Evolution of norms for judging social behavior.

Reputations provide a powerful mechanism to sustain cooperation, as individuals cooperate with those of good social standing. But how should someone's reputation be updated as we observe their social behavior, and when will a population converge on a shared norm for judging behavior? Here, we develop a mathematical model of cooperation conditioned on reputations, for a population that is stratified into groups. Each group may subscribe to a different social norm for assessing reputations and so norms compete as individuals choose to move from one group to another. We show that a group initially comprising a minority of the population may nonetheless overtake the entire population-especially if it adopts the Stern Judging norm, which assigns a bad reputation to individuals who cooperate with those of bad standing. When individuals do not change group membership, stratifying reputation information into groups tends to destabilize cooperation, unless individuals are strongly insular and favor in-group social interactions. We discuss the implications of our results for the structure of information flow in a population and for the evolution of social norms of judgment.

Development shapes the evolutionary diversification of rodent stripe patterns.

Vertebrate groups have evolved strikingly diverse color patterns. However, it remains unknown to what extent the diversification of such patterns has been shaped by the proximate, developmental mechanisms that regulate their formation. While these developmental mechanisms have long been inaccessible empirically, here we take advantage of recent insights into rodent pattern formation to investigate the role of development in shaping pattern diversification across rodents. Based on a broad survey of museum specimens, we first establish that various rodents have independently evolved diverse patterns consisting of longitudinal stripes, varying across species in number, color, and relative positioning. We then interrogate this diversity using a simple model that incorporates recent molecular and developmental insights into stripe formation in African striped mice. Our results suggest that, on the one hand, development has facilitated pattern diversification: The diversity of patterns seen across species can be generated by a single developmental process, and small changes in this process suffice to recapitulate observed evolutionary changes in pattern organization. On the other hand, development has constrained diversification: Constraints on stripe positioning limit the scope of evolvable patterns, and although pattern organization appears at first glance phylogenetically unconstrained, development turns out to impose a cryptic constraint. Altogether, this work reveals that pattern diversification in rodents can in part be explained by the underlying development and illustrates how pattern formation models can be leveraged to interpret pattern evolution.

When do stereotypes undermine indirect reciprocity?

Social reputations provide a powerful mechanism to stimulate human cooperation, but observing individual reputations can be cognitively costly. To ease this burden, people may rely on proxies such as stereotypes, or generalized reputations assigned to groups. Such stereotypes are less accurate than individual reputations, and so they could disrupt the positive feedback between altruistic behavior and social standing, undermining cooperation. How do stereotypes impact cooperation by indirect reciprocity? We develop a theoretical model of group-structured populations in which individuals are assigned either individual reputations based on their own actions or stereotyped reputations based on their groups' behavior. We find that using stereotypes can produce either more or less cooperation than using individual reputations, depending on how widely reputations are shared. Deleterious outcomes can arise when individuals adapt their propensity to stereotype. Stereotyping behavior can spread and can be difficult to displace, even when it compromises collective cooperation and even though it makes a population vulnerable to invasion by defectors. We discuss the implications of our results for the prevalence of stereotyping and for reputation-based cooperation in structured populations.

When being flexible matters: Ecological underpinnings for the evolution of collective flexibility and task allocation.

Task allocation is a central feature of collective organization. Living collective systems, such as multicellular organisms or social insect colonies, have evolved diverse ways to allocate individuals to different tasks, ranging from rigid, inflexible task allocation that is not adjusted to changing circumstances to more fluid, flexible task allocation that is rapidly adjusted to the external environment. While the mechanisms underlying task allocation have been intensely studied, it remains poorly understood whether differences in the flexibility of task allocation can be viewed as adaptive responses to different ecological contexts­for example, different degrees of temporal variability. Motivated by this question, we develop an analytically tractable mathematical framework to explore the evolution of task allocation in dynamic environments. We find that collective flexibility is not necessarily always adaptive, and fails to evolve in environments that change too slowly (relative to how long tasks can be left unattended) or too quickly (relative to how rapidly task allocation can be adjusted). We further employ the framework to investigate how environmental variability impacts the internal organization of task allocation, which allows us to propose adaptive explanations for some puzzling empirical observations, such as seemingly unnecessary task switching under constant environmental conditions, apparent task specialization without efficiency benefits, and high levels of individual inactivity. Altogether, this work provides a general framework for probing the evolved diversity of task allocation strategies in nature and reinforces the idea that considering a system's ecology is crucial to explaining its collective organization.

