Genetic relatedness in viscous populations

Summary Hamilton's inclusive fitness rule shows that the evolution of altruism is facilitated by high genetic relatedness of altruists to their beneficiaries. But the evolution of altruism is inhibited when the beneficiaries are also close competitors of the altruist, as will often be true in structured or viscous populations. However, Hamilton's rule still gives the correct condition for the evolution of altruism if relatedness is measured with respect to the local competitive neighbourhood.     

Relatedness with different interaction configurations

In an inclusive fitness model of social behaviour, a key concept is that of the relatedness between two interactants. This is typically calculated with reference to a “focal” actor taken to be representative of all actors, but when there are different interaction configurations, relatedness must be constructed as an average over all such configurations. We provide an example of such a calculation in an island model with local reproduction but global mortality, leading to variable island size and hence variable numbers of individual interactions. We find that the analysis of this example significantly sharpens our understanding of relatedness. As an application, we obtain a version of Hamilton's rule for a tag-based model of altruism in a randomly mixed population. For large populations, the selective advantage of altruism is enhanced by low (but not too low) tag mutation rates and large numbers of tags. For moderate population sizes and moderate numbers of tags, we find a window of tag mutation rates with critical benefit/cost ratios of between 1 and 3.     

Lower group productivity under kin-selected reproductive altruism

Abstract Hamilton's rule provides the foundation for understanding the genetic evolution of social behavior, showing that altruism is favored by increased relatedness and increased productivity of altruists. But how likely is it that a new altruistic mutation will satisfy Hamilton's rule by increasing the reproductive efficiency of the group? Altruism per se does not improve efficiency, and hence we would not expect a typical altruistic mutation to increase the mean productivity of the population. We examined the conditions under which a mutation causing reproductive altruism can spread when it does not increase productivity. We considered a population divided into temporary groups of genetically similar individuals (typically family groups). We show that the spread of altruism requires a pleiotropic link between altruism and enhanced productivity in diploid organisms, but not in haplodiploid organisms such as Hymenoptera. This result provides a novel biological understanding of the barrier to the spread of reproductive altruism in diploids. In haplodiploid organisms, altruism within families that lowers productivity may spread, provided daughters sacrifice their own reproduction to raise full‐sisters. We verified our results using three single‐locus genetic models that explore a range of the possible reproductive costs of helping. The advantage of female‐to‐female altruism in haplodiploids is a well‐known prediction of Hamilton's rule, but its importance in relaxing the linkage between altruism and efficiency has not been explored. We discuss the possible role of such unproductive altruism in the origins of sociality. We also note that each model predicts a large region of parameter space were polymorphism between altruism and selfishness is maintained, a pattern independent of dominance.     

Altruism in insect societies and beyond: voluntary or enforced?

The altruism of insect workers has puzzled researchers for decades. Inclusive fitness theory suggests that high relatedness has been key in promoting such altruism. Recent theory, however, indicates that the intermediate levels of relatedness found within insect societies are too low to directly cause the extreme altruism observed in many species. Instead, recent results show that workers are frequently coerced into acting altruistically. Hence, the altruism seen in many modern-day insect societies is not voluntary but enforced. Here, we also consider the role of coercion in promoting altruism and cooperation in other social systems, such as vertebrate and human societies, and interspecific mutualisms.     

Altruism can evolve when relatedness is low: evidence from bacteria committing suicide upon phage infection

High relatedness among interacting individuals has generally been considered a precondition for the evolution of altruism. However, kin-selection theory also predicts the evolution of altruism when relatedness is low, as long as the cost of the altruistic act is minor compared with its benefit. Here, we demonstrate evidence for a low-cost altruistic act in bacteria. We investigated Escherichia coli responding to the attack of an obligately lytic phage by committing suicide in order to prevent parasite transmission to nearby relatives. We found that bacterial suicide provides large benefits to survivors at marginal costs to committers. The cost of suicide was low, because infected cells are moribund, rapidly dying upon phage infection, such that no more opportunity for reproduction remains. As a consequence of its marginal cost, host suicide was selectively favoured even when relatedness between committers and survivors approached zero. Altogether, our findings demonstrate that low-cost suicide can evolve with ease, represents an effective host-defence strategy, and seems to be widespread among microbes. Moreover, low-cost suicide might also occur in higher organisms as exemplified by infected social insect workers leaving the colony to die in isolation.     

