Group selection, kin selection, altruism and cooperation: When inclusive fitness is right and when it can be wrong

Group selection theory has a history of controversy. After a period of being in disrepute, models of group selection have regained some ground, but not without a renewed debate over their importance as a theoretical tool. In this paper I offer a simple framework for models of the evolution of altruism and cooperation that allows us to see how and to what extent both a classification with and one without group selection terminology are insightful ways of looking at the same models. Apart from this dualistic view, this paper contains a result that states that inclusive fitness correctly predicts the direction of selection for one class of models, represented by linear public goods games. Equally important is that this result has a flip side: there is a more general, but still very realistic class of models, including models with synergies, for which it is not possible to summarize their predictions on the basis of an evaluation of inclusive fitness.     

The robustness of altruism as an evolutionary strategy

Kin selection, reciprocity and group selection are widely regarded as evolutionary mechanisms capable of sustaining altruism among humans andother cooperative species. Our research indicates, however, that these mechanisms are only particular examples of a broader set of evolutionary possibilities.In this paper we present the results of a series of simple replicator simulations, run on variations of the 2–player prisoner's dilemma, designed to illustrate the wide range of scenarios under which altruism proves to be robust under evolutionary pressures. The set of mechanisms we explore is divided into four categories:correlation, group selection, imitation, and punishment. We argue that correlation is the core phenomenon at work in all four categories.     

Group selection in plant populations

Summary Several mechanisms have been proposed for group selection, to account for the evolution of altruistic traits. One type, Neighbourhood models, suggests that individuals react with those immediately around them, but with no recognition mechanism. The organization of plant populations seems especially favorable for this type of selection. The possibility of Neighbourhood selection was investigated by simulating a plant population. It was possible for an altruistic trait to evolve, though only under restricted conditions. The main requirement was gene flow only by very restricted pollen dispersal, and a high benefit : cost ratio in the altruistic relationship. Under conditions favourable for such evolution, the starting frequency of the allele, the initial pattern, and the population size, had little effect. Inbreeding tended to prevent the increase of the altruism allele, though this depended on the mechanism of selfing. Known ecological features of plants are discussed that could be considered altruistic and hence require some form of group selection for their evolution, and whether the benefit : cost requirements are likely to be met. Neighbourhood models of group selection are a possibility in plant populations, and we therefore cannot exclude the possibility of altruism in plants. However, Neighbourhood selection is weak force, unlikely to be effective in the face of opposing individual selection. It may be more important as reinforcement of individual selection.     

Why kin and group selection models may not be enough to explain human other-regarding behaviour

Models of kin or group selection usually feature only one possible fitness transfer. The phenotypes are either to make this transfer or not to make it and for any given fitness transfer, Hamilton's rule predicts which of the two phenotypes will spread. In this article we allow for the possibility that different individuals or different generations face similar, but not necessarily identical possibilities for fitness transfers. In this setting, phenotypes are preference relations, which concisely specify behaviour for a range of possible fitness transfers (rather than being a specification for only one particular situation an animal or human can be in). For this more general set-up, we find that only preference relations that are linear in fitnesses can be explained using models of kin selection and that the same applies to a large class of group selection models. This provides a new implication of hierarchical selection models that could in principle falsify them, even if relatedness--or a parameter for assortativeness--is unknown. The empirical evidence for humans suggests that hierarchical selection models alone are not enough to explain their other-regarding or altruistic behaviour.     

Natural selection and social preferences

A large number of individuals are randomly matched into groups, where each group plays a finite symmetric game. Individuals breed true. The expected number of surviving offspring depends on own material payoff, but may also, due to cooperative breeding and/or reproductive competition, depend on the material payoffs to other group members. The induced population dynamic is equivalent with the replicator dynamic for a game with payoffs derived from those in the original game. We apply this selection dynamic to a number of examples, including prisoners' dilemma games with and without a punishment option, coordination games, and hawk-dove games. For each of these, we compare the outcomes with those obtained under the standard replicator dynamic. By way of a revealed-preference argument, our selection dynamic can explain certain "altruistic" and "spiteful" behaviors that are consistent with individuals having social preferences.     