Structured foraging of soil predators unveils functional responses to bacterial defenses.

Predators and their foraging strategies often determine ecosystem structure and function. Yet, the role of protozoan predators in microbial soil ecosystems remains elusive despite the importance of these ecosystems to global biogeochemical cycles. In particular, amoebae-the most abundant soil protozoan predator of bacteria-remineralize soil nutrients and shape the bacterial community. However, their foraging strategies and their role as microbial ecosystem engineers remain unknown. Here, we present a multiscale approach, connecting microscopic single-cell analysis and macroscopic whole ecosystem dynamics, to expose a phylogenetically widespread foraging strategy, in which an amoeba population spontaneously partitions between cells with fast, polarized movement and cells with slow, unpolarized movement. Such differentiated motion gives rise to efficient colony expansion and consumption of the bacterial substrate. From these insights, we construct a theoretical model that predicts how disturbances to amoeba growth rate and movement disrupt their predation efficiency. These disturbances correspond to distinct classes of bacterial defenses, which allows us to experimentally validate our predictions. All considered, our characterization of amoeba foraging identifies amoeba mobility, and not amoeba growth, as the core determinant of predation efficiency and a key target for bacterial defense systems.

Response thresholds alone cannot explain empirical patterns of division of labor in social insects.

The effects of heterogeneity in group composition remain a major hurdle to our understanding of collective behavior across disciplines. In social insects, division of labor (DOL) is an emergent, colony-level trait thought to depend on colony composition. Theoretically, behavioral response threshold models have most commonly been employed to investigate the impact of heterogeneity on DOL. However, empirical studies that systematically test their predictions are lacking because they require control over colony composition and the ability to monitor individual behavior in groups, both of which are challenging. Here, we employ automated behavioral tracking in 120 colonies of the clonal raider ant with unparalleled control over genetic, morphological, and demographic composition. We find that each of these sources of variation in colony composition generates a distinct pattern of behavioral organization, ranging from the amplification to the dampening of inherent behavioral differences in heterogeneous colonies. Furthermore, larvae modulate interactions between adults, exacerbating the apparent complexity. Models based on threshold variation alone only partially recapitulate these empirical patterns. However, by incorporating the potential for variability in task efficiency among adults and task demand among larvae, we account for all the observed phenomena. Our findings highlight the significance of previously overlooked parameters pertaining to both larvae and workers, allow the formulation of theoretical predictions for increasing colony complexity, and suggest new avenues of empirical study.

Polarized information ecosystems can reorganize social networks via information cascades.

The precise mechanisms by which the information ecosystem polarizes society remain elusive. Focusing on political sorting in networks, we develop a computational model that examines how social network structure changes when individuals participate in information cascades, evaluate their behavior, and potentially rewire their connections to others as a result. Individuals follow proattitudinal information sources but are more likely to first hear and react to news shared by their social ties and only later evaluate these reactions by direct reference to the coverage of their preferred source. Reactions to news spread through the network via a complex contagion. Following a cascade, individuals who determine that their participation was driven by a subjectively "unimportant" story adjust their social ties to avoid being misled in the future. In our model, this dynamic leads social networks to politically sort when news outlets differentially report on the same topic, even when individuals do not know others' political identities. Observational follow network data collected on Twitter support this prediction: We find that individuals in more polarized information ecosystems lose cross-ideology social ties at a rate that is higher than predicted by chance. Importantly, our model reveals that these emergent polarized networks are less efficient at diffusing information: Individuals avoid what they believe to be "unimportant" news at the expense of missing out on subjectively "important" news far more frequently. This suggests that "echo chambers"-to the extent that they exist-may not echo so much as silence.

Interindividual cooperation mediated by partisanship complicates Madison's cure for "mischiefs of faction".

