Pathways to social evolution: reciprocity, relatedness, and synergy

Many organisms live in populations structured by space and by class, exhibit plastic responses to their social partners, and are subject to non-additive ecological and fitness effects. Social evolution theory has long recognized that all of these factors can lead to different selection pressures but has only recently attempted to synthesize how these factors interact. Using models for both discrete and continuous phenotypes, we show that analyzing these factors in a consistent framework reveals that they interact with one another in ways previously overlooked. Specifically, behavioral responses (reciprocity), genetic relatedness, and synergy interact in non-trivial ways that cannot be easily captured by simple summary indices of assortment. We demonstrate the importance of these interactions by showing how they have been neglected in previous synthetic models of social behavior both within and between species. These interactions also affect the level of behavioral responses that can evolve in the long run; proximate biological mechanisms are evolutionarily stable when they generate enough responsiveness relative to the level of responsiveness that exactly balances the ecological costs and benefits. Given the richness of social behavior across taxa, these interactions should be a boon for empirical research as they are likely crucial for describing the complex relationship linking ecology, demography, and social behavior.Comment: 4 figure

New Approaches to the Evolution of Social Behavior

One of the most fascinating topics in evolutionary biology is how and why organisms cooperate with each other. Natural selection works through competition between alleles for representation in the next generation. Yet one sees everywhere organisms actually helping each other, from mutualisms between ants and plants to the altruistic acts of firefighters storming into burning buildings to rescue people. But how can natural selection lead to cooperation? This, of course, is not a new question, and a tremendous amount of work in evolutionary theory in the last 40 years has shown that helping others can frequently be the winning strategy in the struggle for existence. We have a sophisticated theory of social evolution, dealing not only with helping behaviors, but also other behaviors such as policing, spiteful harm-doing, and so on

Social Inheritance Can Explain the Structure of Animal Social Networks

The social network structure of animal populations has major implications to survival, reproductive success, sexual selection, and pathogen transmission. Recent studies showed in various species that the structure of social networks and individuals’ positions in it are influenced by individual traits such as sex, age, and social rank, and can be heritable between generations. But as of yet, no general theory of social network structure exists that can explain the diversity of social networks observed in nature, and serve as a null model for detecting species and population-specific factors. Here we propose such a general model of social network structure. We consider the emergence of network structure as a result of two types of social bond formation: via social inheritance, in which newborns are likely to bond with maternal contacts, and via forming bonds randomly. We compare model output to data from several species, showing that it can generate networks with properties such as those observed in real social systems. Our model demonstrates that some of the observed properties of social networks, such as heritability of network position or assortative associations, can be understood as a consequence of social inheritance. Our results highlight the need to consider the dynamic processes that generate social structure in order to explain patterns of variation in social networks

The Evolution of Payoff Matrices: Providing Incentives to Cooperate

Most of the work in evolutionary game theory starts with a model of a social situation that gives rise to a particular payoff matrix and analyses how behaviour evolves through natural selection. Here, we invert this approach and ask, given a model of how individuals behave, how the payoff matrix will evolve through natural selection. In particular, we ask whether a prisoner’s dilemma game is stable against invasions by mutant genotypes that alter the payoffs. To answer this question, we develop a two-tiered framework with goal-oriented dynamics at the behavioural time scale and a diploid population genetic model at the evolutionary time scale. Our results are two-fold: first, we show that the prisoner’s dilemma is subject to invasions by mutants that provide incentives for cooperation to their partners, and that the resulting game is a coordination game similar to the hawk – dove game. Second, we find that for a large class of mutants and symmetric games, a stable genetic polymorphism will exist in the locus determining the payoff matrix, resulting in a complex pattern of behavioural diversity in the population. Our results highlight the importance of considering the evolution of payoff matrices to understand the evolution of animal social systems

Extra-Pair Parentage: A New Theory Based on Transactions in a Cooperative Game

Question: What is the adaptive significance of extra-pair parentage? Theoretical approach:We view parentage as a ‘transaction currency’ for exchanges of ecological benefits. We develop a multi-player cooperative game, using the core and the Nash bargaining solution as solution concepts. Model assumptions: Birds can negotiate about who pairs with whom. Parentage can be exchanged between individuals as a result of negotiations. Number of offspring fledged from a nest depends on the experience and situation of the social parents and not on their genes (i.e. only direct benefits, no genetic benefits). Predictions: We predict extra-pair parentage to occur when individuals with higher breeding capability are paired to individuals with lower breeding capability. Social interactions between males are predicted to precede the occurrence of extra-pair paternity. We give an example experiment to test our model

