Hamilton's Inclusive Fitness Research Articles

Kin selection theory and the design of cooperative crops.

In agriculture and plant breeding, plant traits may be favoured because they benefit neighbouring plants and ultimately increase total crop yield. This idea of promoting cooperation among crop plants has existed almost as long as W.D. Hamilton's inclusive fitness (kin selection) theory, the leading framework for explaining cooperation in biology. However, kin selection thinking has not been adequately applied to the idea of cooperative crops. Here, I give an overview of modern kin selection theory and consider how it explains three key strategies for designing cooperative crops: (1)selection for a less-competitive plant type (a 'communal ideotype'); (2) group-level selection for yield; and (3) exploiting naturally selected cooperation. The first two strategies, using artificial selection, have been successful in the past but suffer from limitations that could hinder future progress. Instead, I propose an alternative strategy and a new 'colonial ideotype' that exploits past natural selection for cooperation among the modules (e.g., branches or stems) of individual plants. More generally, I suggest that Hamiltonian agriculture-a kin selection view of agriculture and plant breeding-transforms our understanding of how to improve crops of the future.

Twin study of genetic relatedness and bereavement related measures: Updated analyses and the mediating role of grief

A Twin Loss Survey was completed by MZ and same-sex DZ twins following loss of a cotwin and nontwin relatives. Twin survivors (N = 612; MZ = 506; DZ, n = 106) included twins whose age at loss was 15 years or older. Participation age was M = 47.66 years (SD = 15.31). Hamilton's inclusive fitness theory generated two hypotheses: (1) MZ twins will recall greater grief intensity at loss than DZ twins; (2) loss of a twin will receive greater grief intensity ratings than loss of nontwin relatives. We expected females to grieve more intensely for deceased cotwins than males. Males cannot be certain a child conceived by their partner is theirs (paternity uncertainty). As such, grief for the loss of a twin brother (whose child would indirectly transmit common genes) should be reduced by surviving male twins, relative to surviving female twins. Part I: Hypotheses regarding grief intensity were supported. Part II: A structural equation model was estimated; grief significantly mediated relationships between exogenous and endogenous predictors and grief predicted greater preoccupation and less effective coping. MZ twins and females expressed greater grief intensity than DZ twins and males. Associations between genetic relatedness and grief, consistent with evolutionary-based predictions, are highlighted.

Belief in an Afterlife Influences Altruistic Helping Intentions in Alignment With Adaptive Tendencies.

Evolutionary definitions of altruism are only concerned with reproductive consequences and not motives or other psychological mechanisms, making them ideal for generalization to all forms of organisms. Hamilton's inclusive fitness theory explains altruistic behavior toward genetic relatives and has generated extensive empirical support. Trivers' theory of reciprocal altruism helps explain patterns of helping among non-kin, and other research has demonstrated that human helping intentions follow fitness consequences from age-based reproductive value on altruism. The current study examines a novel psychological factor, belief in the afterlife, which may influence altruistic helping intentions. Belief in the afterlife was incorporated into a previous study design assessing the effects of a target's genetic relatedness and age-based reproductive value. The influences of inclusive fitness and target age were reproduced in a non-Western sample of participants (N = 300) in Iran. Belief in the afterlife predicted the overall confidence of risking one's life to save another across all targets, and also moderated the effects of genetic relatedness and target age. Rather than promoting altruism equitably or advantaging those favored by adaptive tendencies, higher belief in an afterlife aligned with these tendencies in promoting further favoritism toward close kin and younger targets with higher reproductive value.

Kin selection explains the evolution of cooperation in the gut microbiota

Through the secretion of "public goods" molecules, microbes cooperatively exploit their habitat. This is known as a major driver of the functioning of microbial communities, including in human disease. Understanding why microbial species cooperate is therefore crucial to achieve successful microbial community management, such as microbiome manipulation. A leading explanation is that of Hamilton's inclusive-fitness framework. A cooperator can indirectly transmit its genes by helping the reproduction of an individual carrying similar genes. Therefore, all else being equal, as relatedness among individuals increases, so should cooperation. However, the predictive power of relatedness, particularly in microbes, is surrounded by controversy. Using phylogenetic comparative analyses across the full diversity of the human gut microbiota and six forms of cooperation, we find that relatedness is predictive of the cooperative gene content evolution in gut-microbe genomes. Hence, relatedness is predictive of cooperation over broad microbial taxonomic levels that encompass variation in other life-history and ecology details. This supports the generality of Hamilton's central insights and the relevance of relatedness as a key parameter of interest to advance microbial predictive and engineering science.

