Relatedness threshold and the degree of relatedness

Introduction

Sociality reflects a balance between co-operation and competition (Alexander 1974, Silk 1987, Walters & Seyfarth 1987). Kinship has had an important effect on the structure of social relationships among primates, especially in female-bonded groups with male dispersal (Gouzoules & Gouzoules 1987). Maternal kinship in primates frequently coincides with proximity patterns and a higher frequency of grooming with grooming being reciprocal among kin (e.g., Kurland 1977, Gouzoules & Gouzoules 1987, Kapsalis & Berman 1996a, reviewed by Dugatkin 1997). Relatives tolerate each other more often at feeding sites than non-kin (Kawai 1958, Stewart & Harcourt 1987, Pastor-Nieto 2001, Belisle & Chapais 2001.) and food sharing is more common among kin than among non-kin (Goodall 1968, Silk 1978, 1979). Female primates also prefer to support their kin in aggressive interactions against non-kin and take more risk on behalf of close kin (e.g., Kurland 1977, Kaplan 1977, 1978, Massey 1977, Walters 1980, Silk 1982, Bernstein & Ehardt 1985a, reviewed in Gouzoules & Gouzoules 1987). On the other hand, agonistic interactions of immature rhesus monkeys are more frequent among strongly affiliated partners (i.e., maternal half-siblings) than among weakly affiliated partners (i.e., non-siblings) (Janus 1991). Female relatives do not refrain from acting aggressively toward kin, and are often disproportionately more aggressive towards maternal kin than non-kin (Kurland 1977; Bernstein & Ehardt 1986a), but Silk et al. (1981) found that female bonnet macaques, M. radiata, direct more severe aggression towards non-kin than towards kin.

Although there is a lot of evidence that primates bias their social behaviour towards their (maternal) kin, less is known about how this bias varies with the degree of relatedness between individuals. Some scientists have suggested that kin bias might decrease proportionally with the degree of relatedness and in addition, a relatedness threshold may be expected under which distant kin are treated like unrelated individuals (Chapais et al. 1997). Others have suggested that the distribution of social behaviour may asymptotically decrease with the degree of relatedness, as it pays more to give as much as possible to the closest kin to gain the highest possible benefit as predicted from the probability theory (S. Altmann 1979). However, data from the same population as studied here, suggest that adult female rhesus macaques behave preferentially toward close maternal kin compared to distant maternal kin, but do not discriminate between distant maternal kin (r<0.125) and non-kin, suggesting that a relatedness threshold limits nepotism (Kapsalis & Berman 1996a). Among captive Japanese macaques, mothers and sisters supported their daughters and younger sisters to outrank peers (Chapais 1988a). Likewise, in the presence of their grandmother, granddaughters were able to outrank all dominant peers, but in the presence of their aunt, nieces were not. These results also point to a relatedness threshold for effective nepotistic aiding above the aunt–niece level of relatedness (again r<0.125) (Chapais et al. 1997). In addition, Japanese macaque great-grandmothers support great-grandsons more often than aunts support nephews, despite identical levels of relatedness (Chapais et al. 2001) indicating that kin category in addition to the degree of relatedness modifies primate behaviour. Again, nothing is known about the degree of relatedness with respect to paternal kinship.

One means of examining more precisely how relatedness affects affiliative and agonistic interactions is to scrutinise the role of both paternal and maternal relatedness, given that offspring are equally related to their mothers as to their fathers. Establishing the role of paternal kinship is problematic because females tend to mate with multiple males. Therefore, this chapter aims to investigate the effect of the degree of relatedness on affiliation and aggression among a wider range of relatedness for both maternal and paternal kinship than presented in the previous chapter. The existence of a relatedness threshold will be tested and a comparison will be made between individuals who share the same degree of relatedness but belong to a different kin category (e.g., dyads of maternal half-siblings vs. grandmother-granddaughter). Finally, data on both kin lineage will be compared.

Results Testing the effect of the degree of relatedness on affiliation and aggression

Table 5.1 shows data on affiliation and aggression for a number of kinship categories (see Methods) which were restricted to non-peer dyads in order to control for familiarity among peers which has been demonstrated in the previous chapter.

