Group-size-dependent punishment of idle subordinates in a cooperative breeder where helpers pay to stay

In cooperative breeding systems, dominant breeders sometimes tolerate unrelated individuals even if they inflict costs on the dominants. According to the ‘pay-to-stay’ hypothesis, (i) subordinates can outweigh these costs by providing help and (ii) dominants should be able to enforce help by punishing subordinates that provide insufficient help. This requires that dominants can monitor helping and can recognize group members individually. In a field experiment, we tested whether cooperatively breeding cichlid Neolamprologus pulcher subordinates increase their help after a forced ‘idle’ period, how other group members respond to a previously idle helper, and how helper behaviour and group responses depend on group size. Previously, idle helpers increased their submissiveness and received more aggression than control helpers, suggesting that punishment occurred to enforce help. Subordinates in small groups increased their help more than those in large groups, despite receiving less aggression. When subordinates were temporarily removed, dominants in small groups were more likely to evict returning subordinates. Our results suggest that only in small groups do helpers face a latent threat of punishment by breeders as predicted by the pay-to-stay hypothesis. In large groups, cognitive constraints may prevent breeders from tracking the behaviour of a large number of helpers.     

Costly punishment prevails in intergroup conflict

Understanding how societies resolve conflicts between individual and common interests remains one of the most fundamental issues across disciplines. The observation that humans readily incur costs to sanction uncooperative individuals without tangible individual benefits has attracted considerable attention as a proximate cause as to why cooperative behaviours might evolve. However, the proliferation of individually costly punishment has been difficult to explain. Several studies over the last decade employing experimental designs with isolated groups have found clear evidence that the costs of punishment often nullify the benefits of increased cooperation, rendering the strong human tendency to punish a thorny evolutionary puzzle. Here, we show that group competition enhances the effectiveness of punishment so that when groups are in direct competition, individuals belonging to a group with punishment opportunity prevail over individuals in a group without this opportunity. In addition to competitive superiority in between-group competition, punishment reduces within-group variation in success, creating circumstances that are highly favourable for the evolution of accompanying group-functional behaviours. We find that the individual willingness to engage in costly punishment increases with tightening competitive pressure between groups. Our results suggest the importance of intergroup conflict behind the emergence of costly punishment and human cooperation.     

Why cooperation is not running away

A growing number of experimental and theoretical studies show the importance of partner choice as a mechanism to promote the evolution of cooperation, especially in humans. In this paper, we focus on the question of the precise quantitative level of cooperation that should evolve under this mechanism. When individuals compete to be chosen by others, their level of investment in cooperation evolves towards higher values, a process called competitive altruism, or runaway cooperation. Using a classic adaptive dynamics model, we first show that when the cost of changing partner is low, this runaway process can lead to a profitless escalation of cooperation. In the extreme, when partner choice is entirely frictionless, cooperation even increases up to a level where its cost entirely cancels out its benefit. That is, at evolutionary equilibrium, individuals gain the same payoff than if they had not cooperated at all. Second, importing models from matching theory in economics we, however, show that when individuals can plastically modulate their choosiness in function of their own cooperation level, partner choice stops being a runaway competition to outbid others and becomes a competition to form the most optimal partnerships. In this case, when the cost of changing partner tends towards zero, partner choice leads to the evolution of the socially optimum level of cooperation. This last result could explain the observation that human cooperation seems to be often constrained by considerations of social efficiency.     

Experimental evidence that partner choice is a driving force in the payoff distribution among cooperators or mutualists: the cleaner fish case

Supply and demand largely determine the price of goods on human markets. It has been proposed that in animals, similar forces influence the payoff distribution between trading partners in sexual selection, intraspecific cooperation and interspecific mutualism. Here we present the first experimental evidence supporting biological market theory in a study on cleaner fish, Labroides dimidiatus . Cleaners interact with two classes of clients: choosy client species with access to several cleaners usually do not queue for service and do not return if ignored, while resident client species with access to only one cleaning station do queue or return. We used plexiglas plates with equal amounts of food to simulate these behaviours of the two client classes. Cleaners soon inspected 'choosy' plates before 'resident' plates. This supports previous field observations that suggest that client species with access to several cleaners exert choice to receive better (immediate) service.     