Hamilton's inclusive fitness maintains heritable altruism polymorphism through rb = c

How can altruism evolve or be maintained in a selfish world? Hamilton's rule shows that the former process will occur when rb > c-the benefits to the recipients of an altruistic act b, weighted by the relatedness between the social partners r, exceed the costs to the altruists c-drives altruistic genotypes spreading against nonaltruistic ones. From this rule, we infer that altruistic genotypes will persist in a population by forming a stable heritable polymorphism with nonaltruistic genotypes if rb = c makes inclusive fitness of the two morphs equal. We test this prediction using the data of 12 years of study on a cooperatively breeding bird, the Tibetan ground tit Pseudopodoces humilis, where helping is performed by males only and kin-directed. Individual variation in ever acting as a helper was heritable (h2 = 0.47), and the resultant altruism polymorphism remained stable as indicated by low-level annual fluctuation of the percentage of helpers among all adult males (24-28%). Helpers' indirect fitness gains from increased lifetime reproductive success of related breeders statistically fully compensated for their lifetime direct fitness losses, suggesting that rb = c holds. While our work provides a fundamental support for Hamilton's idea, it highlights the equivalent inclusive fitness returns to altruists and nonaltruists mediated by rb = c as a theoretically and realistically important mechanism to maintain social polymorphism.

Kinship reinforces cooperative predator inspection in a cichlid fish.

Kin selection theory predicts that cooperation is facilitated between genetic relatives, as by cooperating with kin an individual might increase its inclusive fitness. Although numerous theoretical papers support Hamilton's inclusive fitness theory, experimental evidence is still underrepresented, in particular in noncooperative breeders. Cooperative predator inspection is one of the most intriguing antipredator strategies, as it implies high costs on inspectors. During an inspection event, one or more individuals leave the safety of a group and approach a potential predator to gather information about the current predation risk. We investigated the effect of genetic relatedness on cooperative predator inspection in juveniles of the cichlid fish Pelvicachromis taeniatus, a species in which juveniles live in shoals under natural conditions. We show that relatedness significantly influenced predator inspection behaviour with kin dyads being significantly more cooperative. Thus, our results indicate a higher disposition for cooperative antipredator behaviour among kin as predicted by kin selection theory.

Hamilton's inclusive fitness in finite-structured populations

Hamilton's formulation of inclusive fitness has been with us for 50 years. During the first 20 of those years attention was largely focused on the evolutionary trajectories of different behaviours, but over the past 20 years interest has been growing in the effect of population structure on the evolution of behaviour and that is our focus here. We discuss the evolutionary journey of the inclusive-fitness effect over this epoch, nurtured as it was in an essentially homogeneous environment (that of 'transitive' structures) having to adapt in different ways to meet the expectations of heterogeneous structures. We pay particular attention to the way in which the theory has managed to adapt the original constructs of relatedness and reproductive value to provide a formulation of inclusive fitness that captures a precise measure of allele-frequency change in finite-structured populations.

ON MULTILEVEL SELECTION AND KIN SELECTION: CONTEXTUAL ANALYSIS MEETS DIRECT FITNESS

When Hamilton defined the concept of inclusive fitness, he specifically was looking to define the fitness of an individual in terms of that individual's behavior, and the effects of its' behavior on other related individuals. Although an intuitively attractive concept, issues of accounting for fitness, and correctly assigning it to the appropriate individual make this approach difficult to implement. The direct fitness approach has been suggested as a means of modeling kin selection while avoiding these issues. Whereas Hamilton's inclusive fitness approach assigns to the focal individual the fitness effects of its behavior on other related individuals, the direct fitness approach assigns the fitness effects of other actors to the focal individual. Contextual analysis was independently developed as a quantitative genetic approach for measuring multilevel selection in natural populations. Although the direct fitness approach and contextual analysis come from very different traditions, both methods rely on the same underlying equation, with the primary difference between the two approaches being that the direct fitness approach uses fitness optimization modeling, whereas with contextual analysis, the same equation is used to solve for the change in fitness associated with a change in phenotype when the population is away from the optimal phenotype.

