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.     

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.     

Joint evolution of multiple social traits: a kin selection analysis

General models of the evolution of cooperation, altruism and other social behaviours have focused almost entirely on single traits, whereas it is clear that social traits commonly interact. We develop a general kin-selection framework for the evolution of social behaviours in multiple dimensions. We show that whenever there are interactions among social traits new behaviours can emerge that are not predicted by one-dimensional analyses. For example, a prohibitively costly cooperative trait can ultimately be favoured owing to initial evolution in other (cheaper) social traits that in turn change the cost–benefit ratio of the original trait. To understand these behaviours, we use a two-dimensional stability criterion that can be viewed as an extension of Hamilton''s rule. Our principal example is the social dilemma posed by, first, the construction and, second, the exploitation of a shared public good. We find that, contrary to the separate one-dimensional analyses, evolutionary feedback between the two traits can cause an increase in the equilibrium level of selfish exploitation with increasing relatedness, while both social (production plus exploitation) and asocial (neither) strategies can be locally stable. Our results demonstrate the importance of emergent stability properties of multidimensional social dilemmas, as one-dimensional stability in all component dimensions can conceal multidimensional instability.     

Modeling reciprocation and cooperation in primates: evidence for a punishing strategy

Experiments in which animals strategically interact with one another or search over some controlled domain are becoming common. While these experiments often promise to illuminate sophisticated animal behavior, the analyses brought to bear on these data are often quite coarse. For example, many papers simply tally the number of observations consistent with a behavioral theory. This analysis is simple, but ignores a potentially rich source of information by failing to take into account patterns and systematic variation among observations inconsistent with the theory. Using a new data set generated by cotton-top tamarin monkeys playing a repeated food-exchange game, we apply a maximum-likelihood estimation technique (more commonly used to study human economic behavior) which utilizes much more of the information in these data, and which uncovers unexpectedly sophisticated cooperative behavior from our subjects. Tamarin cooperation remains stable as long as both actors consistently cooperate, but requires at least two consecutive unexpected acts of cooperation to restart cooperation after it has collapsed, a strategy that resembles two-tits for a tat. We conclude by enumerating the benefits of a maximum-likelihood approach in experimental settings such as ours, and suggest other areas in which these techniques may be fruitful.     

Natural selection. VII. History and interpretation of kin selection theory

Kin selection theory is a kind of causal analysis. The initial form of kin selection ascribed cause to costs, benefits and genetic relatedness. The theory then slowly developed a deeper and more sophisticated approach to partitioning the causes of social evolution. Controversy followed because causal analysis inevitably attracts opposing views. It is always possible to separate total effects into different component causes. Alternative causal schemes emphasize different aspects of a problem, reflecting the distinct goals, interests and biases of different perspectives. For example, group selection is a particular causal scheme with certain advantages and significant limitations. Ultimately, to use kin selection theory to analyse natural patterns and to understand the history of debates over different approaches, one must follow the underlying history of causal analysis. This article describes the history of kin selection theory, with emphasis on how the causal perspective improved through the study of key patterns of natural history, such as dispersal and sex ratio, and through a unified approach to demographic and social processes. Independent historical developments in the multivariate analysis of quantitative traits merged with the causal analysis of social evolution by kin selection.     

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.     

Reciprocity explains food sharing in humans and other primates independent of kin selection and tolerated scrounging: a phylogenetic meta-analysis

Helping, i.e. behaviour increasing the fitness of others, can evolve when directed towards kin or reciprocating partners. These predictions have been tested in the context of food sharing both in human foragers and non-human primates. Here, we performed quantitative meta-analyses on 32 independent study populations to (i) test for overall effects of reciprocity on food sharing while controlling for alternative explanations, methodological biases, publication bias and phylogeny and (ii) compare the relative effects of reciprocity, kinship and tolerated scrounging, i.e. sharing owing to costs imposed by others. We found a significant overall weighted effect size for reciprocity of r = 0.20–0.48 for the most and least conservative measure, respectively. Effect sizes did not differ between humans and other primates, although there were species differences in in-kind reciprocity and trade. The relative effect of reciprocity in sharing was similar to those of kinship and tolerated scrounging. These results indicate a significant independent contribution of reciprocity to human and primate helping behaviour. Furthermore, similar effect sizes in humans and primates speak against cognitive constraints on reciprocity. This study is the first to use meta-analyses to quantify these effects on human helping and to directly compare humans and other primates.     