Mutualism, market effects and partner control

Intraspecific cooperation and interspecific mutualism often feature a marked asymmetry in the scope for exploitation. Cooperation may nevertheless persist despite one-sided opportunities for cheating, provided that the partner vulnerable to exploitation has sufficient control over the duration of interaction. The effectiveness of the threat of terminating an encounter, however, depends upon the ease with which both the potential victim and the potential exploiter can find replacement partners. Here, we extend a simple, game-theoretical model of this form of partner control to incorporate variation in the relative abundance of potential victims and exploiters, which leads to variation in the time required for individuals of each type to find a new partner. We show that such market effects have a dramatic influence on the stable level of exploitation (and consequent duration of interaction). As the relative abundance of victims decreases, they become less tolerant to exploitation, terminating encounters earlier (for a given level of exploitation), whereas exploiters behave in a more cooperative manner. As a result, the stable duration of interaction actually increases, despite the decreasing tolerance of the victims. Below a critical level of relative victim abundance, the model suggests that the cost of finding a replacement partner becomes so great that it does not pay to exploit at all.     

Context dependence in the coevolution of plant and rhizobial mutualists

Several mechanisms are expected to rapidly rid mutualisms of genetic variation in partner quality. Variation for mutualist quality, however, appears to be widespread. We used a model legume-rhizobium mutualism to test for evidence that context-dependent selection may maintain variation in partner quality. In a greenhouse experiment using 10 natural populations of Medicago truncatula and two strains of Sinorhizobium medicae, we detected significant genotype x genotype (G x G) interactions for plant fitness, indicating that the most beneficial rhizobium strain depends on the host genotype. In a second experiment using a subset of the plant populations used in the first experiment, we detected significant G x G interactions for both plant and rhizobium fitness. Moreover, the plant population with which rhizobium strains gained the greatest benefit depended on the nitrogen environment. Finally, we found that in a high nitrogen environment, all plant populations had lower fitness when inoculated with a 1:1 mixture of strains than with the worse single strain alone, suggesting that nitrogen shifts the exchange of benefits in favour of rhizobia. Our data suggest that genotype, nitrogen and biotic dependency might contribute to the maintenance of genetic variation in mutualist quality when coupled with spatial or temporal heterogeneity in the environment.     

Partner switching can favour cooperation in a biological market

Intraspecific cooperation and interspecific mutualisms can be promoted by mechanisms that reduce the frequency with which cooperative organisms are exploited by unhelpful partners. One such mechanism consists of changing partners after interacting with an uncooperative individual. I used McNamara et al.'s (Nature, 451, 2008, 189) partner switching model as a framework to examine whether this mechanism can select for increased cooperative investment by house sparrows (Passer domesticus) collaborating to rear offspring; previous research on this species has shown that substantial cooperative investments by both pair members are required to achieve high pay‐offs from collaborating. I found that the poorer the outcome of a breeding attempt relative to the number of eggs the female invested, the greater the likelihood of partner switching. The incidence of partner switching changed seasonally, with peak switching coinciding with an increase in the number of alternative partners available to females. After females switched partners, their breeding outcomes rose to match those of females that remained with the same partner; this was not the case for males that switched partners. Consistent with the model's prediction, males in stable partnerships achieved over 25% higher than average reproductive success, which was attributable to both persistently good breeding outcomes and their older partners' high fecundity. These results provide empirical support for the hypothesis that partner switching favours increased cooperative investment levels, and they demonstrate that variation in the relative value of by‐product benefits can enhance that process.     

