Inclusive Fitness Theory Research Articles

Individuals and groups in evolution: Darwinian pluralism and the multilevel selection debate.

Outlined here is an updated review of the long-standing 'kin selection vs group selection' debate. Group selection is a highly contentious concept, scientifically and philosophically. In 2012, Dawkins' attack against Wilson's latest book about eusociality concentrated all the attention on group selection and its mutual exclusivity with respect to inclusive fitness theory. Both opponents seem to be wrong, facing the general consensus in the field, which favours a pluralistic approach. Historically, despite some misunderstandings in current literature, such a perspective is clearly rooted in Darwin's writings, which suggested a plurality of levels of selection and a general view that we propose to call 'imperfect selfishness'. Today, the mathematically updated hypothesis of group selection has little to do with earlier versions of 'group selection'. It does not imply ontologically unmanageable notions of 'groups'. We propose here population structure as the main criterion of compatibility between kin selection and group selection. The latter is now evidently a pattern among others within a more general 'multilevel selection' theory. Different explanations and patterns are not mutually exclusive. Such a Darwinian pluralism is not a piece of the past, but a path into the future. A challenge in philosophy of biology will be to figure out the logical structure of this emerging pluralistic theory of evolution in such contentious debates.

Inclusive fitness theory for the evolution of religion

We describe and evaluate an integrative hypothesis for the origin and evolution of human religious cognition and behaviour, based on maximization of inclusive fitness. By this hypothesis, the concept of God is represented by one's circle of kin and social salience, such that serving God and serving this circle become synonymous. The theory is supported by data from anthropology, evolutionary theory, psychology, neuroscience, psychiatry, endocrinology and genetics. It is largely compatible with, yet can subsume, previous theories of religion that are also based on adaptation and natural selection.

Fitness, inclusive fitness, and optimization

Individual-as-maximizing agent analogies result in a simple understanding of the functioning of the biological world. Identifying the conditions under which individuals can be regarded as fitness maximizing agents is thus of considerable interest to biologists. Here, we compare different concepts of fitness maximization, and discuss within a single framework the relationship between Hamilton’s (J Theor Biol 7:1–16, 1964) model of social interactions, Grafen’s (J Evol Biol 20:1243–1254, 2007a) formal Darwinism project, and the idea of evolutionary stable strategies. We distinguish cases where phenotypic effects are additive separable or not, the latter not being covered by Grafen’s analysis. In both cases it is possible to define a maximand, in the form of an objective function ϕ(z), whose argument is the phenotype of an individual and whose derivative is proportional to Hamilton’s inclusive fitness effect. However, this maximand can be identified with the expression for fecundity or fitness only in the case of additive separable phenotypic effects, making individual-as-maximizing agent analogies unattractive (although formally correct) under general situations of social interactions. We also feel that there is an inconsistency in Grafen’s characterization of the solution of his maximization program by use of inclusive fitness arguments. His results are in conflict with those on evolutionary stable strategies obtained by applying inclusive fitness theory, and can be repaired only by changing the definition of the problem.

Towards greater realism in inclusive fitness models: the case of worker reproduction in insect societies

The conflicts over sex allocation and male production in insect societies have long served as an important test bed for Hamilton's theory of inclusive fitness, but have for the most part been considered separately. Here, we develop new coevolutionary models to examine the interaction between these two conflicts and demonstrate that sex ratio and colony productivity costs of worker reproduction can lead to vastly different outcomes even in species that show no variation in their relatedness structure. Empirical data on worker-produced males in eight species of Melipona bees support the predictions from a model that takes into account the demographic details of colony growth and reproduction. Overall, these models contribute significantly to explaining behavioural variation that previous theories could not account for.

Genes underlying altruism

William D. Hamilton postulated the existence of 'genes underlying altruism', under the rubric of inclusive fitness theory, a half-century ago. Such genes are now poised for discovery. In this article, we develop a set of intuitive criteria for the recognition and analysis of genes for altruism and describe the first candidate genes affecting altruism from social insects and humans. We also provide evidence from a human population for genetically based trade-offs, underlain by oxytocin-system polymorphisms, between alleles for altruism and alleles for non-social cognition. Such trade-offs between self-oriented and altruistic behaviour may influence the evolution of phenotypic diversity across all social animals.