Distinctions among reciprocal altruism,kin selection,and cooperation and a model for the initial evolution of beneficent behavior

Reciprocal altruism is usually regarded as distinct from kin selection. However, because reciprocators are likely to establish long-term relations and to deliver most of their aid to other individuals genetically predisposed to reciprocation, most acts of reciprocal altruism should involve indirect increments to inclusive fitness, at least as regards alleles for reciprocation. Thus, as usually defined, reciprocal altruism is not clearly distinct from kin selection because both involve indirect increments to inclusive fitness. We propose a new definition for reciprocal altruism that makes the phenomenon distinct from kin selection and allows for reciprocation between nonrelatives in which current costs exceed future benefits returned to the reciprocal altruist. Cooperation and reciprocal altruism are often considered synonymous or different only in the timing of donating and receiving aid. We show, however, that there are other critical differences between reciprocal altruism and other forms of cooperation, most importantly, the latter often involve no clearly identifiable aid. We propose a four-category system to encompass the range of cooperative and beneficent behaviors that occur in nature (reciprocal altruism, pseudoreciprocity, simultaneous cooperation and by-product beneficence). Reciprocal altruism must involve aid that is returned to an original donor as a result of behavior that has a net cost to an original recipient. Our simplest category of cooperative/beneficent behavior, “by-product beneficence,” occurs when a selfish act also benefits another individual and requires no prior or subsequent interactions between the individuals involved. By-product beneficence may be the primitive state from which more complicated types of cooperative/beneficent behavior evolved. We show via simple models that by-product beneficence can allow for the initial increase of helping behavior in a completely unstructured population although the individuals showing such behavior pay all the costs while sharing the benefits with other individuals. Previous models that attempted to explain the initial increase of cooperative/beneficent behavior were much more complex and were based on the prisoner's dilemma, which does not accurately reflect most forms of cooperation and beneficence that occur in nature.     

The volunteer's dilemma and the optimal size of a social group

If one or few individuals are enough to perform an action that produces a collective good and if this action has a cost, living in group can be beneficial because the cost can be shared with other individuals. Without coordination, however, the production of a collective good by the contribution of one or few individuals is inefficient and can be modelled as a volunteer's dilemma. In the volunteer's dilemma the individuals that pay the cost for the production of the collective good benefit from their action if nobody else volunteers, but the cost is wasted if too many individuals volunteer. Increasing group size reduces the need of volunteering for each member of the group; the overall benefit for the group, however, decreases too because the larger the group is, the less likely it is that the collective good is produced. This problem persists even with a high degree of relatedness between group members; an optimal, intermediate group size exists that maximizes the probability to produce the collective good.     

A theoretical basis for measures of kin selection in subdivided populations: finite populations and localized dispersal

The analysis of kin selection in subdivided populations has been hampered by the lack of well‐defined measures of genealogical relatedness in the presence of localized dispersal. Furthermore, the usual arguments underlying the definition of game‐theoretical measures of inclusive fitness are not exact under localized dispersal. We define such measures to give the first‐order effects of selection on the probability of fixation of an allele. The derived measures of kin selection and relatedness are valid in finite populations and under localized dispersal. For the infinite island model, the resulting measure of kin selection is equivalent to a previously used measure. In other cases its definition is based on definitions of relatedness which are different from the usual ones. To illustrate the approach, we reanalyse a model with localized dispersal. We consider sex ratio evolution under sex‐specific dispersal behaviour, and the results confirm the earlier conclusion that the sex ratio is biased towards the sex with the dispersal rate closer to the optimal dispersal rate in the absence of sex‐specific dispersal behaviour.     

Variation and the response to variation as a basis for successful cooperation

In applying game theory to problems in biology, differences between individuals are often ignored. In particular, when analysing the evolution of cooperation it is often implicitly assumed that ignoring variation will produce predictions that approximate the solution when differences are included. This need not be true. As we demonstrate, differences are not innocuous noise, but can fundamentally change the nature of a game. Even small amounts of variability can stabilize cooperation by, for example, maintaining the need to deal with cheaters. Differences promote the need to learn about others in an interaction, leading to contingent behaviour that can reduce conflict, and to negotiated outcomes that may or may not be more cooperative than unconditional actions. Once there are mechanisms such as mutation and environmental influences that maintain variation within populations, whether cooperation evolves may depend on the variation in the cooperativeness trait. Variation means that it may be worth taking a chance that a partner is cooperative by being cooperative. When there are markets, so that individuals can break off interactions to seek a better partner, variation promotes choosiness and hence penalizes those uncooperative individuals, who are rejected. Variation promotes the need to monitor the previous behaviour of others, and once this social sensitivity exists, the need to maintain a good reputation can promote cooperation.     