Biological trade and markets

Cooperation between organisms can often be understood, like trade between merchants, as a mutually beneficial exchange of services, resources or other ‘commodities’. Mutual benefits alone, however, are not sufficient to explain the evolution of trade-based cooperation. First, organisms may reject a particular trade if another partner offers a better deal. Second, while human trade often entails binding contracts, non-human trade requires unwritten ‘terms of contract’ that ‘self-stabilize’ trade and prevent cheating even if all traders strive to maximize fitness. Whenever trading partners can be chosen, market-like situations arise in nature that biologists studying cooperation need to account for. The mere possibility of exerting partner choice stabilizes many forms of otherwise cheatable trade, induces competition, facilitates the evolution of specialization and often leads to intricate forms of cooperation. We discuss selected examples to illustrate these general points and review basic conceptual approaches that are important in the theory of biological trade and markets. Comparing these approaches with theory in economics, it turns out that conventional models—often called ‘Walrasian’ markets—are of limited relevance to biology. In contrast, early approaches to trade and markets, as found in the works of Ricardo and Cournot, contain elements of thought that have inspired useful models in biology. For example, the concept of comparative advantage has biological applications in trade, signalling and ecological competition. We also see convergence between post-Walrasian economics and biological markets. For example, both economists and biologists are studying ‘principal–agent’ problems with principals offering jobs to agents without being sure that the agents will do a proper job. Finally, we show that mating markets have many peculiarities not shared with conventional economic markets. Ideas from economics are useful for biologists studying cooperation but need to be taken with caution.     

Phenotype and individual investment in cooperative foundress associations of the fire ant, Solenopsis invicta

Fire ant (Solenopsis invida) queens founding a colony with unrelatednest mates potentially face a trade-off. Increased individualinvestment enhances worker production, colony survival, andgrowth. However, increased investment may reduce a queen's probabilityof surviving fights that invariably arise after worker eclosion.Indeed, previous studies showed that queens lose less weight(a measure of investment) when initiating colonies with cofoundressesthan when alone, and that within associations the queen losingmore weight is more likely to die. In this study, we testedwhether queens adjust weight loss to social environment andfighting ability and whether restraining weight loss directlyincreases survival prospects. Experimental manipulation of coloniesshowed that reduced investment by queens within associationsis primarily a response to the presence of a nest mate and notsimply a response to per-queen brood-care demands. Differencesin head width were associated with relative and combined weightloss of cofoundresses, as well as with queen survival. In contrast,the investment strategies of queens were not significantly influencedby their nest mates' initial weight. Similarly, manipulationof the queens' relative weight by feeding and exposure to contrastingsocial environment (queens kept alone or in groups) did notsignificantly affect survivaL These results indicate that headwidth differences or correlated phenotypic atthbutes of fightingability influenced both investment strategies and survival probabilityof queens. That queens with larger heads invested less energyinto brood rearing and were more likely to survive reveals moreselfish interactions among cofoundresses than has previouslybeen assumed and casts some doubts about the idea that groupselection must be invoked to account for the maintenance ofcooperation in foundress associations of ants.     

Outsourcing punishment to God: beliefs in divine control reduce earthly punishment

The sanctioning of norm-transgressors is a necessary--though often costly--task for maintaining a well-functioning society. Prior to effective and reliable secular institutions for punishment, large-scale societies depended on individuals engaging in 'altruistic punishment'--bearing the costs of punishment individually, for the benefit of society. Evolutionary approaches to religion suggest that beliefs in powerful, moralizing Gods, who can distribute rewards and punishments, emerged as a way to augment earthly punishment in large societies that could not effectively monitor norm violations. In five studies, we investigate whether such beliefs in God can replace people's motivation to engage in altruistic punishment, and their support for state-sponsored punishment. Results show that, although religiosity generally predicts higher levels of punishment, the specific belief in powerful, intervening Gods reduces altruistic punishment and support for state-sponsored punishment. Moreover, these effects are specifically owing to differences in people's perceptions that humans are responsible for punishing wrongdoers.     

