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 evolution of altruism: Correlation,cost, and benefit

A simple and general criterion is derived for the evolution of altruism when individuals interact in pairs. It is argued that the treatment of this problem in kin selection theory and in game theory are special cases of this general criterion.My thanks to James Crow, Carter Denniston, Lee Dugarkin, David Wilson, and an anonymous referee of this journal for helpful discussion.     

Grooming and group cohesion in primates: implications for the evolution of language

It is well established that allogrooming, which evolved for a hygienic function, has acquired an important derived social function in many primates. In particular, it has been postulated that grooming may play an essential role in group cohesion and that human language, as verbal grooming or gossip, evolved to maintain group cohesion in the hominin lineage with its unusually large group sizes. Here, we examine this group cohesion hypothesis and test it against the alternative grooming-need hypothesis which posits that rates of grooming are higher in species where grooming need (i.e. the motivation to groom for hygiene and its associated psychological reward) is more pronounced. This alternative predicts that the derived social function of grooming evolved mostly in those lineages that had the highest exposure to ectoparasites and dirt, i.e. terrestrial species. A detailed comparative analysis of 74 species of wild primates, controlling for phylogenetic non-independence, showed that terrestriality was a highly significant predictor of allogrooming time, consistent with the prediction. The predictions of the group cohesion hypothesis were not supported, however. Group size did not predict grooming time across primates, nor did it do so in separate intra-population analyses in 17 species. Thus, there is no comparative support for the group-cohesion function of allogrooming, which questions the role of grooming in the evolution of human language.     

The evolution of extreme altruism and inequality in insect societies

In eusocial organisms, some individuals specialize in reproduction and others in altruistic helping. The evolution of eusociality is, therefore, also the evolution of remarkable inequality. For example, a colony of honeybees (Apis mellifera) may contain 50 000 females all of whom can lay eggs. But 100 per cent of the females and 99.9 per cent of the males are offspring of the queen. How did such extremes evolve? Phylogenetic analyses show that high relatedness was almost certainly necessary for the origin of eusociality. However, even the highest family levels of kinship are insufficient to cause the extreme inequality seen in e.g. honeybees via ‘voluntary altruism’. ‘Enforced altruism’ is needed, i.e. social pressures that deter individuals from attempting to reproduce. Coercion acts at two stages in an individual''s life cycle. Queens are typically larger so larvae can be coerced into developing into workers by being given less food. Workers are coerced into working by ‘policing’, in which workers or the queen eat worker-laid eggs or aggress fertile workers. In some cases, individuals rebel, such as when stingless bee larvae develop into dwarf queens. The incentive to rebel is strong as an individual is the most closely related to its own offspring. However, because individuals gain inclusive fitness by rearing relatives, there is also a strong incentive to ‘acquiesce’ to social coercion. In a queenright honeybee colony, the policing of worker-laid eggs is very effective, which results in most workers working instead of attempting to reproduce. Thus, extreme altruism is due to both kinship and coercion. Altruism is frequently seen as a Darwinian puzzle but was not a puzzle that troubled Darwin. Darwin saw his difficulty in explaining how individuals that did not reproduce could evolve, given that natural selection was based on the accumulation of small heritable changes. The recognition that altruism is an evolutionary puzzle, and the solution was to wait another 100 years for William Hamilton.     

Population viscosity and the evolution of altruism

The term population viscosity refers to limited dispersal, which increases the genetic relatedness of neighbors. This effect both supports the evolution of altruism by focusing the altruists' gifts on relatives of the altruist, and also limits the extent to which altruism may emerge by exposing clusters of altruists to stiffer local competition. Previous analyses have emphasized the way in which these two effects can cancel, limiting the viability of altruism. These papers were based on models in which total population density was held fixed. We present here a class of models in which population density is permitted to fluctuate, so that patches of altruists are supported at a higher density than patches of non-altruists. Under these conditions, population viscosity can support the selection of both weak and strong altruism.     

Kin recognition and the evolution of altruism

In 1964, Hamilton formalized the idea of kin selection to explain the evolution of altruistic behaviours. Since then, numerous examples from a diverse array of taxa have shown that seemingly altruistic actions towards close relatives are a common phenomenon. Although many species use kin recognition to direct altruistic behaviours preferentially towards relatives, this important aspect of social biology is less well understood theoretically. I extend Hamilton's classic work by defining the conditions for the evolution of kin-directed altruism when recognizers are permitted to make acceptance (type I) and rejection (type II) errors in the identification of social partners with respect to kinship. The effect of errors in recognition on the evolution of kin-directed altruism depends on whether the population initially consists of unconditional altruists or non-altruists (i.e. alternative forms of non-recognizers). Factors affecting the level of these error rates themselves, their evolution and their long-term stability are discussed.     