Altruism, cheating, and anticheater adaptations in cellular slime molds

Cellular slime molds (CSMs) possess a remarkable life cycle that encompasses an extreme act of altruism. CSM cells live as individual amoebae until starved, then aggregate and ultimately transform themselves into a multicellular fruiting body. This fruiting body consists of stalk cells (altruists that eventually die) and spores (the beneficiaries of this sacrifice). Altruistic systems such as this are vulnerable to cheaters, which are individuals unrelated to the altruists that obtain the benefits provided by them without reciprocating. Here, we investigate two forces that can maintain CSM altruism despite cheating: kin selection and anticheater adaptations. First, we present new kinship-based models based on CSM developmental biology to evaluate the efficacy of kin selection. These models show that stalk-making genotypes can still be maintained when aggregations are initiated by multiple "founder" spores, provided that spores of stalkless fruiting bodies have low rates of dispersal and dispersal success is a concave function of stalk height. Second, we review proposals that several features of CSM development, such as the chemical suppression of the redifferentiation of prestalk cells into prespores, act as anticheater adaptations.     

Cultural transmission and the evolution of human behaviour: a general approach based on the Price equation

Transmitted culture can be viewed as an inheritance system somewhat independent of genes that is subject to processes of descent with modification in its own right. Although many authors have conceptualized cultural change as a Darwinian process, there is no generally agreed formal framework for defining key concepts such as natural selection, fitness, relatedness and altruism for the cultural case. Here, we present and explore such a framework using the Price equation. Assuming an isolated, independently measurable culturally transmitted trait, we show that cultural natural selection maximizes cultural fitness, a distinct quantity from genetic fitness, and also that cultural relatedness and cultural altruism are not reducible to or necessarily related to their genetic counterparts. We show that antagonistic coevolution will occur between genes and culture whenever cultural fitness is not perfectly aligned with genetic fitness, as genetic selection will shape psychological mechanisms to avoid susceptibility to cultural traits that bear a genetic fitness cost. We discuss the difficulties with conceptualizing cultural change using the framework of evolutionary theory, the degree to which cultural evolution is autonomous from genetic evolution, and the extent to which cultural change should be seen as a Darwinian process. We argue that the nonselection components of evolutionary change are much more important for culture than for genes, and that this and other important differences from the genetic case mean that different approaches and emphases are needed for cultural than genetic processes.     

Altruism via kin-selection strategies that rely on arbitrary tags with which they coevolve

Hamilton's rule explains when natural selection will favor altruism between conspecifics, given their degree of relatedness. In practice, indicators of relatedness (such as scent) coevolve with strategies based on these indicators, a fact not included in previous theories of kin recognition. Using a combination of simulation modeling and mathematical extension of Hamilton's rule, we demonstrate how altruism can emerge and be sustained in a coevolutionary setting where relatedness depends on an individual's social environment and varies from one locus to another. The results support a very general expectation of widespread, and not necessarily weak, conditional altruism in nature.     

SPATIAL DISTRIBUTION OF A PRIMITIVELY SOCIAL BEE: DOES GENETIC POPULATION STRUCTURE FACILITATE ALTRUISM?

Exoneura bicolor is a univoltine, facultatively social bee exhibiting a solitary/quasisocial/semisocial colony polymorphism (Schwarz, 1986, 1987). Intracolony relatedness in semisocial colonies has been previously estimated at 0.49 ± 0.06 (Schwarz, 1987), although the crucial relatedness between altruists and the brood that they rear will be about half this value. This value is unlikely to be increased by the preferential rearing of only close relatives (Schwarz, 1988a) and no known morphological specializations preclude workers from reproducing in this species. Hamilton (1972, 1975) suggested that relatedness may be increased through population subdivision, if this leads to significant inbreeding and increased between-colony genetic variance. The same process may also operate at higher levels of population structure (e.g., Wade, 1978). Population structure and intracolony relatedness in E. bicolor were investigated in seven localities in southern Victoria, Australia, to determine if inbreeding at any level of population structure was contributing to relatedness between altruists and beneficiaries within these colonies. Population structure was described using hierarchical F-statistics and an identity by descent measure, developed by Queller and Goodnight (1989), was used to estimate intracolony relatedness. It was found that inbreeding was not contributing to between-group genetic variance, at any level, in a consistent manner across localities. Therefore relatedness, considered in isolation, does not seem sufficient to account for the presence of worker behavior. It is suggested that large benefits for group living may be responsible for maintaining altruistic behavior, in part, in this species. Significant heterogeneity among localities for all F-statistics estimated in our analysis was found and this may be attributable to stochastic elements such as cofounding behavior and the low percentage of males in the brood. The possible consequences of such heterogeneity in population structure for the maintenance of altruism in E. bicolor are discussed.     

