A reconciliation of inclusive fitness and personal fitness approaches: a proposed correcting term for the inclusive fitness formula

Hamilton implicitly defined the inclusive fitness of an individual as the number of genomes, identical by descent to its own, but not in its own body, which owe their existence to expression of genes in said individual. Hamilton regarded inclusive fitness as the true metric of evolutionary success and the thin- maximized by selection. Williams, Stern and Orlove either claimed this property for mean reproductive success, or stated that expected reproductive success equals expected inclusive fitness. These statements are reconciled if a correcting term is added to Hamilton's inclusive fitness formula.This change completely accounts for inclusive fitness in personal fitness terminology. The use of ? in place of r renders the new formula exact. This has less numerical impact than the addition of the correcting term to begin with, but helps show inclusive fitness theory holds exactly.     

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.     

Social dynamics of mammals: Reproductive success, kinship and individual fitness

Apparent altruism, in which an individual seemingly decreases its evolutionary fitness by assisting others, can confer benefits if the individual assists kin. Thus, an animal can increase its total or inclusive fitness by producing offspring (direct fitness) and/or helping kin to reproduce (indirect fitness). Although kin selection has been suggested as the mechanism underlying the formation of mammalian societies, many species act as if they attempt to maximize the direct fitness component of their inclusive fitness.     

Are flies kind to kin? The role of intra- and inter-sexual relatedness in mediating reproductive conflict

As individual success often comes at the expense of others, interactions between the members of a species are frequently antagonistic, especially in the context of reproduction. In theory, this conflict may be reduced in magnitude when kin interact, as cooperative behaviour between relatives can result in increased inclusive fitness. Recent tests of the potential role of cooperative behaviour between brothers in Drosophila melanogaster have proved to be both exciting and controversial. We set out to replicate these experiments, which have profound implications for the study of kin selection and sexual conflict, and to expand upon them by also examining the potential role of kinship between males and females in reproductive interactions. While we did observe reduced fighting and courtship effort between competing brothers, contrary to previous studies we did not detect any fitness benefit to females as a result of the modification of male antagonistic behaviours. Furthermore, we did not observe any differential treatment of females by their brothers, as would be expected if the intensity of sexual conflict was mediated by kin selection. In the light of these results, we propose an alternative explanation for observed differences in male–male conflict and provide preliminary empirical support for this hypothesis.     

A New Metric of Inclusive Fitness Predicts the Human Mortality Profile

Biological species have evolved characteristic patterns of age-specific mortality across their life spans. If these mortality profiles are shaped by natural selection they should reflect underlying variation in the fitness effect of mortality with age. Direct fitness models, however, do not accurately predict the mortality profiles of many species. For several species, including humans, mortality rates vary considerably before and after reproductive ages, during life-stages when no variation in direct fitness is possible. Variation in mortality rates at these ages may reflect indirect effects of natural selection acting through kin. To test this possibility we developed a new two-variable measure of inclusive fitness, which we term the extended genomic output or EGO. Using EGO, we estimate the inclusive fitness effect of mortality at different ages in a small hunter-gatherer population with a typical human mortality profile. EGO in this population predicts 90% of the variation in age-specific mortality. This result represents the first empirical measurement of inclusive fitness of a trait in any species. It shows that the pattern of human survival can largely be explained by variation in the inclusive fitness cost of mortality at different ages. More generally, our approach can be used to estimate the inclusive fitness of any trait or genotype from population data on birth dates and relatedness.     

Darwin's ‘one special difficulty’: celebrating Darwin 200

Darwin identified eusocial evolution, especially of complex insect societies, as a particular challenge to his theory of natural selection. A century later, Hamilton provided a framework for selection on inclusive fitness. Hamilton''s rule is robust and fertile, having generated multiple subdisciplines over the past 45 years. His suggestion that eusociality can be explained via kin selection, however, remains contentious. I review the continuing debate on the role of kin selection in eusocial evolution and suggest some lines of research that should resolve that debate.     