Seven Misconceptions About the Mereological Fallacy: A Compilation for the Perplexed

If someone commits the mereological fallacy, then he ascribes psychological predicates to parts of an animal that apply only to the (behaving) animal as a whole. This incoherence is not strictly speaking a fallacy, i.e. an invalid argument, since it is not an argument but an illicit predication. However, it leads to invalid inferences and arguments, and so can loosely be called a fallacy. However, discussions of this particular illicit predication, the mereological fallacy, show that it is often misunderstood. Many misunderstandings concern the use of this illicit predication in the course of discussions of understanding the mind/body problem. Our aim here is to provide an accessible overview through discussing common misconceptions of the fallacy. We also discuss how conceptual investigations of the relation between living organisms and their parts fit within the framework of modern evolutionary theory, i.e. inclusive fitness theory.

Inclusive fitness and the sociobiology of the genome

Inclusive fitness theory provides conditions for the evolutionary success of a gene. These conditions ensure that the gene is selfish in the sense of Dawkins (The selfish gene, Oxford University Press, Oxford, 1976): genes do not and cannot sacrifice their own fitness on behalf of the reproductive population. Therefore, while natural selection explains the appearance of design in the living world (Dawkins in The blind watchmaker: why the evidence of evolution reveals a universe without design, W. W. Norton, New York, 1996), inclusive fitness theory does not explain how. Indeed, Hamilton’s rule is equally compatible with the evolutionary success of prosocial altruistic genes and antisocial predatory genes, whereas only the former, which account for the appearance of design, predominate in successful organisms. Inclusive fitness theory, however, permits a formulation of the central problem of sociobiology in a particularly poignant form: how do interactions among loci induce utterly selfish genes to collaborate, or to predispose their carriers to collaborate, in promoting the fitness of their carriers? Inclusive fitness theory, because it abstracts from synergistic interactions among loci, does not answer this question. Fitness-enhancing collaboration among loci in the genome of a reproductive population requires suppressing alleles that decrease, and promoting alleles that increase the fitness of its carriers. Suppression and promotion are effected by regulatory networks of genes, each of which is itself utterly selfish. This implies that genes, and a fortiori individuals in a social species, do not maximize inclusive fitness but rather interact strategically in complex ways. It is the task of sociobiology to model these complex interactions.

Limitations of inclusive fitness

Until recently, inclusive fitness has been widely accepted as a general method to explain the evolution of social behavior. Affirming and expanding earlier criticism, we demonstrate that inclusive fitness is instead a limited concept, which exists only for a small subset of evolutionary processes. Inclusive fitness assumes that personal fitness is the sum of additive components caused by individual actions. This assumption does not hold for the majority of evolutionary processes or scenarios. To sidestep this limitation, inclusive fitness theorists have proposed a method using linear regression. On the basis of this method, it is claimed that inclusive fitness theory (i) predicts the direction of allele frequency changes, (ii) reveals the reasons for these changes, (iii) is as general as natural selection, and (iv) provides a universal design principle for evolution. In this paper we evaluate these claims, and show that all of them are unfounded. If the objective is to analyze whether mutations that modify social behavior are favored or opposed by natural selection, then no aspect of inclusive fitness theory is needed.

Sex ratio biases in termites provide evidence for kin selection

Inclusive fitness theory, also known as kin selection theory, is the most general expansion of Darwin's natural selection theory. It is supported by female-biased investment by workers in the social Hymenoptera where relatedness to sisters is higher than to brothers because of haplodiploidy. However, a strong test of the theory has proven difficult in diploid social insects because they lack such relatedness asymmetry. Here we show that kin selection can result in sex ratio bias in eusocial diploids. Our model predicts that allocation will be biased towards the sex that contributes more of its genes to the next generation when sex-asymmetric inbreeding occurs. The prediction matches well with the empirical sex allocation of Reticulitermes termites where the colony king can be replaced by a queen's son. Our findings open broad new avenues to test inclusive fitness theory beyond the well-studied eusocial Hymenoptera.