Deleterious mutation and the evolution of eusociality

Abstract.— Certain arguments concerning the evolution of eusociality form a classic example of the application of the principles of kin selection. These arguments center on the different degrees of relatedness of potential beneficiaries of an individual's efforts, for example a female's higher relatedness to her sisters than to her daughters in a haplodiploid system. This type of reasoning is insufficient to account for the evolution and maintainence of sexual reproduction, because parthenogenic females produce offspring that are more closely related to them than are offspring produced sexually. Among the forces invoked to explain sexual reproduction is deleterious mutation. This factor can be shown to favor eusociality as well, because siblings produced by helping carry fewer deleterious alleles on average than would offspring. The strength of this effect depends on the genomewide deleterious mutation rate, U, and on the selection coefficient, s, associated with deleterious alleles. For small s, the effect depends approximately on the product Us. This phenomenon illustrates that an assumption implicit in some analyses–that the relatedness of an individual to an actor is all that matters to its value to that actor–can fail for the evolution of eusociality as it does for the evolution of sex.     

Are individuals really subordinated to genes? A theory of living entities

Modern evolutionary theory consists of an explicit theory of change and an implicit theory of the existence of living entities. A theory of the latter type, called the theory of the process of living (POL), is proposed. It contains a two-level definition of living entities, an analysis of possible and impossible similarity and differences between parents and offspring, and a logical division of the information governing the functioning of a living organism. The theory of POL emphasizes the proceeding of living entities in time while the modern evolutionary theory emphasizes the types of entities proceeding in time. The theory of POL produces a basis for reanalysing relations between individuals, their genes and the environment. It produces some predictions deviating from classic evolutionary theory. These conflicts occur in areas where analyses of genetic dynamics have made implicit assumptions of rules of POL. For example, the theory of POL states that the genetic relatedness of successive generations is a technical solution more than the reason of reproduction, that genetic relatedness as such does not imply altruism between individuals and that genes are the tools whereby organisms exist and not the contrary. Implications of the theory of POL on paradoxes of evolutionary theory are discussed.     

INTERACTING PHENOTYPES AND THE EVOLUTIONARY PROCESS. III. SOCIAL EVOLUTION

Interactions among conspecifics influence social evolution through two distinct but intimately related paths. First, they provide the opportunity for indirect genetic effects (IGEs), where genes expressed in one individual influence the expression of traits in others. Second, interactions can generate social selection when traits expressed in one individual influence the fitness of others. Here, we present a quantitative genetic model of multivariate trait evolution that integrates the effects of both IGEs and social selection, which have previously been modeled independently. We show that social selection affects evolutionary change whenever the breeding value of one individual covaries with the phenotype of its social partners. This covariance can be created by both relatedness and IGEs, which are shown to have parallel roles in determining evolutionary response. We show that social selection is central to the estimation of inclusive fitness and derive a version of Hamilton's rule showing the symmetrical effects of relatedness and IGEs on the evolution of altruism. We illustrate the utility of our approach using altruism, greenbeards, aggression, and weapons as examples. Our model provides a general predictive equation for the evolution of social phenotypes that encompasses specific cases such as kin selection and reciprocity. The parameters can be measured empirically, and we emphasize the importance of considering both IGEs and social selection, in addition to relatedness, when testing hypotheses about social evolution.     

