The tragedy of the commons in evolutionary biology

Garrett Hardin's tragedy of the commons is an analogy that shows how individuals driven by self-interest can end up destroying the resource upon which they all depend. The proposed solutions for humans rely on highly advanced skills such as negotiation, which raises the question of how non-human organisms manage to resolve similar tragedies. In recent years, this question has promoted evolutionary biologists to apply the tragedy of the commons to a wide range of biological systems. Here, we provide tools to categorize different types of tragedy and review different mechanisms, including kinship, policing and diminishing returns that can resolve conflicts that could otherwise end in tragedy. A central open question, however, is how often biological systems are able to resolve these scenarios rather than drive themselves extinct through individual-level selection favouring self-interested behaviours.     

Multilevel selection analysis of a microbial social trait

The study of microbial communities often leads to arguments for the evolution of cooperation due to group benefits. However, multilevel selection models caution against the uncritical assumption that group benefits will lead to the evolution of cooperation. We analyze a microbial social trait to precisely define the conditions favoring cooperation. We combine the multilevel partition of the Price equation with a laboratory model system: swarming in Pseudomonas aeruginosa. We parameterize a population dynamics model using competition experiments where we manipulate expression, and therefore the cost‐to‐benefit ratio of swarming cooperation. Our analysis shows that multilevel selection can favor costly swarming cooperation because it causes population expansion. However, due to high costs and diminishing returns constitutive cooperation can only be favored by natural selection when relatedness is high. Regulated expression of cooperative genes is a more robust strategy because it provides the benefits of swarming expansion without the high cost or the diminishing returns. Our analysis supports the key prediction that strong group selection does not necessarily mean that microbial cooperation will always emerge.     

Density-dependent cooperation as a mechanism for persistence and coexistence

To overcome stress, such as resource limitation, an organism often needs to successfully mediate competition with other members of its own species. This may favor the evolution of defective traits that are harmful to the species population as a whole, and that may lead to its dilution or even to its extinction (the tragedy of the commons). Here, we show that this phenomenon can be circumvented by cooperation plasticity, in which an individual decides, based on environmental conditions, whether to cooperate or to defect. Specifically, we analyze the evolution of density-dependent cooperation. In our model, the population is spatially subdivided, periodically remixed, and comprises several species. We find that evolution pushes individuals to be more cooperative when their own species is at lower densities, and we show that not only could this cooperation prevent the tragedy of the commons, but it could also facilitate coexistence between many species that compete for the same resource.     

Demography and the tragedy of the commons

Individual success in group‐structured populations has two components. First, an individual gains by outcompeting its neighbours for local resources. Second, an individual's share of group success must be weighted by the total productivity of the group. The essence of sociality arises from the tension between selfish gains against neighbours and the associated loss that selfishness imposes by degrading the efficiency of the group. Without some force to modulate selfishness, the natural tendencies of self interest typically degrade group performance to the detriment of all. This is the tragedy of the commons. Kin selection provides the most widely discussed way in which the tragedy is overcome in biology. Kin selection arises from behavioural associations within groups caused either by genetical kinship or by other processes that correlate the behaviours of group members. Here, I emphasize demography as a second factor that may also modulate the tragedy of the commons and favour cooperative integration of groups. Each act of selfishness or cooperation in a group often influences group survival and fecundity over many subsequent generations. For example, a cooperative act early in the growth cycle of a colony may enhance the future size and survival of the colony. This time‐dependent benefit can greatly increase the degree of cooperation favoured by natural selection, providing another way in which to overcome the tragedy of the commons and enhance the integration of group behaviour. I conclude that analyses of sociality must account for both the behavioural associations of kin selection theory and the demographic consequences of life history theory.     

Competition over Personal Resources Favors Contribution to Shared Resources in Human Groups

Members of social groups face a trade-off between investing selfish effort for themselves and investing cooperative effort to produce a shared group resource. Many group resources are shared equitably: they may be intrinsically non-excludable public goods, such as vigilance against predators, or so large that there is little cost to sharing, such as cooperatively hunted big game. However, group members'' personal resources, such as food hunted individually, may be monopolizable. In such cases, an individual may benefit by investing effort in taking others'' personal resources, and in defending one''s own resources against others. We use a game theoretic “tug-of-war” model to predict that when such competition over personal resources is possible, players will contribute more towards a group resource, and also obtain higher payoffs from doing so. We test and find support for these predictions in two laboratory economic games with humans, comparing people''s investment decisions in games with and without the options to compete over personal resources or invest in a group resource. Our results help explain why people cooperatively contribute to group resources, suggest how a tragedy of the commons may be avoided, and highlight unifying features in the evolution of cooperation and competition in human and non-human societies.     

