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.
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.
Some of these later arguments were produced by other scientists, including biologists and anthropologists, against Wilson's 1975 book Sociobiology: The New Synthesis, which was influenced by (though not necessarily endorsed by) Hamilton's work on inclusive fitness theory.
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."
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.
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.
[1] 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.
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: The selective advantage which makes behaviour conditional in the right sense on the discrimination of factors which correlate with the relationship of the individual concerned is therefore obvious.
In fact, the individual may not need to perform any discrimination so sophisticated as we suggest here; a difference in the generosity of his behaviour according to whether the situations evoking it were encountered near to, or far from, his own home might occasion an advantage of a similar kind."
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.
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).
Due to conflicting genetic similarity in the rest of the genome, there would be selection pressure for green-beard altruistic sacrifices to be suppressed via meitoic drive.
There is a huge theoretical literature on the possible role of limited dispersal reviewed by Platt & Bever (2009) and West et al. (2002a), as well as experimental evolution tests of these models (Diggle et al., 2007; Griffin et al., 2004; Kümmerli et al., 2009).
Furthermore, a large number of authors appear to have implicitly or explicitly assumed that kin discrimination is the only mechanism by which altruistic behaviours can be directed towards relatives... [T]here is a huge industry of papers reinventing limited dispersal as an explanation for cooperation.
Although mammals exist in a wide variety of ecological conditions and varying demographic arrangements, certain contexts of interaction between genetic relatives are nevertheless reliable enough for selection to act upon.
These conditions lead to a reliable spatial context in which there is a statistical association of replica genes between a reproductive female and her infant offspring (and has been evolutionary typical) for most mammal species.
(Bekoff 1981, 309)In addition to the above examples, a wide variety of evidence from mammal species supports the finding that shared context and familiarity mediate social bonding, rather than genetic relatedness per se.
The debate about how to interpret the implications of Inclusive fitness theory for human social cooperation has paralleled some of the key misunderstandings outlined above.
In other words, many biologists assumed that strong social bonds accompanied by altruism and cooperation in human societies (long studied by the anthropological field of kinship) were necessarily built upon recognizing genetic relatedness (or 'blood ties').
Anthropologists have gathered very extensive ethnographic data on human social patterns and behaviour over a century or more, from a wide spectrum of different cultural groups.
The data demonstrates that many cultures do not consider 'blood ties' (in the genealogical sense) to underlie their close social relationships and kinship bonds.
Compatible with biologists' emphasis on familiarity and shared context mediating social bonds, the concept of nurture kinship in the anthropological study of human social relationships highlights the extent to which such relationships are brought into being through the performance of various acts of sharing, acts of care, and performance of nurture between individuals who live in close proximity.
Additionally the concept highlights ethnographic findings that, in a wide swath of human societies, people understand, conceptualize and symbolize their relationships predominantly in terms of giving, receiving and sharing nurture.
Both Schneider and Holland argue that the earlier blood theory of kinship derived from an unwarranted extension of symbols and values from anthropologists' own cultures (see ethnocentrism).