Multilevel selection: the evolution of cooperation in non-kin groups

Hamiltons (1964a, 1964b) landmark papers are rightly recognized as the formal basis for our understanding of the evolution of altruistic traits. However, Hamiltons equation as he originally expressed it is simplistic. A genetically oriented approach to studying multilevel selection can provide insights into how the terminology and assumptions used by Hamilton can be generalized. Using contextual analysis I demonstrated that Hamiltons rule actually embodies three distinct processes, group selection, individual selection, and transmission genetics or heritability. Whether an altruistic trait will evolve depends the balance of all of these factors. The genetical approach, and particularly, contextual analysis provides a means of separating these factors and examining them one at a time. Perhaps the greatest issue with Hamiltons equation is the interpretation of r. Hamilton (1964a) interpreted this as relatedness. In this paper I show that what Hamilton called relatedness is more generally interpreted as the proportion for variance among groups, and that many processes in addition to relatedness can increase the variance among groups. I also show that the evolution of an altruistic trait is driven by the ratio of the heritability at the group level to the heritability at the individual level. Under some circumstances this ratio can be greater than 1. In this situation altruism can evolve even if selection favoring selfish behavior is stronger than selection favoring altruism.     

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.     

Mutability as an altruistic trait in finite asexual populations

Mutation rate (MR) is a crucial determinant of the evolutionary process. Optimal MR may enable efficient evolutionary searching and therefore increase the fitness of the population over time. Nevertheless, individuals may favor MRs that are far from being optimal for the whole population. Instead, each individual may tend to mutate at rates that selfishly increase its own relative fitness. We show that in some cases, undergoing a mutation is altruistic, i.e., it increases the expected fitness of the population, but decreases the expected fitness of the mutated individual itself. In this case, if the population is uniform (completely mixed, undivided), immutability is evolutionary stable and is probably selected for. However, our examination of a segregated population, which is divided into several groups (or patches), shows that the optimal, altruistic MR may out-compete the selfish MR if the coupling between the groups is neither too strong nor too weak. This demonstrates that the population structure is crucial for the succession of the evolutionary process itself. For example, in a uniform population, the evolutionary process may be stopped before the highest fitness is reached, as demonstrated in a one-pick fitness landscape. In addition, we show that the dichotomy between evolutionary stable and optimal MRs can be seen as a special case of a more general phenomenon in which optimal behaviors may be destabilized in finite populations, since optimal sub-populations may become extinct before the benefit of their behavior is expressed.     

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.     

Multilevel selection and human altruism

Views on the evolution of altruism based upon multilevel selection on structured populations pay little attention to the difference between fortuitous and deliberate processes leading to assortative grouping. Altruism may evolve when assortative grouping is fortuitously produced by forces external to the organism. But when it is deliberately produced by the same proximate mechanism that controls altruistic responses, as in humans, exploitation of altruists by selfish individuals is unlikely and altruism evolves as an individually advantageous trait. Groups formed with altruists of this sort are special, because they are not affected by subversion from within. A synergistic process where altruism is selected both at the individual and at the group level can take place.     

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.     

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.     

Kin selection and coefficients of relatedness in family-structured populations with inbreeding

We consider family specific fitnesses that depend on mixed strategies of two basic phenotypes or behaviours. Pairwise interactions are assumed, but they are restricted to occur between sibs. To study the change in frequency of a rare mutant allele, we consider two different forms of weak selection, one applied through small differences in genotypic values determining individual mixed strategies, the other through small differences in viabilities according to the behaviours chosen by interacting sibs. Under these two specific forms of weak selection, we deduce conditions for initial increase in frequency of a rare mutant allele for autosomal genes in the partial selfing model as well as autosomal and sex-linked genes in the partial sib-mating model with selection before mating or selection after mating. With small differences in mixed strategies, we show that conditions for protection of a mutant allele are tantamount to conditions for initial increase in frequency obtained in additive kin selection models. With particular reference to altruism versus selfishness, we provide explicit ranges of values for the selfing or sib-mating rate based on a fixed cost-benefit ratio and the dominance scheme that allow the spreading of a rare mutant allele into the population. This study confirms that more inbreeding does not necessarily promote the evolution of altruism. Under the hypothesis of small differences in viabilities, the situation is much more intricate unless an additive model is assumed. In general however, conditions for initial increase in frequency of a mutant allele can be obtained in terms of fitness effects that depend on the genotypes of interacting individuals or their mates and generalized conditional coefficients of relatedness according to the inbreeding condition of the interacting individuals.     

