In social mammals, kinship is an important factor that often affects the interactions among individuals within groups. In primates that live in a multilevel society, kinship may affect afﬁliative patterns be- tween individuals at different scales within the larger group. For this study, we use ﬁeld observations and molecular methods to reveal the proﬁles of how kinship affects afﬁliative behaviors between indi- viduals in a breeding band of wild golden snub-nosed monkeys (Rhinopithecus roxellana). We use a novel nonparametric test, the partition Mantel test, to measure independently the correlation between kinship and each of three afﬁliative behaviors. Our results show that more closely related females are more likely to groom each other. Average relatedness between adult females within the same one- male unit (OMU) is higher than that between adult females from different OMUs. We suggest that closely related females may reside in the same OMU in order to attain inclusive ﬁtness beneﬁts, and that kinship plays an important role in maintaining the social structure of this species. Key words: golden snub-nosed monkey, kinship, afﬁliative behavior, partition mantel test. High kinship among individuals is known to facilitate positive social Within nonhuman primates positive social interactions, which interactions in a variety of animal taxa such as insects (Foster et al. are typically regarded as affiliative behaviors, are generally classified 2006), amphibians (Blaustein and Waldman 1992), reptiles (Davis as grooming, close proximity distances, food sharing, and agonistic 2012), birds (Nam et al. 2010), and mammals (Mateo 2002). support (Strayer and Harris 1979; Sussman et al. 2005). Affiliative According to kin selection theory, positive kin bias among individuals behaviors account for >80% of the time that primates spend on so- can evolve via inclusive fitness (Hamilton 1964). Many nonhuman cial activities (60 primate species from 28 genera) (Sussman et al. primate species have complex social structures based on variable hier- 2005). This suggests that affiliative behaviors play an important role archies within each group, which are often established through social in the formation of social alliances among individuals, and are im- ties via the implementation of different strategies and behaviors portant for maintaining complex primate social systems. Other stud- (Morin and Goldberg 2004). Such species are thus ideal model sys- ies have found that behaviors associated with affiliation also reduce tems for investigating the role of relatedness among individuals, and competition within groups by increasing the likelihood of groups ac- how this helps maintain a stable social structure within groups. cessing resources, ease social tensions after fighting with each other V C The Author (2017). Published by Oxford University Press. 441 This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact email@example.com Downloaded from https://academic.oup.com/cz/article-abstract/64/4/441/3964668 by Ed 'DeepDyve' Gillespie user on 22 August 2018 442 Current Zoology, 2018, Vol. 64, No. 4 and other groups (Mitani and Watts 2010), and maintain or im- Materials and Methods prove social status within a group (Surbeck and Hohmann 2011), Study site each of which may increase the reproductive rates of some individ- Our study site is located near to YuHuang Miao Village, in the uals (Pope 2000; Surbeck and Hohmann 2011). ZhouZhi National Nature Reserve (ZNNR, 108 14’ – 108 18’E, Previous studies on kinship in primates were often conducted via 33 45’ – 33 50’N), on the northern slope of the Qinling Mountains. long-term recording of individual specific behaviors in the field and This region has a temperate climate and ranges in altitude from focused mainly on terrestrial species, rather than those that are pri- 1400 to 2890 m above sea level (Figure 1). The annual average tem- marily arboreal such as colobine monkeys (Silk 2002). The disad- perature is 10.7 C, and its annual average rainfall is 894 mm vantage of such an approach is that kinship determined solely from (Li et al. 2000). field observation may be inaccurate, due to environmental vari- The Nancha River separates the two monkey troops present in ations and vegetation barriers, and a lack of standardization in the our study site: the East Ridge Troop (ERT), which is comprised of methods used among researchers. Thus, molecular methods have the HSG and GTS herds, and the West Ridge Troop (WRT), which been used in addition to the data obtained from ‘traditional’ field is consisted of the GNG and DJF herds. This study only involved the work in order to efficiently and correctly measure kinship between GNG herd, which has been studied for the last 16 years using partial individuals (Widdig et al. 2002). For instance, Widdig et al. (2002) food provision in order to enable close observation. In the summer measured the pairwise kinships between 91 female rhesus macaques and in the autumn, the WRT mainly occupies areas characterized by Macaca mulatta based on data from 15 microsatellite loci and field high densities of trees, which sometimes makes behavioral observa- records of patterns of several social