“Understanding the evolutionary origins and mechanisms involved in the maintenance of cooperation is a central problem in biology. Specifically, it is unclear why an individual (donor) should help another individual (beneficiary) if doing so is costly.
In light of this evolutionary puzzle, the theoretical constructs of kin selection (Hamilton, 1964), reciprocal altruism (Trivers,1971), direct benefits (also called by-product mutualisms) and group selection have surfaced as potential explanations.
In particular, the concept that cooperative traits may spread via kin selection is now a central paradigm in evolutionary biology. Although Robert A. Fisher (1930), John B. S. Haldane (1932) and Charles Darwin (1859) independently raised the notion that kinship might explain social evolution, it was William D. Hamilton (1964) who revolutionized evolutionary theory with his elegant inequality: b x r > c. Hamilton’s rule predicts that individuals should generally direct helpful behaviour towards relatives.
Now widely referred to as Hamilton’s Rule, this influential inequality predicts the spread of helpful behaviours via kin selection when the:
– net fitness benefits (b) to the beneficiary
– multiplied by the coefficient of relatedness between the donor and beneficiary (r)
– are greater than the costs (c) to the donor.
Hamilton’s seminal contribution has now inspired scholars for half of a century, giving rise to a large body of empirical evidence….Novel tests of Hamilton’s rule based on long-term behavioural and molecular data continue to offer exciting new insights…
Hamilton (1964) predicted that, if individuals possess the ability to discriminate on the basis of kinship, then they should gain inclusive fitness benefits by biasing helpful behaviour towards relatives, and harmful behaviour away from them. Kin selection therefore requires that animals either recognize specific individuals as genetic relatives (‘kin recognition’) or be able to discriminate between genetically related and genetically unrelated individuals (‘kin discrimination’). Indeed, kin discrimination is widely documented for mammals and operates largely via two major mechanisms: familiarity and phenotypic matching.
Kin discrimination based on familiarity, or shared associations, involves learning during a critical period of development during which relatives interact within contexts that vary with relatedness. For example, spatial overlap is common when family members share a burrow or den location. Individuals born at different times might also recognize each other as kin based on shared associations with a common parent.
Kin discrimination via phenotypic matching occurs when phenotypic similarity and genetic similarity are highly correlated.
In such circumstances, an individual assesses its relationships to others on the basis of one or more shared traits. This phenomenon is often referred to as the ‘arm-pit effect’ or ‘referential phenotype matching’ because some individuals make inferences about relatedness based on the smell (e.g. smelling their own ‘arm-pits’). Odour-based discrimination is often associated with genetic variation in the major histocompatibility complex (MHC)…Recognition may also be based on visual (e.g. chimpanzees, Pan troglodytes: vocal (e.g. spotted hyaenas), or both modes of information (rhesus macaques, Macaca mulatta). [Skin color and language in humans?]
Recent tests of kin discrimination revealed two new domains for assessing kin selection in social mammals.
First, studies now consider the role of paternal kinship in addition to maternal kinship in mammalian social evolution. This is important because nepotism is expected to occur to similar extents for both maternal and paternal kin…
Second, [studies show] that individual animals possess knowledge of third-party kin relationships, defined as an understanding of the kin-biased social bonds that exist among other individuals within their groups. That is, individuals who have just been involved in an aggressive interaction are most likely to redirect aggression towards the close relatives of their former opponent or avoid group mates that were heard fighting with the close relative of a higher-ranking female…These data importantly extend historical perspectives because they indicate that paternal and extra dyadic kin relationships are important, yet largely overlooked, targets of selection.
I focus primarily on evaluating the evidence for kin selection favouring three less well understood, yet equally salient, targets of selection: social partner choice, coalition formation and social tolerance (withholding aggression).
Evaluating these largely ignored domains is important because Hamilton originally proposed that kin selection might promote cooperation in viscous populations composed mostly of close relatives. Limited dispersal may indeed act as a cohesive force to promote cooperation among closely related neighbours, but may also expose relatives to intense local competition. In such cases, the direct costs of competition among kin may counteract the benefits of cooperation.
Theoretical work attempts to clarify the selective forces shaping the tensions between competition and cooperation among relatives, and identifies the need for a synthesis of the empirical evidence on this topic. Thus, a major goal of this review is to quantify the extent to which kinship promotes cooperation and protects against competition in mammals. Because females of most mammalian species are philopatric, remaining at home throughout their entire lives, cooperation is expected to evolve more often via kin selection in female than in male mammals. Given this, I focus primarily on the social acts of adult females and include some data on species for which males are the philopatric sex.”
Pedigree construction now allows for the evaluation of the extent to which individuals cooperate with their kin – based on coefficients of relatedness, r, which ranges from 0 to 1.:
– direct paternal and maternal descendants (e.g. offspring: r ¼ 0.5
– grandoffspring: r ¼ 0.25)
– collateral kin (e.g. r ¼ 0.5 for full siblings, r ¼ 0.25 for half siblings, r ¼ 0.125 for aunts or uncles)
Genetic estimators are useful in cases for which full pedigrees are unavailable. For example,
R reflects how similar two individuals are at a specific genetic locus relative to other individuals in the same population.
