There is abundant evidence of nepotistic biases in primate groups. Altruistic behaviours, including grooming, coalitionary support and food sharing, are selectively directed towards genetic relatives. Moreover, these behaviours are preferentially directed towards closer kin over more distant kin. Both these patterns are consistent with qualitative predictions derived from kin selection theory and are commonly interpreted as the product of kin selection.
It is much more difficult to determine whether the distribution of altruistic behaviour fits quantitative predictions derived from Hamilton's rule, br > c
. This is because we are unable to measure the fitness benefits of altruistic acts for recipients and the costs of altruistic acts for donors. There is not even complete agreement about whether particular forms of behaviour are altruistic (Chapais 2001
; Chapais & Bélisle 2004
). For example, Dunbar (1988)
and Dunbar & Sharman (1984
) concluded that grooming must not be costly to perform because females do not reduce the amount of time that they devote to social grooming when they are under time budget constraints and do reduce the amount of time that they devote to other energetically expensive activities. But the same data could be interpreted to mean that grooming is costly, but serves essential social functions, and is too important to be neglected even in difficult times. Similarly, there is debate about the costs and benefits of coalitionary aggression, sharing access to food, giving alarm calls, forming friendships with new mothers and so on.
Quantitative predictions about the distribution of altruism are difficult to formulate because they depend on assumptions about the shape of the curve of benefits across time. For example, if the benefits of being groomed are constant across time, then all grooming should be directed towards the closest kin available (Altmann 1979
). But if there are declining returns from grooming across time, then groomers should eventually switch to less closely related partners. Constraints on time and energy, variation in the availability of preferred categories of partners, the opportunity costs of choosing more closely related partners over more competent partners, the possible benefits derived from reciprocity and a number of other factors further complicate predictions about the deployment of altruism in primate groups (Chapais & Bélisle 2004
). As a result, ‘the optimal allocation of altruism is unknown’ (Altmann 1979
), and Hamilton's rule cannot be tested with any degree of precision.
Chapais has suggested that this ambiguity may have encouraged us to overestimate the role of kin selection and underestimate the importance of other forces in the distribution of altruistic behaviour (Chapais 2001
; Chapais & Bélisle 2004
). There are at least two processes besides kin selection that could generate high rates of interaction among kin: (i) kin biases could reflect an attraction to animals of similar rank or (ii) kin biases could be a by-product of extended associations between mothers and their offspring.
In species with matrilineal dominance hierarchies, nepotistic biases may reflect an attraction to animals of similar rank, not an attraction to kin per se
. This argument was first proposed by Seyfarth (1977
), who suggested that females might exchange grooming for support in agonistic conflicts. Because high-ranking females make the most powerful allies, he predicted that all females would direct their grooming efforts towards the highest ranking females in their groups. However, time budgets constrain the amount of time available for being groomed (Dunbar 1991
), so females would have to compete for access to the highest ranking females. High-ranking females would be able to monopolize access to other high-ranking females, forcing lower ranking females to settle for grooming partners closer to their own rank and to trade grooming in kind. Related females occupy adjacent ranks, so this process would incidentally generate high rates of grooming among kin. Thus, kin biases emerge from competition over access to high-ranking allies. Several of the primary predictions of Seyfarth's model are well supported. Correlations between grooming and support are consistently observed, and monkeys interact at high rates with those of similar rank (Schino 2001
; Schino & Aureli 2007
However, there are several reasons to suspect that kin biases in behaviour are not simply an artefact of an attraction to females of similar rank. First, in baboons and macaques, females' preferences for maternal kin are stronger than their preference for unrelated females of adjacent rank (Silk 1982
; De Waal 1991
; Kapsalis & Berman 1996
; Silk et al. 1999
). Second, dominance rank and maternal kinship are disassociated in some species, but nepotistic biases persist (hanuman langurs, Borries et al. 1992
; mountain gorillas, Watts & Pusey 1993
; capuchins, Perry et al. 2008
; ring-tailed lemurs, Sauther et al. 1999
). Third, female baboons and macaques show preferences for paternal kin, who do not hold adjacent ranks (references above).
In species with female philopatry, matrilineal biases in behaviour may be the by-product of mother–infant association patterns, not the products of kin selection (Chapais 2001
). Mothers form close and enduring ties with their offspring. This means that as mothers wean one infant and produce another, they continue to associate with their older offspring. Maternal siblings are drawn together by their joint association with their mother. As daughters mature and produce offspring of their own, grandmothers and their grandoffspring will be brought together often. Aunts are similarly connected to their sister's daughters, their own nieces. If females interacted at random with their associates, high rates of interaction among kin would emerge without any deliberate preference for interacting with relatives.
This sort of process may influence the interactions of females in some situations. Young macaques interact at higher rates with the offspring of females that their mothers associate with at higher rates, and the degree of infants' kin biases is linked to the degree of their mothers' kin biases (Berman 2004
). In the Amboseli baboon groups, females groom and associate with their adult sisters and their sisters' daughters (nieces) at higher rates than they associate with unrelated females. Rates of interactions between aunts and nieces decline when the female who connects them dies (the aunt's sister and the niece's mother; Silk et al. 2006a
). But there are several reasons to believe that this is not the whole story. In the Amboseli baboon population, rates of interaction among maternal and paternal sisters rise after their mothers' deaths. This suggests that relationships among sisters are the product of a positive attraction towards preferred categories of partners. Moreover, if high rates of affiliation among close kin are simply a by-product of high rates of association, then we would also expect to observe elevated rates of aggression among them (Perry et al. 2008
). But rates of aggression among capuchins do not track rates of affiliation or the degree of relatedness among females, suggesting that ‘kin-biased distribution of grooming and coalitionary support is a product of selection for specifically benign dispositions towards females recognized as close kin’ (Perry et al. 2008
Chapais also points out that cooperative interactions among related females may be regulated by contingent reciprocity and mutualism, rather than kin selection. In fact, there is good reason to believe that these processes will reinforce each other. Kinship can enhance the stability of contingent reciprocity by making defections less costly and would also increase the benefits derived from mutualistic partnerships. There is some evidence that kinship enhances contingent reciprocity in baboon groups as females form more well-balanced grooming relationships with close female kin than with more distantly related kin and unrelated partners (Silk et al
; see also Janus 1989
). Similarly, high-ranking matrilines show the most pronounced nepotistic biases (Berman 1980
; Silk et al. 1999
), perhaps because kin selection enhances the individual benefits derived from developing alliances with powerful partners.
At the same time, reciprocity and mutualism do not provide plausible explanations for some forms of unilateral costly kin-biased behaviour described earlier. These include rank reversals among aged female baboons and their daughters, support for immature macaques involved in disputes with individuals from higher ranking families, fathers' protection of offspring from infanticidal attacks and female macaques' tolerance of subordinate relatives at feeding sites.