Inclusive fitness,asymmetric competition and kin selection in plants

The findings that some plants alter their competitive phenotype in response to genetic relatedness of its conspecific neighbour (and presumed competitor) has spurred an increasing interest in plant kin‐interactions. This phenotypic response suggests the ability to assess the genetic relatedness of conspecific competitors, proposing kin selection as a process that can influence plant competitive interactions. Kin selection can favour restrained competitive growth towards kin, if the fitness loss from reducing own growth is compensated by increased fitness in the related neighbour. This may lead to positive frequency dependency among related conspecifics with important ecological consequences for species assemblage and coexistence. However, kin selection in plants is still controversial. First, many studies documenting a plastic response to neighbour relatedness do not estimate fitness consequences of the individual that responds, and when estimated, fitness of individuals grown in competition with kin did not necessarily exceed that of individuals grown in non‐kin groups. Although higher fitness in kin groups could be consistent with kin selection, this could also arise from mechanisms like asymmetric competition in the non‐kin groups. Here we outline the main challenges for studying kin selection in plants taking genetic variation for competitive ability into account. We emphasize the need to measure inclusive fitness in order to assess whether kin selection occurs, and show under which circumstances kin selected responses can be expected. We also illustrate why direct fitness estimates of a focal plant, and group fitness estimates are not suitable for documenting kin selection. Importantly, natural selection occurs at the individual level and it is the inclusive fitness of an individual plant – not the mean fitness of the group – that can capture if a differential response to neighbour relatedness is favoured by kin selection.     

Kin recognition in social bees

Kin recognition in social insects has become a central issue in sociobiology because studies of the recognition abilities of social insects provide a test of kin selection theory. W.D. Hamilton(1) formalized kin selection theory by showing how individuals can gain fitness by increasing the reproductive output of relatives (kin). The social interactions of individuals, or groups, should be influenced by the genetic structure of the population. The ability to recognize kin can increase the adaptive value of social behavior by modulating it according to genetic relationship. From this, the specific prediction emerges: if individuals can distinguish among others with which they interact on the basis of the degree to which they are related, then behavior should be biased preferentially toward more closely related reproductive individuals.     

Female reproductive competition in Eulemur rufifrons: eviction and reproductive restraint in a plurally breeding Malagasy primate

In mammals with female philopatry, co-resident females inevitably compete with each other for resources or reproductive opportunities, thereby reducing the kin-selected benefits of altruism towards relatives. These counteracting forces of cooperation and competition among kin should be particularly pronounced in plurally breeding species with limited alternative breeding opportunities outside the natal group. However, little is still known about the costs of reproductive competition on females' fitness and the victims' potential counter-strategies. Here we summarize long-term behavioural, demographic and genetic data collected on a plurally breeding primate from Madagascar to illuminate mechanisms and effects of female reproductive competition, focusing on forcible eviction and potential reproductive restraint. The main results of our study indicate that females in groups of redfronted lemurs (Eulemur rufifrons) above a critical size suffer from competition from their close relatives: females in larger groups face an increased probability of not giving birth as well as a higher probability of being evicted, especially during the annual mating and birth seasons. Eviction is not predicted by the number of adult females, the number of close female relatives, female age or inter-annual variation in rainfall but only by total group size. Thus, eviction in this species is clearly linked with reproductive competition, it cannot be forestalled by reproductive restraint or having many relatives in the group, and it occurs in the absence of a clear dominance hierarchy. Our study therefore also underscores the notion that potential inclusive fitness benefits from living with relatives may have been generally over-rated and should not be taken for granted.     

Kin selection in age-structured populations

There have been several discussions in the literature as to how to weight interactions between individuals of different ages in models of kin selection. It has commonly been assumed that the reproductive value of a given age is the most appropriate weight, for the purpose of calculating its contribution to inclusive fitness. This paper analyses a model of kin selection in an age-structured population. It is shown that reproductive value is relevant to behavioural interactions involving effects on survival, although the reproductive value of a given age does not provide an exact weighting of its fitness contribution in either discrete- or continuous-time populations. Reproductive value is not relevant to interactions involving effects on fecundity. The results are discussed in relation to observations on behavioural asymmetries involving age differences.     

Detecting kin selection at work using inclusive fitness

A recent model shows that altruism can evolve with limited migration and variable group sizes, and the authors claim that kin selection cannot provide a sufficient explanation of their results. It is demonstrated, using a recent reformulation of Hamilton's original arguments, that the model falls squarely within the scope of inclusive fitness theory, which furthermore shows how to calculate inclusive fitness and the relevant relatedness. A distinction is drawn between inclusive fitness, which is a method of analysing social behaviour; and kin selection, a process that operates through genetic similarity brought about by common ancestry, but not by assortation by genotype or by direct assessment of genetic similarity. The recent model is analysed, and it turns out that kin selection provides a sufficient explanation to considerable quantitative accuracy, contrary to the authors' claims. A parallel analysis is possible and would be illuminating for all models of social behaviour in which individuals' effects on each other's offspring numbers combine additively.     