Relatedness and the fraternal major transitions

Many of the major transitions in evolution involved the coalescence of independent lower-level units into a higher organismal level. This paper examines the role of kinship, focusing on the transitions to multicellularity in animals and to coloniality in insects. In both, kin selection based on high relatedness permitted cooperation and a reproductive division of labour. The higher relatedness of haplodiploid females to their sisters than to their offspring might not have been crucial in the origin of insect societies, and the transition to multicellularity shows that such special relationships are not required. When multicellular forms develop from a single cell, selfish conflict is minimal because each selfish mutant obtains only one generation of within-individual advantage in a chimaera. Conditionally expressed traits are particularly immune to within-individual selfishness because such mutations are rarely expressed in chimaeras. Such conditionally expressed altruism genes lead easily to the evolution of the soma, and the germ line might simply be what is left over. In most social insects, differences in relatedness ensure that there will be potential conflicts. Power asymmetries sometimes lead to such decisive settlements of conflicts that social insect colonies can be considered to be fully organismal.     

Gene mobility and the concept of relatedness

Cooperation is rife in the microbial world, yet our best current theories of the evolution of cooperation were developed with multicellular animals in mind. Hamilton’s theory of inclusive fitness is an important case in point: applying the theory in a microbial setting is far from straightforward, as social evolution in microbes has a number of distinctive features that the theory was never intended to capture. In this article, I focus on the conceptual challenges posed by the project of extending Hamilton’s theory to accommodate the effects of gene mobility. I begin by outlining the basics of the theory of inclusive fitness, emphasizing the role that the concept of relatedness is intended to play. I then provide a brief history of this concept, showing how, over the past fifty years, it has departed from the intuitive notion of genealogical kinship to encompass a range of generalized measures of genetic similarity. I proceed to argue that gene mobility forces a further revision of the concept. The reason in short is that, when the genes implicated in producing social behaviour are mobile, we cannot talk of an organism’s genotype simpliciter; we can talk only of an organism’s genotype at a particular stage in its life cycle. We must therefore ask: with respect to which stage(s) in the life cycle should relatedness be evaluated? For instance: is it genetic similarity at the time of social interaction that matters to the evolution of social behaviour, or is it genetic similarity at the time of reproduction? I argue that, strictly speaking, it is neither of these: what really matters to the evolution of social behaviour is diachronic genetic similarity between the producers of fitness benefits at the time they produce them and the recipients of those benefits at the end of their life-cycle. I close by discussing the implications of this result. The main payoff is that it makes room for a possible new mechanism for the evolution of altruism in microbes that does not require correlated interaction among bearers of the genes for altruism. The importance of this mechanism in nature remains an open empirical question.     

Environmentally induced responses co-opted for reproductive altruism

Reproductive altruism is an extreme form of altruism best typified by sterile castes in social insects and somatic cells in multicellular organisms. Although reproductive altruism is central to the evolution of multicellularity and eusociality, the mechanistic basis for the evolution of this behaviour is yet to be deciphered. Here, we report that the gene responsible for the permanent suppression of reproduction in the somatic cells of the multicellular green alga, Volvox carteri, evolved from a gene that in its unicellular relative, Chlamydomonas reinhardtii, is part of the general acclimation response to various environmental stress factors, which includes the temporary suppression of reproduction. Furthermore, we propose a model for the evolution of soma, in which by simulating the acclimation signal (i.e. a change in cellular redox status) in a developmental rather than environmental context, responses beneficial to a unicellular individual can be co-opted into an altruistic behaviour at the group level. The co-option of environmentally induced responses for reproductive altruism can contribute to the stability of this behaviour, as the loss of such responses would be costly for the individual. This hypothesis also predicts that temporally varying environments, which will select for more efficient acclimation responses, are likely to be more conducive to the evolution of reproductive altruism.     

Evolution of eusociality by kin selection: the effect of inbreeding between siblings

The effect of sib-sib inbreeding on the evolution of eusocial altruism in Hymenoptera by kin selection is examined by computer simulations. Inbreeding has minor effects on the ratio of relatedness to siblings: relatedness to offspring, but this ratio remains approximately one no matter what the degree of inbreeding. This implies that although inbreeding increases relatedness to siblings, relatedness to offspring increases to the same degree. Hence, inbreeding does not make the evolution of altruism more likely. If all the brothers of (non-mating) altruists outbreed, thereby increasing the frequency of altruism alleles in the outbred fraction of the population especially at low gene frequency, then altruism can be promoted by inbreeding. However, this is an indirect advantage, not attributable to inbreeding per se.     

