Democracy in animals: the evolution of shared group decisions

A 'consensus decision' is when the members of a group choose, collectively, between mutually exclusive actions. In humans, consensus decisions are often made democratically or in an 'equally shared' manner, i.e. all group members contribute to the decision. Biologists are only now realizing that shared consensus decisions also occur in social animals (other than eusocial insects). Sharing of decisions is, in principle, more profitable for groups than accepting the 'unshared' decision of a single dominant member. However, this is not true for all individual group members, posing a question as to how shared decision making could evolve. Here, we use a game theory model to show that sharing of decisions can evolve under a wide range of circumstances but especially in the following ones: when groups are heterogeneous in composition; when alternative decision outcomes differ in potential costs and these costs are large; when grouping benefits are marginal; or when groups are close to, or above, optimal size. Since these conditions are common in nature, it is easy to see how mechanisms for shared decision making could have arisen in a wide range of species, including early human ancestors.     

Conflicts of interest and the evolution of decision sharing

Social animals regularly face consensus decisions whereby they choose, collectively, between mutually exclusive actions. Such decisions often involve conflicts of interest between group members with respect to preferred action. Conflicts could, in principle, be resolved, either by sharing decisions between members (‘shared decisions’) or by one ‘dominant’ member making decisions on behalf of the whole group (‘unshared decisions’). Both, shared and unshared decisions, have been observed. However, it is unclear as to what favours the evolution of either decision type. Here, after a brief literature review, we present a novel method, involving a combination of self-organizing system and game theory modelling, of investigating the evolution of shared and unshared decisions. We apply the method to decisions on movement direction. We find that both, shared and unshared, decisions can evolve without individuals having a global overview of the group''s behaviour or any knowledge about other members'' preferences or intentions. Selection favours unshared over shared decisions when conflicts are high relative to grouping benefits, and vice versa. These results differ from those of group decision models relating to activity timings. We attribute this to fundamental differences between collective decisions about modalities that are disjunct (here, space) or continuous (here, time) with respect to costs/benefits.     

Shared or unshared consensus decision in macaques?

Members of a social group have to make collective decisions in order to synchronise their activities. In a shared consensus decision, all group members can take part in the decision whereas in an unshared consensus decision, one individual, usually a dominant member of the group, takes the decision for the rest of the group. It has been suggested that the type of decision-making of a species could be influenced by its social style. To investigate this further, we studied collective movements in two species with opposed social systems, the Tonkean macaque (Macaca tonkeana) and the rhesus macaque (Macaca mulatta). From our results, it appears that the decision to move is the result of the choices and actions of several individuals in both groups. However, this consensus decision involved nearly all group members in Tonkean macaques whereas dominant and old individuals took a prominent role in rhesus macaques. Thus, we suggest that Tonkean macaques display equally shared consensus decisions to move, whereas in the same context rhesus macaque exhibit partially shared consensus decisions. Such a difference in making a collective decision might be linked to the different social systems of the two studied species.     

Collective decision‐making promotes fitness loss in a fusion‐fission society

While collective decision‐making is recognised as a significant contributor to fitness in social species, the opposite outcome is also logically possible. We show that collective movement decisions guided by individual bison sharing faulty information about habitat quality promoted the use of ecological traps. The frequent, but short‐lived, associations of bison with different spatial knowledge led to a population‐wide shift from avoidance to selection of agricultural patches over 9 years in and around Prince Albert National Park, Canada. Bison were more likely to travel to an agricultural patch for the first time by following conspecifics already familiar with agricultural patches. Annual adult mortality increased by 12% due to hunting of bison on agricultural lands. Maladaptive social behaviour accordingly was a major force that contributed to a ~50% population decline in less than a decade. In human‐altered landscapes, social learning by group‐living species can lead to fitness losses, particularly in fusion‐fission societies.     