Cell values are mean frequencies per hour (± SD) for proximity, grooming, approach, physical or non-physical aggression. Abbreviations are as follows: dyads of mother-daughters (MD), maternal half-siblings (MS), maternal grandmother-granddaughters (MGMD), maternal aunt-nieces (MAN), maternal grandaunt-grandnieces (MGAN), maternal cousins (MC), paternal half-siblings (PS), paternal aunt-nieces (PAN), non-kin (NK), degree of relatedness (r), sample size (N). Data were based on all of the 34 focal females who had at least one kin in a specified kin class, e.g., 32 out of the 34 females had a mother-daughter relation, 10 out of 34 females had a grandmother-granddaughter relation etc. All categories include only data for female non-peer dyads to control for familiarity among peers. Dyads that fit in more than one category (e.g., being paternal half-siblings and maternal aunt-niece) were excluded in all analyses.
r

N

Proximity

Grooming

Approach

Physical Aggression

Non-physical Aggression

MD

0.5

32

6.060 ± 2.112

2.070 ± 0.978

3.896 ± 1.281

1.117 ± 0.151

0.080 ± 0.088

MS

0.25

34

2.117 ± 1.087

0.372 ± 0.301

1.581 ± 0.754

0.017 ± 0.022

0.050 ± 0.041

MGMD

0.25

10

1.437 ± 1.194

0.446 ± 0.456

1.109 ± 0.895

0.021 ± 0.036

0.016 ± 0.025

MAN

0.125

34

0.927 ± 0.480

0.095 ± 0.156

0.645 ± 0.345

0.010 ± 0.017

0.021 ± 0.018

MGAN

0.0625

25

0.510 ± 0.331

0.031 ± 0.077

0.349 ± 0.193

0.006 ± 0.014

0.018 ± 0.026

MC

0.0625

28

0.488 ± 0.310

0.020 ± 0.025

0.352 ± 0.168

0.004 ± 0.007

0.019 ± 0.017

PS

0.25

19

0.450 ± 0.302

0.012 ± 0.026

0.308 ± 0.160

0.002 ± 0.007

0.024 ± 0.040

PAN

0.125

19

0.352 ± 0.274

0.029 ± 0.065

0.258 ± 0.243

0.001 ± 0.003

0.008 ± 0.015

NK

~0.0

34

0.350 ± 0.111

0.011 ± 0.007

0.232 ± 0.054

0.003 ± 0.002

0.013 ± 0.006

Table 5.5.1: The effect of degrees of relatedness on affiliation and aggression in different kin categories

Not surprisingly, the highest rates of affiliation were found in mother-daughter dyads, while the lowest rates occurred among non-kin. There is a proportional decrease with degree of relatedness among maternal and paternal kin, even though values of paternal kin were always lower than the equivalent maternal degree of relatedness. Note, some paternal cousins existed in the study group, but as these females were not adults they were not focal subjects.

Data from Table 5.1 were tested for a possible correlation between degree of relatedness and frequency of affiliation or aggression respectively. From kin selection theory (Hamilton 1964) one predicts that an increase in the degree of relatedness will result in an increase in affiliation and a decrease in aggression. Spearman’s rank correlation coefficient is presented in Table 5.2 using only maternal degrees of relatedness introduced in Table 5.1, because just two paternal degrees of relatedness were available.

N

Proximity

Grooming

Approach

Physical Aggression

Non-physical Aggression

Maternal kin

163

r_s=0.840

r_s=0.844

r_s=0.860

r_s=0.413

r_s=0.352

P<0.001

P<0.001

P<0.001

P<0.001

P<0.001

Table 5.5.2: Correlation between various maternal degrees of relatedness and affiliation or aggression, respectively

Spearman’s rank correlation coefficient (r _s ) between various maternal degrees of relatedness and affiliation or aggression, respectively. Data were the same presented in Table 5.1 using only non-peers. N is the number of focal females tested treating the same focal female with social partners from different kin categories as independent.