Open Access, Open Systems: Pastoral Management of Common-Pool Resources in the Chad Basin

The discussion about the impact of pastoralists on ecosystems has been profoundly shaped by Hardin’s tragedy of the commons that held pastoralists responsible for overgrazing the range. Research has shown that grazing ecosystems are much more complex and dynamic than was previously assumed and that they can be managed adaptively as commons. However, proponents and critics of Hardin’s thesis continue to argue that open access to common-pool resources inevitably leads to a tragedy of the commons. A longitudinal study that we conducted of pastoral mobility and primary production in the Logone floodplain in the Far North Region of Cameroon suggest that open access does not have to lead to a tragedy of the commons. We argue that this pastoral system is best conceptualized as an open system, in which a combination of individual decision-making and coordination of movements leads to an ideal-free type of distribution of mobile pastoralists. We explain how this self-organizing system of open access works and its implications for theories of management of common-pool resources and our understanding of pastoral systems.     

Resolving the tragedy of the commons: the feedback between intraspecific conflict and population density

Competition and conflict among individuals can favour exploitative strategies that undermine the common good. Theory suggests that this can lead to a tragedy of the commons and ultimately population extinction, a phenomenon known as evolutionary suicide. Here, I present a model of the evolutionary tragedy of the commons that explicitly considers the population dynamics where individuals invest in individually costly competitive traits. In the simplest form, this supports the notion that selection for high levels of conflict can cause evolutionary suicide. However, as competition comes with survival and fecundity costs, a feedback between the investment in competition and population density can act to reduce the level of conflict and prevent the population from going extinct. This suggests that the interaction between population ecology and the evolution of competition and conflict among individuals may be an important mechanism in resolving the level of competition and conflict among individuals.     

How do we decide when (not) to free-ride? Risk tolerance predicts behavioral plasticity in cooperation

In collaborations, group productivity typically increases with more cooperators, but is also often subject to diminishing returns. This pattern provides a different view about cooperation from traditional social dilemmas: defection is not necessarily the dominant strategy. Rather, a frequency-dependent “anti-conformist” strategy (cooperate if many others defect, and vice versa) is often individually rational. This study addresses human cooperation under such marginally diminishing group productivity, focusing on the plasticity of cooperative choices. We conducted a two-part “team foraging” experiment, in which the most- or least-cooperative members in the first part were re-grouped separately for the second part. We observed that cooperating and defecting “types” emerged within a group over time but did not completely persist across groups, with some of the most cooperative members switching to become the least cooperative (and vice versa). Risk attitude was a key factor in this switching behavior: greater risk-takers showed greater behavioral plasticity. These results imply that human cooperation may be more context-dependent and behaviorally plastic than previously thought.     

Shame and honour drive cooperation

Can the threat of being shamed or the prospect of being honoured lead to greater cooperation? We test this hypothesis with anonymous six-player public goods experiments, an experimental paradigm used to investigate problems related to overusing common resources. We instructed the players that the two individuals who were least generous after 10 rounds would be exposed to the group. As the natural antithesis, we also test the effects of honour by revealing the identities of the two players who were most generous. The non-monetary, reputational effects induced by shame and honour each led to approximately 50 per cent higher donations to the public good when compared with the control, demonstrating that both shame and honour can drive cooperation and can help alleviate the tragedy of the commons.     

Sexual conflict and the tragedy of the commons

It is widely understood that the costs and benefits of mating can affect the fecundity and survival of individuals. Sexual conflict may have profound consequences for populations as a result of the negative effects it causes males and females to have on one another's fitness. Here we present a model describing the evolution of sexual conflict, in which males inflict a direct cost on female fitness. We show that these costs can drive the entire population to extinction. To males, females are an essential but finite resource over which they have to compete. Population extinction owing to sexual conflict can therefore be seen as an evolutionary tragedy of the commons. Our model shows that a positive feedback between harassment and the operational sex ratio is responsible for the demise of females and, thus, for population extinction. We further show that the evolution of female resistance to counter harassment can prevent a tragedy of the commons. Our findings not only demonstrate that sexual conflict can drive a population to extinction but also highlight how simple mechanisms, such as harassment costs to males and females and the coevolution between harassment and resistance, can help avert a tragedy of the commons caused by sexual conflict.     