Models of the evolution of altruism

There are two ways of calculating the spread of a gene for altruism. One, originally proposed by Hamilton, is to allow for the effects of the gene on the survival and reproduction of collateral relatives of the individual carrying it (i.e., “inclusive fitness”); this leads to the condition k > 1/r for the spread of the gene, where k is a benefit/cost ratio. The other is to count only the direct offspring of a carrier, but to allow for the altruistic acts performed toward the carrier by its relatives (“neighbour modulated fitness” or “personal fitness”). A recent personal fitness model (L. L. Cavalli Sforza and M. W. Feldman, 1978, Theor. Pop. Biol.14, 268–280) analyses parent-offspring and sib-sib altruism and concludes that k > 1/r is applicable only when fitness components are combined additively. The present paper analyses some simple models in which the phenotypic effects are carefully specified. It is concluded that it is sometimes, but not always, appropriate to combine fitness components additively. The relative roles of inclusive and personal fitness models are compared. The former have the virtue of being easier to think about in causal terms; and the latter of incorporating the evolution of altruism into the corpus of population genetics as an example of frequency-dependent selection.     

Questioning the cultural evolution of altruism

The evolutionary foundations of helping among nonkin in humans have been the object of intense debates in the past decades. One thesis has had a prominent influence in this debate: the suggestion that genuine altruism, strictly defined as a form of help that comes at a net fitness cost for the benefactor, might have evolved owing to cultural transmission. The gene–culture coevolution literature is wont to claim that cultural evolution changes the selective pressures that normally act to limit the emergence of altruistic behaviours. This paper aims to recall, however, that cultural transmission yields altruism only to the extent that it relies on maladaptive mechanisms, such as conformist imitation and (in some cases) payoff‐biased transmission. This point is sometimes obscured in the literature by a confusion between genuine altruism, maladaptive by definition, and mutualistic forms of cooperation, that benefit all parties in the long run. Theories of cultural altruism do not lift the selective pressures weighing on strictly altruistic actions; they merely shift the burden of maladaptation from social cognition to cultural transmission.     

The evolution of altruism between siblings: Hamilton's rule revisited

This paper explores the validity of Hamilton's rule in the case of other-only altruism in which the benefits are shared by other members of the sibling group excluding the donor. It presents a model of competition between two alleles which code for different kinds of altruism. It derives a simple replicator equation for allele frequencies under conditions of strong selection. This equation does not depend on the size of the sibling group. In mathematical form, the equation is similar to Hamilton's original rule in the case of inbreeding, although the causal mechanism is different. The paper derives a simple criterion to determine whether there will be a polymorphism in which both alleles coexist permanently. Such an event is rare and victory will normally go to the allele with the higher value of 1/2b-c, where b is the total benefit which an offspring confers on its siblings and c is the cost to the donor. The paper also considers how an offspring will behave in particular circumstances. Using a specialized version of the basic model, it shows how, in the absence of polymorphism, natural selection should take the system towards the point of 50% marginal altruism. With this type of altruism, an offspring will perform any act for which the expected cost to the donor is at most half the expected benefit to its siblings. Acts which do not satisfy this criterion are not performed. This accords with Haldane's quip that he would sacrifice his own life for two of his brothers, but not for less. Numerical simulation is used to explore these issues in greater depth. The paper also examines briefly the implications of heterozygote advantage for Hamilton's rule. It concludes with a brief discussion of the connection between other-only altruism and whole-group altruism, in which the donor gains some benefit from its actions.     

Urbanization and the temporal patterns of social networks and group foraging behaviors

Urbanization causes dramatic and rapid changes to natural environments, which can lead the animals inhabiting these habitats to adjust their behavioral responses. For social animals, urbanized environments may alter group social dynamics through modification of the external environment (e.g., resource distribution). This might lead to changes in how individuals associate or engage in group behaviors, which could alter the stability and characteristics of social groups. However, the potential impacts of urban habitat use, and of habitat characteristics in general, on the nature and stability of social associations remain poorly understood. Here, we quantify social networks and dynamics of group foraging behaviors of black‐capped chickadees (N = 82, Poecile atricapillus), at four urban and four rural sites weekly throughout the nonbreeding season using feeders with radio frequency identification of individual birds. Because anthropogenic food sources in urban habitats (e.g., bird feeders) provide abundant and reliable resources, we predicted that social foraging associations may be of less value in urban groups, and thus would be less consistent than in rural groups. Additionally, decreased variability of food resources in urban habitats could lead to more predictable foraging patterns (group size, foraging duration, and the distribution of foraging events) in contrast to rural habitats. Networks were found to be highly consistent through time in both urban and rural habitats. No significant difference was found in the temporal clumping of foraging events between habitats. However, as predicted, the repeatability of the clumping of foraging events in time was significantly higher in urban than rural habitats. Our results suggest that individuals living in urban areas have more consistent foraging behaviors throughout the nonbreeding season, whereas rural individuals adjust their tactics due to less predictable foraging conditions. This first examination of habitat‐related differences in the characteristics and consistency of social networks along an urbanization gradient suggests that anthropic habitat use results in subtle modifications in social foraging patterns. Future studies should examine potential implications of these differences for variation in predation risk, energy intake, and information flow.     

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.     