The maternal degree of relatedness was significantly associated with the frequency of affiliation and aggression in such a way that there was an increase in affiliation the closer females were related, but different from what was expected, there was also an increase in aggression the closer females were related.

Testing the relatedness threshold concept on affiliation and aggression

Table 5.3 presents data testing the relatedness threshold concept. This concept predicts that distant kin and non-kin are treated alike below a certain degree of relatedness. Furthermore, it supposes that depending upon the cost-benefit ratio different behaviours may differ in respect to their relatedness threshold.

Testing the relatedness threshold concept on affiliation and aggression using paired t-tests between kin groups of various degree of relatedness. Data and abbreviations are from Table 5.1, but include only matched samples, i.e., focal females who had a kin in both test groups. P’ represents the Dunn-Šidák correction for multiple testing undertaken for 10 simultaneous tests, i.e., per single behaviour for Table 4.2-4.4 chapter 4 and Table 5.3-5.4 this chapter (see Methods). Recall from the Methods that only P-values less than or equal to the corrected P-value (P’) indicate a significant test result which will be marked in bold.
Kin class

R

N

Proximity

Grooming

Approach

Physical Aggression

Non-physical Aggression

MGAN

vs. NK

0.0625

vs. 0.0

25

t=-3.044
P=0.006
P’=0.006

t=-1.413

P=0.171

P’=0.009

t=-3.183
P=0.004
P’=0.009

t=-1.318

P=0.200

P’=0.009

t=-1.046

P=0.306

P’=0.017

MC

vs. NK

0.0625

vs. 0.0

28

t=-2.773

P=0.010

P’=0.007

t=-2.073

P=0.048

P’=0.006

t=-4.111
P<0.001
P’=0.007

t=-0.948

P=0.351

P’=0.013

t=-2.384

P=0.024

P’=0.006

PAN

vs. NK

0.125

vs. 0.0

19

t=0.101

P=0.921

P’=0.050

t=-1.103

P=0.284

P’=0.013

t=-0.599

P=0.557

P’=0.025

t=3.112
P=0.005
P’=0.005

t=1.632

P=0.120

P’=0.010

PS

vs. PAN

0.25

vs. 0.125

14

t=-3.466
P=0.004
P’=0.006

t=-1.140

P=0.275

P’=0.010

t=-5.005
P=0.001
P’=0.006

t=0.012

P=0.991

P’=0.050

t=-2.061

P=0.060

P’=0.007

Table 5.5.3: Testing the relatedness threshold concept on affiliation and aggression

Maternal grandaunt-grandniece dyads (r=0.0625) had higher rates of proximity and approach, but not of grooming, than non-kin dyads (r~0.0). No difference between them was found for aggressive interactions. Maternal cousins (r=0.0625) differed in approach from non-kin (r~0.0), with a trend evident in proximity, grooming and non-physical aggression. Paternal aunt-niece dyads (r=0.125) showed similar rates of affiliative interactions, but significantly less physical aggression, than non-kin (r~0.0). In addition, it was tested whether paternal half-siblings differ in their behaviour from paternal aunt nieces, as predicted by the higher degree of relatedness. Indeed, paternal half-siblings (r=0.25) exhibited higher rates of proximity and approach, and tended to express less non-physical aggression, than paternal aunt-nieces (r=0.125).

Testing the effect of different kin categories on affiliation and aggression controlling for degree of relatedness

A comparison will be made between individuals who share the same degree of relatedness but belong to different kin categories (Table 5.4). For example, dyads of maternal grandmother-granddaughters and dyads of maternal half-siblings both share on average 0.25 of their genes, but the former are direct descendants (direct line) while the latter are collateral kin (cf. Chapais et al. 2001). As a second example, dyads of maternal grandaunt-grandniece and maternal cousins both share on average 0.0625 of their genes, but both are collateral kin.