behaviors. Gagneux et al. tions difficult. Our field work was thus mainly conducted in winter (1999) genotyped 11 microsatellite loci from a total of 21 chimpan- and spring, when temperatures are often low and the ground is cov- zees Pan troglodytes to identify which female chimpanzee had off- ered with snow. The study was conducted from October 2012 to spring fathered by a male from a different group. Silk et al. (2006) June 2013, when the breeding band of the GNG herd comprised of amplified 14 microsatellite loci from baboons Papio cynocephalus 13 OMUs and 71 adult individuals. We focused on the adult females to successfully identify the paternities of 286 individuals. in four OMUs because their compositions were more stable during The golden snub-nosed monkey Rhinopithecus roxellana is a colo- the observation period than the other OMUs. The unit compositions bine monkey species endemic to the broadleaved and mixed temperate and sampling information are presented in Table 1. The adult indi- mountain forests of central and southwestern China (Li et al. 2003). viduals from other OMUs were also sampled so as to accurately esti- The social structure of R. roxellana is characterized by the multilevel mate the allele frequencies and relatedness coefficients among society, which is organized into four nested levels of social associations: OMUs. unit, band, herd, and troop. More specifically, units can be further div- ided into: (1) one-male units (OMU), consisting of a single adult male and 1–7 adult females with their immature ones including infants, and Behavioral observations (2) all male units (AMU), which consist of multiple young ‘bachelor’ Adult females were observed with both focal animal sampling and males yet to secure reproductive opportunities and some adult males scan sampling methods (Altmann 1974), and using both continuous that have been usurped from OMUs. Bands can also be divided into ei- recording (all-occurrence recording) and instantaneous sampling ther: (1) breeding bands (BB) (each an association of several OMUs), methods (Martin and Patrick 2006). Each of twenty-one females and all-male bands (AMB) (each an association of several AMUs). An from four OMUs (PK, HB, SH, RX) were randomly selected and AMB will usually be closely associated with a BB. Collectively, an observed continuously for a period of three hours. Affiliative behav- AMB, a BB and several solitary males aggregate to form a herd (Qi ior patterns of the females, such as grooming another female, prox- et al. 2014), the size of which commonly exceeds 100 individuals imity to another female and approaching or being approached by (Zhang et al. 2006). Neighboring herds periodically fuse to form a another female, were recorded. Two focal females were monitored troop (Qi et al. 2014). Males leave their natal OMU before reaching during each observation day. If the target female moved out of view, sexual maturity and join an all-male band. Some females stay in their or if most of the OMU members of the target female moved away, a natal OMU and produce offspring. However, most females disperse new target female was chosen to follow for 3 h. Both focal-animal into other OMUs within the same breeding band, or occasionally, into behavioral sampling and continuous (all-occurrence) recording a neighboring breeding band (Qi et al. 2009). Most social activities methods were used to record grooming and approach behaviors. occur among individuals within the same unit. The behavioral patterns The initiator and receiver of each interaction, the duration of each of the individuals from different OMUs include playing among juven- interaction and the behaviors exhibited after the initial approach, iles, and aggression among adults (Zhang et al. 2008). were recorded. The scan sampling and instantaneous recording Golden snub-nosed monkeys are mainly arboreal, making it diffi- methods were used for recording proximity behavior, which cult to measure kinship between individuals via behaviors associated involved the recorded individuals near to the focal adult female. The with kinship through field observations alone. Therefore, direct genetic definitions of grooming, approach, and proximity are defined as evidence is also required to obtain kinship measurements between pairs follows. of individuals. Furthermore, due to the long-term provisioning of food Grooming one adult female grooms another adult female, to the study breeding band, different behavioral patterns and associ- including picking out small objects (e.g., dirt or parasites) from the ations among individuals can be relatively easily quantified. hair or the skin of the individual being groomed. Any parasites that There were two main aims in this study: (1) to determine the role were removed were either put into the mouth of the groomer if of kinship among adult females in maintaining social cohesion removed by the hands of the groomer or were directly removed by within golden snub-nosed monkey OMUs; and (2) to determine if the groomer with its mouth (Li et al. 2002). kinship among females is positively associated with the likelihood of Approach one focal female moved towards another female, from occurrence of social affiliative