Political theorists have long argued that enlarging the political sphere to include a greater diversity of interests would cure the ills of factions in a pluralistic society. While the scope of politics has expanded dramatically over the past 75 y, polarization is markedly worse. Motivated by this paradox, we take a bottom-up approach to explore how partisan individual-level dynamics in a diverse (multidimensional) issue space can shape collective-level factionalization via an emergent dimensionality reduction. We extend a model of cultural evolution grounded in evolutionary game theory, in which individuals accumulate benefits through pairwise interactions and imitate (or learn) the strategies of successful others. The degree of partisanship determines the likelihood of learning from individuals of the opposite party. This approach captures the coupling between individual behavior, partisan-mediated opinion dynamics, and an interaction network that changes endogenously according to the evolving interests of individuals. We find that while expanding the diversity of interests can indeed improve both individual and collective outcomes, increasingly high partisan bias promotes a reduction in issue dimensionality via party-based assortment that leads to increasing polarization. When party bias becomes extreme, it also boosts interindividual cooperation, thereby further entrenching extreme polarization and creating a tug-of-war between individual cooperation and societal cohesion. These dangers of extreme partisanship are highest when individuals' interests and opinions are heavily shaped by peers and there is little independent exploration. Overall, our findings highlight the urgency to study polarization in a coupled, multilevel context.

Large herbivores suppress liana infestation in an African savanna.

African savannas are the last stronghold of diverse large-mammal communities, and a major focus of savanna ecology is to understand how these animals affect the relative abundance of trees and grasses. However, savannas support diverse plant life-forms, and human-induced changes in large-herbivore assemblages-declining wildlife populations and their displacement by livestock-may cause unexpected shifts in plant community composition. We investigated how herbivory affects the prevalence of lianas (woody vines) and their impact on trees in an East African savanna. Although scarce (<2% of tree canopy area) and defended by toxic latex, the dominant liana, Cynanchum viminale (Apocynaceae), was eaten by 15 wild large-herbivore species and was consumed in bulk by native browsers during experimental cafeteria trials. In contrast, domesticated ungulates rarely ate lianas. When we experimentally excluded all large herbivores for periods of 8 to 17 y (simulating extirpation), liana abundance increased dramatically, with up to 75% of trees infested. Piecewise exclusion of different-sized herbivores revealed functional complementarity among size classes in suppressing lianas. Liana infestation reduced tree growth and reproduction, but herbivores quickly cleared lianas from trees after the removal of 18-y-old exclosure fences (simulating rewilding). A simple model of liana contagion showed that, without herbivores, the long-term equilibrium could be either endemic (liana-tree coexistence) or an all-liana alternative stable state. We conclude that ongoing declines of wild large-herbivore populations will disrupt the structure and functioning of many African savannas in ways that have received little attention and that may not be mitigated by replacing wildlife with livestock.

Eco-evolutionary significance of "loners".

Loners-individuals out of sync with a coordinated majority-occur frequently in nature. Are loners incidental byproducts of large-scale coordination attempts, or are they part of a mosaic of life-history strategies? Here, we provide empirical evidence of naturally occurring heritable variation in loner behavior in the model social amoeba Dictyostelium discoideum. We propose that Dictyostelium loners-cells that do not join the multicellular life stage-arise from a dynamic population-partitioning process, the result of each cell making a stochastic, signal-based decision. We find evidence that this imperfectly synchronized multicellular development is affected by both abiotic (environmental porosity) and biotic (signaling) factors. Finally, we predict theoretically that when a pair of strains differing in their partitioning behavior coaggregate, cross-signaling impacts slime-mold diversity across spatiotemporal scales. Our findings suggest that loners could be critical to understanding collective and social behaviors, multicellular development, and ecological dynamics in D. discoideum. More broadly, across taxa, imperfect coordination of collective behaviors might be adaptive by enabling diversification of life-history strategies.

A theoretical foundation for multi-scale regular vegetation patterns.

