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. Disciplines Behavior and Ethology | Biology | Population Biology CommentsAt the time of publication, author Erol Akçay was affiliated with the University of Tennessee. Currently, he is a faculty member at the Department of Biology at the University of Pennsylvania. Online enhancement: appendix.abstract: 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 respons...
Cheating is a focal concept in the study of mutualism, with the majority of researchers considering cheating to be both prevalent and highly damaging. However, current definitions of cheating do not reliably capture the evolutionary threat that has been a central motivation for the study of cheating. We describe the development of the cheating concept and distill a relative-fitness-based definition of cheating that encapsulates the evolutionary threat posed by cheating, i.e. that cheaters will spread and erode the benefits of mutualism. We then describe experiments required to conclude that cheating is occurring and to quantify fitness conflict more generally. Next, we discuss how our definition and methods can generate comparability and integration of theory and experiments, which are currently divided by their respective prioritisations of fitness consequences and traits. To evaluate the current empirical evidence for cheating, we review the literature on several of the best-studied mutualisms. We find that although there are numerous observations of low-quality partners, there is currently very little support from fitness data that any of these meet our criteria to be considered cheaters. Finally, we highlight future directions for research on conflict in mutualisms, including novel research avenues opened by a relative-fitness-based definition of cheating.
Strategic interactions arise in all domains of life. This form of competition often plays out in dynamically changing environments. The strategies employed in a population may alter the state of the environment, which may in turn feedback to change the incentive structure of strategic interactions. Feedbacks between strategies and the environment are common in social-ecological systems, evolutionary-ecological systems, and even psychological-economic systems. Here we develop a framework of 'eco-evolutionary game theory' that enables the study of strategic and environmental dynamics with feedbacks. We consider environments governed either by intrinsic growth, decay, or tipping points. We show how the joint dynamics of strategies and the environment depend on the incentives for individuals to lead or follow behavioral changes, and on the relative speed of environmental versus strategic change. Our analysis unites dynamical phenomena that occur in settings as diverse as human decision-making, plant nutrient acquisition, and resource harvesting. We discuss implications in fields ranging from ecology to economics.
Although much previous work describes evolutionary mechanisms that promote or stabilize different social behaviors, we still have little understanding of the factors that drive animal behavior proximately. Here we present a modeling approach to answer this question. Our model rests on motivations to achieve objectives as the proximate determinants of behavior. We develop a two-tiered framework by first modeling the dynamics of a social interaction at the behavioral time scale and then find the evolutionarily stable objectives that result from the outcomes these dynamics produce. We use this framework to ask whether "other-regarding" motivations, which result from a kind of nonselfish objective, can evolve when individuals are engaged in a social interaction that entails a conflict between their material payoffs. We find that, at the evolutionarily stable state, individuals can be other-regarding in that they are motivated to increase their partners' payoff as well as their own. In contrast to previous theories, we find that such motivations can evolve because of their direct effect on fitness and do not require kin selection or a special group structure. We also derive general conditions for the evolutionary stability of other-regarding motivations. Our conditions indicate that other-regarding motivations are more likely to evolve when social interactions and behavioral objectives are both synergistic.A nimal behavior is determined both by proximate mechanisms that dictate an animal's actions in real time and by evolutionary forces that shape these proximate mechanisms. Even though the evolutionary dynamics of social behavior have been extensively studied (1-4), proximate mechanisms of behavior and how they interface with evolutionary forces remain poorly understood (4). In recent years, some models have integrated a proximate mechanism with an evolutionary analysis (5, 6). Furthermore, an explicitly two-tiered approach with potentially cooperative behavioral dynamics embedded in an evolutionary dynamic has been proposed (7) as necessary to understand the evolution of social behavior. We contribute to this literature by developing a unified framework for modeling the evolution of a specific type of behavioral interaction based on a well-defined proximate mechanism.Our proximate mechanism is based on the notion that animals are motivated to achieve certain objectives. Goal-seeking behavior has been a recurring theme in animal behavior and has been an integral part of earlier ethological thinking (e.g. 8, 9). However, this idea lost its prominence after the emergence of modern behavioral ecology, which focuses mainly on the fitness consequences of behavior (see, for example, page 6 of ref. 10). In addition, proximate models of behavior based on goal-seeking have focused mostly on nonsocial behaviors such as foraging (9) and have rarely considered social interactions. Here, we study goal-seeking behavior in the context of a social interaction by developing a model of a pair of interacting animals whose motivations ...
The social network structure of animal populations has major implications for survival, reproductive success, sexual selection and pathogen transmission of individuals. 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 a simple and generally applicable model of social network structure. We consider the emergence of network structure as a result of social inheritance, in which newborns are likely to bond with maternal contacts, and via forming bonds randomly. We compare model output with data from several species, showing that it can generate networks with properties such as those observed in real social systems. Our model demonstrates that important observed properties of social networks, including heritability of network position or assortative associations, can be understood as consequences of social inheritance.
Theories about sexual selection can be traced back to Darwin in 1871. He proposed that males fertilize as many females as possible with inexpensive sperm, whereas females, with a limited supply of large eggs, select the genetically highest quality males to endow their offspring with superior capabilities. Since its proposal, problems with this narrative have continued to accumulate, and it is our view that sexual selection theory needs to be replaced. We suggest an approach that relies on the exchange of direct ecological benefits among cooperating animals without reference to genetic benefits. This approach can be expressed mathematically in a branch of game theory that pertains to bargaining and side payments.
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. Disciplines Biology | Developmental Biology | Evolution CommentsAt the time of publication, author Erol Akçay was affiliated with the University of Tennessee. Currently, he is a faculty member at the Department of Biology at the University of Pennsylvania. Online enhancements: appendix, Mathematica file.abstract: 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...
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