Preventing the Tragedy of the Commons Through Punishment of Over-Consumers and Encouragement of Under-Consumers

The conditions that can lead to the exploitative depletion of a shared resource, i.e., the tragedy of the commons, can be reformulated as a game of prisoner’s dilemma: while preserving the common resource is in the best interest of the group, over-consumption is in the interest of each particular individual at any given point in time. One way to try and prevent the tragedy of the commons is through infliction of punishment for over-consumption and/or encouraging under-consumption, thus selecting against over-consumers. Here, the effectiveness of various punishment functions in an evolving consumer-resource system is evaluated within a framework of a parametrically heterogeneous system of ordinary differential equations (ODEs). Conditions leading to the possibility of sustainable coexistence with the common resource for a subset of cases are identified analytically using adaptive dynamics; the effects of punishment on heterogeneous populations with different initial composition are evaluated using the reduction theorem for replicator equations. Obtained results suggest that one cannot prevent the tragedy of the commons through rewarding of under-consumers alone—there must also be an implementation of some degree of punishment that increases in a nonlinear fashion with respect to over-consumption and which may vary depending on the initial distribution of clones in the population.     

Balancing contest competition,scramble competition,and social tolerance at feeding sites in wild common marmosets (Callithrix jacchus)

Models of primate sociality focus on the costs and benefits of group living and how factors such as rank, feeding competition, alliance formation, and cooperative behavior shape within‐group social relationships. We conducted a series of controlled field experiments designed to investigate how resource distribution (one or three of four reward platforms) and amount of food on a reward platform affected foraging strategies and individual feeding success in four groups of wild common marmosets (Callithrix jacchus) living in the Caatinga of northeastern Brazil. At our field site, common marmoset groups are characterized by a single breeding female who can produce twin litters twice per year, strong social cohesion, and cooperative infant care provided principally by several adult male helpers. We found that except for the dominant breeding female, rank (based on aggression) was not a strong predictor of feeding success. Although the breeding female in each group occupied the highest rank position and obtained the greatest daily feeding success, all other group members, including adults and juveniles experienced relatively equal feeding success across most experimental conditions. This was accomplished using a balance of behavioral strategies related to contest competition, scramble competition (associated with a finder's advantage), and social tolerance (sharing the same feeding platform). Based on these results, the social structure of common marmosets is best described as “single female dominance,” with the breeding female maximizing food intake needed to offset the energetic costs associated with reproductive twinning and the ability to produce two litters per year. Cooperative infant caregiving, in which the number of helpers is positively correlated with offspring survivorship, requires a set of behavioral strategies that serve to reduce contest competition and promote prosocial behaviors at feeding sites.     

Intra-plant versus Inter-plant Root Competition in Beans: avoidance,resource matching or tragedy of the commons

Root competition inhibits root proliferation. All else equal, a plant should invest roots in a nutrient patch devoid of roots rather than one already occupied by roots. Less clear is how a plant should respond to intra-plant versus inter-plant root competition. We consider three responses for how a plant may select habitats based on intra-versus inter-plant root competition: inter-plant avoidance, resource matching, or intra-plant avoidance. The first assumes that plants prefer to have their own space and preferentially proliferate roots away from neighboring plants. The second response, based on the ideal free distribution, assumes that plants invest so as to equalize average returns from roots, regardless of the identity of the neighboring roots. The third, based on game theory, assumes that the plant proliferates roots so as to maximize whole-plant fitness, in which case it is better to proliferate plants among a neighbor's roots than to continue proliferating amongst one's own roots. To test among these models we grew beans (Phaseolus varigaris, var. Kenya) in a greenhouse under two planting scenarios. Both scenario were tested under 0.5 and 0.1 strength of nutrient solution. Under scenario A (fence-sitters), two split-root plants each shared two patches by virtue of having roots in each. Under scenario B (owners) two plants each had their own patch. The results supported the game theory model of intra-plant avoidance (whole plant habitat selection). Fence-sitters produced 150% more root mass per individual than owners. Owners produced 90% more yield (dry mass of pods) than fence-sitters. Furthermore, owners had significantly higher shoot-root ratios than fence-sitters. These effects did not vary with high or low nutrient levels. The over-proliferation of roots under inter-plant competition (fence-sitters) was manifest by the tenth day after planting. In short, the fence-sitters engaged in a tragedy of the commons in which they competed with each other through root proliferation. At the ESS, the fitness maximizing strategy of the individual is to sacrifice collective yield in a quest to `steal' nutrients from its neighbor. The research has three implications. First, plants may be able to assess and respond to local opportunities in a manner that maximizes the good of the whole plant. Second, nutrient foraging as a game may provide a fresh perceptive for viewing root competition either intra-specifically or inter-specifically. Third, it may be possible to increase the yield of certain crop species by breeding more `docile' cultivars that do not overproduce roots in response to inter-plant competition.     