Mycorrhizal Fungi Respond to Resource Inequality by Moving Phosphorus from Rich to Poor Patches across Networks

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The Effects of Landmarks on Territorial Behavior in a Convict Cichlid,Amatitlania siquia

Defense of a territory is a primary factor determining the fitness of territorial individuals. Thus, territorial animals use a variety of means to lower the cost of territorial defense. Although landmarks are known to lower the defense costs of territories, little is known about how they could affect fundamental properties of territories, which could ultimately affect the demography, population regulation, individual behavior, and spatial ecology of a territorial species. This field study examined the effects of natural landmarks on territory size, shape, and defensive costs in Amatitlania siquia, a little‐studied member of the convict cichlid group native to Costa Rica and Nicaragua. We investigated the territorial behavior of 103 breeding pairs in a caldera lake in Nicaragua. During 10‐min focal observations, we recorded the locations at which residents chased intruders and then used these locations to outline the territory boundaries. Landmarks affected both size and shape of A. siquia territories. Territory size decreased as the percentage of the boundary at landmarks increased. Territories with <20% of their boundaries at landmarks were approximately circular in shape, while territories with 20–60% of their boundaries at landmarks were on average more elongated. These variations in territory size and shape significantly affected defense costs, with higher numbers of chases per square meter in small and elongated territories. These effects of landmarks on territory size and shape and defense costs are useful to understand the widely seen size and shape variations in naturally occurring territories.     

Density effects on life-history traits in a wild population of the great tit Parus major: analyses of long-term data with GIS techniques

1. Population density often has strong effects on the population dynamics and reproductive processes of territorial animals. However, most estimates of density-dependent effects use the number of breeding pairs per unit area in a given season and look for correlations across seasons, a technique that assigns the same density score to each breeding pair, irrespective of local spatial variation. 2. In this study, we employed GIS techniques to estimate individual breeding densities for great tits breeding in Wytham Woods UK, between 1965 and 1996. We then used linear mixed modelling to analyse the effect of density on reproductive processes. 3. The areas of Thiessen polygons formed around occupied nestboxes were used to approximate territory size (necessarily inverse of breeding density). There were significant, independent and positive relationships between clutch size, fledging mass and the number of offspring recruited to the population, and territory size (all P < 0.001), but no effect of territory size on lay-date or egg mass. 4. Thiessen polygons are contiguous and cover all of the available area. Therefore, at low nest densities territory polygons were excessively oversized. Using a novel procedure to address this limitation, territory sizes were systematically capped through a range of maxima, with the greatest effect in the models when territories were capped at 0.9-2.3 ha. This figure approximates to the maximum effective territory size in our population and is in close agreement with several field-based studies. This capping refinement also revealed a significant negative relationship between lay-date and territory size capped at 0.9 ha (P < 0.001). 5. These density-dependent effects were also detected when analyses were restricted to changes within individual females, suggesting that density effects do not merely result from either increased proportions of low-quality individuals, or increased occupation of poor sites, when population density is high. 6. Overall, these results suggest that, in the current population, great tits with territories smaller than c. 2 ha independently lay smaller and later clutches, have lighter fledglings, and recruit fewer offspring to the breeding population. These analyses thus suggest a pervasive and causal role of local population density in explaining individual reproductive processes.     

Fitness correlates with the extent of cheating in a bacterium

There is growing awareness of the importance of cooperative behaviours in microbial communities. Empirical support for this insight comes from experiments using mutant strains, termed ‘cheats’, which exploit the cooperative behaviour of wild‐type strains. However, little detailed work has gone into characterising the competitive dynamics of cooperative and cheating strains. We test three specific predictions about the fitness consequences of cheating to different extents by examining the production of the iron‐scavenging siderophore molecule, pyoverdin, in the bacterium Pseudomonas aeruginosa. We create a collection of mutants that differ in the amount of pyoverdin that they produce (from 1% to 96% of the production of paired wild types) and demonstrate that these production levels correlate with both gene activity and the ability to bind iron. Across these mutants, we found that (1) when grown in a mixed culture with a cooperative wild‐type strain, the relative fitness of a mutant is negatively correlated with the amount of pyoverdin that it produces; (2) the absolute and relative fitness of the wild‐type strain in the mixed culture is positively correlated with the amount of pyoverdin that the mutant produces; and (3) when grown in a monoculture, the absolute fitness of the mutant is positively correlated with the amount of pyoverdin that it produces. Overall, we demonstrate that cooperative pyoverdin production is exploitable and illustrate how variation in a social behaviour determines fitness differently, depending on the social environment.     

