. We implement this interdependence in a parsimonious two-parameter model and apply it to several human and non-human primates' datasets to demonstrate that this model detects even small and short perturbations of the networks that cannot be detected using the standard technique of successive aggregated networks. Our model solves a long-standing problem by providing a simple and natural way to describe the dynamic evolution of social networks, with far-reaching consequences for the study of social networks and social evolution.

Computerized assessment of dominance hierarchy in baboons (Papio papio).

Dominance hierarchies are an important aspect of Primate social life, and there is an increasing need to develop new systems to collect social information automatically. The main goal of this research was to explore the possibility to infer the dominance hierarchy of a group of Guinea baboons (Papio papio) from the analysis of their spontaneous interactions with freely accessible automated learning devices for monkeys (ALDM, Fagot & Bonté Behavior Research Methods, 42, 507-516, 2010). Experiment 1 compared the dominance hierarchy obtained from conventional observations of agonistic behaviours to the one inferred from the analysis of automatically recorded supplanting behaviours within the ALDM workstations. The comparison, applied to three different datasets, shows that the dominance hierarchies obtained with the two methods are highly congruent (all rs ≥ 0.75). Experiment 2 investigated the experimental potential of inferring dominance hierarchy from ALDM testing. ALDM data previously published in Goujon and Fagot (Behavioural Brain Research, 247, 101-109, 2013) were re-analysed for that purpose. Results indicate that supplanting events within the workstations lead to a transient improvement of cognitive performance for the baboon supplanting its partners and that this improvement depends on the difference in rank between the two baboons. This study therefore opens new perspectives for cognitive studies conducted in a social context.

Taking into account the wider evolutionary context of cumulative cultural evolution.

The target article reviews evidence showing that technological reasoning is crucial to cumulative technological culture but it fails to discuss the implications for the emergence of cumulative cultural evolution (CCE) in general. The target article supports the social view of CCE against the more ecological alternative and suggests that CCE appears when specialised individual-learning mechanisms evolve.

High-fidelity copying is not necessarily the key to cumulative cultural evolution: a study in monkeys and children.

The unique cumulative nature of human culture has often been explained by high-fidelity copying mechanisms found only in human social learning. However, transmission chain experiments in human and non-human primates suggest that cumulative cultural evolution (CCE) might not necessarily depend on high-fidelity copying after all. In this study, we test whether defining properties of CCE can emerge in a non-copying task. We performed transmission chain experiments in Guinea baboons and human children where individuals observed and produced visual patterns composed of four squares on touchscreen devices. In order to be rewarded, participants had to avoid touching squares that were touched by a previous participant. In other words, they were rewarded for innovation rather than copying. Results nevertheless exhibited fundamental properties of CCE: an increase over generations in task performance and the emergence of systematic structure. However, these properties arose from different mechanisms across species: children, unlike baboons, converged in behaviour over generations by copying specific patterns in a different location, thus introducing alternative copying mechanisms into the non-copying task. In children, prior biases towards specific shapes led to convergence in behaviour across chains, while baboon chains showed signs of lineage specificity. We conclude that CCE can result from mechanisms with varying degrees of fidelity in transmission and thus that high-fidelity copying is not necessarily the key to CCE.

The baboon: A model for the study of language evolution.

Comparative research on the origins of human language often focuses on a limited number of language-related cognitive functions or anatomical structures that are compared across species. The underlying assumption of this approach is that a single or a limited number of factors may crucially explain how language appeared in the human lineage. Another potentially fruitful approach is to consider human language as the result of a (unique) assemblage of multiple cognitive and anatomical components, some of which are present in other species. This paper is a first step in that direction. It focuses on the baboon, a non-human primate that has been studied extensively for years, including several brain, anatomical, cognitive and cultural dimensions that are involved in human language. This paper presents recent data collected on baboons regarding (1) a selection of domain-general cognitive functions that are core functions for language, (2) vocal production, (3) gestural production and cerebral lateralization, and (4) cumulative culture. In all these domains, it shows that the baboons share with humans many cognitive or brain mechanisms which are central for language. Because of the multidimensionality of the knowledge accumulated on the baboon, that species is an excellent nonhuman primate model for the study of the evolutionary origins of language.

Emotion-Cognition Interaction in Nonhuman Primates: Cognitive Avoidance of Negative Stimuli in Baboons (Papio papio)

It is well established that emotion and cognition interact in humans, but such an interaction has not been extensively studied in nonhuman primates. We investigated whether emotional value can affect nonhuman primates' processing of stimuli that are only mentally represented, not visually available. In a short-term memory task, baboons memorized the location of two target squares of the same color, which were presented with a distractor of a different color. Through prior long-term conditioning, one of the two colors had acquired a negative valence. Subjects were slower and less accurate on the memory task when the targets were negative than when they were neutral. In contrast, subjects were faster and more accurate when the distractors were negative than when they were neutral. Some of these effects were modulated by individual differences in emotional disposition. Overall, the results reveal a pattern of cognitive avoidance of negative stimuli, and show that emotional value alters cognitive processing in baboons even when the stimuli are not physically present. This suggests that emotional influences on cognition are deeply rooted in evolutionary continuity.