behaviors. a distance of >1 m to a distance of 0.5 m. The individual to which Downloaded from https://academic.oup.com/cz/article-abstract/64/4/441/3964668 by Ed 'DeepDyve' Gillespie user on 22 August 2018 Ren et al. Kinship and affiliative behaviors 443 Shuangmiaozi Shuangmiaozi Shuangmiaozi N N Guangtou peak Guangtou peak Guangtou peak Dujiafen Dujiafen Dujiafen Xiaowangjian Xiaowangjian Xiaowangjian Y Y Yu u uhuangmiao huangmiao huangmiao DJF-Herd DJF-Herd DJF-Herd GNG-Herd GNG-Herd GNG-Herd Legend Legend Legend 0 1.5 3 6 0 1.5 3 6 0 1.5 3 6 V V Viillage illage llage River River River Kilometers Kilometers Kilometers Figure 1. Map of the study site: Yuhuangmiao Village, Zhouzhi National Nature Reserve, Shaanxi Province, China. The shadows show the home ranges of the GNG and DJF herds. Table 1. Unit composition and sampling information of the GNG We calculated the genetic diversity parameters for each locus herd using CERVUS V3.0 (Kalinowski et al. 2007). A Hardy–Weinberg equilibrium test was performed with GENEPOP V4.3 (Rousset 2008), Age–sex classes OMU and sequential Bonferroni correction was used to adjust each P-value for multiple tests. Loci in Hardy–Weinberg disequilibrium PK HB SH RX JB BX FZ WX SQ LD ZB HT SX were excluded from further analysis. The relatedness coefficient was Adult male 1/1 1/1 1/1 1/1 1/1 1/1 1/1 1/1 1/1 1/1 1/1 1/1 1/1 estimated with Lynch and Ritland’s (1999) estimator with null allele Adult female 7/7 6/6 5/5 3/3 2/3 4/4 3/3 4/4 2/3 3/4 7/7 5/5 4/4 correction (Huang et al. 2016b). The null allele frequency was Juvenile 4 4 3 2 2 2 1 3 2 3 4 3 2 estimated by Kalinowski and Taper’s (2006) estimator in POLYRELATEDNESS V1.6 (Huang et al. 2016 b). A linkage disequilib- The ﬁrst numbers in the cells of adult male and adult female are the number rium test was performed with GENEPOP V4.3 (Rousset 2008) to avoid of individuals sampled and the second numbers are the number of individuals within OMU. inference of linked loci, and each locus was weighted conservatively for relatedness estimation by 1/(nþ 1), where n is the number of linked loci (determined by FDR corrected Q< 0.05). the focal individual moved did not move its location within 10 s of The relatedness between each pair of individuals was calculated, the event. and each dyad was classified into one of the five categories: male– Proximity the distance between the two female individuals, not male (MM), female–female within the same unit (FFW), female–fe- including their tails, is less than two adult-individual female body lengths. male between units (FFB), female–male within the same unit (FMW), and female–male between units (FMB). To test if kinship affects the likelihood of association between dyads, we assessed the Molecular methods relatedness between female–female dyads (FFW versus FFB) and fe- Hair and fecal samples were collected noninvasively for genetic ana- male–male dyads (FMW versus FMB) with a matrix permutation lysis. A stick with adhesive at each end and food bait in the center test because dyadic data are not independent (Guo et al. 2015). In was used to collect hair, which was then stored in the laboratory at order to determine the correlation between kinship and each behav- room temperature after being dried with silica gel. Fresh fecal sam- ior, we selected female dyads from the four observed units to gener- ples were collected and stored in DETs solution (20% DMSO, ate a 21 21 pairwise relatedness matrix. 0.25 M sodium–EDTA, 100 mM Tris–HCl, pH 7.5, and NaCl to sat- uration) at 20 C. The DNA samples extracted from hairs were processed with pro- Behavioral analyses teinase K digestion in a PCR compatible buffer (Allen et al. 1998); We calculated the proximity index (PI) (Matsumura and Okamoto those from feces were extracted with QIAamp DNA Stool Mini Kits (1997) for the three affiliative behavior patterns measured. This (Qiagen, Germany). Nineteen highly polymorphic microsatellites index is defined as the ratio of the numbers scanned between the were amplified from each sample (Huang et al. 2016a), which were two individuals (A and B) to the total number of the scans involving sent to Shanghai Sangon Biotech for genotyping. In order to prevent A or B. To standardize all behavioral data, we extended the proxim- genotyping errors, such as false alleles and/or allelic dropouts ity index to an all-occurrence recording method. For example, the PI (Taberlet et al. 1996), homozygote genotypes were clarified by repli- for grooming is the ratio of twice the total time that A and B cation at least seven times, while all heterozygotes were clarified by groomed each other to the total time that A or B initiated and at least three separate reactions (Taberlet et al. 1996). Alleles were received grooming. Similarly, the PI for approaching is the ratio of segregated with an ABI PRISM 3100 Genetic Analyser, and their twice number of approaches between A and B to the total sizes, relative to an internal standard (ROX-labeled HD400), were approaches that either A or B initiated and received. determined with GeneMapper V3.7 (Applied Biosystems). MICRO- The PI is also dependent on the size of the unit, for this study the CHECKER V2.2.3 (van Oosterhout et al. 2004) was