The Organization of Collective Group Movements in Wild Barbary Macaques (Macaca sylvanus): Social Structure Drives Processes of Group Coordination in Macaques

Social animals have to coordinate activities and collective movements to benefit from the advantages of group living. Animals in large groups maintain cohesion by self-organization processes whereas in smaller groups consensus decisions can be reached. Where consensus decisions are relevant leadership may emerge. Variation in the organization of collective movements has been linked to variation in female social tolerance among macaque species ranging from despotic to egalitarian. Here we investigated the processes underlying group movements in a wild macaque species characterized by a degree of social tolerance intermediate to previously studied congeneric species. We focused on processes before, during and after the departure of the first individual. To this end, we observed one group of wild Barbary macaques (Macaca sylvanus) in the Middle Atlas, Morocco using all-occurrence behaviour sampling of 199 collective movements. We found that initiators of a collective movement usually chose the direction in which more individuals displayed pre-departure behavior. Dominant individuals contributed to group movements more than subordinates, especially juveniles, measured as frequencies of successful initiations and pre-departure behaviour. Joining was determined by affiliative relationships and the number of individuals that already joined the movement (mimetism). Thus, in our study group partially shared consensus decisions mediated by selective mimetism seemed to be prevalent, overall supporting the suggestion that a species’ social style affects the organization of group movements. As only the most tolerant species show equally shared consensus decisions whereas in others the decision is partially shared with a bias to dominant individuals the type of consensus decisions seems to follow a stepwise relation. Joining order may also follow a stepwise, however opposite, relationship, because dominance only determined joining in highly despotic, but not in intermediate and tolerant species.     

Consensus decision making in animals

Individual animals routinely face decisions that are crucial to their fitness. In social species, however, many of these decisions need to be made jointly with other group members because the group will split apart unless a consensus is reached. Here, we review empirical and theoretical studies of consensus decision making, and place them in a coherent framework. In particular, we classify consensus decisions according to the degree to which they involve conflict of interest between group members, and whether they involve either local or global communication; we ask, for different categories of consensus decision, who makes the decision, what are the underlying mechanisms, and what are the functional consequences. We conclude that consensus decision making is common in non-human animals, and that cooperation between group members in the decision-making process is likely to be the norm, even when the decision involves significant conflict of interest.     

Is Leadership a Reliable Concept in Animals? An Empirical Study in the Horse

Leadership is commonly invoked when accounting for the coordination of group movements in animals, yet it remains loosely defined. In parallel, there is increased evidence of the sharing of group decisions by animals on the move. How leadership integrates within this recent framework on collective decision-making is unclear. Here, we question the occurrence of leadership in horses, a species in which this concept is of prevalent use. The relevance of the three main definitions of leadership – departing first, walking in front travel position, and eliciting the joining of mates – was tested on the collective movements of two semi-free ranging groups of Przewalski horses (Equus ferus przewalskii). We did not find any leader capable of driving most group movements or recruiting mates more quickly than others. Several group members often displayed pre-departure behaviours at the same time, and the simultaneous departure of several individuals was common. We conclude that the decision-making process was shared by several group members a group movement (i.e., partially shared consensus) and that the leadership concept did not help to depict individual departure and leading behaviour across movements in both study groups. Rather, the different proxies of leadership produced conflicting information about individual contributions to group coordination. This study discusses the implications of these findings for the field of coordination and decision-making research.     

To follow or not? How animals in fusion–fission societies handle conflicting information during group decision‐making

When group members possess differing information about the environment, they may disagree on the best movement decision. Such conflicts result in group break‐ups, and are therefore a fundamental driver of fusion–fission group dynamics. Yet, a paucity of empirical work hampers our understanding of how adaptive evolution has shaped plasticity in collective behaviours that promote and maintain fusion–fission dynamics. Using movement data from GPS‐collared bison, we found that individuals constantly associated with other animals possessing different spatial knowledge, and both personal and conspecific information influenced an individual's patch choice decisions. During conflict situations, bison used group familiarity coupled with their knowledge of local foraging options and recently sampled resource quality when deciding to follow or leave a group – a tactic that led to energy‐rewarding movements. Natural selection has shaped collective behaviours for coping with social conflicts and resource heterogeneity, which maintain fusion–fission dynamics and play an essential role in animal distribution.     

How many for dinner? Recruitment and monitoring by glances in capuchins

Group members present physical and physiological differences according to their age, sex or social status, which could generate motivation differences among individuals during travel. In spite of these divergences of interest among individuals, the group succeeds more often than not in making a collective decision about departure time and which direction to take. To reach a consensus decision, animals should exchange information relating to characteristics of group movement through different communication channels. The main purpose of this study is to understand the function of behaviour patterns displayed during movements of white-faced capuchins (Cebus capucinus). We designed experiments in which we provoked collective movements involving a binary choice. During experiments, a video camera recorded the behaviour of each capuchin, which enabled us to determine which individuals displayed a behavioural pattern during travel and how this behaviour influenced the other group members. We found that looking backwards seemed to permit the recruitment of group mates during collective movement. This behaviour also seemed to allow the quantification of the number of followers, since the emitter modified its locomotion speed according to this number. In this preliminary study, we showed that visual behaviour was used to recruit and monitor group mates during collective movements and provided information on mechanisms involved in maintaining cohesion and coordination among group members during travel.     