Demography,life history and the evolution of age‐dependent social behaviour

Since the inception of modern social evolution theory, a vast majority of studies have sought to explain cooperation using relatedness‐driven hypotheses. Natural populations, however, show a substantial amount of variation in social behaviour that is uncorrelated with relatedness. Age offers a major alternative explanation for variation in behaviour that remains unaccounted for. Most natural populations are structured into age‐classes, with ageing being a nearly universal feature of most major taxa, including eukaryotic and prokaryotic organisms. Despite this, the theoretical underpinnings of age‐dependent social behaviour remain limited. Here, I investigate how group age‐composition, demography and life history shape trajectories of age‐dependent behaviours that are expressed conditionally on an actor and recipient's age. I show that demography introduces novel age‐dependent selective pressures acting on social phenotypes. Furthermore, I find that life history traits influence the costs and benefits of cooperation directly, but also indirectly. Life history has a strong impact not only on the genetic structure of the population but also on the distribution of group age‐compositions, with both of these processes influencing the expression of age‐dependent cooperation. Age of peak reproductive performance, in particular, is of chief importance for the evolution of cooperation, as this will largely determine the age and relatedness of social partners. Moreover, my results suggest that later‐life reproductive senescence may occur because of demographic effects alone, which opens new vistas on the evolution of menopause and related phenomena.     

Size inequality and the tragedy of the commons phenomenon in plant competition

Game theory predicts that the evolutionarily stable level of root production is greater for plants grown with neighbours compared to plants grown alone, even when the available resources per plant are constant. This follows from the fact that for plants grown alone, new roots compete only with other roots on the same plant, whereas for multiple plants grown in a group, new roots can also compete with the roots of other plants, thereby potentially acquiring otherwise unavailable resources at their neighbours’ expense. This phenomenon, which results in plants grown with neighbours over-proliferating roots at the expense of above-ground biomass, has been described as a ‘tragedy of the commons’, and requires that plants can distinguish self from non-self tissues. While this game theoretical model predicts the evolutionarily stable strategies of individual plants, it has only been tested on average allocation patterns of groups of plants. This is problematic, because average patterns can appear to reflect a tragedy of the commons, even when none has occurred. In particular, assuming (1) a decelerating relationship between individual plant biomass and the amount of resources available, and (2) greater size inequality in plants grown with neighbours compared to plants grown alone (due to asymmetric competition), then plants grown with neighbours should, at least on average, be smaller than plants grown alone. This is a manifestation of ‘Jensen’s Inequality’, which states that for decelerating functions, the average value of the function is less than the function of the average value. We suggest that Jensen’s Inequality should serve as an appropriate null hypothesis for examining biologically-based explanations of changes in biomass allocation strategies.     

Tragedy of the commons among antibiotic resistance plasmids

As social interactions are increasingly recognized as important determinants of microbial fitness, sociobiology is being enlisted to better understand the evolution of clinically relevant microbes and, potentially, to influence their evolution to aid human health. Of special interest are situations in which there exists a "tragedy of the commons," where natural selection leads to a net reduction in fitness for all members of a population. Here, I demonstrate the existence of a tragedy of the commons among antibiotic resistance plasmids of bacteria. In serial transfer culture, plasmids evolved a greater ability to superinfect already-infected bacteria, increasing plasmid fitness when evolved genotypes were rare. Evolved plasmids, however, fell victim to their own success, reducing the density of their bacterial hosts when they became common and suffering reduced fitness through vertical transmission. Social interactions can thus be an important determinant of evolution for the molecular endosymbionts of bacteria. These results also identify an avenue of evolution that reduces proliferation of both antibiotic resistance genes and their bacterial hosts.     