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.     

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.     

Kin groups and trait groups: population structure and epidemic disease selection

A Monte Carlo simulation based on the population structure of a small-scale human population, the Semai Senoi of Malaysia, has been developed to study the combined effects of group, kin, and individual selection. The population structure resembles D.S. Wilson's structured deme model in that local breeding populations (Semai settlements) are subdivided into trait groups (hamlets) that may be kin-structured and are not themselves demes. Additionally, settlement breeding populations are connected by two-dimensional stepping-stone migration approaching 30% per generation. Group and kin-structured group selection occur among hamlets the survivors of which then disperse to breed within the settlement population. Genetic drift is modeled by the process of hamlet formation; individual selection as a deterministic process, and stepping-stone migration as either random or kin-structured migrant groups. The mechanism for group selection is epidemics of infectious disease that can wipe out small hamlets particularly if most adults become sick and social life collapses. Genetic resistance to a disease is an individual attribute; however, hamlet groups with several resistant adults are less likely to disintegrate and experience high social mortality. A specific human gene, hemoglobin E, which confers resistance to malaria, is studied as an example of the process. The results of the simulations show that high genetic variance among hamlet groups may be generated by moderate degrees of kin-structuring. This strong microdifferentiation provides the potential for group selection. The effect of group selection in this case is rapid increase in gene frequencies among the total set of populations. In fact, group selection in concert with individual selection produced a faster rate of gene frequency increase among a set of 25 populations than the rate within a single unstructured population subject to deterministic individual selection. Such rapid evolution with plausible rates of extinction, individual selection, and migration and a population structure realistic in its general form, has implications for specific human polymorphisms such as hemoglobin variants and for the more general problem of the tempo of evolution as well.     

From quorum to cooperation: lessons from bacterial sociality for evolutionary theory

The study of cooperation and altruism, almost since its inception, has been carried out without reference to the most numerous, diverse and very possibly most cooperative domain of life on the planet: bacteria. This is starting to change, for good reason. Far from being clonal loners, bacteria are highly social creatures capable of astonishingly complex collective behaviour that is mediated, as it is in colonial insects, by chemical communication. The article discusses recent experiments that explore different facets of current theories of the evolution and maintenance of cooperation using bacterial models. Not only do bacteria hold great promise as experimentally tractable, rapidly evolving systems for testing hypotheses, bacterial experiments have already raised interesting questions about the assumptions on which our current understanding of cooperation and altruism rests.     

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.     

Kin selection and ethnic group selection

Ethnicity looks something like kinship on a larger scale. The same math can be used to measure genetic similarity within ethnic/racial groups and relatedness within families. For example, members of the same continental race are about as related (r = 0.18–0.26) as half-siblings (r = 0.25). However (contrary to some claims) the theory of kin selection does not apply straightforwardly to ethnicity, because inclusive fitness calculations based on Hamilton's rule break down when there are complicated social interactions within groups, and/or groups are large and long-lasting. A more promising approach is a theory of ethnic group selection, a special case of cultural group selection. An elementary model shows that the genetic assimilation of a socially enforced cultural regime can promote group solidarity and lead to the regulation of recruitment to groups, and to altruism between groups, based on genetic similarity – in short, to ethnic nepotism. Several lines of evidence, from historical population genetics and political psychology, are relevant here.     

Diffusion approximations for one-locus multi-allele kin selection,mutation and random drift in group-structured populations: a unifying approach to selection models in population genetics

Diffusion approximations are ascertained from a two-time-scale argument in the case of a group-structured diploid population with scaled viability parameters depending on the individual genotype and the group type at a single multi-allelic locus under recurrent mutation, and applied to the case of random pairwise interactions within groups. The main step consists in proving global and uniform convergence of the distribution of the group types in an infinite population in the absence of selection and mutation, using a coalescent approach. An inclusive fitness formulation with coefficient of relatedness between a focal individual J affecting the reproductive success of an individual I, defined as the expected fraction of genes in I that are identical by descent to one or more genes in J in a neutral infinite population, given that J is allozygous or autozygous, yields the correct selection drift functions. These are analogous to the selection drift functions obtained with pure viability selection in a population with inbreeding. They give the changes of the allele frequencies in an infinite population without mutation that correspond to the replicator equation with fitness matrix expressed as a linear combination of a symmetric matrix for allozygous individuals and a rank-one matrix for autozygous individuals. In the case of no inbreeding, the mean inclusive fitness is a strict Lyapunov function with respect to this deterministic dynamics. Connections are made between dispersal with exact replacement (proportional dispersal), uniform dispersal, and local extinction and recolonization. The timing of dispersal (before or after selection, before or after mating) is shown to have an effect on group competition and the effective population size. In memory of Sam Karlin.     

