Evolution and the classification of social behavior

Recent studies in the evolution of cooperation have shifted focus from altruistic to mutualistic cooperation. This change in focus is purported to reveal new explanations for the evolution of prosocial behavior. We argue that the common classification scheme for social behavior used to distinguish between altruistic and mutualistic cooperation is flawed because it fails to take into account dynamically relevant game-theoretic features. This leads some arguments about the evolution of cooperation to conflate dynamical scenarios that differ regarding the basic conditions on the emergence and maintenance of cooperation. We use the tools of evolutionary game theory to increase the resolution of the classification scheme and analyze what evolutionary inferences classifying social behavior can license.     

Benevolent Characteristics Promote Cooperative Behaviour among Humans

Cooperation is fundamental to the evolution of human society. We regularly observe cooperative behaviour in everyday life and in controlled experiments with anonymous people, even though standard economic models predict that they should deviate from the collective interest and act so as to maximise their own individual payoff. However, there is typically heterogeneity across subjects: some may cooperate, while others may not. Since individual factors promoting cooperation could be used by institutions to indirectly prime cooperation, this heterogeneity raises the important question of who these cooperators are. We have conducted a series of experiments to study whether benevolence, defined as a unilateral act of paying a cost to increase the welfare of someone else beyond one''s own, is related to cooperation in a subsequent one-shot anonymous Prisoner''s dilemma. Contrary to the predictions of the widely used inequity aversion models, we find that benevolence does exist and a large majority of people behave this way. We also find benevolence to be correlated with cooperative behaviour. Finally, we show a causal link between benevolence and cooperation: priming people to think positively about benevolent behaviour makes them significantly more cooperative than priming them to think malevolently. Thus benevolent people exist and cooperate more.     

Active linking in evolutionary games

In the traditional approach to evolutionary game theory, the individuals of a population meet each other at random, and they have no control over the frequency or duration of interactions. Here we remove these simplifying assumptions. We introduce a new model, where individuals differ in the rate at which they seek new interactions. Once a link between two individuals has formed, the productivity of this link is evaluated. Links can be broken off at different rates. In a limiting case, the linking dynamics introduces a simple transformation of the payoff matrix. We outline conditions for evolutionary stability. As a specific example, we study the interaction between cooperators and defectors. We find a simple relationship that characterizes those linking dynamics which allow natural selection to favour cooperation over defection.     

Game theory and human evolution: a critique of some recent interpretations of experimental games

Economists and psychologists have been testing Nash equilibrium predictions of game theory models of human behavior. In many instances, humans do not conform to the predictions. These results are of great interest to biologists because they also raise questions about well-known ESS models of cooperation. Cooperation in certain one-shot, anonymous interactions, and a willingness to punish others at a net cost to oneself are some of the most intriguing deviations from standard theory. One proposed explanation for these results that is receiving increasing attention invokes the cultural group selection of 'other regarding' social norms. We critically review this explanation. We conclude that experimental results reveal limits in two implicit models of cognitive structure commonly employed by economists and evolutionary biologists.     

Maintenance affects the stability of a two-tiered microbial 'food chain'?

Recent studies have shown that constraints on available resources may play an important role in the evolution of cooperation, especially when individuals do not posses the capacity to recognize other individuals, memory or other developed abilities, as it is the case of most unicellular organisms, algae or even plants. We analyze the evolution of cooperation in the case of a limiting resource, which is necessary for reproduction and survival. We show that, if the strategies determine a prisoner's dilemma, the outcome of the interactions may be modified by the limitation of resources allowing cooperators to invade the entire population. Analytic expressions for the region of cooperation are provided. Furthermore we derive expressions for the connection between fitness, as understood in evolutionary game theory, and resource exchanges, which may be of help to link evolutionary game theoretical results with resource based models.     

Relating coupled map lattices to integro-difference equations: dispersal-driven instabilities in coupled map lattices

Recently there has been a great deal of interest within the ecological community about the interactions of local populations that are coupled only by dispersal. Models have been developed to consider such scenarios but the theory needed to validate model outcomes has been somewhat lacking. In this paper, we present theory which can be used to understand these types of interaction when population exhibit discrete time dynamics. In particular, we consider a spatial extension to discrete-time models, known as coupled map lattices (CMLs) which are discrete in space. We introduce a general form of the CML and link this to integro-difference equations via a special redistribution kernel. General conditions are then derived for dispersal-driven instabilities. We then apply this theory to two discrete-time models; a predator-prey model and a host-pathogen model.     