The many-demes limit for selection and drift in a subdivided population

A diffusion approximation is obtained for the frequency of a selected allele in a population comprised of many subpopulations or demes. The form of the diffusion is equivalent to that for an unstructured population, except that it occurs on a longer time scale when migration among demes is restricted. This many-demes diffusion limit relies on the collection of demes always being in statistical equilibrium with respect to migration and drift for a given allele frequency in the total population. Selection is assumed to be weak, in inverse proportion to the number of demes, and the results hold for any deme sizes and migration rates greater than zero. The distribution of allele frequencies among demes is also described.     

Ribotyping of adherent Lactobacillus from weaning pigs: a basis for probiotic selection based on diet and gut compartment

Dietary inoculates for weaned pigs often include lacobacilli, but the effects of age and diet on the ecology of adherent lactobacilli are not well known. Four experimental treatments included 16 newborn piglets: a pre-weaning treatment (PW) included four pigs that were sacrificed at 28 days of age; a sow treatment (Sow) had four pigs that remained with the sow (Sow) from 28 to 38 days of age and were sacrificed at 38 days of age; and two treatments in which four pigs each, were placed on a corn-soy diet with (CSL), or without (CS) 40% lactose. Adherent lactobacilli were isolated from the pars esophagus, ileum, and cecum, and characterised phenotypically. A 23S rDNA probe hydrized toEcoRI orPstI digested DNA, and a 74.8% cut-off individualize isolates into 36 clusters. The most predominant strains found in the Sow, CSL, and CS treatments were the same, but different strains predominated in the PW animals. The most predominant strains found in the pars esophagus and ileum were the same, but different strains predominated in the cecum.     

Correlated responses to selection for stress resistance and longevity in a laboratory population of Drosophila melanogaster

Laboratory studies on Drosophila have revealed that resistance to one environmental stress often correlates with resistance to other stresses. There is also evidence on genetic correlations between stress resistance, longevity and other fitness-related traits. The present work investigates these associations using artificial selection in Drosophila melanogaster. Adult flies were selected for increased survival after severe cold, heat, desiccation and starvation stresses as well as increased heat-knockdown time and lifespan (CS, HS, DS, SS, KS and LS line sets, respectively). The number of selection generations was 11 for LS, 27 for SS and 21 for other lines, with selection intensity being around 0.80. For each set of lines, the five stress-resistance parameters mentioned above as well as longevity (in a nonstressful environment) were estimated. In addition, preadult developmental time, early age productivity and thorax length were examined in all lines reared under nonstressful conditions. Comparing the selection lines with unselected control revealed clear-cut direct selection responses for the stress-resistance traits. Starvation resistance increased as correlated response in all sets of selection lines, with the exception of HS. Positive correlated responses were also found for survival after cold shock (HS and DS) and heat shock (KS and DS). With regard to values of resistance across different stress assays, the HS and KS lines were most similar. The resistance values of the SS lines were close to those of the LS lines and tended to be the lowest among all selection lines. Developmental time was extended in the SS and KS lines, whereas the LS lines showed a reduction in thorax length. The results indicate a possibility of different multiple-stress-resistance mechanisms for the examined traits and fitness costs associated with stress resistance and longevity.     

Sexual selection and non-random mating for shell colour in a natural population of the marine snailLittorina mariae (Gastropoda: Prosobranchia)

In order to estimate the three independent components of mating behaviour, sexual selection in females, sexual selection in males and mating pattern, we studied the distribution of shell colour morphs among mating pairs and between copulating and non-copulating snails in four subsamples of a natural population ofL. mariae. The colour of the shell, the sex and a qualitative estimate of age was recorded for every snail. We found sexual selection acting against one of the two commonest colours (yellow) among the young females. However, in males none of the eight shell colour morphs was favoured during matings. Male sexual choice or differences in female sexual activity may cause the sexual fitness disadvantage of yellow females. Moreover, individuals of different colour morphs did not mate at random, rather dissasortatively. A behavioural choice among shell colour morphs or a non-random microdistribution of the morphs may cause the departure from random mating in this population.     