Self-organized regular vegetation patterns are widespread and thought to mediate ecosystem functions such as productivity and robustness, but the mechanisms underlying their origin and maintenance remain disputed. Particularly controversial are landscapes of overdispersed (evenly spaced) elements, such as North American Mima mounds, Brazilian murundus, South African heuweltjies, and, famously, Namibian fairy circles. Two competing hypotheses are currently debated. On the one hand, models of scale-dependent feedbacks, whereby plants facilitate neighbours while competing with distant individuals, can reproduce various regular patterns identified in satellite imagery. Owing to deep theoretical roots and apparent generality, scale-dependent feedbacks are widely viewed as a unifying and near-universal principle of regular-pattern formation despite scant empirical evidence. On the other hand, many overdispersed vegetation patterns worldwide have been attributed to subterranean ecosystem engineers such as termites, ants, and rodents. Although potentially consistent with territorial competition, this interpretation has been challenged theoretically and empirically and (unlike scale-dependent feedbacks) lacks a unifying dynamical theory, fuelling scepticism about its plausibility and generality. Here we provide a general theoretical foundation for self-organization of social-insect colonies, validated using data from four continents, which demonstrates that intraspecific competition between territorial animals can generate the large-scale hexagonal regularity of these patterns. However, this mechanism is not mutually exclusive with scale-dependent feedbacks. Using Namib Desert fairy circles as a case study, we present field data showing that these landscapes exhibit multi-scale patterning-previously undocumented in this system-that cannot be explained by either mechanism in isolation. These multi-scale patterns and other emergent properties, such as enhanced resistance to and recovery from drought, instead arise from dynamic interactions in our theoretical framework, which couples both mechanisms. The potentially global extent of animal-induced regularity in vegetation-which can modulate other patterning processes in functionally important ways-emphasizes the need to integrate multiple mechanisms of ecological self-organization.

Resource availability and heterogeneity shape the self-organisation of regular spatial patterning.

Explaining large-scale ordered patterns and their effects on ecosystem functioning is a fundamental and controversial challenge in ecology. Here, we coupled empirical and theoretical approaches to explore how competition and spatial heterogeneity govern the regularity of colony dispersion in fungus-farming termites. Individuals from different colonies fought fiercely, and inter-nest distances were greater when nests were large and resources scarce-as expected if competition is strong, large colonies require more resources and foraging area scales with resource availability. Building these principles into a model of inter-colony competition showed that highly ordered patterns emerged under high resource availability and low resource heterogeneity. Analysis of this dynamical model provided novel insights into the mechanisms that modulate pattern regularity and the emergent effects of these patterns on system-wide productivity. Our results show how environmental context shapes pattern formation by social-insect ecosystem engineers, which offers one explanation for the marked variability observed across ecosystems.

Spatial patterning of soil microbial communities created by fungus-farming termites.

Spatially overdispersed mounds of fungus-farming termites (Macrotermitinae) are hotspots of nutrient availability and primary productivity in tropical savannas, creating spatial heterogeneity in communities and ecosystem functions. These termites influence the local availability of nutrients in part by redistributing nutrients across the landscape, but the links between termite ecosystem engineering and the soil microbes that are the metabolic agents of nutrient cycling are little understood. We used DNA metabarcoding of soils from Odontotermes montanus mounds to examine the influence of termites on soil microbial communities in a semi-arid Kenyan savanna. We found that bacterial and fungal communities were compositionally distinct in termite-mound topsoils relative to the surrounding savanna, and that bacterial communities were more diverse on mounds. The higher microbial alpha and beta diversity associated with mounds created striking spatial patterning in microbial community composition, and boosted landscape-scale microbial richness and diversity. Selected enzyme assays revealed consistent differences in potential enzymatic activity, suggesting links between termite-induced heterogeneity in microbial community composition and the spatial distribution of ecosystem functions. We conducted a large-scale field experiment in which we attempted to simulate termites' effects on microbes by fertilizing mound-sized patches; this altered both bacterial and fungal communities, but in a different way than natural mounds. Elevated levels of inorganic nitrogen, phosphorus and potassium may help to explain the distinctive fungal communities in termite-mound soils, but cannot account for the distinctive bacterial communities associated with mounds.

On the origin of biological construction, with a focus on multicellularity.