Developing unified theories in ecology as exemplified with diversity gradients

A scientific field matures as its theoretical underpinnings consolidate around unified theories: conceptual structures consisting of a few general propositions that encompass a wide domain of phenomena and from which can be derived an array of models. We demonstrate this process with a synthetic theory of ecological gradients and species richness. Our unified theory rests on four propositions. First, variation in some environmental factor effects variation in the number of individuals creating a gradient. Second, in a uniform environment of fixed area, more individuals lead to more species. Third, the variance of an environmental factor increases with its mean for sites of equal area. Fourth, all nonmonotonic relationships (i.e., hump shaped or U shaped) require a trade-off in organismal performance or in population characteristics with respect to the environmental gradient. We identify 17 models that link environmental gradients with diversity, show their relationship to our framework, and describe issues surrounding their empirical testing. We illustrate how a general theory can be used to build new models such as that for the U-shaped productivity-diversity relationship. Finally, we discuss how our theory could be unified further with other theories of diversity and indicate other areas of ecology that are ripe for unification. By providing an example of the process of theory unification, we hope to encourage such efforts throughout ecology.     

Indirect reciprocity and the evolution of “moral signals”

Signals regarding the behavior of others are an essential element of human moral systems and there are important evolutionary connections between language and large-scale cooperation. In particular, social communication may be required for the reputation tracking needed to stabilize indirect reciprocity. Additionally, scholars have suggested that the benefits of indirect reciprocity may have been important for the evolution of language and that social signals may have coevolved with large-scale cooperation. This paper investigates the possibility of such a coevolution. Using the tools of evolutionary game theory, we present a model that incorporates primitive “moral signaling” into a simple setting of indirect reciprocity. This model reveals some potential difficulties for the evolution of “moral signals.” We find that it is possible for “moral signals” to evolve alongside indirect reciprocity, but without some external pressure aiding the evolution of a signaling system, such a coevolution is unlikely.     

Cooperation in animals: An evolutionary overview

Evolutionary biologists have grappled with the question of the emergenceand maintenance of cooperation since Darwin first listed animal cooperation asapotential problem for his theory of natural selection. Here I review four pathsthat have been delineated in the study of intra-specific cooperation amonganimals. These paths – kinship, reciprocity, byproduct mutualism andgroupselection – serve as a starting point for behavioral ecologistsinterestedstudying the initiation and maintenance of cooperation. After reviewing theempirical and theoretical underpinnings of these paths to cooperation, I touchupon some recent work that has attempted to examine (or reexamine) the role ofphylogeny, punishment and morality in the light of cooperative behavior.     

From the editors

[T]here had been theories that homosexuality might have a genetic basis. In June this year, these theories received a somewhat firmer basis. Researchers at the United States National Cancer Institute reported new evidence which suggests that some gay men may have a genetic predisposition to homosexuality. The research team led by molecular biologist Dean Hamer tested 40 pairs of homosexual brothers and found that 33 of the pairs shared genetic markers on a particular area of the X chromosome (called Xq28), indicating a link between homosexuality and a gene in that area. If followed-up research were to confirm the findings, then, it has been claimed, this would be the first example of a behavioral trait that has been found to have a genetic basis. The study does, however, leave some central questions unanswered. Some revolve around the link between genetics and the nature of sexuality itself. The others concern the ethical and social implications of the research....     

The interplay of cognition and cooperation

Cooperation often involves behaviours that reduce immediate payoffs for actors. Delayed benefits have often been argued to pose problems for the evolution of cooperation because learning such contingencies may be difficult as partners may cheat in return. Therefore, the ability to achieve stable cooperation has often been linked to a species'' cognitive abilities, which is in turn linked to the evolution of increasingly complex central nervous systems. However, in their famous 1981 paper, Axelrod and Hamilton stated that in principle even bacteria could play a tit-for-tat strategy in an iterated Prisoner''s Dilemma. While to our knowledge this has not been documented, interspecific mutualisms are present in bacteria, plants and fungi. Moreover, many species which have evolved large brains in complex social environments lack convincing evidence in favour of reciprocity. What conditions must be fulfilled so that organisms with little to no brainpower, including plants and single-celled organisms, can, on average, gain benefits from interactions with partner species? On the other hand, what conditions favour the evolution of large brains and flexible behaviour, which includes the use of misinformation and so on? These questions are critical, as they begin to address why cognitive complexity would emerge when ‘simple’ cooperation is clearly sufficient in some cases. This paper spans the literature from bacteria to humans in our search for the key variables that link cooperation and deception to cognition.     