Using Automated Learning Devices for Monkeys (ALDM) to study social networks.

Social network analysis has become a prominent tool to study animal social life, and there is an increasing need to develop new systems to collect social information automatically, systematically, and reliably. Here we explore the use of a freely accessible Automated Learning Device for Monkeys (ALDM) to collect such social information on a group of 22 captive baboons (Papio papio). We compared the social network obtained from the co-presence of the baboons in ten ALDM testing booths to the social network obtained through standard behavioral observation techniques. The results show that the co-presence network accurately reflects the social organization of the group, and also indicate under which conditions the co-presence network is most informative. In particular, the best correlation between the two networks was obtained with a minimum of 40 days of computer records and for individuals with at least 500 records per day. We also show through random permutation tests that the observed correlations go beyond what would be observed by simple synchronous activity, to reflect a preferential choice of closely located testing booths. The use of automatized cognitive testing therefore presents a new way of obtaining a large and regular amount of social information that is necessary to develop social network analysis. It also opens the possibility of studying dynamic changes in network structure with time and in relation to the cognitive performance of individuals.

Wild vervet monkeys copy alternative methods for opening an artificial fruit.

Experimental studies of animal social learning in the wild remain rare, especially those that employ the most discriminating tests in which alternative means to complete naturalistic tasks are seeded in different groups. We applied this approach to wild vervet monkeys (Chlorocebus aethiops) using an artificial fruit ('vervetable') opened by either lifting a door panel or sliding it left or right. In one group, a trained model lifted the door, and in two others, the model slid it either left or right. Members of each group then watched their model before being given access to multiple baited vervetables with all opening techniques possible. Thirteen of these monkeys opened vervetables, displaying a significant tendency to use the seeded technique on their first opening and over the course of the experiment. The option preferred in these monkeys' first successful manipulation session was also highly correlated with the proportional frequency of the option they had previously witnessed. The social learning effects thus documented go beyond mere stimulus enhancement insofar as the same door knob was grasped for either technique. Results thus suggest that through imitation, emulation or both, new foraging techniques will spread across groups of wild vervet monkeys to create incipient foraging traditions.

Cultural evolution of systematically structured behaviour in a non-human primate.

Culture pervades human life and is at the origin of the success of our species. A wide range of other animals have culture too, but often in a limited form that does not complexify through the gradual accumulation of innovations. We developed a new paradigm to study cultural evolution in primates in order to better evaluate our closest relatives' cultural capacities. Previous studies using transmission chain experimental paradigms, in which the behavioural output of one individual becomes the target behaviour for the next individual in the chain, show that cultural transmission can lead to the progressive emergence of systematically structured behaviours in humans. Inspired by this work, we combined a pattern reproduction task on touch screens with an iterated learning procedure to develop transmission chains of baboons (Papio papio). Using this procedure, we show that baboons can exhibit three fundamental aspects of human cultural evolution: a progressive increase in performance, the emergence of systematic structure and the presence of lineage specificity. Our results shed new light on human uniqueness: we share with our closest relatives essential capacities to produce human-like cultural evolution.

Network analysis of social changes in a captive chimpanzee community following the successful integration of two adult groups.

Chimpanzees are highly territorial and have the potential to be extremely aggressive toward unfamiliar individuals. In the wild, transfer between groups is almost exclusively completed by nulliparous females, yet in captivity there is often a need to introduce and integrate a range of individuals, including adult males. We describe the process of successfully integrating two groups of chimpanzees, each containing 11 individuals, in the Budongo Trail facility at the Royal Zoological Society of Scotland's Edinburgh Zoo. We use social network analysis to document changes in group dynamics within this population over the 16 months following integration. Aggression rates were low overall and members of the two original groups engaged in significantly fewer aggressive interactions over time. Association and grooming data indicate that relationships between members of the original groups became stronger and more affiliative with time. Despite these positive indicators the association data revealed the continued existence of two distinct subgroups, a year after integration. Our data show that when given complex space and freedom to exhibit natural fission-fusion groupings, in which the chimpanzees choose whom they wish to associate and interact with, the building of strong affiliative relationships with unfamiliar individuals is a very gradual process.

Bringing cumulative technological culture beyond copying versus reasoning.

