Opposing Responses to Scarcity Emerge from Functionally Unique Sociality Drivers.

AbstractFrom biofilms to whale pods, organisms across taxa live in groups, thereby accruing numerous diverse benefits of sociality. All social organisms, however, pay the inherent cost of increased resource competition. One expects that when resources become scarce, this cost will increase, causing group sizes to decrease. Indeed, this occurs in some species, but there are also species for which group sizes remain stable or even increase under scarcity. What accounts for these opposing responses? We present a conceptual framework, literature review, and theoretical model demonstrating that differing responses to sudden resource shifts can be explained by which sociality benefit exerts the strongest selection pressure on a particular species. We categorize resource-related benefits of sociality into six functionally distinct classes and model their effect on the survival of individuals foraging in groups under different resource conditions. We find that whether, and to what degree, the optimal group size (or correlates thereof) increases, decreases, or remains constant when resource abundance declines depends strongly on the dominant sociality mechanism. Existing data, although limited, support our model predictions. Overall, we show that across a wide diversity of taxa, differences in how group size shifts in response to resource declines can be driven by differences in the primary benefits of sociality.

Beyond collective intelligence: Collective adaptation.

We develop a conceptual framework for studying collective adaptation in complex socio-cognitive systems, driven by dynamic interactions of social integration strategies, social environments and problem structures. Going beyond searching for 'intelligent' collectives, we integrate research from different disciplines and outline modelling approaches that can be used to begin answering questions such as why collectives sometimes fail to reach seemingly obvious solutions, how they change their strategies and network structures in response to different problems and how we can anticipate and perhaps change future harmful societal trajectories. We discuss the importance of considering path dependence, lack of optimization and collective myopia to understand the sometimes counterintuitive outcomes of collective adaptation. We call for a transdisciplinary, quantitative and societally useful social science that can help us to understand our rapidly changing and ever more complex societies, avoid collective disasters and reach the full potential of our ability to organize in adaptive collectives.

Stewardship of global collective behavior.

Collective behavior provides a framework for understanding how the actions and properties of groups emerge from the way individuals generate and share information. In humans, information flows were initially shaped by natural selection yet are increasingly structured by emerging communication technologies. Our larger, more complex social networks now transfer high-fidelity information over vast distances at low cost. The digital age and the rise of social media have accelerated changes to our social systems, with poorly understood functional consequences. This gap in our knowledge represents a principal challenge to scientific progress, democracy, and actions to address global crises. We argue that the study of collective behavior must rise to a "crisis discipline" just as medicine, conservation, and climate science have, with a focus on providing actionable insight to policymakers and regulators for the stewardship of social systems.

Individual error correction drives responsive self-assembly of army ant scaffolds.

An inherent strength of evolved collective systems is their ability to rapidly adapt to dynamic environmental conditions, offering resilience in the face of disruption. This is thought to arise when individual sensory inputs are filtered through local interactions, producing an adaptive response at the group level. To understand how simple rules encoded at the individual level can lead to the emergence of robust group-level (or distributed) control, we examined structures we call "scaffolds," self-assembled by Eciton burchellii army ants on inclined surfaces that aid travel during foraging and migration. We conducted field experiments with wild E. burchellii colonies, manipulating the slope over which ants traversed, to examine the formation of scaffolds and their effects on foraging traffic. Our results show that scaffolds regularly form on inclined surfaces and that they reduce losses of foragers and prey, by reducing slipping and/or falling of ants, thus facilitating traffic flow. We describe the relative effects of environmental geometry and traffic on their growth and present a theoretical model to examine how the individual behaviors underlying scaffold formation drive group-level effects. Our model describes scaffold growth as a control response at the collective level that can emerge from individual error correction, requiring no complex communication among ants. We show that this model captures the dynamics observed in our experiments and is able to predict the growth-and final size-of scaffolds, and we show how the analytical solution allows for estimation of these dynamics.

The wisdom of stalemates: consensus and clustering as filtering mechanisms for improving collective accuracy.

Groups of organisms, from bacteria to fish schools to human societies, depend on their ability to make accurate decisions in an uncertain world. Most models of collective decision-making assume that groups reach a consensus during a decision-making bout, often through simple majority rule. In many natural and sociological systems, however, groups may fail to reach consensus, resulting in stalemates. Here, we build on opinion dynamics and collective wisdom models to examine how stalemates may affect the wisdom of crowds. For simple environments, where individuals have access to independent sources of information, we find that stalemates improve collective accuracy by selectively filtering out incorrect decisions (an effect we call stalemate filtering). In complex environments, where individuals have access to both shared and independent information, this effect is even more pronounced, restoring the wisdom of crowds in regions of parameter space where large groups perform poorly when making decisions using majority rule. We identify network properties that tune the system between consensus and accuracy, providing mechanisms by which animals, or evolution, could dynamically adjust the collective decision-making process in response to the reward structure of the possible outcomes. Overall, these results highlight the adaptive potential of stalemate filtering for improving the decision-making abilities of group-living animals.

