Jessica C. Flack

Policing stabilizes construction of social niches in primates.

All organisms interact with their environment, and in doing so shape it, modifying resource availability. Termed niche construction, this process has been studied primarily at the ecological level with an emphasis on the consequences of construction across generations. We focus on the behavioural process of construction within a single generation, identifying the role a robustness mechanism—conflict management—has in promoting interactions that build social resource networks or social niches. Using ‘knockout’ experiments on a large, captive group of pigtailed macaques (Macaca nemestrina), we show that a policing function, performed infrequently by a small subset of individuals, significantly contributes to maintaining stable resource networks in the face of chronic perturbations that arise through conflict. When policing is absent, social niches destabilize, with group members building smaller, less diverse, and less integrated grooming, play, proximity and contact-sitting networks. Instability is quantified in terms of reduced mean degree, increased clustering, reduced reach, and increased assortativity. Policing not only controls conflict, we find it significantly influences the structure of networks that constitute essential social resources in gregarious primate societies. The structure of such networks plays a critical role in infant survivorship, emergence and spread of cooperative behaviour, social learning and cultural traditions.

Social Structure, Robustness, and Policing Cost in a Cognitively Sophisticated Species

Conflict management is one of the primary requirements for social complexity. Of the many forms of conflict management, one of the rarest and most interesting is third‐party policing, or intervening impartially to control conflict. Third‐party policing should be hard to evolve because policers personally pay a cost for intervening, while the benefits are diffused over the whole group. In this study we investigate the incidence and costs of policing in a primate society. We report quantitative evidence of non–kin policing in the nonhuman primate, the pigtailed macaque. We find that policing is effective at reducing the intensity of or terminating conflict when performed by the most powerful individuals. We define a measure, social power consensus, that predicts effective low‐cost interventions by powerful individuals and ineffective, relatively costly interventions by low‐power individuals. Finally, we develop a simple probabilistic model to explore whether the degree to which policing can effectively reduce the societal cost of conflict is dependent on variance in the distribution of power. Our data and simple model suggest that third‐party policing effectiveness and cost are dependent on power structure and might emerge only in societies with high variance in power.

Robustness mechanisms in primate societies: a perturbation study

Conflict management mechanisms have a direct, critical effect on system robustness because they mitigate conflict intensity and help repair damaged relationships. However, robustness mechanisms can also have indirect effects on system integrity by facilitating interactions among components. We explore the indirect role that conflict management mechanisms play in the maintenance of social system robustness, using a perturbation technique to ‘knockout’ components responsible for effective conflict management. We explore the effects of knockout on pigtailed macaque (Macaca nemestrina) social organization, using a captive group of 84 individuals. This system is ideal in addressing this question because there is heterogeneity in performance of conflict management. Consequently, conflict managers can be easily removed without disrupting other control structures. We find that powerful conflict managers are essential in maintaining social order for the benefit of all members of society. We show that knockout of components responsible for conflict management results in system destabilization by significantly increasing mean levels of conflict and aggression, decreasing socio-positive interaction and decreasing the operation of repair mechanisms.

Context modulates signal meaning in primate communication

A central issue in the evolution of social complexity and the evolution of communication concerns the capacity to communicate about increasingly abstract objects and concepts. Many animals can communicate about immediate behavior, but to date, none have been reported to communicate about behavior during future interactions. In this study, we show that a special, unidirectional, cost-free dominance-related signal used by monkeys (pigtailed macaques: Macaca nemestrina) means submission (immediate behavior) or subordination (pattern of behavior) depending on the context of usage. We hypothesize that to decrease receiver uncertainty that the signal object is subordination, senders shift contextual usage from the conflict context, where the signal evolved, to a peaceful one, in which submission is unwarranted. We predict and find that deceasing receiver uncertainty through peaceful signal exchange facilitates the development of higher quality social relationships: Individuals exchanging the peaceful variant groom and reconcile more frequently and fight less frequently than individuals exchanging signals only in the conflict context or no signals. We rule out alternative hypotheses, including an underlying reciprocity rule, temperament, and proximity effects. Our results suggest that primates can communicate about behavioral patterns when these concern relationship rules. The invention of signals decreasing uncertainty about relationship state is likely to have been critical for the evolution of social complexity and to the emergence of robust power structures that feed down to influence rapidly changing individual behavior.

Play Signaling and the Perception of Social Rules by Juvenile Chimpanzees (Pan troglodytes)

Prescriptive social rules are enforced statistical regularities. The authors investigated whether juvenile chimpanzees (Pan troglodytes) recognize and use enforced statistical regularities to guide dyadic play behavior. They hypothesized (a) that proximity of adults, especially mothers of younger play partners, to play bouts will increase the play signaling of older partners and (b) that when juvenile-juvenile play bouts occur in proximity to adults, older partners will play at a lower intensity than when no adults are present. They found that older and younger partners increase their play signaling in the presence of the mothers of younger partners, particularly as the intensity of play bouts increases. In contrast to their hypothesis, older partners played more roughly when the mothers of younger partners were in proximity. These results suggest that juvenile chimpanzees increase play signaling to prevent termination of the play bouts by mothers of younger partners.