Queen control of a key life-history event in a eusocial insect

In eusocial insects, inclusive fitness theory predicts potential queen-worker conflict over the timing of events in colony life history. Whether queens or workers control the timing of these events is poorly understood. In the bumble-bee Bombus terrestris, queens exhibit a 'switch point' in which they switch from laying diploid eggs yielding females (workers and new queens) to laying haploid eggs yielding males. By rearing foundress queens whose worker offspring were removed as pupae and sexing their eggs using microsatellite genotyping, we found that queens kept in the complete absence of adult workers still exhibit a switch point. Moreover, the timing of their switch points relative to the start of egg-laying did not differ significantly from that of queens allowed to produce normal colonies. The finding that bumble-bee queens can express the switch point in the absence of workers experimentally demonstrates queen control of a key life-history event in eusocial insects. In addition, we found no evidence that workers affect the timing of the switch point either directly or indirectly via providing cues to queens, suggesting that workers do not fully express their interests in queen-worker conflicts over colony life history.

We were all young once: an intragenomic perspective on parent–offspring conflict

Parent-offspring conflict (POC) describes the evolutionary conflict between offspring and their parents over parental resource allocation. Offspring are expected to demand more resources than their parents are willing to supply because these offspring are more related to their own than to their siblings' offspring. Kin selection acts to limit these divergent interests. Our model departs from previous models by describing POC as an intragenomic conflict between genes determining life-history traits during infancy or parenthood. We explain why a direct fitness approach that measures the total fitness effect during exactly one generation is required to correctly assess POC in interbrood rivalry. We find that incorrect assumptions in previous models led to an overestimation of the scope of POC. Moreover, we show why the degree of monogamy is more important for POC than previously thought. Overall, we demonstrate that a life-history-centred intragenomic approach is necessary to correctly interpret POCs. We further discuss how our work relates to the current debate about the usefulness of inclusive fitness theory.

Beyond promiscuity: mate-choice commitments in social breeding.

Obligate eusociality with distinct caste phenotypes has evolved from strictly monogamous sub-social ancestors in ants, some bees, some wasps and some termites. This implies that no lineage reached the most advanced form of social breeding, unless helpers at the nest gained indirect fitness values via siblings that were identical to direct fitness via offspring. The complete lack of re-mating promiscuity equalizes sex-specific variances in reproductive success. Later, evolutionary developments towards multiple queen-mating retained lifetime commitment between sexual partners, but reduced male variance in reproductive success relative to female's, similar to the most advanced vertebrate cooperative breeders. Here, I (i) discuss some of the unique and highly peculiar mating system adaptations of eusocial insects; (ii) address ambiguities that remained after earlier reviews and extend the monogamy logic to the evolution of soldier castes; (iii) evaluate the evidence for indirect fitness benefits driving the dynamics of (in)vertebrate cooperative breeding, while emphasizing the fundamental differences between obligate eusociality and cooperative breeding; (iv) infer that lifetime commitment is a major driver towards higher levels of organization in bodies, colonies and mutualisms. I argue that evolutionary informative definitions of social systems that separate direct and indirect fitness benefits facilitate transparency when testing inclusive fitness theory.

Going that extra mile: individuals travel further to maintain face-to-face contact with highly related kin than with less related kin.

The theory of inclusive fitness has transformed our understanding of cooperation and altruism. However, the proximate psychological underpinnings of altruism are less well understood, and it has been argued that emotional closeness mediates the relationship between genetic relatedness and altruism. In this study, we use a real-life costly behaviour (travel time) to dissociate the effects of genetic relatedness from emotional closeness. Participants travelled further to see more closely related kin, as compared to more distantly related kin. For distantly related kin, the level of emotional closeness mediated this relationship - when emotional closeness was controlled for, there was no effect of genetic relatedness on travel time. However, participants were willing to travel further to visit parents, children and siblings as compared to more distantly related kin, even when emotional closeness was controlled for. This suggests that the mediating effect of emotional closeness on altruism varies with levels of genetic relatedness.