Fisheries-induced selection against schooling behaviour in marine fishes.

Group living is a common strategy used by fishes to improve their fitness. While sociality is associated with many benefits in natural environments, including predator avoidance, this behaviour may be maladaptive in the Anthropocene. Humans have become the dominant predator in many marine systems, with modern fishing gear developed to specifically target groups of schooling species. Therefore, ironically, behavioural strategies which evolved to avoid non-human predators may now actually make certain fish more vulnerable to predation by humans. Here, we use an individual-based model to explore the evolution of fish schooling behaviour in a range of environments, including natural and human-dominated predation conditions. In our model, individual fish may leave or join groups depending on their group-size preferences, but their experienced group size is also a function of the preferences of others in the population. Our model predicts that industrial fishing selects against individual-level behaviours that produce large groups. However, the relationship between fishing pressure and sociality is nonlinear, and we observe discontinuities and hysteresis as fishing pressure is increased or decreased. Our results suggest that industrial fishing practices could be altering fishes' tendency to school, and that social behaviour should be added to the list of traits subject to fishery-induced evolution.

Modular structure within groups causes information loss but can improve decision accuracy.

Many animal groups exhibit signatures of persistent internal modular structure, whereby individuals consistently interact with certain groupmates more than others. In such groups, information relevant to a collective decision may spread unevenly through the group, but how this impacts the quality of the resulting decision is not well understood. Here, we explicitly model modularity within animal groups and examine how it affects the amount of information represented in collective decisions, as well as the accuracy of those decisions. We find that modular structure necessarily causes a loss of information, effectively silencing the input from a fraction of the group. However, the effect of this information loss on collective accuracy depends on the informational environment in which the decision is made. In simple environments, the information loss is detrimental to collective accuracy. By contrast, in complex environments, modularity tends to improve accuracy. This is because small group sizes typically maximize collective accuracy in such environments, and modular structure allows a large group to behave like a smaller group (in terms of its decision-making). These results suggest that in naturalistic environments containing correlated information, large animal groups may be able to exploit modular structure to improve decision accuracy while retaining other benefits of large group size. This article is part of the theme issue 'Liquid brains, solid brains: How distributed cognitive architectures process information'.

MAPLE (modular automated platform for large-scale experiments), a robot for integrated organism-handling and phenotyping.

Lab organisms are valuable in part because of large-scale experiments like screens, but performing such experiments over long time periods by hand is arduous and error-prone. Organism-handling robots could revolutionize large-scale experiments in the way that liquid-handling robots accelerated molecular biology. We developed a modular automated platform for large-scale experiments (MAPLE), an organism-handling robot capable of conducting lab tasks and experiments, and then deployed it to conduct common experiments in Saccharomyces cerevisiae, Caenorhabditis elegans, Physarum polycephalum, Bombus impatiens, and Drosophila melanogaster. Focusing on fruit flies, we developed a suite of experimental modules that permitted the automated collection of virgin females and execution of an intricate and laborious social behavior experiment. We discovered that (1) pairs of flies exhibit persistent idiosyncrasies in social behavior, which (2) require olfaction and vision, and (3) social interaction network structure is stable over days. These diverse examples demonstrate MAPLE's versatility for automating experimental biology.

Counteracting estimation bias and social influence to improve the wisdom of crowds.

Aggregating multiple non-expert opinions into a collective estimate can improve accuracy across many contexts. However, two sources of error can diminish collective wisdom: individual estimation biases and information sharing between individuals. Here, we measure individual biases and social influence rules in multiple experiments involving hundreds of individuals performing a classic numerosity estimation task. We first investigate how existing aggregation methods, such as calculating the arithmetic mean or the median, are influenced by these sources of error. We show that the mean tends to overestimate, and the median underestimate, the true value for a wide range of numerosities. Quantifying estimation bias, and mapping individual bias to collective bias, allows us to develop and validate three new aggregation measures that effectively counter sources of collective estimation error. In addition, we present results from a further experiment that quantifies the social influence rules that individuals employ when incorporating personal estimates with social information. We show that the corrected mean is remarkably robust to social influence, retaining high accuracy in the presence or absence of social influence, across numerosities and across different methods for averaging social information. Using knowledge of estimation biases and social influence rules may therefore be an inexpensive and general strategy to improve the wisdom of crowds.

Collective animal navigation and migratory culture: from theoretical models to empirical evidence.

Animals often travel in groups, and their navigational decisions can be influenced by social interactions. Both theory and empirical observations suggest that such collective navigation can result in individuals improving their ability to find their way and could be one of the key benefits of sociality for these species. Here, we provide an overview of the potential mechanisms underlying collective navigation, review the known, and supposed, empirical evidence for such behaviour and highlight interesting directions for future research. We further explore how both social and collective learning during group navigation could lead to the accumulation of knowledge at the population level, resulting in the emergence of migratory culture.This article is part of the theme issue 'Collective movement ecology'.