Fluctuation in the physical environment as a mechanism for reinforcing evolutionary transitions

We hypothesize a mechanism for reinforcing transitions between levels of selection, involving physiological homeostasis and amplification of variation in the physical environment. Groups experience a stronger selection pressure than individuals for homeostasis with respect to reproductively limiting variables, because their greater longevity exposes them more often to suboptimal physical conditions, and greater physical size means they encompass a larger fraction of any resource/nutrient gradient. Groups achieve homeostasis by differentiation into microcosms with specialist functions, e.g. cell types. Such differentiation is more limited in individuals due to their smaller size and shorter lifespan. Hence tolerance of fluctuation in certain physical variables is proposed to be weaker in individuals than in groups. We show that a trait providing increased tolerance (alpha) to fluctuation (V-V(opt)) in a limiting abiotic variable (V), at relative fitness cost (C), can increase from rarity if the condition alpha.mid R:V-V(opt)|>C is met. Groups also sequester larger absolute quantities of resource than individuals, and group death is less frequent, hence the population dynamics of groups cause resource/nutrient availability to fluctuate with greater amplitude than that of individuals. Increasing the amplitude of fluctuation in a reproductively limiting environmental variable is proposed as a mechanism by which a group can limit reproduction of parasitic "cheat" individuals. Enhancing physical fluctuation is frequency dependent, hence only an increase in tolerance to fluctuation can explain the group's increase from rarity. However, once groups reach intermediate frequencies, a positive feedback process can be initiated in which a differentiated group enhances physical fluctuation beyond the tolerance of any "cheat", and in so doing enhances the selection pressure it experiences for homeostasis. This may help explain the persistence of transitions in individuality, and the coincidence of some such transitions with periods of change and oscillation in global scale environmental variables.     

The different limits of weak selection and the evolutionary dynamics of finite populations

Evolutionary theory often resorts to weak selection, where different individuals have very similar fitness. Here, we relate two ways to introduce weak selection. The first considers evolutionary games described by payoff matrices with similar entries. This approach has recently attracted a lot of interest in the context of evolutionary game dynamics in finite populations. The second way to introduce weak selection is based on small distances in phenotype space and is a standard approach in kin-selection theory. Whereas both frameworks are interchangeable for constant fitness, frequency-dependent selection shows significant differences between them. We point out the difference between both limits of weak selection and discuss the condition under which the differences vanish. It turns out that this condition is fulfilled by the popular parametrization of the prisoner's dilemma in benefits and costs. However, for general payoff matrices differences between the two frameworks prevail.     

Human Beings as Evolved Nepotists

Inclusive fitness theory provides a compelling explanation for the evolution of altruism among kin. However, a completely satisfactory account of non-kin altruism is still lacking. The present study compared the level of altruism found among siblings with that found among friends and mates and sought to reconcile the findings with an evolutionary explanation for human altruism. Participants (163 males and 156 females) completed a questionnaire about help given to a sibling, friend, or mate. Overall, participants gave friends and mates as much or more help than they gave siblings. However, as the cost of help increased, siblings received a progressively larger share of the help, whereas friends and mates received a progressively smaller share, despite the fact that participants were closer emotionally to friends and mates than they were to siblings. These findings help to explain the relative standing of friends and mates as recipients of altruistic aid.

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.     

Allomothering behaviour of new and old world monkeys

The holding or transferring of newborn infants at less than 1 month old by individuals other than the mothers was studied in 24 species of New and Old World monkeys under captive conditions. The observed monkey species could be divided into two types. Group A included eight species of three families where the mothers were tolerant to ‘infant transfer’ and readily retrieved their infants from other individuals, the frequency of infant transfer being high. The infant transfer of this group was termed allomothering behaviour. Group B included 16 species of two families where infant transfer did not occur at all or its frequency was very low and the mothers were possessive of their infants. Once transfer did occur, the infant could not be reclaimed with ease. The relationships between the two groups and taxonomic status, life forms and social types were evaluated in a total of 45 species from the present study and the literature. Correspondences were found with social type and taxonomic status. That is, species of Group A were seen only in the family or one-male type, except for one species, although none of this group appeared in the Cercopithecinae regardless of social types. The significance of infant transfer is discussed in relation to the participants' responses to it and the correlations between the two groups and social types.