Hamilton goes empirical: estimation of inclusive fitness from life-history data

Hamilton's theory of kin selection is one of the most important advances in evolutionary biology since Darwin. Central to the kin-selection theory is the concept of inclusive fitness. However, despite the importance of inclusive fitness in evolutionary theory, empirical estimation of inclusive fitness has remained an elusive task. Using the concept of individual fitness, I present a method for estimating inclusive fitness and its components for diploid organisms with age-structured life histories. The method presented here: (i) allows empirical estimation of inclusive fitness from life-history data; (ii) simultaneously considers all components of fitness, including timing and magnitude of reproduction; (iii) is consistent with Hamilton's definition of inclusive fitness; and (iv) adequately addresses shortcomings of existing methods of estimating inclusive fitness. I also demonstrate the application of this new method for testing Hamilton's rule.     

Reciprocal altruism in bats and other mammals

In this paper five conditions are specified which must be met before reciprocal altruism, rather than kin selection, should be invoked. Four purported mammalian examples— social grooming in coati, cluster position in roosting pallid bats, information exchange among greater spear-nosed bats, and blood regurgitation among vampire bats—are examined to determine if reciprocal altruism is necessary to plausibly explain each situation. Results from a computer simulation which apportions the relative selective advantage of vampire bat food sharing to kin selection and reciprocal altruism are then presented. The results demonstrate that the increase in individual survivorship due to reciprocal food sharing events in this species provides a greater increase in inclusive fitness than can be attributed to aiding relatives. This analysis suggests that reciprocal altruism can be selectively more important than kin selection when altruistic behaviors in a relatively large social group occur frequently and provide a major fitness benefit to the recipient even when that recipient is related to the donor.     

Evolution of social behaviour in the primitively eusocial wasp Ropalidia marginata: do we need to look beyond kin selection?

Ropalidia marginata is a primitively eusocial wasp widely distributed in peninsular India. Although solitary females found a small proportion of nests, the vast majority of new nests are founded by small groups of females. In such multiple foundress nests, a single dominant female functions as the queen and lays eggs, while the rest function as sterile workers and care for the queen''s brood. Previous attempts to understand the evolution of social behaviour and altruism in this species have employed inclusive fitness theory (kin selection) as a guiding framework. Although inclusive fitness theory is quite successful in explaining the high propensity of the wasps to found nests in groups, several features of their social organization suggest that forces other than kin selection may also have played a significant role in the evolution of this species. These features include lowering of genetic relatedness owing to polyandry and serial polygyny, nest foundation by unrelated individuals, acceptance of young non-nest-mates, a combination of well-developed nest-mate recognition and lack of intra-colony kin recognition, a combination of meek and docile queens and a decentralized self-organized work force, long reproductive queues with cryptic heir designates and conflict-free queen succession, all resulting in extreme intra-colony cooperation and inter-colony conflict.     

Influences on communication about reproduction: the cultural evolution of low fertility

The cultural norms of traditional societies encourage behavior that is consistent with maximizing reproductive success but those of modern post-demographic transition societies do not. Newson et al (2005) proposed that this might be because interaction between kin is relatively less frequent in modern social networks. Assuming that people's evaluations of reproductive decisions are influenced by a desire to increase their inclusive fitness, they will be inclined to prefer their kin to make fitness-enhancing choices. Such a preference will encourage the emergence of pronatal cultural norms if social networks are dense with kin. Less pronatal norms will emerge if contact between kin makes up a small proportion of social interactions. This article reports evidence based on role-play studies that supports the assumption of the kin influence hypothesis that evaluations of reproductive decisions are influenced by a desire to increase inclusive fitness. It also presents a cultural evolutionary model demonstrating the long-term effect of declining kin interaction if people are more likely to encourage fitness-enhancing choices when interacting with their kin than with nonrelatives.     