The effect of kin category on affiliation and aggression using paired t-tests between different kin categories who share the same degree of relatedness. Data and abbreviations are from Table 5.1, but include only matched samples, i.e., focal females who had a kin in both test groups. P’ represents the Dunn-Šidák correction for multiple testing (see Methods).
Kin class

r

N

Proximity

Grooming

Approach

Physical Aggression

Non-physical Aggression

MGMD

vs. MS

both

0.25

10

t=1.323
P=0.219
P’=0.010

t=-0.248
P=0.810
P’=0.025

t=0.155
P=0.154
P’=0.017

t=-1.057
P=0.318
P’=0.010

t=2.202
P=0.055
P’=0.006

MGAN

vs. MC

both

0.0625

22

t=-0.288
P=0.776
P’=0.025

t=-1.060
P=0.301
P’=0.017

t=-0.373
P=0.713
P’=0.050

t=-0.789
P=0.439
P’=0.017

t=0.059
P=0.954
P’=0.050

Table 5.5.4: The effect of kin category on affiliation and aggression

Both comparisons reveal that kin category (neither direct vs. collateral nor collateral vs. collateral) did not influence the extent of affiliation and aggression, when they share the same degree of relatedness.

Testing the effect of kin lineage and degree of relatedness on affiliation and aggression

A two-way analysis of variance was applied to simultaneously examine the influence of both kin lineage (either maternal or paternal) and degree of relatedness (either half-siblings with r=0.25 or aunt-nieces with r=0.125) on all affiliative and agonistic behaviours. For maternal half-siblings I used data on 34 focal females, for paternal half-siblings 19 focal females, for maternal aunt-nieces 34 focal females and for paternal aunt-nieces 19 focal females. Indices of the same focal animal with social partners of different levels of relatedness were treated as independent. Two kin categories for both kin lineages could be tested, because these two were only available for paternal kin (Table 5.5) .

Data from Table 5.1. Kin lineage was either maternal or paternal kin, r is the degree of relatedness either 0.25 or 0.125 and kin lineage * r represents the interaction, d.f. are the degrees of freedom. All data on non-peers.
ANOVA Two- way

Proximity

Grooming

Approach

Physical Aggression

Non-physical Aggression

Kin lineage (d.f.=1)

F=63.074

F=28.979

F=70.664

F=13.609

F=8.985

Maternal vs. Paternal

P<0.001

P<0.001

P<0.001

P<0.001

P<0.003

r (d.f.=1)

F=20.803

F=10.892

F=24.959

F=1.686

F=12.669

0.25 vs. 0.125

P<0.001

P=0.001

P<0.001

P=0.197

P<0.001

Kin lineage * r (d.f.=1,102)

F=14.949

F=13.893

F=20.162

F=0.660

F=0.962

P<0.001

P<0.001

P<0.001

P=0.418

P<0.329

Table 5.5.5: Testing the effect of kin lineage and degree of relatedness on affiliation and aggression

Kin lineage had a significant impact on all affiliative and aggressive interactions investigated and likewise the degree of relatedness with the exception on physical aggression. However, the interaction between kin lineage and degree of relatedness was significant for all three affiliative interaction, but for none of the two aggressive interactions (see also Fig. 5.1).

Fig. 5.5.1 Mean frequency of proximity, grooming, approach, physical and non-physical aggression as a function of the degree of relatedness for maternal kin (squares) and paternal kin (triangle). The interaction between kin lineage and degree of relatedness is significant when the lines for maternal and paternal kin are different from parallel.

Discussion

Using a wider range of degree of relatedness for both maternal and paternal kinship than just half-siblings (see chapter 4), there emerge four main results from this chapter. First, affiliation and aggression both increase as the degree of maternal relatedness among females increases supporting findings of other studies. Second, no evidence was found in this study for the existence of a relatedness threshold, because distant kin could still be differentiated from non-kin. Third, females from different kin categories sharing the same degree of relatedness do not differ in affiliation and aggression, suggesting that kin category is not as important as reported by other studies. Fourth, there emerged an asymmetry in affiliation and aggression between maternal and paternal kin lineage, with the maternal kin lineage being both more affiliate and aggressive than the paternal kin lineage. These points will now be discussed in more detail.