Multilevel selection, cooperation, and altruism

Unto Others (Sober and Wilson 1998) shows how the general principles of Multi-Level Selection (MLS) theory apply to selection at multiple levels of the biological hierarchy. It also argues for the existence of "genuine" evolutionary and psychological altruism. The authors’ views on altruism do not follow logically from principles of MLS, and their failure do disentangle these two themes undermines their otherwise excellent presentation of MLS theory. Rebuttal of the view that human nature is completely selfish depends not on the prevalence of altruism but on the importance of group-advantageous traits that benefit both self and other group members without necessarily inflicting direct costs on outsiders.     

Shifting values partly explain the debate over group selection

I argue that images of the notion of group, in correspondence with their social and political values, shape the debate over the evolution of altruism by group selection. Important aspects of this debate are empirical, and criteria can decide among a variety of selection processes. However, leading researchers undermine or reinterpret such tests, explaining the evolution of altruism on the basis of a single extreme metaphor of ‘group’ and a single inclusive selection process. I shall argue that the extreme images for the notion of group are associated with ideologies that these researchers support or fear. Hence, the history of social and political uses of ‘group’ and ‘group selection’ can explain, at least in part, some of the empirical deficiencies of the debate, and why it has continued without resolution or dissolution.     

Rationality and social behavior

This article penetrates the relationship between social behavior and rationality. A critical analysis is made of efforts to classify some behaviors as altruistic, as they simultaneously meet criteria of rationality by not truly being self-destructive. Newcomb's paradox is one attempt to create a hybrid behavior that is both irrational and still meets some criterion of rationality. Such dubious rationality is often seen as a source of altruistic behavior. Group selection is a controversial topic. Sober and Wilson (Unto Others--The Evolution and Psychology of Unselfish Behavior, Harvard University Press, Cambridge, MA, 1998) suggest that a very wide concept of group selection might be used to explain altruism. This concept also includes kin selection and reciprocity, which blurs its focus. The latter mechanisms hardly need further arguments to prove their existence. This article suggests that it is group selection in a strict sense that should be investigated to limit semantic neologism and confusion. In evaluation, the effort to muster a mechanism for altruism out of group selection has not been successful. However, this is not the end to group selection, but rather a good reason to investigate more promising possibilities. There is little reason to burden group selection with the instability of altruism caused by altruistic members of a group having lower fitness than egoistic members. Group selection is much more likely to develop in combination with group egoism. A common project is supported by incitement against free riding, where conformist members joined in solidarity achieve a higher fitness than members pursuing more individualistic options. Group egoism is in no conflict with rationality, and the effects of group selection will be supported rather than threatened by individual selection. Empirical evidence indicates a high level of traits such as conformism and out-group antagonism in line with group egoism. These traits are also likely candidates for behavior favored by group selection since they homogenize the group and link the different individuals closer to one another and a similar fate.     

The natural selection of altruistic traits

Proponents of the standard evolutionary biology paradigm explain human “altruism” in terms of either nepotism or strict reciprocity. On that basis our underlying nature is reduced to a function of inclusive fitness: human nature has to be totally selfish or nepotistic. Proposed here are three possible paths to giving costly aid to nonrelatives, paths that are controversial because they involve assumed pleiotropic effects or group selection. One path is pleiotropic subsidies that help to extend nepotistic helping behavior from close family to nonrelatives. Another is “warfare”—if and only if warfare recurred in the Paleolithic. The third and most plausible hypothesis is based on the morally based egalitarian syndrome of prehistoric hunter-gatherers, which reduced phenotypic variation at the within-group level, increased it at the between-group level, and drastically curtailed the advantages of free riders. In an analysis consistent with the fundamental tenets of evolutionary biology, these three paths are evaluated as explanations for the evolutionary development of a rather complicated human social nature. This paper (in a series of drafts) has profited from comments by Michael Boehm, Donald T. Campbell, Bruce Knauft, Jane Lancaster, Martin Muller, Peter J. Richerson, Gary Seaman, Craig Stanford, George Williams, Edward O. Wilson, David Sloan Wilson, and two reviewers for Human Nature. Christopher Boehm is a professor of anthropology and the director of the Jane Goodall Research Center, University of Southern California. His research interests in political anthropology concern egalitarianism, feuding, warfare, and conflict resolution (humans and chimpanzees). In biosocial anthropology he is interested in altruism, group selection, and decisions.     