The challenges and scope of theoretical biology

Scientific theories seek to provide simple explanations for significant empirical regularities based on fundamental physical and mechanistic constraints. Biological theories have rarely reached a level of generality and predictive power comparable to physical theories. This discrepancy is explained through a combination of frozen accidents, environmental heterogeneity, and widespread non-linearities observed in adaptive processes. At the same time, model building has proven to be very successful when it comes to explaining and predicting the behavior of particular biological systems. In this respect biology resembles alternative model-rich frameworks, such as economics and engineering. In this paper we explore the prospects for general theories in biology, and suggest that these take inspiration not only from physics, but also from the information sciences. Future theoretical biology is likely to represent a hybrid of parsimonious reasoning and algorithmic or rule-based explanation. An open question is whether these new frameworks will remain transparent to human reason. In this context, we discuss the role of machine learning in the early stages of scientific discovery. We argue that evolutionary history is not only a source of uncertainty, but also provides the basis, through conserved traits, for very general explanations for biological regularities, and the prospect of unified theories of life.

Robustness and complexity co-constructed in multimodal signalling networks

In animal communication, signals are frequently emitted using different channels (e.g. frequencies in a vocalization) and different modalities (e.g. gestures can accompany vocalizations). We explore two explanations that have been provided for multimodality: (i) selection for high information transfer through dedicated channels and (ii) increasing fault tolerance or robustness through multichannel signals. Robustness relates to an accurate decoding of a signal when parts of a signal are occluded. We show analytically in simple feed-forward neural networks that while a multichannel signal can solve the robustness problem, a multimodal signal does so more effectively because it can maximize the contribution made by each channel while minimizing the effects of exclusion. Multimodality refers to sets of channels where within each set information is highly correlated. We show that the robustness property ensures correlations among channels producing complex, associative networks as a by-product. We refer to this as the principle of robust overdesign. We discuss the biological implications of this for the evolution of combinatorial signalling systems; in particular, how robustness promotes enough redundancy to allow for a subsequent specialization of redundant components into novel signals.

Multiple time-scales and the developmental dynamics of social systems

To build a theory of social complexity, we need to understand how aggregate social properties arise from individual interaction rules. Here, I review a body of work on the developmental dynamics of pigtailed macaque social organization and conflict management that provides insight into the mechanistic causes of multi-scale social systems. In this model system coarse-grained, statistical representations of collective dynamics are more predictive of the future state of the system than the constantly in-flux behavioural patterns at the individual level. The data suggest that individuals can perceive and use these representations for strategical decision-making. As an interaction history accumulates the coarse-grained representations consolidate. This constrains individual behaviour and provides the foundations for new levels of organization. The time-scales on which these representations change impact whether the consolidating higher-levels can be modified by individuals and collectively. The time-scales appear to be a function of the ‘coarseness’ of the representations and the character of the collective dynamics over which they are averages. The data suggest that an advantage of multiple timescales is that they allow social systems to balance tradeoffs between predictability and adaptability. I briefly discuss the implications of these findings for cognition, social niche construction and the evolution of new levels of organization in biological systems.

Inductive Game Theory and the Dynamics of Animal Conflict

Conflict destabilizes social interactions and impedes cooperation at multiple scales of biological organization. Of fundamental interest are the causes of turbulent periods of conflict. We analyze conflict dynamics in an monkey society model system. We develop a technique, Inductive Game Theory, to extract directly from time-series data the decision-making strategies used by individuals and groups. This technique uses Monte Carlo simulation to test alternative causal models of conflict dynamics. We find individuals base their decision to fight on memory of social factors, not on short timescale ecological resource competition. Furthermore, the social assessments on which these decisions are based are triadic (self in relation to another pair of individuals), not pairwise. We show that this triadic decision making causes long conflict cascades and that there is a high population cost of the large fights associated with these cascades. These results suggest that individual agency has been over-emphasized in the social evolution of complex aggregates, and that pair-wise formalisms are inadequate. An appreciation of the empirical foundations of the collective dynamics of conflict is a crucial step towards its effective management.

Encoding Power in Communication Networks

In animal societies, conflicts can be resolved by combatants or through third‐party intervention. In gregarious species, conflicts among pairs can spread to involve multiple individuals. In the case of large conflicts, containment and termination of aggression by third parties is important. Successful intervention relies on consensus among combatants about the intervener’s capacity to use force. We refer to this consensus as power. We measure it and study how it arises, using as our model system a pigtailed macaque (Macaca nemestrina) society. In macaques, the degree to which one individual perceives another as capable of using force is communicated using a special dominance signal. Group consensus about an individual’s capacity to use force arises from the network of signaling interactions. We derive a formalism to quantify consensus in the network. We find that the power distribution is fat tailed and power is a strong predictor of social variables including request for support, intervention cost, and intensity. We develop models to show how dominance‐signaling strategies promote robust power distributions despite individual signaling errors. We suggest that when considering correlated interactions among many individuals it can be more useful to emphasize coarse‐grained information stored at the group level—behavioral macrostates—over detailed information at the individual level.