Degree of relatedness

The results of the present chapter suggest that affiliation, but likewise aggression increase proportionally with an increase in the degree of maternal relatedness. Few studies have investigated how nepotism varied according to the degree of relatedness, but they all report that frequencies of affiliation or tolerated co-feeding increase with an increase in the degree of maternal relatedness (Kurland 1977, Berman 1982, Beckerman Glick et al. 1986, Singh et al. 1992, Kapsalis & Berman 1996a, Belisle & Chapais 2001). The latter study further indicates that patterns of spatial proximity decreased asymptotically with decreasing degree of relatedness, while grooming decreased proportionally with decreasing degree of relatedness which may also indicate context-dependent kin discrimination among maternal kin (cf. Kapsalis & Berman 1996a, Fig. 4). However, Kapsalis & Berman (1996a) concluded from their study that distinguishing close kin (r≥0.125) from non-kin explains better the distribution of behaviour than using the all degrees of relatedness.

Hamilton’s kin selection theory (1964) predicts that the more individuals are related the more they should direct affiliation towards each other, but likewise, the less they should direct aggression towards each other (cf. Hamilton 1987). The first prediction was met by the data presented, but aggression was in contrast to what is predicted. Nevertheless, the data seem plausible, as close kin spend an enormous time in close spatial proximity, that the likelihood of aggression, both initiated and received, is higher too. High levels of aggression among close kin were also reported from other studies on Japanese macaques (Kurland 1977) and rhesus macaques (Bernstein & Ehardt 1986a). Silk et al. (1981) found that female bonnet macaques direct more severe aggression towards non-kin than towards kin, but the present study suggests that less affiliative dyads (i.e., distant kin and non-kin) direct less physical aggression than non-physical aggression towards each other (cf. Table 5.1). The most frequent aggression in the present study was found in mother-daughter pairs, directed from mother to their daughters, which reflects the importance of aggression in the socialisation of rhesus macaques (Bernstein & Ehardt 1986a) given the fact that this species has the most despotic hierarchy among all macaques species. Bernstein & Ehardt (1986a) noted that aggression received from kin declined as individuals matured, with females of all ages directing aggression more to kin than non-kin, whereas males involvement in kin aggression decreases with age.

Relatedness threshold

As a second result, distant maternal kin with a degree of relatedness of r=0.0625 still affiliate more than unrelated females, but no difference was found in respect to aggression. On the other hand, paternal kin sharing a degree of relatedness of r=0.125 show no difference in affiliation in comparison to unrelated females, but show significantly less physical aggression than unrelated females. These results contradict previous studies (Kapsalis & Berman 1996a, Chapais et al. 1997, 2001) which found no difference between distant kin and non-kin for any behaviour measured concluding the existence of a relatedness threshold (but cf. also Silk et al. 2002). As mentioned above, the concept of a relatedness threshold predicts that, despite differences in the degree of relatedness, distant kin and non-kin do not differ in the extent of their behavioural interactions. However, maternal and paternal kin in the present study differed in comparison to non-kin, but the context expressing this differences was not the same, as there emerged a higher level of affiliation among maternal kin in comparison to non-kin, but a reduced level of aggression among paternal kin in comparison to non-kin.

The contradictions found across studies could be due to different behaviour examined, as the concept of a relatedness threshold predicts that depending upon their cost-benefit ratio different behaviours may have a different relatedness threshold (cf. Chapais 2001). From experimental study on captive Japanese macaques, Chapais et al. (2001) suggested a relatedness threshold among direct kin at r=0.125 (great-grandmothers) and among collateral kin at r=0.25 (half-siblings), because effective kin support was only observed at or above this degree of relatedness and never below. Chapais et al. (1997, 2001) studied the concept of relatedness threshold on coalition formation, a behaviour which can be very costly for the actor compared to the behaviours I used here. However, analyses on coalition formation (see next chapter) need to consider the observed and expected frequency of support, as the opportunities of interventions depend upon the likelihood that certain individuals (e.g., kin) are involved in aggressive conflicts. In other words, if one has only one paternal half-sister who tends to be rarely involved in dyadic aggression, then one rarely has the chance to support her. Chapais et al. (1997, 2001), in contrast, induces experimental conditions by isolating kin of certain degrees of relatedness to study coalition formation which is not comparable with studying coalition formation in free-ranging animals.