Group decision-making in fission-fusion societies

The prevalent view of group splitting during group decisions is that a beneficial consensus has not been reached because time constraints, different individual information, or inter-individual conflicts lead to fission instead of a compromise. However, societies with high fission-fusion dynamics may allow their members to avoid consensus decisions that are not in their favour without foregoing grouping benefits that arise from collective behaviour. Moreover, by forming temporary subgroups that represent individual preferences better than the group as a whole fission-fusion societies could avoid a permanent break up even in situations where conflicts among their members are to strong to reach a consensus.     

Collective decision‐making and fission–fusion dynamics: a conceptual framework

Sociality exists in an extraordinary range of ecological settings. For individuals to accrue the benefits associated with social interactions, they are required to maintain a degree of spatial and temporal coordination in their activities, and make collective decisions. Such coordination and decision‐making has been the focus of much recent research. However, efforts largely have been directed toward understanding patterns of collective behaviour in relatively stable and cohesive groups. Less well understood is how fission–fusion dynamics mediate the process and outcome of collective decisions making. Here, we aim to apply established concepts and knowledge to highlight the implications of fission–fusion dynamics for collective decisions, presenting a conceptual framework based on the outcome of a small‐group discussion INCORE meeting (funded by the European Community's Sixth Framework Programme). First, we discuss how the degree of uncertainty in the environment shapes social flexibility and therefore the types of decisions individuals make in different social settings. Second, we propose that the quality of social relationships and the energetic needs of each individual influence fission decisions. Third, we explore how these factors affect the probability of individuals to fuse. Fourth, we discuss how group size and fission–fusion dynamics may affect communication processes between individuals at a local or global scale to reach a consensus or to fission. Finally, we offer a number of suggestions for future research, capturing emerging ideas and concepts on the interaction between collective decisions and fission–fusion dynamics.     

Quorum responses and consensus decision making

Animal groups are said to make consensus decisions when group members come to agree on the same option. Consensus decisions are taxonomically widespread and potentially offer three key benefits: maintenance of group cohesion, enhancement of decision accuracy compared with lone individuals and improvement in decision speed. In the absence of centralized control, arriving at a consensus depends on local interactions in which each individual''s likelihood of choosing an option increases with the number of others already committed to that option. The resulting positive feedback can effectively direct most or all group members to the best available choice. In this paper, we examine the functional form of the individual response to others'' behaviour that lies at the heart of this process. We review recent theoretical and empirical work on consensus decisions, and we develop a simple mathematical model to show the central importance to speedy and accurate decisions of quorum responses, in which an animal''s probability of exhibiting a behaviour is a sharply nonlinear function of the number of other individuals already performing this behaviour. We argue that systems relying on such quorum rules can achieve cohesive choice of the best option while also permitting adaptive tuning of the trade-off between decision speed and accuracy.     

Where Next? Group Coordination and Collective Decision Making by Primates

Primate groups need to remain coordinated in their activities and collectively decide when and where to travel if they are to accrue the benefits and minimize the costs of sociality. The achievement of coordinated activity and group decision making therefore has important implications for individual survival and reproduction. The aim of this special issue is to bring together a collection of empirical, theoretical, and commentary articles by primatologists studying this rapidly expanding topic. In this article, we introduce the contributions within the special issue and provide a background to the topic. We begin by focusing on decisions that involve a collective transition between a resting and a moving state, a transition we term making the move. We examine whether specific predeparture behaviors seen during transitions represent intentional processes or more simple response facilitation. Next we classify decisions according to the contribution of individual group members, and describe how, and why, certain individuals can have a disproportionate influence over group-mates?? behavior. We then review how primate groups make decisions on the move. In particular, we focus on how variability in group size and spatial organization helps or hinders information transmission and coordination. We end with a discussion of new tools and methodology that will allow future investigators to address some outstanding questions in primate coordination and decision-making research. We conclude that a better integration of concepts and terminology, along with a focus on how individuals integrate environmental and social information, will be critical to developing a satisfactory understanding of collective patterns of behavior in primate systems.     