DEEP SOCIALITY

DEEP SOCIALITY

The stationary distribution of a continuously varying strategy in a class‐structured population under mutation–selection–drift balance

Many traits and/or strategies expressed by organisms are quantitative phenotypes. Because populations are of finite size and genomes are subject to mutations, these continuously varying phenotypes are under the joint pressure of mutation, natural selection and random genetic drift. This article derives the stationary distribution for such a phenotype under a mutation-selection-drift balance in a class-structured population allowing for demographically varying class sizes and/or changing environmental conditions. The salient feature of the stationary distribution is that it can be entirely characterized in terms of the average size of the gene pool and Hamilton's inclusive fitness effect. The exploration of the phenotypic space varies exponentially with the cumulative inclusive fitness effect over state space, which determines an adaptive landscape. The peaks of the landscapes are those phenotypes that are candidate evolutionary stable strategies and can be determined by standard phenotypic selection gradient methods (e.g. evolutionary game theory, kin selection theory, adaptive dynamics). The curvature of the stationary distribution provides a measure of the stability by convergence of candidate evolutionary stable strategies, and it is evaluated explicitly for two biological scenarios: first, a coordination game, which illustrates that, for a multipeaked adaptive landscape, stochastically stable strategies can be singled out by letting the size of the gene pool grow large; second, a sex-allocation game for diploids and haplo-diploids, which suggests that the equilibrium sex ratio follows a Beta distribution with parameters depending on the features of the genetic system.

Sex Differences in Violent versus Non-Violent Life-Threatening Altruism

Many studies on Hamilton's (1964) inclusive fitness theory have used the burning house and kidney donation examples of life-threatening altruism. However, these examples may not be sufficiently exhibiting the risk involved with life-threatening altruism that would have occurred in hunter-gatherer societies, such as fighting off attackers and/or predators. The present study examined participants' estimated likelihood to perform altruistic acts for specific kin members/friends in two violent life-threatening situations (i.e., being mugged and being chased) and two non-violent life-threatening situations (i.e., the burning house and kidney donation examples). Participants were 216 undergraduate students who completed a questionnaire on altruism toward an actual kin member/friend. Each questionnaire contained four life-or-death scenarios (two violent and two non-violent) in which either the participant's sibling, cousin, or best friend was in danger and needed help. Results indicated that people were more likely to help siblings than cousins and friends in both the violent and non-violent hypothetical scenarios. Participants indicated a greater likelihood to help people in violent situations than in non-violent situations. Women indicated a greater estimated likelihood than men to help people in non-violent situations while men indicated a greater estimated likelihood than women to help people in violent situations. Both male and female participants indicated a greater estimated likelihood to help women than men in violent situations.

A heritable component in sex ratio and caste determination in a Cardiocondyla ant

Studies on sex ratios in social insects provide among the most compelling evidence for the importance of kin selection in social evolution. The elegant synthesis of Fisher's sex ratio principle and Hamilton's inclusive fitness theory predicts that colony-level sex ratios vary with the colonies' social and genetic structures. Numerous empirical studies in ants, bees, and wasps have corroborated these predictions. However, the evolutionary optimization of sex ratios requires genetic variation, but one fundamental determinant of sex ratios - the propensity of female larvae to develop into young queens or workers ("queen bias") - is thought to be largely controlled by the environment. Evidence for a genetic influence on sex ratio and queen bias is as yet restricted to a few taxa, in particular hybrids.Because of the very short lifetime of their queens, ants of the genus Cardiocondyla are ideal model systems for the study of complete lifetime reproductive success, queen bias, and sex ratios. We found that lifetime sex ratios of the ant Cardiocondyla kagutsuchi have a heritable component. In experimental single-queen colonies, 22 queens from a genetic lineage with a highly female-biased sex ratio produced significantly more female-biased offspring sex ratios than 16 queens from a lineage with a more male-biased sex ratio (median 91.5% vs. 58.5% female sexuals). Sex ratio variation resulted from different likelihood of female larvae developing into sexuals (median 50% vs. 22.6% female sexuals) even when uniformly nursed by workers from another colony.Consistent differences in lifetime sex ratios and queen bias among queens of C. kagutsuchi suggest that heritable, genetic or maternal effects strongly affect caste determination. Such variation might provide the basis for adaptive evolution of queen and worker strategies, though it momentarily constrains the power of workers and queens to optimize caste ratios.