Biology is marked by a hierarchical organization: all life consists of cells; in some cases, these cells assemble into groups, such as endosymbionts or multicellular organisms; in turn, multicellular organisms sometimes assemble into yet other groups, such as primate societies or ant colonies. The construction of new organizational layers results from hierarchical evolutionary transitions, in which biological units (e.g., cells) form groups that evolve into new units of biological organization (e.g., multicellular organisms). Despite considerable advances, there is no bottom-up, dynamical account of how, starting from the solitary ancestor, the first groups originate and subsequently evolve the organizing principles that qualify them as new units. Guided by six central questions, we propose an integrative bottom-up approach for studying the dynamics underlying hierarchical evolutionary transitions, which builds on and synthesizes existing knowledge. This approach highlights the crucial role of the ecology and development of the solitary ancestor in the emergence and subsequent evolution of groups, and it stresses the paramount importance of the life cycle: only by evaluating groups in the context of their life cycle can we unravel the evolutionary trajectory of hierarchical transitions. These insights also provide a starting point for understanding the types of subsequent organizational complexity. The central research questions outlined here naturally link existing research programs on biological construction (e.g., on cooperation, multilevel selection, self-organization, and development) and thereby help integrate knowledge stemming from diverse fields of biology.

Farming and public goods production in Caenorhabditis elegans populations.

The ecological and evolutionary dynamics of populations are shaped by the strategies they use to produce and use resources. However, our understanding of the interplay between the genetic, behavioral, and environmental factors driving these strategies is limited. Here, we report on a Caenorhabditis elegans-Escherichia coli (worm-bacteria) experimental system in which the worm-foraging behavior leads to a redistribution of the bacterial food source, resulting in a growth advantage for both organisms, similar to that achieved via farming. We show experimentally and theoretically that the increased resource growth represents a public good that can benefit all other consumers, regardless of whether or not they are producers. Mutant worms that cannot farm bacteria benefit from farming by other worms in direct proportion to the fraction of farmers in the worm population. The farming behavior can therefore be exploited if it is associated with either energetic or survival costs. However, when the individuals compete for resources with their own type, these costs can result in an increased population density. Altogether, our findings reveal a previously unrecognized mechanism of public good production resulting from the foraging behavior of C. elegans, which has important population-level consequences. This powerful system may provide broad insight into exploration-exploitation tradeoffs, the resultant ecoevolutionary dynamics, and the underlying genetic and neurobehavioral driving forces of multispecies interactions.

Demographic noise can reverse the direction of deterministic selection.

Deterministic evolutionary theory robustly predicts that populations displaying altruistic behaviors will be driven to extinction by mutant cheats that absorb common benefits but do not themselves contribute. Here we show that when demographic stochasticity is accounted for, selection can in fact act in the reverse direction to that predicted deterministically, instead favoring cooperative behaviors that appreciably increase the carrying capacity of the population. Populations that exist in larger numbers experience a selective advantage by being more stochastically robust to invasions than smaller populations, and this advantage can persist even in the presence of reproductive costs. We investigate this general effect in the specific context of public goods production and find conditions for stochastic selection reversal leading to the success of public good producers. This insight, developed here analytically, is missed by the deterministic analysis as well as by standard game theoretic models that enforce a fixed population size. The effect is found to be amplified by space; in this scenario we find that selection reversal occurs within biologically reasonable parameter regimes for microbial populations. Beyond the public good problem, we formulate a general mathematical framework for models that may exhibit stochastic selection reversal. In this context, we describe a stochastic analog to [Formula: see text] theory, by which small populations can evolve to higher densities in the absence of disturbance.

Fitness tradeoffs between spores and nonaggregating cells can explain the coexistence of diverse genotypes in cellular slime molds.

Cellular slime molds, including the well-studied Dictyostelium discoideum, are amoebae whose life cycle includes both a single-cellular and a multicellular stage. To achieve the multicellular stage, individual amoebae aggregate upon starvation to form a fruiting body made of dead stalk cells and reproductive spores, a process that has been described in terms of cooperation and altruism. When amoebae aggregate they do not perfectly discriminate against nonkin, leading to chimeric fruiting bodies. Within chimeras, complex interactions among genotypes have been documented, which should theoretically reduce genetic diversity. This is however inconsistent with the great diversity of genotypes found in nature. Recent work has shown that a little-studied component of D. discoideum fitness--the loner cells that do not participate in the aggregation--can be selected for depending on environmental conditions and that, together with the spores, they could represent a bet-hedging strategy. We suggest that in all cellular slime molds the existence of loners could resolve the apparent diversity paradox in two ways. First, if loners are accounted for, then apparent genotypic skew in the spores of chimeras could simply be the result of different investments into spores versus loners. Second, in an ecosystem with multiple local environments differing in their food recovery characteristics and connected globally via weak-to-moderate dispersal, coexistence of multiple genotypes can occur. Finally, we argue that the loners make it impossible to define altruistic behavior, winners or losers, without a clear description of the ecology.