Grunt to go—Vocal coordination of group movements in redfronted lemurs

To remain cohesive as a group, individuals must coordinate their movements between resources. In many species, vocalisations are used in this context. While some species have specific movement calls, others use calls which are also employed in different contexts. The use of such multicontextual calls has rarely been studied quantitatively, especially during both the pre‐departure and departure period associated with collective decisions. We thus investigated the use of close calls (“grunts”) for the coordination of collective movements in four groups of wild redfronted lemurs (Eulemur rufifrons) in Kirindy Forest, Western Madagascar. Group movements are started by an initiator, who moves away from the group and is joined by followers setting out in the same direction. We observed collective movements and recorded vocalisations from 18 focal individuals (54 movements recorded for followers, 21 for initiators). The grunt rate of both initiators and followers was higher in the pre‐departure period than in a control context (i.e., during foraging). Initiators of collective movements grunted more often than followers in the pre‐departure period as well as at individual departure. The latter difference was due to the initiators’ grunt rates increasing earlier than the followers’ and remaining at an elevated level for longer. These observations suggest that grunts serve to coordinate the departure by indicating the individual's readiness to move. The pre‐departure period, in which both initiators and followers showed an elevated grunt rate, may provide the basis for a shared decision on departure time. The difference in initiator and follower call rates suggests that grunts may have a recruitment function, but playback experiments are required to test this potential function. Overall, our study describes how multicontextual close calls can function as movement calls, with changes in call rate providing a potential feedback mechanism for the timing of group movements. This study thus contributes to a more detailed understanding of the mechanisms of group coordination and collective decision‐making.     

Imitation Combined with a Characteristic Stimulus Duration Results in Robust Collective Decision-Making

For group-living animals, reaching consensus to stay cohesive is crucial for their fitness, particularly when collective motion starts and stops. Understanding the decision-making at individual and collective levels upon sudden disturbances is central in the study of collective animal behavior, and concerns the broader question of how information is distributed and evaluated in groups. Despite the relevance of the problem, well-controlled experimental studies that quantify the collective response of groups facing disruptive events are lacking. Here we study the behavior of small-sized groups of uninformed individuals subject to the departure and stop of a trained conspecific. We find that the groups reach an effective consensus: either all uninformed individuals follow the trained one (and collective motion occurs) or none does. Combining experiments and a simple mathematical model we show that the observed phenomena results from the interplay between simple mimetic rules and the characteristic duration of the stimulus, here, the time during which the trained individual is moving away. The proposed mechanism strongly depends on group size, as observed in the experiments, and even if group splitting can occur, the most likely outcome is always a coherent collective group response (consensus). The prevalence of a consensus is expected even if the groups of naives face conflicting information, e.g. if groups contain two subgroups of trained individuals, one trained to stay and one trained to leave. Our results indicate that collective decision-making and consensus in (small) animal groups are likely to be self-organized phenomena that do not involve concertation or even communication among the group members.     

Collective Learning and Optimal Consensus Decisions in Social Animal Groups

Learning has been studied extensively in the context of isolated individuals. However, many organisms are social and consequently make decisions both individually and as part of a collective. Reaching consensus necessarily means that a single option is chosen by the group, even when there are dissenting opinions. This decision-making process decouples the otherwise direct relationship between animals'' preferences and their experiences (the outcomes of decisions). Instead, because an individual''s learned preferences influence what others experience, and therefore learn about, collective decisions couple the learning processes between social organisms. This introduces a new, and previously unexplored, dynamical relationship between preference, action, experience and learning. Here we model collective learning within animal groups that make consensus decisions. We reveal how learning as part of a collective results in behavior that is fundamentally different from that learned in isolation, allowing grouping organisms to spontaneously (and indirectly) detect correlations between group members'' observations of environmental cues, adjust strategy as a function of changing group size (even if that group size is not known to the individual), and achieve a decision accuracy that is very close to that which is provably optimal, regardless of environmental contingencies. Because these properties make minimal cognitive demands on individuals, collective learning, and the capabilities it affords, may be widespread among group-living organisms. Our work emphasizes the importance and need for theoretical and experimental work that considers the mechanism and consequences of learning in a social context.     