Lineage, Sex, and Wealth as Moderators of Kin Investment : Evidence from Inheritances.

Supporting Hamilton's inclusive fitness theory, archival analyses of inheritance patterns in wills have revealed that people invest more of their estates in kin of closer genetic relatedness. Recent classroom experiments have shown that this genetic relatedness effect is stronger for relatives of direct lineage (children, grandchildren) than for relatives of collateral lineage (siblings, nieces, nephews). In the present research, multilevel modeling of more than 1,000 British Columbian wills revealed a positive effect of genetic relatedness on proportions of estates allocated to relatives. This effect was qualified by an interaction with lineage, such that it was stronger for direct than for collateral relatives. Exploratory analyses of the moderating role of benefactors' sex and estate values showed the genetic relatedness effect was stronger among female and wealthier benefactors. The importance of these moderators to understanding kin investment in modern humans is discussed.

Social closeness of MZ and DZ twin parents towards nieces and nephews

Twins' marriages to non‐twins yield genetically and socially informative kinships. Monozygotic (MZ) twins' genetic identity makes them ‘genetic parents’ of their nieces/nephews, and their nieces/nephews their ‘genetic children’. The present study is the first to apply twin‐family models to study social relatedness. Analyses of twin families (MZ: N = 248; DZ: N = 75) tested evolutionary‐based concepts concerning social closeness, perceived similarity and caretaking. Hypotheses based on Hamilton's inclusive fitness theory were supported: MZ twin aunts/uncles expressed greater social closeness towards their nieces/nephews than DZ twin aunts/uncles; and female twins from same‐sex pairs expressed greater closeness towards their nieces/nephews than male twins from same‐sex pairs. This study underlines benefits of associations between behavioural‐genetic and evolutionary psychological theories, methods and interpretations. Copyright © 2007 John Wiley & Sons, Ltd.

Population Genetics and Sociobiology: Conflicting Views of Evolution

This article explores the tension between the population genetics and sociobiological approaches to the study of evolution. Whereas population geneticists, like Stanford's Marc Feldman, insist that the genetic complexities of organisms cannot be overlooked, sociobiologists (many of whom now prefer to call themselves "behavioral ecologists") rely on optimization models that are based on the simplest possible genetics.These optimization approaches have their roots in the classical result known as the fundamental theorem of natural selection, formulated by R. A. Fisher in 1930. From the start there was great uncertainty over the proper interpretation of Fisher's theorem, which became confused with Sewall Wright's immensely influential adaptive landscape concept. In the 1960s, a new generation of mathematical biologists proved that Fisher's theorem did not hold when fitness depended on more than one locus. Similar reasoning was used to attack W. D. Hamilton's inclusive fitness theory. A new theory, known as the theory of long-term evolution, attempts to reconcile the rigorous population genetics approach with the long-standing sociobiological view that natural selection acts to increase the fitness of organisms.

PSYCHOLOGICAL ASPECTS OF ADAPTATIONS FOR KIN DIRECTED ALTRUISTIC HELPING BEHAVIORS

This questionnaire study sheds light on the psychological component of kin selecting tendencies predicted by Hamilton's (1964b) inclusive fitness theory of discriminatory altruistic behavior based on genetic similarity. Participants rated donations of assistance aiding survival and material wealth as more rational and ethical when these actions were performed for closer relatives. Participants also felt a greater obligation to perform these acts for a close relation. A comparison condition where assistance was unlikely to affect survival or reproductive success did not exhibit these tendencies.

Evolution of Dispersal in a Stepping-Stone Population with Overlapping Generations

We use Hamilton's inclusive fitness method to calculate the evolutionarily stable dispersal rate in 1- and 2-dimensional stepping-stone populations. This extends previous results by introducing a positive probability for adults to survive into the next generation and breed again. Relatedness between nearby individuals generally decreases with increasing survival, decreasing competition with kin and favouring greater dispersal rates.