A second study on the same population than studied here concluded that a relatedness threshold among maternal kin might operate at the level of r=0.125 (Kapsalis & Berman 1996a) investigating similar affiliative interactions than the present study. First, it seems likely that the discrepancy between Kapsalis & Berman (1996a) and the present study is influenced by the number of kin available, as the former study group had up to 320 individuals which may exceed the natural ability of a monkey to recognise such a high number of individuals and/or kin. Second, due to the lack of paternity data in their study, paternal kin were not differentiated from non-kin so both were pooled as maternally unrelated individuals. Third, Kapsalis & Berman (1996a) found that extremely distant kin (r≥0.0005) were treated similarly to non-kin. As the present study was unable to investigate extremely distant kin (with r<0.0625), then contradictions may have arose due to the use of different degrees of relatedness. With respect to the importance of paternal kinship and age proximity on female social relationships (see previous chapter), as well as methodological differences among studies, the idea of a relatedness threshold should be re-evaluated in more detail.

Finally, it should also be emphasised, that the absence of nepotism may also reflect limits of kin recognition. Because any female would benefit from supporting any of her relatives that are within the relatedness threshold, two alternatives for the absence of nepotism between distant kin are likely: (i) females recognise their distant kin, but they do not derive a net benefit from helping them and (ii) females do not recognise their distant kin even though they are within the relatedness threshold and nepotism might still be profitable (cf. Beecher 1991, Mateo 2002).

Kin categories

As a third result, no significant difference was found for maternal kin who shared the same degree of relatedness but belonged to different kin categories (e.g., for r=0.25 between maternal grandmother-granddaughters vs. maternal half-siblings). This also contrasts the results found by Chapais et al. (2001) who suggested that kinship category (e.g., direct or collateral), in addition to the degree of relatedness, is a key variable affecting the occurrence of altruistic behaviour. Chapais et al. (2001) concluded this from their study on female Japanese macaques who provided support to maternal kin. They found that great-grandmothers (r=0.125, direct kin) provided constantly support to their great-grandchildren, but aunts (r=0.125, collateral kin), grandaunts and cousins (both r=0.0625, collateral kin) abstained from doing so (ibid.). Although it seems likely that direct kin are more familiar than collateral kin, rank is inherited in a vertical way, with direct kin occupying adjacent ranks. It is therefore likely that competition over rank is higher among collateral kin than among direct kin, since in the latter case the higher-ranking individual (e.g., mother) passes on its own rank towards the other individual of the dyad (e.g., daughter) with the mother having a self-interest that her daughter acquires the rank predicted from birth in order to develop strong alliances with her in the future.

Kin lineage

As a fourth result revealed from the data, kin lineage either maternal or paternal was influencing all measurements of affiliation and aggression. In addition, the degree of relatedness (whether r=0.25 or r=0.125) was significantly influencing all measurements of affiliation and non-physical aggression and the interaction between kin lineage and degree of relatedness was significantly influencing all measurements on affiliation. Again, a context-dependent impact emerged from the data, but likewise a strong asymmetry between maternal and paternal kin. Given that maternal kin are generally closer in rank than paternal kin or non-kin (unpubl. data), the bias towards maternal kin may be a by-product of the attraction to similar ranking females as suggested by de Waal (1991), Kapsalis & Berman (1996a,b) and Chapais et al. (1991, 1994).

Summary

The results of this chapter extend earlier findings demonstrating that paternal kin discrimination regulates affiliative and aggressive interactions among adult female rhesus macaques (Widdig et al. 2001 and previous chapter). Both affiliation and aggression declined with decreasing degrees of relatedness among maternal kin. Distant kin still differentiated each other from non-kin, contradicting the existence of a relatedness threshold. Furthermore, individuals sharing the same degree of relatedness but belonging to different kinship category (direct vs. collateral) seemed not to differ in exhibiting social behaviour. Individuals who were maternally related adjusted their affiliation and aggression according to their degree of relatedness, this trend was not as clear for paternal kin with only two kin categories available for testing. This asymmetry in social relationships when the degree of relatedness was held constantly suggests that maternal kinship was more important than paternal kinship in the study group.