Effects of Imprinted Genes on the Development of Communicative Behavior: A Hypothesis

The kinship theory of genomic imprinting predicts that imprinted genes affect parent–child and child–child interactions. During prenatal and neonatal stages, patrigenes promote selfish and matrigenes altruistic behavior. Models predict that this imprinted gene expression pattern is reversed starting with the juvenile stage. This article explores possible effects of imprinted genes on nonverbal and simple and complex linguistic behaviors before and after the reversal. A hypothesis is discussed that is based on the observation language evolved as a new form of communicative behavior. Inclusive fitness theory is used for explaining how and why new forms of communicative behaviors evolved as an extension of behaviors and gestures displayed by our predecessors. The hypothesis is elaborated through discussing a scenario of early language evolution. This scenario is used for explaining early stages in child development and for discussing possible effects of patrigenes and matrigenes on the development of children’s communicative behaviors.

A mathematical description of the inclusive fitness theory

Recent developments in the inclusive fitness theory have revealed that the direction of evolution can be analytically predicted in a wider class of models than previously thought, such as those models dealing with network structure. This paper aims to provide a mathematical description of the inclusive fitness theory. Specifically, we provide a general framework based on a Markov chain that can implement basic models of inclusive fitness. Our framework is based on the probability distribution of “offspring-to-parent map”, from which the key concepts of the theory, such as fitness function, relatedness and inclusive fitness, are derived in a straightforward manner. We prove theorems showing that inclusive fitness always provides a correct prediction on which of two competing genes more frequently appears in the long run in the Markov chain. As an application of the theorems, we prove a general formula of the optimal dispersal rate in the Wright’s island model with recurrent mutations. We also show the existence of the critical mutation rate, which does not depend on the number of islands and below which a positive dispersal rate evolves. Our framework can also be applied to lattice or network structured populations.

J.P. Rushton’s theory of ethnic nepotism

Unreciprocated aid among co-ethnics and the emotional intensity of ethnic conflict have long been explanatory challenges to evolutionary science. J.P. Rushton’s theory of assortative ethnic affiliation–altruism, mating and friendship directed towards fellow ethnics–derives from his more general theory of genetic similarity (GST). GST proposes that humans give preferential treatment to others in whom they detect genetic resemblance and that such behavior enhances genetic fitness. The theory coincides with W.D. Hamilton’s theory of inclusive fitness as applied to relations between populations. GST helps explain core features of ethnicity, including its basis in putative kinship and correlation with gene frequencies. Ethnic nepotism due to similarity is a weak social force compared to social identity. However its pervasiveness makes it a potential driver of evolutionary and social change, a potential borne out by sociological studies of the impact of ethnic diversity on social cohesion and public altruism. Genomics confirms the theory for interactions within populations with sufficient genetic diversity, such as ethnically mixed societies. GST applied to ethnicity is promising for further research in evolutionary social science because it unifies evolutionary and behavioral mechanisms in a single theory.

Mosaic structure of native ant supercolonies

According to the inclusive fitness theory, some degree of positive relatedness is required for the evolution and maintenance of altruism. However, ant colonies are sometimes large interconnected networks of nests, which are genetically homogenous entities, causing a putative problem for the theory. We studied spatial structure and genetic relatedness in two supercolonies of the ant Formica exsecta, using nuclear and mitochondrial markers. We show that there may be multiple pathways to supercolonial social organization leading to different spatial genetic structures. One supercolony formed a genetically homogenous population dominated by a single mtDNA haplotype, as expected if founded by a small number of colonizers, followed by nest propagation by budding and domination of the habitat patch. The other supercolony had several haplotypes, and the spatial genetic structure was a mosaic of nuclear and mitochondrial clusters. Genetic diversity probably originated from long-range dispersal, and the mosaic population structure is likely a result of stochastic short-range dispersal of individuals. Such a mosaic spatial structure is apparently discordant with the current knowledge about the integrity of ant colonies. Relatedness was low in both populations when estimated among nestmates, but increased significantly when estimated among individuals sharing the same genetic cluster or haplogroup. The latter association indicates the important historical role of queen dispersal in the determination of the spatial genetic structure.

Evolution of alarm cues: a role for kin selection?

