Inclusive fitness in humans is the application of inclusive fitness theory to human social behaviour, relationships and cooperation.
Inclusive fitness theory (and the related kin selection theory) are general theories in evolutionary biology that propose a method to understand the evolution of social behaviours in organisms. While various ideas related to these theories have been influential in the study of the social behaviour of non-human organisms, their application to human behaviour has been debated.
Inclusive fitness theory is broadly understood to describe a "statistical" criterion by which social traits can "evolve" to become widespread in a population of organisms. However, beyond this some scientists have interpreted the theory to make predictions about how the "expression" of social behavior is mediated in both humans and other animals – typically that genetic relatedness determines the expression of social behaviour. Other biologists and anthropologists maintain that beyond its statistical evolutionary relevance the theory does not necessarily imply that genetic relatedness "per se" determines the "expression" of social behavior in organisms. Instead, the expression of social behavior may be mediated by correlated conditions, such as shared location, shared rearing environment, familiarity or other contextual cues which correlate with shared genetic relatedness, thus meeting the statistical evolutionary criteria without being deterministic. While the former position still attracts controversy, the latter position has a better empirical fit with anthropological data about human kinship practices, and is accepted by cultural anthropologists.
History.
Applying evolutionary biology perspectives to humans and human society has often resulted in periods of controversy and debate, due to their apparent incompatibility with alternative perspectives about humanity. Examples of early controversies include the reactions to "On the Origin of Species", and the Scopes Monkey Trial. Examples of later controversies more directly connected with inclusive fitness theory and its use in sociobiology include physical confrontations at meetings of the Sociobiology Study Group and more often intellectual arguments such as Sahlins' 1976 book "The use and abuse of biology", Lewontin et al.'s 1984 "Not in Our Genes", and Kitcher's 1985 "Vaulting Ambition:Sociobiology and the Quest for Human Nature". Some of these later arguments were produced by other scientists, including biologists and anthropologists, against Wilson's 1975 book "", which was influenced by (though not necessarily endorsed by) Hamilton's work on inclusive fitness theory.
A key debate in applying inclusive fitness theory to humans has been between biologists and anthropologists around the extent to which human kinship relationships (considered to be a large component of human solidarity and altruistic activity and practice) are necessarily based on or influenced by genetic relationships or blood-ties ('consanguinity'). The position of most social anthropologists is summarized by Sahlins (1976), that for humans "the categories of 'near' and 'distant' [kin] vary independently of consanguinal distance and that these categories organize actual social practice" (p. 112). Biologists wishing to apply the theory to humans directly disagree, arguing that "the categories of 'near' and 'distant' do not 'vary independently of consanguinal distance', not in any society on earth." (Daly et al. 1997, p282).
This disagreement is central because of the way the association between blood ties/genetic relationships and altruism are conceptualized by many biologists. It is frequently understood by biologists that inclusive fitness theory makes predictions about "how behaviour is mediated" in both humans and other animals. For example, a recent experiment conducted on humans by the evolutionary psychologist Robin Dunbar and colleagues was, as they understood it, designed "to test the prediction that altruistic behaviour is mediated by Hamilton's rule" (inclusive fitness theory) and more specifically that "If participants follow Hamilton's rule, investment (time for which the [altruistic] position was held) should increase with the recipient's relatedness to the participant. In effect, we tested whether investment flows differentially down channels of relatedness." From their results, they concluded that "human altruistic behaviour is mediated by Hamilton's rule ... humans behave in such a way as to maximize inclusive fitness: they are more willing to benefit closer relatives than more distantly related individuals." (Madsen et al. 2007). This position continues to be rejected by social anthropologists as being incompatible with the large amount of ethnographic data on kinship and altruism that their discipline has collected over many decades, that demonstrates that in many human cultures, kinship relationships (accompanied by altruism) do not necessarily map closely onto genetic relationships.
Whilst the above understanding of inclusive fitness theory as necessarily making predictions about how human kinship and altruism is mediated is common amongst evolutionary psychologists, other biologists and anthropologists have argued that it is at best a limited (and at worst a mistaken) understanding of inclusive fitness theory. These scientists argue that the theory is better understood as simply describing an "evolutionary" criterion for the emergence of altruistic behaviour, which is explicitly statistical in character, not as predictive of "proximate" or "mediating" mechanisms of altruistic behaviour, which may not necessarily be determined by genetic relatedness (or blood ties) "per se". These alternative non-deterministic and non-reductionist understandings of inclusive fitness theory and human behavior have been argued to be compatible with anthropologists' decades of data on human kinship, and compatible with anthropologists' perspectives on human kinship. This position (e.g. nurture kinship) has been largely accepted by social anthropologists, whilst the former position (still held by evolutionary psychologists, see above) remains rejected by social anthropologists.
Theoretical background.
Theoretical overview.
Inclusive fitness theory, first proposed by Bill Hamilton in the early 1960s, proposes a selective criterion for the potential evolution of social traits in organisms, where social behavior that is costly to an individual organism's survival and reproduction could nevertheless emerge under certain conditions. The key condition relates to the statistical likelihood that significant benefits of a social trait or behavior accrue to (the survival and reproduction of) other organisms who also carry the social trait. Inclusive fitness theory is a general treatment of the statistical probabilities of social traits accruing to any other organisms likely to propagate a copy of the same social trait. Kin selection theory treats the narrower but more straightforward case of the benefits accruing to close genetic relatives (or what biologists call 'kin') who may also carry and propagate the trait. Under conditions where the social trait sufficiently correlates (or more properly, "regresses") with other likely bearers, a net overall increase in reproduction of the social trait in future generations can result.