When is bigger better? The effects of group size on the evolution of helping behaviours

Understanding the evolution of sociality in humans and other species requires understanding how selection on social behaviour varies with group size. However, the effects of group size are frequently obscured in the theoretical literature, which often makes assumptions that are at odds with empirical findings. In particular, mechanisms are suggested as supporting large‐scale cooperation when they would in fact rapidly become ineffective with increasing group size. Here we review the literature on the evolution of helping behaviours (cooperation and altruism), and frame it using a simple synthetic model that allows us to delineate how the three main components of the selection pressure on helping must vary with increasing group size. The first component is the marginal benefit of helping to group members, which determines both direct fitness benefits to the actor and indirect fitness benefits to recipients. While this is often assumed to be independent of group size, marginal benefits are in practice likely to be maximal at intermediate group sizes for many types of collective action problems, and will eventually become very small in large groups due to the law of decreasing marginal returns. The second component is the response of social partners on the past play of an actor, which underlies conditional behaviour under repeated social interactions. We argue that under realistic conditions on the transmission of information in a population, this response on past play decreases rapidly with increasing group size so that reciprocity alone (whether direct, indirect, or generalised) cannot sustain cooperation in very large groups. The final component is the relatedness between actor and recipient, which, according to the rules of inheritance, again decreases rapidly with increasing group size. These results explain why helping behaviours in very large social groups are limited to cases where the number of reproducing individuals is small, as in social insects, or where there are social institutions that can promote (possibly through sanctioning) large‐scale cooperation, as in human societies. Finally, we discuss how individually devised institutions can foster the transition from small‐scale to large‐scale cooperative groups in human evolution.     

Optimal growth strategies of larval helminths in their intermediate hosts

We consider optimal growth of larval stages in complex parasite life cycles where there is no constraint because of host immune responses. Our model predicts an individual's asymptotic size in its intermediate host, with and without competition from conspecific larvae. We match observed variations in larval growth patterns in pseudophyllid cestodes with theoretical predictions of our model. If survival of the host is vital for transmission, larvae should reduce asymptotic size as intensity increases, to avoid killing the host. The life history strategy (LHS) model predicts a size reduction <1/intensity, thus increasing the parasite burden on the host. We discuss whether body size of competing parasites is an evolved LHS or simply reflects resource constraints (RC) on growth fixed by the host, leading to a constant total burden with intensity. Growth under competition appears comparable with "the tragedy of the commons", much analysed in social sciences. Our LHS prediction suggests that evolution generates a solution that seems cooperative but is actually selfish.     

Consequences of fluctuating group size for the evolution of cooperation

Studies of cooperation have traditionally focused on discrete games such as the well-known prisoner’s dilemma, in which players choose between two pure strategies: cooperation and defection. Increasingly, however, cooperation is being studied in continuous games that feature a continuum of strategies determining the level of cooperative investment. For the continuous snowdrift game, it has been shown that a gradually evolving monomorphic population may undergo evolutionary branching, resulting in the emergence of a defector strategy that coexists with a cooperator strategy. This phenomenon has been dubbed the ‘tragedy of the commune’. Here we study the effects of fluctuating group size on the tragedy of the commune and derive analytical conditions for evolutionary branching. Our results show that the effects of fluctuating group size on evolutionary dynamics critically depend on the structure of payoff functions. For games with additively separable benefits and costs, fluctuations in group size make evolutionary branching less likely, and sufficiently large fluctuations in group size can always turn an evolutionary branching point into a locally evolutionarily stable strategy. For games with multiplicatively separable benefits and costs, fluctuations in group size can either prevent or induce the tragedy of the commune. For games with general interactions between benefits and costs, we derive a general classification scheme based on second derivatives of the payoff function, to elucidate when fluctuations in group size help or hinder cooperation.     

Cuckoldry and the stability of biparental care

In socially monogamous species, females may engage in extra-pair fertilizations to gain direct or indirect benefits not provided by the social mate, with the potential risk of a reduction in the social mate’s paternal effort. I present an ESS model of cuckoldry frequencies, which considers both facultative and nonfacultative male responses to losses in paternity. Two possible equilibria exist: stable social monogamy with varying degrees of extra-pair paternity, and polygamy with little or no male care. Monogamy with limited cuckoldry can be stable only if the initial cuckoldry frequency is low, intrinsic cuckoldry benefits are not high, males can reasonably accurately detect cuckoldry, and female compensation for losses in male care is incomplete. Deviations from these assumptions lead to stronger mate acquisition in males at the expense of paternal care, and eventually to runaway evolution towards polygamy. Average female fitness is reduced in the runaway, although it is initiated by females maximizing the survival of offspring – a potential “tragedy of the commons” in breeding systems.