Evolutionary kinship therapy: basic principles and treatment implications.

The idiom of kinship is a powerful one that stretches across many levels of social behaviour (van den Berghe, 1979), and Daly, Salmon & Wilson (1997) recently outlined the basic principles of a comprehensive, evolution-based kinship psychology. Their approach merges traditional kinship theory, Hamilton's inclusive fitness model and the broader realm of evolutionary psychology into an exciting and provocative call to arms. They address biological, psychological (viz. fictive kinship) and kin-like levels of analysis, and they argue for a relationship-specific kinship psychology that deals with the particular demands of being a mother, father, mate, offspring or grandparent. Our particular approach to kinship psychology has focused primarily on the distinction between biological kinship and psychological kinship (Bailey, 1988; Bailey & Wood, 1993; Nava & Bailey, 1991), and more recently on the role of kin-like relations in psychotherapy and other social contexts (Bailey, 1997a; Wood, 1997). The kin-like category is especially noteworthy in modern industrialized countries where acquaintanceships and stranger-to-stranger interactions often predominate over biological and psychological kinships (Ahern & Bailey, 1997).

Prolactin and helping in birds: has natural selection strengthened helping behavior?

The evolution of helping behavior in birds has been hotly debated. Hamilton's inclusive fitness theory has received much support from ecological cost-benefit studies; however, the hypothesis that helping has not been selected per se but is simply a phenotypicalfy plastic response to altered social conditions has been proposed. In this view helping by nonbreeding birds occur* when at independence they fail to leave their parents and are exposed to the critical stimulus, the begging of young birds to be fed. We report that levels of prolactin, a hormone associated with parental behavior, are conspicuously higher in an avian species with helpers, the Mexican jay (Aphelocoma uttramarina), than in a congeneric and sympatric species without helpers, the western scrub jay (A. caUfornica). Specifically, prolactin in the nonbreeding members of the helping species is higher than the level found in the breeders of the congeneric nonhelping species. In addition, prolactin levels in nonbreeders rise well before the appearance of begging young. These findings reject the phenotypic plasticity hypothesis based purely on a response to begging young and suggest that prolactin is involved in die physiology of helping behavior in birds as part of a complex adaptation. Key words: alloparental behavior, Aphelocoma, altruism, helping, jays, prolactin. [Behav Ecol 9:541-545 (1998)] A contentious issue in the evolution of the behavior of hu/~ mans and other animal* is the origin of altruism. Hamilton's concept of inclusive fitness (Hamilton, 1964) was a major advance in evolutionary theory that helps to explain potentially altruistic behaviors (with a net loss in direct fitness), such as alloparental or helping behavior. Helping behavior is the feeding of young together with the genetic parents by individuals that are not the genetic parents. It is common in humans and has been much studied in social insects (Crozier and Pamilo, 1996), birds (Brown, 1987a; Stacey and Koenig, 1990) and mammal* (Solomon and French, 1996). Cost-benefit studies on birds in the last 25 years have revealed that some helpers may behave altruistically in Hamilton's (1963) original sense (e.g., primary helpers in the pied kingfisher, Cerylt rudis, Reyer, 1980, 1984; helpers in the white-fronted bee-eater, Mewps buUockaides, Emlen and Wrege, 1988,1989), in agreement with inclusive fitness theory applied to birds (Brown, 1974, 1987b; Emlen and Wrege, 1994). Nevertheless, the hypothesis that helping by nonbreeders has not been influenced directly by natural selection but is simply a response to altered social conditions, or flexible strategy, has been advanced both for social insects (West-Eberhard, 1987) and birds (Jamieson, 1989, 1991; Jamieson and Craig, 1987). In this view, helping by nonbreeding birds occurs when at independence they fail to leave their parents because of environmental constraints and are thereby exposed to the critical stimulus, the begging of young birds to be fed, without involving natural selection. An understanding of the physiological basis of a behavior, when used with die comparative method, can provide a powerful tool to test hypotheses in evolutionary ecology (Real, 1994). We used this approach to show that helping and its associated physiology are not mere responses to begging young. To distinguish between hypotheses that invoke selection on helping and one that does not, we compared levels

Genetic relatedness in viscous populations

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.