Spatial Self-Organization of Ecosystems: Integrating Multiple Mechanisms of Regular-Pattern Formation.

Large-scale regular vegetation patterns are common in nature, but their causes are disputed. Whereas recent theory focuses on scale-dependent feedbacks as a potentially universal mechanism, earlier studies suggest that many regular spatial patterns result from territorial interference competition between colonies of social-insect ecosystem engineers, leading to hexagonally overdispersed nest sites and associated vegetation. Evidence for this latter mechanism is scattered throughout decades of disparate literature and lacks a unified conceptual framework, fueling skepticism about its generality in debates over the origins of patterned landscapes. We review these mechanisms and debates, finding evidence that spotted and gapped vegetation patterns generated by ants, termites, and other subterranean animals are globally widespread, locally important for ecosystem functioning, and consistent with models of intraspecific territoriality. Because these and other mechanisms of regular-pattern formation are not mutually exclusive and can coexist and interact at different scales, the prevailing theoretical outlook on spatial self-organization in ecology must expand to incorporate the dynamic interplay of multiple processes.

The ecology and evolution of social behavior in microbes.

Cooperation has been studied extensively across the tree of life, from eusociality in insects to social behavior in humans, but it is only recently that a social dimension has been recognized and extensively explored for microbes. Research into microbial cooperation has accelerated dramatically and microbes have become a favorite system because of their fast evolution, their convenience as lab study systems and the opportunity for molecular investigations. However, the study of microbes also poses significant challenges, such as a lack of knowledge and an inaccessibility of the ecological context (used here to include both the abiotic and the biotic environment) under which the trait deemed cooperative has evolved and is maintained. I review the experimental and theoretical evidence in support of the limitations of the study of social behavior in microbes in the absence of an ecological context. I discuss both the need and the opportunities for experimental investigations that can inform a theoretical framework able to reframe the general questions of social behavior in a clear ecological context and to account for eco-evolutionary feedback.

Seasonality can induce coexistence of multiple bet-hedging strategies in Dictyostelium discoideum via storage effect.

The social amoeba Dictyostelium discoideum has been recently suggested as an example of bet-hedging in microbes. In the presence of resources, amoebae reproduce as unicellular organisms. Resource depletion, however, leads to a starvation phase in which the population splits between aggregators, which form a fruiting body made of a stalk and resistant spores, and non-aggregators, which remain as vegetative cells. Spores are favored when starvation periods are long, but vegetative cells can exploit resources in environments where food replenishes quickly. The investment in aggregators versus non-aggregators can therefore be understood as a bet-hedging strategy that evolves in response to stochastic starvation times. A genotype (or strategy) is defined by the balance between each type of cells. In this framework, if the ecological conditions on a patch are defined in terms of the mean starvation time (i.e. time between the onset of starvation and the arrival of a new food pulse), a single genotype dominates each environment, which is inconsistent with the huge genetic diversity observed in nature. Here we investigate whether seasonality, represented by a periodic, wet-dry alternation in the mean starvation times, allows the coexistence of several strategies in a single patch. We study this question in a non-spatial (well-mixed) setting in which different strains compete for a common pool of resources over a sequence of growth-starvation cycles. We find that seasonality induces a temporal storage effect that can promote the stable coexistence of multiple genotypes. Two conditions need to be met in our model. First, there has to be a temporal niche partitioning (two well-differentiated habitats within the year), which requires not only different mean starvation times between seasons but also low variance within each season. Second, each season's well-adapted strain has to grow and create a large enough population that permits its survival during the subsequent unfavorable season, which requires the number of growth-starvation cycles within each season to be sufficiently large. These conditions allow the coexistence of two bet-hedging strategies. Additional tradeoffs among life-history traits can expand the range of coexistence and increase the number of coexisting strategies, contributing toward explaining the genetic diversity observed in D. discoideum. Although focused on this cellular slime mold, our results are general and may be easily extended to other microbes.