The concept serves to explain how natural selection can perpetuate altruism. If there is an "altruism gene" (or complex of genes or heritable factors) that influence an organism's behavior in such a way that is helpful and protective of relatives and their offspring, this behavior can also increase the proportion of the altruism gene in the population, because relatives are likely to share genes with the altruist due to common descent. In formal terms, if such a complex of genes arises, Hamilton's rule (rb ;c) specifies the selective criteria (in terms of relatedness (r), cost (c) benefit (b)) for such a trait to increase in frequency in the population (see Inclusive fitness for more details). Hamilton noted that inclusive fitness theory does not by itself predict that a given species will necessarily evolve such altruistic behaviors, since an opportunity or context for interaction between individuals is a more primary and necessary requirement in order for any social interaction to occur in the first place. As Hamilton put it, "Altruistic or selfish acts are only possible when a suitable social object is available. In this sense behaviours are conditional from the start." (Hamilton 1987, 420). In other words, whilst inclusive fitness theory specifies a set of necessary criteria for the evolution of certain altruistic traits, it does not specify a sufficient condition for their evolution in any given species, since the typical ecology, demographics and life pattern of the species must also allow for social interactions between individuals to occur before any potential elaboration of social traits can evolve in regard to those interactions.
Initial presentations of the theory.
The initial presentation of inclusive fitness theory (in the mid-1960s, see "The Genetical Evolution of Social Behaviour") focused on making the general mathematical case for the possibility of social evolution. However, since many field biologists mainly use theory as a guide to their observations and analysis of empirical phenomena, Hamilton also speculated about possible proximate behavioural mechanisms that might be observable in organisms whereby a social trait could effectively achieve this necessary statistical correlation between its likely bearers:
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Hamilton here was suggesting two broad proximate mechanisms by which social traits might meet the criterion of correlation specified by the theory:
Kin recognition (active discrimination): If a social trait enables an organism to distinguish between different degrees of genetic relatedness when interacting in a mixed population, and to discriminate (positively) in performing social behaviours on the basis of detecting genetic relatedness, then the average relatedness of the recipients of altruism could be high enough to meet the criterion. In another section of the same paper (page 54) Hamilton considered whether 'supergenes' that identify copies of themselves in others might evolve to give more accurate information about genetic relatedness. He later (1987, see below) considered this to be wrong-headed and withdrew the suggestion.
Viscous populations (spatial cues): Even indiscriminate altruism may achieve the correlation in 'viscous' populations where individuals have low rates of dispersal or short distances of dispersal from their home range (their location of birth). Here, social partners are typically genealogically closely related, and so altruism can flourish even in the absence of kin recognition and kin discrimination faculties – spatial proximity and circumstantial cues provide the necessary correlation.
These two alternative suggestions had important effects on how field biologists understood the theory and what they looked for in the behavior of organisms. Within a few years biologists were looking for evidence that 'kin recognition' mechanisms might occur in organisms, assuming this was a necessary prediction of inclusive fitness theory, leading to a sub-field of 'kin recognition' research.
Later theoretical refinements.
A common source of confusion around inclusive fitness theory is that Hamilton's early analysis included some inaccuracies, that, "although corrected by him in later publications", are often not fully understood by other researchers who attempt to apply inclusive fitness to understanding organisms' behaviour. For example, Hamilton had initially suggested that the statistical correlation in his formulation could be understood by a correlation coefficient of genetic relatedness, but quickly accepted George Price's correction that a general regression coefficient was the more relevant metric, and together they published corrections in 1970. A related confusion is the connection between inclusive fitness and multi-level selection, which are often incorrectly assumed to be mutually exclusive theories. The regression coefficient helps to clarify this connection:
 ;templatestyles src="Template:Blockquote/styles.css" / ;Because of the way it was first explained, the approach using inclusive fitness has often been identified with 'kin selection' and presented strictly as an alternative to 'group selection'. But the foregoing discussion shows that kinship should be considered just one way of getting positive regression of genotype in the recipient, and that it is this positive regression that is vitally necessary for altruism. Thus the inclusive-fitness concept is more general than 'kin selection'.(Hamilton 1996 [1975], 337)
Hamilton also later modified his thinking about likely mediating mechanisms whereby social traits achieve the necessary correlation with genetic relatedness. Specifically he corrected his earlier speculations that an innate ability (and 'supergenes') to recognise actual genetic relatedness was a likely mediating mechanism for kin altruism:
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The point about inbreeding avoidance is significant, since the whole genome of sexual organisms benefits from avoiding close inbreeding; there is a different selection pressure at play compared to the selection pressure on social traits (see Kin recognition for more information).
 ;templatestyles src="Template:Blockquote/styles.css" / ;It does not follow… that ability to discriminate degrees of relatedness automatically implies that kin selection is the model relevant to its origin. In fact, since even earlier than Darwin, it had been realised that most organisms tend to avoid closely inbred matings. The reasons must have to do with the function of sexuality and this is not quite yet resolved (see e.g. Bell, 1982; Shields, 1982; Hamilton, 1982); but whatever the function is, here must be another set of reasons for discriminating. Some animals clearly do use discrimination for purposes of mate selection. Japanese quail for example evidently use an early imprinting of their chick companions towards obtaining, much later, preferred degrees of consanguinity in their mates (Bateson 1983). (Hamilton 1987, 419)
Since Hamiton's 1964 speculations about active discrimination