The evolution of trans-generational altruism: kin selection meets niche construction

A cornerstone result of sociobiology states that limited dispersal can induce kin competition to offset the kin selected benefits of altruism. Several mechanisms have been proposed to circumvent this dilemma but all assume that actors and recipients of altruism interact during the same time period. Here, this assumption is relaxed and a model is developed where individuals express an altruistic act, which results in posthumously helping relatives living in the future. The analysis of this model suggests that kin selected benefits can then feedback on the evolution of the trait in a way that promotes altruistic helping at high rates under limited dispersal. The decoupling of kin competition and kin selected benefits results from the fact that by helping relatives living in the future, an actor is helping individuals that are not in direct competition with itself. A direct consequence is that behaviours which actors gain by reducing the common good of present and future generations can be opposed by kin selection. The present model integrates niche-constructing traits with kin selection theory and delineates demographic and ecological conditions under which altruism can be selected for; and conditions where the 'tragedy of the commons' can be reduced.     

Neoproterozoic 'snowball Earth' glaciations and the evolution of altruism

We hypothesize that a demographic and ecological effect of Neoproterozoic ‘snowball Earth’ glaciations was to increase the fitness of group‐level traits and consequently the likelihood of the evolution of macroscopic form. Extreme and repeated founder effects raised genetic relatedness – and therefore the influence of kin selection on the individuals within a group. This was permissive for the evolution of some highly costly altruistic traits, including those for macroscopic differentiation. In some eukaryotic species, the harsh and fluctuating abiotic conditions made a macroscopic physiology advantageous, perhaps necessary, for collective survival. This caused population‐wide group viability selection, whereby non‐altruist ‘cheat’ genotypes killed the groups they were in, and therefore themselves, by reaching fixation. Furthermore, dispersal between refugia would reach zero under anything near a ‘hard snowball’, which would protect altruists at high local frequency from the influx of cheats from neighbouring groups. We illustrate our hypothesis analytically and with a simple spatial model. We show how removal of between‐group dispersal, in a population with initial between‐group variation in cheat frequency, causes the relative frequency of altruists to increase while the population as a whole decreases in size, as a result of group death caused by cheat invasion. This may be of particular relevance to animal multicellularity because irreversible differentiation (highly altruistic in that it imposes a high fitness cost on the individual cell) is more prevalent than in other multicellular eukaryotes. The relevance of our hypothesis should be scaled by any future consensus on the severity of snowball Earth, but it is theoretically plausible that global‐scale glaciations had a systematic influence on the level of selection during Earth history.     

The evolution of altruism: game theory in multilevel selection and inclusive fitness

Although the prisoner's dilemma (PD) has been used extensively to study reciprocal altruism, here we show that the n-player prisoner's dilemma (NPD) is also central to two other prominent theories of the evolution of altruism: inclusive fitness and multilevel selection. An NPD model captures the essential factors for the evolution of altruism directly in its parameters and integrates important aspects of these two theories such as Hamilton's rule, Simpson's paradox, and the Price covariance equation. The model also suggests a simple interpretation of the Price selection decomposition and an alternative decomposition that is symmetrical and complementary to it. In some situations this alternative shows the temporal changes in within- and between-group selection more clearly than the Price equation. In addition, we provide a new perspective on strong vs. weak altruism by identifying their different underlying game structures (based on absolute fitness) and showing how their evolutionary dynamics are nevertheless similar under selection (based on relative fitness). In contrast to conventional wisdom, the model shows that both strong and weak altruism can evolve in periodically formed random groups of non-conditional strategies if groups are multigenerational. An integrative approach based on the NPD helps unify different perspectives on the evolution of altruism.     

Effects of information and group structure on evolution of altruism: analysis of two-score model by covariance and contextual analyses

An altruistic individual has to gamble on cooperation to a stranger because it does not know whether the stranger is trustworthy before direct interaction. Nowak and Sigmund (Nature 393 (1998a) 573; J. Theor. Biol. 194 (1998b) 561) presented a new theoretical framework of indirect reciprocal altruism by image scoring game where all individuals are informed about a partner's behavior from its image score without direct interaction. Interestingly, in a simplified version of the image scoring game, the evolutionarily stability condition for altruism became a similar form of Hamilton's rule, i.e. inequality that the probability of getting correct information is more than the ratio of cost to benefit. Since the Hamilton's rule was derived by evolutionarily stable analysis, the evolutionary meaning of the probability of getting correct information has not been clearly examined in terms of kin and group selection. In this study, we applied covariance analysis to the two-score model for deriving the Hamilton's rule. We confirmed that the probability of getting correct information was proportional to the bias of altruistic interactions caused by using information about a partner's image score. The Hamilton's rule was dependent on the number of game bouts even though the information reduced the risk of cooperation to selfish one at the first encounter. In addition, we incorporated group structure to the two-score model to examine whether the probability of getting correct information affect selection for altruism by group selection. We calculated a Hamilton's rule of group selection by contextual analysis. Group selection is very effective when either the probability of getting correct information or that of future interaction, or both are low. The two Hamilton's rules derived by covariance and contextual analyses demonstrated the effects of information and group structure on the evolution of altruism. We inferred that information about a partner's behavior and group structure can produce flexible pathways for the evolution of altruism.