Kin selection is the key to altruism

Kin selection theory, also known as inclusive fitness theory, has been the subject of much debate and misunderstanding. Nevertheless, the idea that relatedness among individuals can drive the evolution of altruism has emerged as a central paradigm in evolutionary biology. Or has it? In two recent articles, E.O. Wilson argues that kin selection should no longer be considered the main explanation for the evolution of altruism in insect societies. Here, we discuss what these articles say about kin selection and how it relates to the theory. We conclude that kin selection remains the key explanation for the evolution of altruism in eusocial insects.     

Inheritance of wealth as human kin investment

Like many other animals, humans appear to have evolved to invest time and energy in their relatives in order to maximize inclusive fitness. Inheritance of material wealth may be a uniquely human form of kin investment. If fitness-maximizing dispositions do influence will-makers, beneficiaries may be favored according to their relatedness and reproductive value. An analysis of 1000 probated wills showed that this was the case. Close relatives were favored over distant kin, as were kin of higher reproductive value. Wealthier decedents favored male kin, while poorer decedents favored females. This pattern might reflect a facultative shifting of resources toward males when the family's resources are sufficient to ensure reproductive competitiveness, and toward the safer option of females when resources are less abundant. The results support the possibility that fitness-maximizing dispositions do influence will-makers. It is likely that such dispositions are flexible and responsive to the physical and social environment.     

Comparative statics of games between relatives

According to Hamilton's theory of kin selection, species tend to evolve behavior such that each organism appears to be attempting to maximize its inclusive fitness. In particular, two neighbors are likely to help each other if the cost of doing so is less than the benefit multiplied by r, their coefficient of relatedness. Since the latter is less than unity, mutual altruism benefits both neighbors. However, is it theoretically possible that acting so as to maximize the inclusive, rather than personal, fitness may harm both parties. This may occur in strategic symmetric pairwise interactions (more specifically, nxn games), in which the outcome depends on both sides' actions. In this case, the equilibrium outcome may be less favorable to the interactants' personal fitness than if each of them acted so as to maximize the latter. This paper shows, however, that such negative effect of relatedness on fitness is incompatible with evolutionary stability. If the symmetric equilibrium strategies are evolutionarily stable, a higher coefficient of relatedness can only entail higher personal fitness for the two neighbors. This suggests that negative comparative statics as above are not likely to occur in nature.     

Cannibalistic tadpoles that pose the greatest threat to kin are most likely to discriminate kin

Inclusive fitness theory predicts that altruism should often be directed towards reproductive relatives, but it is unclear whether individuals that are most likely to help or harm relatives are also most likely to identify kin in the first place. Here I show that species and sibships of spadefoot toad tadpoles (Spea bombifrons and S. multiplicata) that were most likely to produce an environmentally induced cannibalistic morph were also most likely to avoid eating kin. Moreover, tadpoles avoided eating kin when they expressed the cannibal phenotype, but not when these same individuals reverted to the non-cannibalistic morph. Thus, individual tadpoles facultatively adjust their level of discrimination according to how likely they are to harm kin. In general, sensory systems and/or decision rules enabling recognition may be especially likely to evolve among those individuals that are most often faced with the problem of discrimination.     

Kin selection in Columbian ground squirrels: direct and indirect fitness benefits

Empirical and theoretical studies have supported kin selection by demonstrating nepotism or modelling its conditions and consequences. As an alternative, we previously found that female Columbian ground squirrels had greater direct fitness when more close kin were present. Extending those results, we used population matrix methods to calculate minimum estimates of individual fitness, estimated direct and indirect components of fitness, estimated inclusive fitness by adding the direct fitness (stripped of estimated influences of the social environment) and indirect fitness components together, and finally looked for inclusive fitness benefits of associations with close kin who seem to be 'genial neighbours'. We examined the estimated fitness of a sample of 35 females for which complete lifetimes were known for themselves, their mothers and their littermate sisters. Six of these females had no cosurviving adult close kin, and their direct fitness was significantly lower than 29 females with such kin (λ = 0.66 vs. λ = 1.23). The net fitness benefit of the presence of close kin was thus 0.57. The estimated indirect component of fitness through benefits to the direct fitness of close kin was 0.43. Thus, estimated inclusive fitness for females with cosurviving close kin (λ = 1.09) was significantly greater than that for females without surviving close kin (viz., λ = 0.66). The presence of closely related and philopatric female kin appeared to result in considerable fitness benefits for female ground squirrels, perhaps through the behavioural mechanisms of lowered aggression and other forms of behavioural cooperation.