The evolution of alarm signals has puzzled evolutionary ecologists for decades. This is particularly true for alarm cues (‘Schreckstoff’) which are present in many fishes. They are passively released through injuries and signal the presence of a predator. Although the benefits for conspecific receivers are obvious (they can adjust their behavior to avoid predation), those for the senders are not which is, however, a necessary requirement for the evolution of alarm signals. Several hypotheses relying on potential direct benefits for the senders have been suggested. Alarm cues might attract secondary predators which in turn might increase the escape probability of the sender. A primary immune enhancing role was suggested as well. An alternative explanation is based on Hamilton’s inclusive fitness theory stating that individuals can indirectly increase their fitness by increasing the survival of genetically related individuals (‘kin selection theory’). If related individuals preferentially benefit from alarm signals, for instance by being more receptive to kin-alarm cues, senders could increase their inclusive fitness. Here, we investigate whether individuals of the cichlid fish Pelvicachromis taeniatus   respond differentially to alarm cues derived from kin and non-kin.  P. taeniatus possesses alarm cues and is known to adjust its behavior when exposed to alarm cues. We measured the change in activity after the addition of alarm cues (derived from kin- and non-kin) relative to a control treatment. Reduced activity is a widespread behavioral adaptation to reduce predation risk in prey organisms. Fish of the alarm cue treatments significantly reduced their activity relative to control fish. However, fish did not respond differentially to alarm cues derived from kin and non-kin suggesting that potential inclusive fitness benefits are not mediated by responses specific to individual alarm cues. We discuss alternative mechanisms such as kin-related grouping and mating preferences potentially leading to kin-biased alarm cue perception.

Evolution of alarm cues: a role for kin selection?

The evolution of alarm signals has puzzled evolutionary ecologists for decades. This is particularly true for alarm cues (‘Schreckstoff’) which are present in many fishes. They are passively released through injuries and signal the presence of a predator. Although the benefits for conspecific receivers are obvious (they can adjust their behavior to avoid predation), those for the senders are not which is, however, a necessary requirement for the evolution of alarm signals. Several hypotheses relying on potential direct benefits for the senders have been suggested. Alarm cues might attract secondary predators which in turn might increase the escape probability of the sender. A primary immune enhancing role was suggested as well. An alternative explanation is based on Hamilton’s inclusive fitness theory stating that individuals can indirectly increase their fitness by increasing the survival of genetically related individuals (‘kin selection theory’). If related individuals preferentially benefit from alarm signals, for instance by being more receptive to kin-alarm cues, senders could increase their inclusive fitness. Here, we investigate whether individuals of the cichlid fish Pelvicachromis taeniatus respond differentially to alarm cues derived from kin and non-kin. P. taeniatus possesses alarm cues and is known to adjust its behavior when exposed to alarm cues. We measured the change in activity after the addition of alarm cues (derived from kin- and non-kin) relative to a control treatment. Reduced activity is a widespread behavioral adaptation to reduce predation risk in prey organisms. Fish of the alarm cue treatments significantly reduced their activity relative to control fish. However, fish did not respond differentially to alarm cues derived from kin and non-kin suggesting that potential inclusive fitness benefits are not mediated by responses specific to individual alarm cues. We discuss alternative mechanisms such as kin-related grouping and mating preferences potentially leading to kin-biased alarm cue perception.

Inclusive Fitness Affects Both Prosocial and Antisocial Behavior: Target Gender and Insult Domain Moderate the Link between Genetic Relatedness and Aggression

Although prior research has examined the relationship between genetic relatedness and helping behavior (Burnstein, Crandall, and Kitayama, 1994), less is known about its role in aggressive responses to insults (Fitzgerald and Ketterer, 2011). Drawing on inclusive fitness theory (Hamilton, 1964) and the Kinship, Acceptance, and Rejection Model of Altruism and Aggression (KARMAA; Webster, 2008; Webster et al., 2012), we designed a 2 (participant gender) × 2 (target gender) × 2 (insult: status vs. reproductive) × 3 (relatedness: stranger vs. cousin vs. sibling) between-person experiment in which 489 participants (a) read vignettes in which a stranger, cousin, or sibling was insulted and (b) reported their emotional reaction and retaliation likelihood (six-item α = .91) in response to the insult. Consistent with theory and prior research, men were significantly more aggressive than women, and people were significantly more aggressive responding to insults against kin than non-kin. These findings support theoretically-derived, dynamic, and domain-specific links among insults, gender, relatedness, and aggression.