R values range from -1 to
1, and are highly variable across mammalian species.
Positive R values indicate that two individuals are more related than expected by chance. In large populations, the R value between any pair of individuals typically reflects the true coefficient of relatedness (r), and is therefore a useful alternative to coefficients of relatedness for testing kin selection theory.
[For example] squirrels only adopt genetic relatives when the benefits to the adopted juvenile (b), discounted by the degree of relatedness between the surrogate and the orphan (r), exceed the direct fitness costs of a female adding an extra juvenile to her litter (c).
Given that the evidence for cooperative breeding via kin selection is so compelling, and given the extensive coverage of this topic elsewhere, the remainder of this review focuses on evaluating the extent to which kin selection favours the evolution of short-lived social acts, such as the maintenance of spatial proximity, agonistic aiding via coalitionary interventions during ongoing fights and social tolerance (withholding aggression)…Here I focus on the best-studied species of nonhuman mammals for which there are sufficient data on genetic relatedness and the short-lived social behaviours identified here. In doing so, I also evaluate the notion that, because of their social complexity, nepotistic patterns in nonhuman primates might be unique among mammals…
Overall, patterns of association, proximity maintenance and spatial associations within social networks generally indicate that individuals prefer kin over nonkin as social partners.
In contrast to commonly held perceptions, primates are no more or less likely than nonprimates to show a kinship bias with respect to spatial proximity …As predicted by kin selection theory, mammals therefore typically bias affiliative behaviour towards genetic relatives, preferentially selecting for genetic kin as social partners with whom to associate. Although evidence for kin-biased proximity is overwhelming, the advantages of sharing space with kin can vary based on the current ecological circumstances, such as population demography and resource competition.
For example, ecological monitoring of our populations of red howler monkeys…suggested that the costs and benefits of nepotism are density dependent. Genetic data indicate that the reproductive
success of these monkeys, attributed primarily to the recruitment of daughters, increases with the degree of relatedness within groups at high population densities. When population density is approaching or at carrying capacity, monkeys are likely to belong to kin groups and, thus, nepotism is greater than when population densities are low. Long-term ecological monitoring of spotted hyaenas
suggests that resource competition also shapes kin-biased
patterns of space use in social carnivores. That is, although social
bonds among both kin and non kin are weakest when resource
competition is most intense for all group mates…
Agonistic aiding, also called intervention or coalition formation,
represents a cooperative act; intervening in a fight is potentially
costly to the donor, who risks physical injury, expends energy
fighting and allocates time to this behaviour that might otherwise
be devoted to other activities.
Agonistic aiding is beneficial to the recipient because it increases
the recipient’s likelihood of winning the fight.
Given this, Hamilton’s rule makes straightforward predictions
about coalition formation when the cost /benefit ratio is held
constant (e.g. within a specific ecological circumstance). That is,
individuals should intervene more often on behalf of kin than
non kin. As expected, all available evidence is consistent with the
notion that kin generally bias coalitionary support towards their
genetic relatives. Intragroup coalitions are generally favoured by
the combined evolutionary forces of indirect and direct benefits in
birds and mammals.
Social Tolerance and Withholding Aggression
Kin selection theory predicts that individuals should direct
fewer attacks or lower intensities of aggression (enhanced social
tolerance) towards closer kin than towards less related individuals.
However, evidence for the protective value of kinship in curtailing
rates of aggression, or promoting social tolerance, in free-living
mammals is limited.
Overall, rates of aggression
were reduced among kin for only 8 out of the 31 (26%) species
reviewed such that species were significantly less likely to be socially
tolerant of genetic relatives than expected by chance. That is, most species either
directed higher rates of aggression towards kin or failed to preferentially
tolerate group mates on the basis of kinship. Moreover, this
lack of nepotistic tolerance was statistically indistinguishable between
primates and nonprimates.
In many species, the overall rates at which adult individuals
direct aggression towards kin and non kin are simply indistinguishable.
For most species, however, individuals also
simultaneously gain indirect benefits from assisting kin and direct
benefits from forming ‘conservative coalitions’, during which allies
join forces to direct attacks towards subordinates, many of whom
are lower-ranking kin. Specifically, donors of
support immediately benefit from reinforcing the status quo in
low-cost contests during which they direct attacks down the
dominance hierarchy. Such findings generally suggest that direct
benefits gained through aggression often overwhelm the indirect
benefits of withholding aggression directed towards kin. For
example, in so far as coalitions help to maintain the status quo, it is
just as important to a female’s reproductive success that she
maintains her dominance over a lower-ranking sister or daughter
as she does over unrelated adult females.
Competition among relatives often emerges because kin are in
close spatial proximity and depend upon the same limited resources…an individual’s closest relatives, and by
extension his/her closest associates and/or social allies, are often
also his/her closest competitors.
The results here support these
notions that when this is true, as it is among most mammals,
competition among kin can reduce, or even negate, the kin-selected
indirect benefits of altruism directed towards relatives. Interestingly,
in such contexts, the direct benefits gained from outcompeting
relatives through forces such as sibling rivalry and
parent conflict generally appear to overwhelm the indirect benefits
of social tolerance among kin. In some species, rates of conflict actually increase with levels of genetic relatedness.