On the relationship between evolutionary and psychological definitions of altruism and selfishness

I examine the relationship between evolutionary definitions of altruism that are based on fitness effects and psychological definitions that are based on the motives of the actor. I show that evolutionary altruism can be motivated by proximate mechanisms that are psychologically either altruistic or selfish. I also show that evolutionary definitions do rely upon motives as a metaphor in which the outcome of natural selection is compared to the decisions of a psychologically selfish (or altruistic) individual. Ignoring the precise nature of both psychological and evolutionary definitions has obscured many important issues, including the biological roots of psychological altruism.     

The concept of group heritability

This paper investigates the role of the concept of group heritability in group selection theory, in relation to the well-known distinction between type 1 and type 2 group selection (GS1 and GS2). I argue that group heritability is required for the operation of GS1 but not GS2, despite what a number of authors have claimed. I offer a numerical example of the evolution of altruism in a multi-group population which demonstrates that a group heritability coefficient of zero is perfectly compatible with the successful operation of group selection in the GS2 sense. A diagnosis of why group heritability has wrongly been regarded as necessary for GS2 is suggested.     

Maynard Smith on the levels of selection question

The levels of selection problem was central to Maynard Smith’s work throughout his career. This paper traces Maynard Smith’s views on the levels of selection, from his objections to group selection in the 1960s to his concern with the major evolutionary transitions in the 1990s. The relations between Maynard Smith’s position and those of Hamilton and G.C. Williams are explored, as is Maynard Smith’s dislike of the Price equation approach to multi-level selection. Maynard Smith’s account of the ‘core Darwinian principles’ is discussed, as is his debate with Sober and Wilson (1998) over the status of trait-group models, and his attitude to the currently fashionable concept of pluralism about the levels of selection.     

Evolution,altruism, and the prisoner's dilemma

I first argue against Peter Singer's exciting thesis that the Prisoner's Dilemma explains why there could be an evolutionary advantage in making reciprocal exchanges that are ultimately motivated by genuine altruism over making such exchanges on the basis of enlightened long-term self-interest. I then show that an alternative to Singer's thesis — one that is also meant to corroborate the view that natural selection favors genuine altruism, recently defended by Gregory Kavka, fails as well. Finally, I show that even granting Singer's and Kavka's claim about the selective advantage of altruism proper, it is doubtful whether that type of claim can be used in a particular sort of sociobiological argument against psychological egoism.     

Sexual selection and magic traits in speciation with gene flow

The extent to which sexual selection is involved in speciation with gene flow remains an open question and the subject of much research.Here,we propose that some insight can be gained from considering the concept of magic traits (i.e.,traits involved in both reproductive isolation and ecological divergence).Both magic traits and other,“non-magic”,traits can contribute to speciation via a number of specific mechanisms.We argue that many of these mechanisms are likely to differ widely in the extent to which they involve sexual selection.Furthermore,in some cases where sexual selection is present,it may be prone to inhibit rather than drive speciation.Finally,there are a priori reasons to believe that certain categories of traits are much more effective than others in driving speciation.The combination of these points suggests a classification of traits that may shed light on the broader role of sexual selection in speciation with gene flow.In particular,we suggest that sexual selection can act as a driver of speciation in some scenarios,but may play a negligible role in potentially common categories of magic traits,and may be likely to inhibit speeiation in common categories of non-magic traits.     

Assortative mating through a mechanism of sexual selection

We propose that assortative mating can arise through a mechanism of sexual selection by active female choice of partners based on a 'self-seeking like' decision rule. Using a mathematical model, we show that a gene can be selected that make females to choose mates that are similar to themselves with respect to an arbitrary tag, even if two independent and unlinked genes determine the preference and the tag. The necessary requisite for this process to apply is an asymmetry between partners, such that the female can choose the male but this one must always accept to mate. The fitness advantage is due to linkage disequilibrium built up between both genes. Simulations have been run to check the algebraic results and to analyse the influence of several factors on the evolution of the system. Any factor that favors linkage disequilibrium also favors the evolution of the preference allele. Moreover, in a large population subdivided in small subpopulations connected by migration, the assortative mating homogenizes the population genotypic structure for the tags in contrast to random mating that maintains most of the variation.     