Limited food induces nepotism in drywood termites

The evolution of cooperation and altruistic behaviour where individuals forego their own reproduction to help others reproduce can be explained by kin selection. Depending on the costs and benefits provided, altruism can be evolutionarily favoured if it is directed at close relatives. A considerable body of data supports the role of relatedness as a key determinant of cooperation and conflict within societies. However, the role of ecological factors and, in particular, how these costs and benefits interact with relatedness remains poorly understood. By studying 16 colonies, here I show that in a drywood termite ecological factors determine the importance of relatedness. In colonies with limited food supply, nestmates restrict cooperative interactions mainly to close relatives, while non-discriminative cooperation occurs when food is abundant. This shows for the first time directly the interaction between ecological conditions and relatedness in shaping cooperation.     

Conflict over male parentage in social insects

Mutual policing is an important mechanism that maintains social harmony in group-living organisms by suppressing the selfish behavior of individuals. In social insects, workers police one another (worker-policing) by preventing individual workers from laying eggs that would otherwise develop into males. Within the framework of Hamilton's rule there are two explanations for worker-policing behavior. First, if worker reproduction is cost-free, worker-policing should occur only where workers are more closely related to queen- than to worker-produced male eggs (relatedness hypothesis). Second, if there are substantial costs to unchecked worker reproduction, worker-policing may occur to counteract these costs and increase colony efficiency (efficiency hypothesis). The first explanation predicts that patterns of the parentage of males (male parentage) are associated with relatedness, whereas the latter does not. We have investigated how male parentage varies with colony kin structure and colony size in 50 species of ants, bees, and wasps in a phylogenetically controlled comparative analysis. Our survey revealed that queens produced the majority of males in most of the species and that workers produced more than half of the males in less than 10% of species. Moreover, we show that male parentage does not vary with relatedness as predicted by the relatedness hypothesis. This indicates that intra- and interspecific variation in male parentage cannot be accounted for by the relatedness hypothesis alone and that increased colony efficiency is an important factor responsible for the evolution of worker-policing. Our study reveals greater harmony and more complex regulation of reproduction in social insect colonies than that expected from simple theoretical expectations based on relatedness only.     

Can natural selection favour altruism between species?

Darwin suggested that the discovery of altruism between species would annihilate his theory of natural selection. However, it has not been formally shown whether between‐species altruism can evolve by natural selection, or why this could never happen. Here, we develop a spatial population genetic model of two interacting species, showing that indiscriminate between species helping can be favoured by natural selection. We then ask if this helping behaviour constitutes altruism between species, using a linear‐regression analysis to separate the total action of natural selection into its direct and indirect (kin selected) components. We show that our model can be interpreted in two ways, as either altruism within species, or altruism between species. This ambiguity arises depending on whether or not we treat genes in the other species as predictors of an individual's fitness, which is equivalent to treating these individuals as agents (actors or recipients). Our formal analysis, which focuses upon evolutionary dynamics rather than agents and their agendas, cannot resolve which is the better approach. Nonetheless, because a within‐species altruism interpretation is always possible, our analysis supports Darwin's suggestion that natural selection does not favour traits that provide benefits exclusively to individuals of other species.     

Evolution of interactions in family-structured populations: mixed mating models

THE EFFECT OF INBREEDING ON SOCIALITY IS STUDIED THEORETICALLY FOR THE EVOLUTION OF INTERACTIONS BETWEEN SIBLINGS IN CERTAIN MIXED MATING SYSTEMS THAT GIVE RISE TO INBREEDING: sib with random mating and selfing with random mating. Two approaches are taken. First, specific models of altruism are studied for the various mating systems. In the case of the additive model, inbreeding facilitates the evolution of altruistic genes. Likewise, for the multiplicative model this is usually the case, as long as the costs of altruism are not too great. Second, the case of total altruism, in which the gene has zero individual fitness but increases the fitness of associates, is studied for a general fitness formulation. In this case, inbreeding often retards the ability of such genes to increase when rare, and the equilibrium frequency of those recessive genes that can increase is totally independent of the mating system and, consequently, of the amount of inbreeding. It appears from the results presented that inbreeding facilitates most forms of altruism, but retards extreme altruism. These results stem from the fact that inbreeding increases the within-family relatedness by increasing the between-family variance in allele frequency. In most cases this facilitates altruism. However, in the case of total altruism, only heterozygotes can pass on the altruistic allele, and inbreeding tends to decrease this heterozygote class. In either case, the important effect of inbreeding lies in altering the genotypic distribution of the interactions.