Partners coordinate territorial defense against simulated intruders in a duetting ovenbird

Duets in breeding pairs may reflect a situation of conflict, whereby an individual answers its partner's song as a form of unilateral acoustic mate guarding or, alternatively, it may reflect cooperation, when individuals share in territory defense or safeguard the partnership. The degree of coordination between the sexes when responding to solo versus paired intruders may elucidate the function of songs in duets. We examined this issue in a study with rufous horneros (Furnarius rufus), a duetting, socially monogamous Neotropical species with low levels of extrapair paternity. We exposed social pairs during the nonbreeding season to playbacks of duets, male solos, female solos, and control heterospecific songs. Partners approached all conspecific stimuli together and responded by singing quickly, at higher rates and by coordinating ~80% of their songs into duets. For both sexes, most response variables (seven of nine) did not vary across conspecific treatments. These results suggest that partners duet and coordinate behaviors to cooperatively defend common territories. However, females spent more time in territorial vigilance, and partners were highly coordinated (correlated responses) in response to duets and female solos in comparison with male solos. This indicates that female intrusions (paired or solo) might be more threatening than male intrusions in the nonbreeding season, especially for territorial females, and that females are less cooperative with their partners in territory defense against male intruders.     

More 'altruistic' punishment in larger societies

If individuals will cooperate with cooperators, and punish non-cooperators even at a cost to themselves, then this strong reciprocity could minimize the cheating that undermines cooperation. Based upon numerous economic experiments, some have proposed that human cooperation is explained by strong reciprocity and norm enforcement. Second-party punishment is when you punish someone who defected on you; third-party punishment is when you punish someone who defected on someone else. Third-party punishment is an effective way to enforce the norms of strong reciprocity and promote cooperation. Here we present new results that expand on a previous report from a large cross-cultural project. This project has already shown that there is considerable cross-cultural variation in punishment and cooperation. Here we test the hypothesis that population size (and complexity) predicts the level of third-party punishment. Our results show that people in larger, more complex societies engage in significantly more third-party punishment than people in small-scale societies.     

Reciprocity in group‐living animals: partner control versus partner choice

Reciprocity is probably the most debated of the evolutionary explanations for cooperation. Part of the confusion surrounding this debate stems from a failure to note that two different processes can result in reciprocity: partner control and partner choice. We suggest that the common observation that group‐living animals direct their cooperative behaviours preferentially to those individuals from which they receive most cooperation is to be interpreted as the result of the sum of the two separate processes of partner control and partner choice. We review evidence that partner choice is the prevalent process in primates and propose explanations for this pattern. We make predictions that highlight the need for studies that separate the effects of partner control and partner choice in a broader variety of group‐living taxa.     

Social dilemmas among supergenes: intragenomic sexual conflict and a selfing solution in Oenothera

Recombination is a powerful policing mechanism to control intragenomic cheats. The “parliament of the genes” can often rapidly block driving genes from cheating during meiosis. But what if the genome parliament is reduced to only two members, or supergenes? Using a series of simple game‐theoretic models inspired by the peculiar genetics of Oenothera sp., we illustrate that a two supergene genome (α and β) can produce a number of surprising evolutionary dynamics, including increases in lineage longevity following a transition from sexuality (outcrossing) to asexuality (clonal self‐fertilization). We end by interpreting the model in the broader context of the evolution of mutualism, which highlights that greater α, β cooperation in the self‐fertilizing model can be viewed as an example of partner fidelity driving multilineage cooperation.