On the further integration of cooperative breeding and cooperation theory

We present a synopsis about the commentaries to the target article "Integrating cooperative breeding into theoretical concepts of cooperation", in which we attempted to integrate general mechanisms to explain cooperative behaviour among unrelated individuals with classic concepts to explain helping behaviour in cooperative breeders that do not invoke kin-based benefits. Here we (1) summarize the positions of the commentators concerning the main issues we raised in the target article and discuss important criticisms and extensions. (2) We relate our target article to some recent reviews on the evolution of cooperation and, (3) clarify how we use terminology with regard to cooperation and cooperative behaviour. (4) We discuss several aspects that were raised with respect to cooperative interactions including by-product mutualism, generalised reciprocity and multi-level selection and, (5) examine the alternatives to our classification scheme as proposed by some commentaries. (6) Finally, we highlight several aspects that might hinder the application of game theoretical mechanisms of cooperation in cooperatively breeding systems. Although there is broad agreement that cooperative breeding theory should be integrated within the more general concepts of cooperation, there is some debate about how this may be achieved. We conclude that the contributions in this special issue provide a fruitful first step and ample suggestions for future directions with regard to a more unified framework of cooperation in cooperative breeders.     

Repeated games and direct reciprocity under active linking

Direct reciprocity relies on repeated encounters between the same two individuals. Here we examine the evolution of cooperation under direct reciprocity in dynamically structured populations. Individuals occupy the vertices of a graph, undergoing repeated interactions with their partners via the edges of the graph. Unlike the traditional approach to evolutionary game theory, where individuals meet at random and have no control over the frequency or duration of interactions, we consider a model in which individuals differ in the rate at which they seek new interactions. Moreover, once a link between two individuals has formed, the productivity of this link is evaluated. Links can be broken off at different rates. Whenever the active dynamics of links is sufficiently fast, population structure leads to a simple transformation of the payoff matrix, effectively changing the game under consideration, and hence paving the way for reciprocators to dominate defectors. We derive analytical conditions for evolutionary stability.     

The psychology of primate cooperation and competition: a call for realigning research agendas

Cooperation and competition are two key components of social life. Current research agendas investigating the psychological underpinnings of competition and cooperation in non-human primates are misaligned. The majority of work on competition has been done in the context of theory of mind and deception, while work on cooperation has mostly focused on collaboration and helping. The current impression that theory of mind is not necessarily implicated in cooperative activities and that helping could not be an integral part of competition might therefore be rather misleading. Furthermore, theory of mind research has mainly focused on cognitive aspects like the type of stimuli controlling responses, the nature of representation and how those representations are acquired, while collaboration and helping have focused primarily on motivational aspects like prosociality, common goals and a sense of justice and other-regarding concerns. We present the current state of these two bodies of research paying special attention to how they have developed and diverged over the years. We propose potential directions to realign the research agendas to investigate the psychological underpinnings of cooperation and competition in primates and other animals.     

Pleiotropic constraints promote the evolution of cooperation in cellular groups

The evolution of cooperation in cellular groups is threatened by lineages of cheaters that proliferate at the expense of the group. These cell lineages occur within microbial communities, and multicellular organisms in the form of tumours and cancer. In contrast to an earlier study, here we show how the evolution of pleiotropic genetic architectures—which link the expression of cooperative and private traits—can protect against cheater lineages and allow cooperation to evolve. We develop an age-structured model of cellular groups and show that cooperation breaks down more slowly within groups that tie expression to a private trait than in groups that do not. We then show that this results in group selection for pleiotropy, which strongly promotes cooperation by limiting the emergence of cheater lineages. These results predict that pleiotropy will rapidly evolve, so long as groups persist long enough for cheater lineages to threaten cooperation. Our results hold when pleiotropic links can be undermined by mutations, when pleiotropy is itself costly, and in mixed-genotype groups such as those that occur in microbes. Finally, we consider features of multicellular organisms—a germ line and delayed reproductive maturity—and show that pleiotropy is again predicted to be important for maintaining cooperation. The study of cancer in multicellular organisms provides the best evidence for pleiotropic constraints, where abberant cell proliferation is linked to apoptosis, senescence, and terminal differentiation. Alongside development from a single cell, we propose that the evolution of pleiotropic constraints has been critical for cooperation in many cellular groups.

The evolution of cooperation in cellular groups is threatened by lineages of cheaters that proliferate at the expense of the group. In this study, an age-structured model of cellular groups shows that pleiotropy promotes the evolution of cooperation and may have been important for the origins of multicellularity.     