Optimal construction of army ant living bridges.

Integrating the costs and benefits of collective behaviors is a fundamental challenge to understanding the evolution of group living. These costs and benefits can rarely be quantified simultaneously due to the complexity of the interactions within the group, or even compared to each other because of the absence of common metrics between them. The construction of 'living bridges' by New World army ants - which they use to shorten their foraging trails - is a unique example of a collective behavior where costs and benefits have been experimentally measured and related to each other. As a result, it is possible to make quantitative predictions about when and how the behavior will be observed. In this paper, we extend a previous mathematical model of these costs and benefits to much broader domain of applicability. Specifically, we exhibit a procedure for analyzing the optimal formation, and final configuration, of army ant living bridges given a means to express the geometrical configuration of foraging path obstructions. Using this procedure, we provide experimentally testable predictions of the final bridge position, as well as the optimal formation process for certain cases, for a wide range of scenarios, which more closely resemble common terrain obstacles that ants encounter in nature. As such, our framework offers a rare benchmark for determining the evolutionary pressures governing the evolution of a naturally occurring collective animal behavior.

Army ants dynamically adjust living bridges in response to a cost-benefit trade-off.

The ability of individual animals to create functional structures by joining together is rare and confined to the social insects. Army ants (Eciton) form collective assemblages out of their own bodies to perform a variety of functions that benefit the entire colony. Here we examine ?bridges" of linked individuals that are constructed to span gaps in the colony's foraging trail. How these living structures adjust themselves to varied and changing conditions remains poorly understood. Our field experiments show that the ants continuously modify their bridges, such that these structures lengthen, widen, and change position in response to traffic levels and environmental geometry. Ants initiate bridges where their path deviates from their incoming direction and move the bridges over time to create shortcuts over large gaps. The final position of the structure depended on the intensity of the traffic and the extent of path deviation and was influenced by a cost-benefit trade-off at the colony level, where the benefit of increased foraging trail efficiency was balanced by the cost of removing workers from the foraging pool to form the structure. To examine this trade-off, we quantified the geometric relationship between costs and benefits revealed by our experiments. We then constructed a model to determine the bridge location that maximized foraging rate, which qualitatively matched the observed movement of bridges. Our results highlight how animal self-assemblages can be dynamically modified in response to a group-level cost-benefit trade-off, without any individual unit's having information on global benefits or costs.

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.

Decision accuracy in complex environments is often maximized by small group sizes.

Individuals in groups, whether composed of humans or other animal species, often make important decisions collectively, including avoiding predators, selecting a direction in which to migrate and electing political leaders. Theoretical and empirical work suggests that collective decisions can be more accurate than individual decisions, a phenomenon known as the 'wisdom of crowds'. In these previous studies, it has been assumed that individuals make independent estimates based on a single environmental cue. In the real world, however, most cues exhibit some spatial and temporal correlation, and consequently, the sensory information that near neighbours detect will also be, to some degree, correlated. Furthermore, it may be rare for an environment to contain only a single informative cue, with multiple cues being the norm. We demonstrate, using two simple models, that taking this natural complexity into account considerably alters the relationship between group size and decision-making accuracy. In only a minority of environments do we observe the typical wisdom of crowds phenomenon (whereby collective accuracy increases monotonically with group size). When the wisdom of crowds is not observed, we find that a finite, and often small, group size maximizes decision accuracy. We reveal that, counterintuitively, it is the noise inherent in these small groups that enhances their accuracy, allowing individuals in such groups to avoid the detrimental effects of correlated information while exploiting the benefits of collective decision-making. Our results demonstrate that the conventional view of the wisdom of crowds may not be informative in complex and realistic environments, and that being in small groups can maximize decision accuracy across many contexts.

Visual sensory networks and effective information transfer in animal groups.

Social transmission of information is vital for many group-living animals, allowing coordination of motion and effective response to complex environments. Revealing the interaction networks underlying information flow within these groups is a central challenge. Previous work has modeled interactions between individuals based directly on their relative spatial positions: each individual is considered to interact with all neighbors within a fixed distance (metric range), a fixed number of nearest neighbors (topological range), a 'shell' of near neighbors (Voronoi range), or some combination (Figure 1A). However, conclusive evidence to support these assumptions is lacking. Here, we employ a novel approach that considers individual movement decisions to be based explicitly on the sensory information available to the organism. In other words, we consider that while spatial relations do inform interactions between individuals, they do so indirectly, through individuals' detection of sensory cues. We reconstruct computationally the visual field of each individual throughout experiments designed to investigate information propagation within fish schools (golden shiners, Notemigonus crysoleucas). Explicitly considering visual sensing allows us to more accurately predict the propagation of behavioral change in these groups during leadership events. Furthermore, we find that structural properties of visual interaction networks differ markedly from those of metric and topological counterparts, suggesting that previous assumptions may not appropriately reflect information flow in animal groups.