A theory for the evolution of other-regard integrating proximate and ultimate perspectives

Abstract

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 ...

Behavioral Responses in Structured Populations Pave the Way to Group Optimality

“…Virtually all organisms exhibit social behaviors that are flexible or conditional on the behaviors of others, from bacteria (e.g., quorum sensing; Miller and Bassler 2001) to insects (e.g., reproductive strategies depending on social context; WestEberhard 1987), birds (e.g., responses of parents to each other; Wright and Cuthill 1989), primates (e.g., reciprocal altruism; Brosnan and de Waal 2002), and obviously, humans. Not surprisingly, a large theoretical literature focuses on the evolutionary consequences of particular kinds of flexible (or conditional) behavior (e.g., Axelrod and Hamilton 1981;McNamara et al 1999; Lehmann and Keller 2006;Akçay et al 2009;Boyd et al 2010). However, the general question of whether and when flexible behaviors can allow group-optimal outcomes to be evolutionarily stable has not been answered.…”

“…Thus, r ij describes the relative behavioral response of j to i; we term it the "response coefficient" of j to i (Akçay et al 2009). …”

“…The mechanistic details of a specific behavioral model, such as coordinated punishment (Boyd et al 2010) or prosocial preferences (Levine 1998;Falk and Fischbacher 2006;Akçay et al 2009), determine the value of the response coefficient. In general, r ij may capture the equilibrium effect of many different behavioral models, including social norms and systems of rewards and punishments (Levin 2009).…”

“…Using a specific proximate mechanism for the production of behavioral responses, we also show how behavioral responses that lead to group optimality might evolve. The proximate mechanism we employ is the social-preferences, or motivations, model of Akçay et al (2009), which we extend to the case of Nplayer public-goods games. Group-optimal outcomes can evolve in this model through the evolution of how much individuals value the public good versus their private costs.…”

The importance of mechanisms for the evolution of cooperation

“…Yet, with some notable exceptions [17][18][19][20][21][22], models for the evolution of behaviour still tend to make the 'least constraining' assumptions on the genetic basis and the physiological and psychological processes underlying behaviour. When the direction and intensity of selection do not change in time and when there is a single optimal behaviour, this may not be problematic.…”