Do ants make direct comparisons?

Many individual decisions are informed by direct comparison of the alternatives. In collective decisions, however, only certain group members may have the opportunity to compare options. Emigrating ant colonies (Temnothorax albipennis) show sophisticated nest-site choice, selecting superior sites even when they are nine times further away than the alternative. How do they do this? We used radio-frequency identification-tagged ants to monitor individual behaviour. Here we show for the first time that switching between nests during the decision process can influence nest choice without requiring direct comparison of nests. Ants finding the poor nest were likely to switch and find the good nest, whereas ants finding the good nest were more likely to stay committed to that nest. When ants switched quickly between the two nests, colonies chose the good nest. Switching by ants that had the opportunity to compare nests had little effect on nest choice. We suggest a new mechanism of collective nest choice: individuals respond to nest quality by the decision either to commit or to seek alternatives. Previously proposed mechanisms, recruitment latency and nest comparison, can be explained as side effects of this simple rule. Colony-level comparison and choice can emerge, without direct comparison by individuals.     

群居动物中的共同决策

群居的个体能够更好的躲避天敌的捕食,增强与同种其它种群的资源竞争,增加生殖机会与生殖成功率,使信息在个体之间顺畅的交流等。但是群内个体又会在有限的资源下产生群内的个体竞争,从而引起动物群的分裂,失去群居的利益。为了保持动物群的聚合力,当动物群内出现冲突时,需要在群内个体间形成协调各种冲突以及在群内达成共识的机制。依据动物社群组成的不同,领导力机制和自组织机制是协调群内冲突,形成一致决策和联合决策的两种主要机制。从行为生态学的角度入手,阐述了动物群内共同决策的类型,群内冲突的协调机制,共同决策的制定过程,比较了信息因素与利益因素在共同决策制定过程中的影响。旨在藉此推进我国相关领域研究的开展, 为群居动物社会与行为生态学研究者启发思路,并为保护群居濒危物种提供科学依据。     

Scalable rules for coherent group motion in a gregarious vertebrate

Individuals of gregarious species that initiate collective movement require mechanisms of cohesion in order to maintain advantages of group living. One fundamental question in the study of collective movement is what individual rules are employed when making movement decisions. Previous studies have revealed that group movements often depend on social interactions among individual members and specifically that collective decisions to move often follow a quorum-like response. However, these studies either did not quantify the response function at the individual scale (but rather tested hypotheses based on group-level behaviours), or they used a single group size and did not demonstrate which social stimuli influence the individual decision-making process. One challenge in the study of collective movement has been to discriminate between a common response to an external stimulus and the synchronization of behaviours resulting from social interactions. Here we discriminate between these two mechanisms by triggering the departure of one trained Merino sheep (Ovis aries) from groups containing one, three, five and seven naïve individuals. Each individual was thus exposed to various combinations of already-departed and non-departed individuals, depending on its rank of departure. To investigate which individual mechanisms are involved in maintaining group cohesion under conditions of leadership, we quantified the temporal dynamic of response at the individual scale. We found that individuals'' decisions to move do not follow a quorum response but rather follow a rule based on a double mimetic effect: attraction to already-departed individuals and attraction to non-departed individuals. This rule is shown to be in agreement with an adaptive strategy that is inherently scalable as a function of group size.     

The empirical question of thresholds and mechanisms of mate choice

Summary Theoretical discussions concerning how animals might best sample and select mates have suggested that individuals could base decisions either on a sample of mates (sampled-based decisions) or on a threshold of comparison (threshold-based decisions). Recent theoretical work demonstrates that threshold-based mating decisions generate higher expected fitness than sample-based mating decisions when search costs exist. Empirical results from most unmanipulated systems, however, either conclude that females make sample-based decisions or are inconclusive. A few experimental studies designed to detect mating thresholds purport to demonstrate threshold-based choice but an examination of these studies indicates such conclusions were premature. We believe that few examples of threshold-based choice exist because protocols designed to identify mating thresholds were often inconsistent with models of threshold choice. We suggest that future empirical work strive not to document mating thresholdsper se. Rather, future work might best reveal decision rules by manipulating the distribution of quality among potential mates; such manipulations predict uniquely how females using sample-based and threshold-based decision rules should behave.