Extra-Pair Paternity in Birds: Review of the Genetic Benefits

Question: How well are genetic benefits hypotheses for extra-pair paternity supported by empirical evidence? Data incorporated: Almost all published studies testing for genetic benefits from 1980 onwards (121 papers, 55 species). Analysis methods: Collected key features and findings of each study in a database. Determined overall level of support for both good genes and compatible genes hypotheses. Conducted a formal meta-analysis on a subset of studies asking the following questions: (1) Do extra-pair mates of females have different phenotypes than their within-pair mates? (2) Do extra-pair offspring differ in viability from within-pair offspring? (3) Is there a correlation between the genetic similarity of a social pair and the incidence of extra-pair paternity? Results: Both the good genes and compatible genes hypotheses failed to be supported in more than half of the species studied. The meta-analysis shows that extra-pair males are on average larger and older than within-pair males, but not different in terms of secondary sexual traits, condition or relatedness to the female. No difference was found between extra-pair and within-pair young in survival to the next breeding season. We found no significant correlation between pair genetic similarity and extra-pair paternity. Conclusions: Genetic benefits are not strongly supported by available empirical data. New hypotheses are needed

Negotiation, Sanctions, and Context Dependency in the Legume-Rhizobium Mutualism

Two important questions about mutualisms are how the fitness costs and benefits to the mutualist partners are determined and how these mechanisms affect the evolutionary dynamics of the mutualism. We tackle these questions with a model of the legumerhizobium symbiosis that regards the mutualism outcome as a result of biochemical negotiations between the plant and its nodules. We explore the fitness consequences of this mechanism to the plant and rhizobia and obtain four main results. First, negotiations permit the plant to differentially reward more-cooperative rhizobia—a phenomenon termed “plant sanctions”—but only when more-cooperative rhizobia also provide the plant with good outside options during negotiations with other nodules. Second, negotiations may result in seemingly paradoxical cases where the plant is worse off when it has a “choice” between two strains of rhizobia than when infected by either strain alone. Third, even when sanctions are effective, they are by themselves not sufficient to maintain cooperative rhizobia in a population: less cooperative strains always have an advantage at the population level. Finally, partner fidelity feedback, together with genetic correlations between a rhizobium strain’s cooperativeness and the outside options it provides, can maintain cooperative rhizobia. Our results show how joint control over the outcome of a mutualism through the proximate mechanism of negotiation can affect the evolutionary dynamics of interspecific cooperation

Behavioral Responses in Structured Populations Pave the Way to Group Optimality

An unresolved controversy regarding social behaviors is exemplified when natural selection might lead to behaviors that maximize fitness at the social-group level but are costly at the individual level. Except for the special case of groups of clones, we do not have a general understanding of how and when group-optimal behaviors evolve, especially when the behaviors in question are flexible. To address this question, we develop a general model that integrates behavioral plasticity in social interactions with the action of natural selection in structured populations. We find that group-optimal behaviors can evolve, even without clonal groups, if individuals exhibit appropriate behavioral responses to each other’s actions. The evolution of such behavioral responses, in turn, is predicated on the nature of the proximate behavioral mechanisms. We model a particular class of proximate mechanisms, prosocial preferences, and find that such preferences evolve to sustain maximum group benefit under certain levels of relatedness and certain ecological conditions. Thus, our model demonstrates the fundamental interplay between behavioral responses and relatedness in determining the course of social evolution. We also highlight the crucial role of proximate mechanisms such as prosocial preferences in the evolution of behavioral responses and in facilitating evolutionary transitions in individuality

Group Size and Social Conflict in Complex Societies

Conflicts of interest over resources or reproduction among individuals in a social group have long been considered to result in automatic and universal costs to group living. However, exploring how social conflict varies with group size has produced mixed empirical results. Here we develop a model that generates alternative predictions for how social conflict should vary with group size depending on the type of benefits gained from being in a social group. We show that a positive relationship between social conflict and group size is favored when groups form primarily for the benefits of sociality but not when groups form mainly for accessing group-defended resources. Thus, increased social conflict in animal societies should not be viewed as an automatic cost of larger social groups. Instead, studying the relationship between social conflict and the types of grouping benefits will be crucial for understanding the evolution of complex societies