An experimental test of the efficiency of family selection in chickens

Summary Responses to single trait selection on individual phenotype and sire-family mean phenotype for survivor's egg weight and rate of lay were measured for a single generation in 13 replicates. Each replicate-selection criterion-trait subclass consisted of eight sire families or 72 females measured and was reproduced from the best 25% of the families or individuals. The realized heritability of egg weight was 0.39 and that of rate of lay was 0.31, both of which were significantly greater than zero but not significantly different from the predicted values based on halfsib correlations in the base population.The standardized response to sire-family selection was less than the response to individual selection for both traits and the difference was significant for rate of lay (0.10; 0.31) but not for egg weight (0.22; 0.39). The predicted responses to sire-family selection were less than those for individual selection for both traits, and the observed responses to sire-family selection were not significantly different from the predicted values for either trait.These experimental results do not disagree with the theoretical expectations of the relative efficiencies of individual and sire-family selection.Journal paper no. 7479, Purdue University, Agricultural Experiment Station. This investigation was conducted as a part of the cooperative research of the NC-89 Regional Poultry Breeding Project entitled Nature and Utilization of Genetic Variation in Poultry Improvement     

Altruism, sex, and inbreeding when the genotype-phenotype map is additive

Recently published theoretical results suggest that, in a sexual population, when genotypes code for phenotypes in a complex manner, it is possible for altruistic genotypes to spread through a metapopulation (i.e. through a collection of subpopulations). This spread tends to occur during periods when the environment deteriorates throughout the metapopulation. By contrast, under asexual reproduction, non-altruistic genotypes seem to be favoured, at least when subpopulations are substantial in size. The most relevant previous study makes use of Kauffman and Levin's "NK model" as a way to relate genotypes to fitness. Unfortunately, there are both conceptual and technical problems with the application of the NK model to populations that contain many different genotypes (e.g. polymorphic diploid populations with more than a few loci under selection). The present study presents a more tractable and biologically plausible model to study the causal relationship between sexual reproduction and altruism. In particular, phenotypes are determined by additive interactions among alleles at different loci in a diploid genome, with up to 200 loci under selection. In addition, subpopulations are substantially larger than those considered in the most relevant previous work. The results show that, so long as there are multiple "fitness peaks" in "phenotype space", the additive genotype-phenotype map leads to results that are similar to those from the NK model. Various parameters are manipulated in an effort to discover the determinants of altruistic and non-altruistic outcomes. The findings should facilitate further investigations, and they should help to establish the plausibility of the suggested relationship between sexual reproduction and altruism. The results also suggest that inbreeding can lead to a similar result as asexuality. That is, inbreeding seems to enhance the probability that altruistic phenotypes will be eliminated.     

A new group-selection model for the evolution of homosexuality

Abstract. Scientists have long puzzled over how homosexual orientation has evolved, given the assumed low relative fitness of homosexual individuals compared to heterosexual individuals. A number of theoretical models for the evolution of homosexuality have been postulated including balance polymorphism, "Fertile females", hypervariability of DNA sequences, kin selection, and "parental manipulation". In this paper, I propose a new group-selection model for the evolution of homosexuality which offers two advantages over existing models: (1) its non-assumption of genetic determinism, and (2) its lack of dependency on an inefficient altruism relation and family dynamics theory.     

Social semantics: altruism, cooperation, mutualism, strong reciprocity and group selection

From an evolutionary perspective, social behaviours are those which have fitness consequences for both the individual that performs the behaviour, and another individual. Over the last 43 years, a huge theoretical and empirical literature has developed on this topic. However, progress is often hindered by poor communication between scientists, with different people using the same term to mean different things, or different terms to mean the same thing. This can obscure what is biologically important, and what is not. The potential for such semantic confusion is greatest with interdisciplinary research. Our aim here is to address issues of semantic confusion that have arisen with research on the problem of cooperation. In particular, we: (i) discuss confusion over the terms kin selection, mutualism, mutual benefit, cooperation, altruism, reciprocal altruism, weak altruism, altruistic punishment, strong reciprocity, group selection and direct fitness; (ii) emphasize the need to distinguish between proximate (mechanism) and ultimate (survival value) explanations of behaviours. We draw examples from all areas, but especially recent work on humans and microbes.