Inclusive Fitness and Hamilton’s Rule

This chapter evaluates the long and intimate association between the gene’s-eye view and the work of W.D. Hamilton. Hamilton’s key insight was that individual organisms can affect the transmission of their genes through personal reproductive success, as well as through the success of close relatives. Inclusive fitness provides a way to view this process from the perspective of individual organisms, but it can also be seen from a gene’s-eye view. Dawkins and others have repeatedly emphasized the formal equivalence of the two perspectives. Yet, this chapter shows there is an underappreciated tension between the two perspectives. It demonstrates how this tension is expressed in both the current kerfuffle over the value of inclusive fitness theory stemming from Martin Nowak and colleagues and in Alan Grafen’s ongoing Formal Darwinism Project. The chapter ends by discussing two recent attempts to resolve this tension.

Non-Parental Investment in Children and Child Outcomes after Parental Death or Divorce in a Patrilocal Society

Children rely on support from parental helpers (alloparents), perhaps especially in high-needs contexts. Considerable evidence indicates that closer relatives and maternal relatives are the most likely to provide this care, as inclusive fitness theory suggests, but whether this is equally true across different family types and in culturally patrilocal societies requires investigation. This structured interview study (N = 208 respondents with 323 dependent children) focuses on who helps raise children in rural Bangladesh after the father’s or mother’s death, or divorce, in comparison to families with both parents present or the father temporarily a migrant laborer. Family types differed in where and with whom children resided, who served as their primary and secondary caregivers, and who provided material support, but mother’s kin played a major role, and were the primary providers of material resources from outside the child’s household in all family types. Despite the patrilineal ideology, only one-quarter of children of divorce lived with the father or his family, and even after the death of the mother, only 59% remained with father or other paternal kin. Household income varied by family type and was a strong predictor of child height and weight. The children of deceased mothers moved between successive caregivers especially frequently, and were uniquely likely to have no schooling. The typology of Bangladeshi society as patrilocal obscures the extent to which matrilateral family support children’s well-being.

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.

Do Somatic Cells Really Sacrifice Themselves? Why an Appeal to Coercion May be a Helpful Strategy in Explaining the Evolution of Multicellularity

An understanding of the factors behind the evolution of multicellularity is one of today’s frontiers in evolutionary biology. This is because multicellular organisms are made of one subset of cells with the capacity to transmit genes to the next generation (germline cells) and another subset responsible for maintaining the functionality of the organism, but incapable of transmitting genes to the next generation (somatic cells). The question arises: why do somatic cells sacrifice their lives for the sake of germline cells? How is germ/soma separation maintained? One conventional answer refers to inclusive fitness theory, according to which somatic cells sacrifice themselves altruistically, because in so doing they enhance the transmission of their genes by virtue of their genetic relatedness to germline cells. In the present article we will argue that this explanation ignores the key role of policing mechanisms in maintaining the germ/soma divide. Based on the pervasiveness of the latter, we argue that the role of altruistic mechanisms in the evolution of multicellularity is limited and that our understanding of this evolution must be enriched through the consideration of coercion mechanisms.

Sociogenetic Organization of the Red Honey Ant (Melophorus bagoti)

Kin selection and inclusive fitness are thought to be key factors explaining the reproductive altruism displayed by workers in eusocial insect species. However, when a colony’s queen has mated with <2 males, workers may increase their fitness by producing their own male offspring. Conversely, when the queen has mated with ≥2 males, workers are expected to increase their inclusive fitness by eschewing the production of their sons and preventing other workers from reproducing as well. Here, we investigated sociogenetic structure and worker reproduction in the red honey ant, Melophorus bagoti. Morphometric analyses revealed that workers belong to one of two distinct subcastes: they are either majors or minors. Using DNA microsatellite markers, we showed that all the colonies had a single, multiple-mated queen and that there was no relationship between worker patriline and worker subcaste. Furthermore, we found that workers were producing males in the presence of the queen, which contrasts with the predictions of inclusive fitness theory. Although our results are based on a small sample, they can serve as the foundation for future research examining worker reproduction in M. bagoti.

Using the Price equation to detect inclusive fitness in class-structured populations

Inclusive fitness theory has transformed the study of adaptive evolution since 1964, contributing to significant empirical findings. However, its status as a theory has been challenged by the proposals of several alternative frameworks. Those challenges have been countered by analyses that use the Price equation and the regression method. The Price equation is a universal description of evolutionary change, and the partitioning of the Price equation using the regression method immediately yields Hamilton’s rule, which embodies the main tenets of inclusive fitness. Hamilton’s rule captures the intensity and direction of selection acting on social behaviour and its underlying causal structure. Recent work, however, has suggested that there is an anomaly in this approach: in some cases, the regression method fails to estimate the correct values of the variables in Hamilton’s rule and the causal structure of the behaviour. Here, I address this apparent anomaly. I argue that the failure of the simple regression method occurs because social players vary in baseline fecundity. I reformulate the Price equation and regression method to recover Hamilton’s rule and I show that the method correctly estimates its key variables. I show that games where baseline fecundity varies among individuals represent a more general set of games that unfold in class-structured populations. This framework supports the robustness and validity of inclusive fitness.

Testing predictions of inclusive fitness theory in inbreeding relatives with biparental care

Inclusive fitness theory predicts that parental care will vary with relatedness between potentially caring parents and offspring, potentially shaping mating system evolution. Systems with extra-pair paternity (EPP), and hence variable parent–brood relatedness, provide valuable opportunities to test this prediction. However, existing theoretical and empirical studies assume that a focal male is either an offspring's father with no inbreeding, or is completely unrelated. We highlight that this simple dichotomy does not hold given reproductive interactions among relatives, complicating the effect of EPP on parent–brood relatedness yet providing new opportunities to test inclusive fitness theory. Accordingly, we tested hierarchical hypotheses relating parental feeding rate to parent–brood relatedness, parent kinship and inbreeding, using song sparrows ( Melospiza melodia ) experiencing natural variation in relatedness. As predicted, male and female feeding rates increased with relatedness to a dependent brood, even controlling for brood size. Male feeding rate tended to decrease as paternity loss increased, and increased with increasing kinship and hence inbreeding between socially paired mates. We thereby demonstrate that variation in a key component of parental care concurs with subtle predictions from inclusive fitness theory. We additionally highlight that such effects can depend on the underlying social mating system, potentially generating status-specific costs of extra-pair reproduction.

Do Relatives With Greater Reproductive Potential Get Help First?: A Test of the Inclusive Fitness Explanation of Kin Altruism

According to inclusive fitness theory, people are more willing to help those they are genetically related to because relatives share a kin altruism gene and are able to pass it along. We tested this theory by examining the effect of reproductive potential on altruism. Participants read hypothetical scenarios and chose between cousins (Studies 1 and 2) and cousins and friends (Study 3) to help with mundane chores or a life-or-death rescue. In life-or-death situations, participants were more willing to help a cousin preparing to conceive rather than adopt a child (Study 1) and a cousin with high rather than low chance of reproducing (Studies 2 and 3). Patterns in the mundane condition were less consistent. Emotional closeness also contributed to helping intentions (Studies 1 and 2). By experimentally manipulating reproductive potential while controlling for genetic relatedness and emotional closeness, we provide a demonstration of the direct causal effects of reproductive potential on helping intentions, supporting the inclusive fitness explanation of kin altruism.