The dominant view of cumulative technological culture suggests that high-fidelity transmission rests upon a high-fidelity copying ability, which allows individuals to reproduce the tool-use actions performed by others without needing to understand them (i.e., without causal reasoning). The opposition between copying versus reasoning is well accepted but with little supporting evidence. In this article, we investigate this distinction by examining the cognitive science literature on tool use. Evidence indicates that the ability to reproduce others' tool-use actions requires causal understanding, which questions the copying versus reasoning distinction and the cognitive reality of the so-called copying ability. We conclude that new insights might be gained by considering causal understanding as a key driver of cumulative technological culture.

Guinea baboons are strategic cooperators.

Humans are strategic cooperators; we make decisions on the basis of costs and benefits to maintain high levels of cooperation, and this is thought to have played a key role in human evolution. In comparison, monkeys and apes might lack the cognitive capacities necessary to develop flexible forms of cooperation. We show that Guinea baboons (Papio papio) can use direct reciprocity and partner choice to develop and maintain high levels of cooperation in a prosocial choice task. Our findings demonstrate that monkeys have the cognitive capacities to adjust their level of cooperation strategically using a combination of partner choice and partner control strategies. Such capacities were likely present in our common ancestor and would have provided the foundations for the evolution of typically human forms of cooperation.

Human and animal dominance hierarchies show a pyramidal structure guiding adult and infant social inferences.

This study investigates the structure of social hierarchies. We hypothesized that if social dominance relations serve to regulate conflicts over resources, then hierarchies should converge towards pyramidal shapes. Structural analyses and simulations confirmed this hypothesis, revealing a triadic-pyramidal motif across human and non-human hierarchies (114 species). Phylogenetic analyses showed that this pyramidal motif is widespread, with little influence of group size or phylogeny. Furthermore, nine experiments conducted in France found that human adults (N = 120) and infants (N = 120) draw inferences about dominance relations that are consistent with hierarchies' pyramidal motif. By contrast, human participants do not draw equivalent inferences based on a tree-shaped pattern with a similar complexity to pyramids. In short, social hierarchies exhibit a pyramidal motif across a wide range of species and environments. From infancy, humans exploit this regularity to draw systematic inferences about unobserved dominance relations, using processes akin to formal reasoning.

Are monkeys sensitive to informativeness: An experimental study with baboons (Papio papio).

Informativeness (defined as reduction of uncertainty) is central in human communication. In the present study, we investigate baboons' sensitivity to informativeness by manipulating the informativity of a cue relative to a response display and by allowing participants to anticipate their answers or to wait for a revealed answer (with variable delays). Our hypotheses were that anticipations would increase with informativity, while response times to revealed trials would decrease with informativity. These predictions were verified in Experiment 1. In Experiments 2 and 3, we manipulated rewards (rewarding anticipation responses at 70% only) to see whether reward tracking alone could account for the results in Experiment 1. We observed that the link between anticipations and informativeness disappeared, but not the link between informativeness and decreased RTs for revealed trials. Additionally, in all three experiments, the number of correct answers in revealed trials with fast reaction times (< 250ms) increased with informativeness. We conclude that baboons are sensitive to informativeness as an ecologically sound means to tracking reward.

Understanding Imitation in Papio papio: The Role of Experience and the Presence of a Conspecific Demonstrator.

What factors affect imitation performance? Varying theories of imitation stress the role of experience, but few studies have explicitly tested its role in imitative learning in non-human primates. We tested several predictions regarding the role of experience, conspecific presence, and action compatibility using a stimulus-response compatibility protocol. Nineteen baboons separated into two experimental groups learned to respond by targeting on a touch screen the same stimulus as their neighbor (compatible) or the opposite stimulus (incompatible). They first performed the task with a conspecific demonstrator (social phase) and then a computer demonstrator (ghost phase). After reaching a predetermined success threshold, they were then tested in an opposite compatibility condition (i.e., reversal learning conditions). Seven baboons performed at least two reversals during the social phase, and we found no significant difference between the compatible and incompatible conditions, although we noticed slightly faster response times (RTs) in the compatible condition that disappeared after the first reversal. During the ghost phase, monkeys showed difficulties in learning the incompatible condition, and the compatible condition RTs tended to be slower than during the social phase. Together, these results suggest that (a) there is no strong movement compatibility effect in our task and that (b) the presence of a demonstrator plays a role in eliciting correct responses but is not essential as has been previously shown in human studies.

The experimental emergence of convention in a non-human primate.