Host-plant selection by insects – a theory based on `appropriate/inappropriate landings'' by pest insects of cruciferous plants

Seven hypotheses, including the `Resource Concentration Hypothesis' and the `Enemies Hypothesis', have been put forward to explain why fewer specialist insects are found on host plants growing in diverse backgrounds than on similar plants growing in bare soil. All seven hypotheses are discussed and discounted, primarily because no one has used any of them to produce a general theory of host plant selection, they still remain as hypotheses. However, we have developed a general theory based on detailed observations of insect behaviour. Our theory is based on the fact that during host plant finding the searching insects land indiscriminately on green objects such as the leaves of host plants (appropriate landings) and non-host plants (inappropriate landings), but avoid landing on brown surfaces, such as soil. The complete system of host plant selection involves a three-link chain of events in which the first link is governed by cues from volatile plant chemicals, the central link by visual stimuli, and the final link by cues from non-volatile plant chemicals. The previously `missing' central link, which is based on what we have described as `appropriate/inappropriate landings', is governed by visual stimuli. Our theory explains why attempts to show that olfaction is the crucial component in the central link of host plant selection proved intractable. The `appropriate/inappropriate landings' theory is discussed to indicate the type of work needed in future studies to improve our understanding of how intercropping, undersowing and companion planting can be used to optimum effect in crop protection. The new theory is used also to suggest how insect biotypes could develop and to describe why pest insects do not decimate wild host plants growing in `natural' situations.     

Criminal Defectors Lead to the Emergence of Cooperation in an Experimental,Adversarial Game

While the evolution of cooperation has been widely studied, little attention has been devoted to adversarial settings wherein one actor can directly harm another. Recent theoretical work addresses this issue, introducing an adversarial game in which the emergence of cooperation is heavily reliant on the presence of “Informants,” actors who defect at first-order by harming others, but who cooperate at second-order by punishing other defectors. We experimentally study this adversarial environment in the laboratory with human subjects to test whether Informants are indeed critical for the emergence of cooperation. We find in these experiments that, even more so than predicted by theory, Informants are crucial for the emergence and sustenance of a high cooperation state. A key lesson is that successfully reaching and maintaining a low defection society may require the cultivation of criminals who will also aid in the punishment of others.     

Network homophily and the evolution of the pay-it-forward reciprocity

The pay-it-forward reciprocity is a type of cooperative behavior that people who have benefited from others return favors to third parties other than the benefactors, thus pushing forward a cascade of kindness. The phenomenon of the pay-it-forward reciprocity is ubiquitous, yet how it evolves to be part of human sociality has not been fully understood. We develop an evolutionary dynamics model to investigate how network homophily influences the evolution of the pay-it-forward reciprocity. Manipulating the extent to which actors carrying the same behavioral trait are linked in networks, the computer simulation model shows that strong network homophily helps consolidate the adaptive advantage of cooperation, yet introducing some heterophily to the formation of network helps advance cooperation's scale further. Our model enriches the literature of inclusive fitness theory by demonstrating the conditions under which cooperation or reciprocity can be selected for in evolution when social interaction is not confined exclusively to relatives.     

No unique effect of intergroup competition on cooperation: non-competitive thresholds are as effective as competitions between groups for increasing human cooperative behavior

Explaining cooperation remains a central topic for evolutionary theorists. Many have argued that group selection provides such an explanation: theoretical models show that intergroup competition could have given rise to cooperation that is costly for the individual. Whether group selection actually did play an important role in the evolution of human cooperation, however, is much debated. Recent experiments have shown that intergroup competitions do increase human cooperation, which has been taken as evidence for group selection as a mechanism for the evolution of cooperation. Here we challenge this standard interpretation. Competitions change the payoff structure by creating a threshold effect whereby the group that contributes more earns an additional prize, which creates some incentive for individuals to cooperate. We present four studies that disentangle competition and thresholds, and strongly suggest that it is thresholds – rather than competitions per se – that increase cooperation. Thus, prior intergroup competition experiments provide no evidence of a unique or special role for intergroup competition in promoting human cooperation, and shed no light on whether group selection shaped human evolution.     

Glutamate slows axonal transport of neurofilaments in transfected neurons

Neurofilaments are transported through axons by slow axonal transport. Abnormal accumulations of neurofilaments are seen in several neurodegenerative diseases, and this suggests that neurofilament transport is defective. Excitotoxic mechanisms involving glutamate are believed to be part of the pathogenic process in some neurodegenerative diseases, but there is currently little evidence to link glutamate with neurofilament transport. We have used a novel technique involving transfection of the green fluorescent protein-tagged neurofilament middle chain to measure neurofilament transport in cultured neurons. Treatment of the cells with glutamate induces a slowing of neurofilament transport. Phosphorylation of the side-arm domains of neurofilaments has been associated with a slowing of neurofilament transport, and we show that glutamate causes increased phosphorylation of these domains in cell bodies. We also show that glutamate activates members of the mitogen-activated protein kinase family, and that these kinases will phosphorylate neurofilament side-arm domains. These results provide a molecular framework to link glutamate excitotoxicity with neurofilament accumulation seen in some neurodegenerative diseases.