Policing and group cohesion when resources vary

The transition from competing individuals to cooperative groups has occurred several times in evolutionary history. The puzzle is why selfish individuals did not subvert cohesive group behaviour by taking resources without contributing to the group’s overall success. Kin selection and reciprocal altruism are the two standard explanations for group cohesion. But many groups have evolved into cooperative units when relatedness was low and opportunities were limited for the strategic alliances required for reciprocity. A new theory was recently proposed in which individuals invest some of their resources into repressing competition between group members. Such policing increases the fair distribution of resources in the group and enhances group cohesion. The surprising aspect of this theory is that low relatedness is more conducive to the spread of policing traits than is high relatedness. Here a new explanation is developed of the biological processes that favour policing. The model is then extended in two ways. First, more realism is added to the theory by accounting for the full range of costs and benefits associated with competitive and cooperative traits within groups. Second, another surprising result is introduced about cooperative evolution. Small variations in individual vigour or resources can lead to large variations in individual contributions to policing the group. Stronger individuals often invest all of their excess resources into policing, but weaker individuals do not contribute to group cohesion. ? 1996 The Association for the Study of Animal Behaviour An important puzzle in biology is how groups of independent units evolve to form a cohesive functional unit (Maynard Smith & Szathmáry 1995). The problem is the ‘tragedy of the commons’, in which competition for limited resources favours rapacious individuals over prudent ones. This competition between neighbours reduces the sustainable yield of the group, lowering the fitness of all members. There are two standard explanations for group cooperation. Kin selection favours self-restraint and prudent behaviour between genetically similar neighbours (Hamilton 1964). Strategic alliance favours cooperation with neighbours who reciprocate, as in the famous Tit-for-Tat strategy of game theory (Axelrod 1984). These two ideas, although fundamental to many important problems, are not sufficient to explain several aspects of cooperative evolution. For example, the puzzle of early cellular life is how different kinds (species) of replicators evolved into a functional unit. Kin selection cannot be the sole factor, because the key interactions are between different species. Strategic alliance models of game theory also fail because they usually require recognition of individuals and memory of past interactions. Even in organisms with the potential for memory and complex strategy, the form of mixing and competition often precludes game theory solutions. I recently proposed a theory to explain how competition between lower-level units is suppressed in the formation of higher-level evolutionary units (Frank 1995; extending earlier work by Alexander 1987; Ratnieks & Visscher 1989; Wilson & Sober 1994). The idea is that individuals may invest some of their resources in repressing competition among group members. Such policing increased the fair distribution of resources in the group, enhances group efficiency and raises the average fitness of group members. The surprising aspect of my new theoretical work is how readily policing traits increase in frequency when relatedness among group Correspondence: S. A. Frank, Department of Ecology and Evolutionary Biology, University of California, Irvine, CA 92697-2525, U.S.A. (email: [email protected]). 0003–3472/96/121163+07 $25.00/0 ? 1996 The Association for the Study of Animal Behaviour