Conventions form an essential part of human social and cultural behaviour and may also be important to other animal societies. Yet, despite the wealth of evidence that has accumulated for culture in non-human animals, we know surprisingly little about non-human conventions beyond a few rare examples. We follow the literature in behavioural ecology and evolution and define conventions as systematic behaviours that solve a coordination problem in which two or more individuals need to display complementary behaviour to obtain a mutually beneficial outcome. We start by discussing the literature on conventions in non-human primates from this perspective and conclude that all the ingredients for conventions to emerge are present and therefore that they ought to be more frequently observed. We then probe the emergence of conventions by using a unique novel experimental system in which pairs of Guinea baboons (Papio papio) can voluntarily participate together in touchscreen-based cognitive testing and we show that conventions readily emerge in our experimental set-up and that they share three fundamental properties of human conventions (arbitrariness, stability and efficiency). These results question the idea that observational learning, and imitation in particular, is necessary to establish conventions; they suggest that positive reinforcement is enough. This article is part of a discussion meeting issue 'The emergence of collective knowledge and cumulative culture in animals, humans and machines'.

Age effect in expert cognitive flexibility in Guinea baboons (Papio papio).

Cognitive flexibility in non-human primates is traditionally measured with the conceptual set shifting task (CSST). In our laboratory, Guinea baboons (N = 24) were continuously tested with a CSST task during approximately 10 years. Our task involved the presentation of three stimuli on a touch screen all made from 3 possible colours and 3 shapes. The subjects had to touch the stimulus containing the stimulus dimension (e.g., green) that was constantly rewarded until the stimulus dimension changed. Analysis of perseveration responses, scores and response times collected during the last two years of testing (approximately 1.6 million trials) indicate (1) that the baboons have developed an "expert" form of cognitive flexibility and (2) that their performance was age-dependent, it was at a developing stage in juveniles, optimal in adults, declining in middle-aged, and strongly impaired in the oldest age group. A direct comparison with the data collected by Bonté , Flemming & Fagot (2011) on some of the same baboons and same task as in the current study indicates that (3) the performance of all age groups has improved after 10 years of training, even for the now old individuals. All these data validate the use of non-human primates as models of human cognitive flexibility and suggest that cognitive flexibility in humans has a long evolutionary history.

Probability matching is not the default decision making strategy in human and non-human primates.

Probability matching has long been taken as a prime example of irrational behaviour in human decision making; however, its nature and uniqueness in the animal world is still much debated. In this paper we report a set of four preregistered experiments testing adult humans and Guinea baboons on matched probability learning tasks, manipulating task complexity (binary or ternary prediction tasks) and reinforcement procedures (with and without corrective feedback). Our findings suggest that probability matching behaviour within primate species is restricted to humans and the simplest possible binary prediction tasks; utility-maximising is seen in more complex tasks for humans as pattern-search becomes more effortful, and we observe it across the board in baboons, altogether suggesting that it is a cognitively less demanding strategy. These results provide further evidence that neither human nor non-human primates default to probability matching; however, unlike other primates, adult humans probability match when the cost of pattern search is low.

Broca's cerebral asymmetry reflects gestural communication's lateralisation in monkeys (Papio anubis).

Manual gestures and speech recruit a common neural network, involving Broca's area in the left hemisphere. Such speech-gesture integration gave rise to theories on the critical role of manual gesturing in the origin of language. Within this evolutionary framework, research on gestural communication in our closer primate relatives has received renewed attention for investigating its potential language-like features. Here, using in vivo anatomical MRI in 50 baboons, we found that communicative gesturing is related to Broca homologue's marker in monkeys, namely the ventral portion of the Inferior Arcuate sulcus (IA sulcus). In fact, both direction and degree of gestural communication's handedness - but not handedness for object manipulation are associated and correlated with contralateral depth asymmetry at this exact IA sulcus portion. In other words, baboons that prefer to communicate with their right hand have a deeper left-than-right IA sulcus, than those preferring to communicate with their left hand and vice versa. Interestingly, in contrast to handedness for object manipulation, gestural communication's lateralisation is not associated to the Central sulcus depth asymmetry, suggesting a double dissociation of handedness' types between manipulative action and gestural communication. It is thus not excluded that this specific gestural lateralisation signature within the baboons' frontal cortex might reflect a phylogenetical continuity with language-related Broca lateralisation in humans.

Technical reasoning bolsters cumulative technological culture through convergent transformations.

Understanding the evolution of human technology is key to solving the mystery of our origins. Current theories propose that technology evolved through the accumulation of modifications that were mostly transmitted between individuals by blind copying and the selective retention of advantageous variations. An alternative account is that high-fidelity transmission in the context of cumulative technological culture is supported by technical reasoning, which is a reconstruction mechanism that allows individuals to converge to optimal solutions. We tested these two competing hypotheses with a microsociety experiment, in which participants had to optimize a physical system in partial- and degraded-information transmission conditions. Our results indicated an improvement of the system over generations, which was accompanied by an increased understanding of it. The solutions produced tended to progressively converge over generations. These findings show that technical reasoning can bolster high-fidelity transmission through convergent transformations, which highlights its role in the cultural evolution of technology.