Fitness consequences of potential assortative mating inside and outside a hybrid zone in Chorthippus parallelus (Orthoptera: Acrididae): implications for reinforcement and sexual selection theory

We have examined the fitness consequences of random and potentially non-random matings within two populations taken from inside, and two from outside a hybrid zone in Chorthippus parallelus. When given the opportunity to mate non-randomly, females from all populations laid egg pods more quickly than females obliged to mate at random. A range of fitness parameters measured on the offspring did not show increased fitness following potential non-random mating for any population. However, in non-hybrid populations, the sons of non-randomly mated females had about twice the mating success of the sons of those females forced to mate at random, suggesting the existence of heritable variation for male reproductive success. Hybrid dysfunction did not occur amongst the offspring of randomly mated hybrid females, demonstrating that the lack of dysfunction within these populations is not due to the evolution of assortative mating within them.     

Reproductive fitness and artificial selection in animal breeding: culling on fitness prevents a decline in reproductive fitness in lines of Drosophila melanogaster selected for increased inebriation time

Summary The maintenance of reproductive fitness in lines subjected to artificial selection is one of the major problems in animal breeding. The decline in reproductive performance has neither been predictable from heritabilities and genetic correlations, nor have conventional selection indices been adequate to avoid the problem. Gowe (1983) has suggested that the heritabilities of reproductive traits are non-linear, with heritabilities being higher on the lower fitness side. Consequently, he has predicted that culling on reproductive fitness in artificial selection lines will be effective in preventing the usual declines in fitness. An experimental evaluation of Gowe's prediction has been carried out by comparing fitnesses of replicated lines of three treatments: selection for increased inebriation time without culling on fitness (HO), selection for inebriation time with culling of 20% (4/20) of selected females on reproductive fitness (HS), and unselected controls (C). Response to selection for inebriation time in the two selection treatments was similar. After 25 generations, the competitive index, a measure of reproductive fitness, was significantly lower in the HO treatment than the HS treatment, while the HS treatment did not differ from the control lines or the base population. These results demonstrate for the first time that culling on reproductive fitness in selection lines can be used to prevent the usual decline in reproductive performance.     

How can dragonflies discern bright and dark waters from a distance? The degree of polarisation of reflected light as a possible cue for dragonfly habitat selection

SUMMARY 1. Based on the findings that some dragonflies prefer either ‘dark’ or ‘bright’ water (as perceived by the human eye viewing downwards perpendicularly to the water surface), while others choose both types of water bodies in which to lay their eggs, the question arises: How can dragonflies distinguish a bright from a dark pond from far away, before they get sufficiently close to see it is bright or dark? 2. Our hypothesis is that certain dragonfly species may select their preferred breeding sites from a distance on the basis of the polarisation of reflected light. Is it that waters viewed from a distance can be classified on the basis of the polarisation of reflected light? 3. Therefore we measured, at an angle of view of 20° from the horizontal, the reflection‐polarisation characteristics of several ponds differing in brightness and in their dragonfly fauna. 4. We show that from a distance, at which the angle of view is 20° from the horizontal, dark water bodies cannot be distinguished from bright ones on the basis of the intensity or the angle of polarisation of reflected light. At a similar angle of view, however, dark waters reflect light with a significantly higher degree of linear polarisation than bright waters in any range of the spectrum and in any direction of view with respect to the sun. 5. Thus, the degree of polarisation of reflected light may be a visual cue for the polarisation‐sensitive dragonflies to distinguish dark and bright water bodies from far away. Future experimental studies should prove if dragonflies do indeed use this cue for habitat selection.     

Evaluation of alkaline pretreatment temperature on a multi-product basis for the co-production of glucose and hemicellulose based films from lignocellulosic biomass

Cotton stalks were subjected to alkaline pretreatment for the co-production of glucose and hemicellulose based films with a multi-product approach. Three pretreatment temperatures (25, 60 and 90 °C) were evaluated for their effects both on the glucose yield and on the properties of hemicellulose based films. Compared to untreated cotton stalks, the glucose yields were enhanced 3.9, 4.1 and 4.2 times for pretreatments conducted at 25, 60 and 90 °C, respectively. The pretreatment temperature of 90 °C was detrimental in terms of film formation. Tensile energy to break values of the films obtained after pretreatments conducted at 25, 60 and 90 °C were 1.1, 0.8, and 0.4 MJ/m³, respectively. The hemicellulosic part of the process, which considers the production of hemicellulose based films, should govern the pretreatment temperature since it was more responsive to the changes in the pretreatment temperature compared to the cellulosic part that accounts for glucose production.