used to check OMU. For example, assuming a certain behavior occurs randomly microsatellite data for scoring errors, allelic dropouts, and null among individuals, and each individual has the same probability of alleles. exhibiting the behavior, thus, the expected PI between any two Downloaded from https://academic.oup.com/cz/article-abstract/64/4/441/3964668 by Ed 'DeepDyve' Gillespie user on 22 August 2018 Ma M Main Ri ain in Ridge Rid dg ge e of Q of of Qinling Qinling inling 444 Current Zoology, 2018, Vol. 64, No. 4 individuals is 1/(n 1), where n is the total number of individuals 0.582 on average. The polymorphic information content (PIC) (adult females) within the unit. Therefore, this value between indi- ranged from 0.229 to 0.729, 0.518 on average. Allelic richness viduals in a larger unit would be smaller, and a larger PI may not ranged from 1.324 to 4.246, 2.562 on average Table 3. imply a closer relationship. Thus, we had to standardize PI for each of the OMUs by subtracting the mean and then divided by the stand- Relatedness analyses ard deviation (the Z-score) of the PI for each unit. For the genotypes at 19 microsatellite loci from 68 individuals, re- Because affiliative behaviors mainly happened within OMUs, we latedness coefficients (r) were estimated using Lynch and Ritland’s excluded those interactions between individuals from different (1999) estimator. The means and standard errors of this coefficient OMUs. Three 21 21 Z-score matrices were then obtained. The for each of the five categories are shown in Figure 2. The relatedness corresponding elements for individuals from different OMUs and coefficient between females within the same OMU (r ¼ 0.045, those on diagonals within each matrix were left blank. n¼ 106) is significantly greater than that between different OMUs (r ¼0.010, n ¼ 1,379, P< 0.001), while the difference in the re- Statistics latedness coefficients between female–male dyads within the same Our dyadic data are not independent because some dyads share the OMU (r ¼0.026, n ¼ 55) and female–male dyads between OMUs same individuals. Taking geographic distance as an example, follow- is not significant (r ¼0.012, n¼ 660, P ¼ 0.098). This shows that ing the change in the coordinates of one location, all distances of other locations relative to the original location will change. Table 2. The descriptive statistics of kinship and afﬁliative behav- Therefore, linear regression cannot be applied to these matrices— iors within OMUs this method assumes all observations are independent. In this case, Behavior Count Time Unit #dyads Mean Std Min Max the Mantel test (Mantel 1976) is usually used to measure the degree of association between two distance matrices. This randomly per- Grooming 248 12.10 h PK 21 0.132 0.121 0.000 0.423 mutes one of the two matrices, and calculates the probability of the 255 13.54 h HB 15 0.189 0.113 0.000 0.372 correlation coefficient between the two matrices after permutation 259 13.12 h SH 10 0.244 0.085 0.092 0.378 is greater than the original value with a Monte-Carlo algorithm. 90 4.92 h RX 3 0.465 0.283 0.176 0.740 Although we can estimate the pairwise relatedness between indi- Proximity 862 PK 21 0.159 0.076 0.027 0.328 viduals within or between OMUs based on molecular data, the 600 HB 15 0.188 0.095 0.023 0.329 538 SH 10 0.250 0.079 0.113 0.370 proximity index can only be calculated for individuals within a same 115 RX 3 0.492 0.133 0.357 0.623 OMU. Therefore, for dyads between individuals in different OMUs, Approach 115 PK 21 0.159 0.072 0.034 0.343 the corresponding proximity index is invalid. Based on the Mantel 145 HB 15 0.191 0.121 0.016 0.415 test, we overcame this problem by developing a novel nonparametric 116 SH 10 0.246 0.076 0.143 0.372 test, the partition Mantel test, to test the correlation between the re- 42 RX 3 0.522 0.247 0.276 0.840 latedness matrix and each Z-score matrix. The individuals within the same unit are randomly permuted, and the blank elements (i.e., the diagonal elements and the elements of the individuals from dif- ferent OMUs) are not used in the calculation for correlation between Table 3. Characteristics of the 19 microsatellite loci used to assess matrices. Similarly, the probability of the correlation between two the genetic structure of 68 individuals of R. roxellana matrices after permutation is greater than original value is calcu- Locus kT% H H PIC Ar F P O E IS lated. Significance values are thus one-tailed. D10s1432 5 98.5 0.567 0.534 0.476 2.147 0.062 0.483 D10s2483 4 100 0.544 0.617 0.544 2.609 0.118 0.251 Results D10s676 3 91.2 0.484 0.402 0.328 1.673 0.203 0.342 D12s375 3 92.6 0.540 0.551 0.449 2.227 0.020 0.898 Behavioral data D14s306 4 98.5 0.776 0.680 0.621 3.128 0.141 0.199 We studied a total of 21 females from four OMUs, the compositions D16s540 3 98.5 0.433 0.499 0.425 1.996 0.132 0.431 of which were stable during the observation period. We made 877 D19s1034 4 97.1 0.606 0.605 0.523 2.529 0.003 0.958 grooming events measurements, 2,127 for of proximity and 431 for D19s248 3 100 0.677 0.607 0.538 2.546 0.114 0.507 “approach”. The proximity indices (PI) of these three affiliative be- D19s582 4 92.6 0.619 0.577 0.531 2.361 0.074 0.469 D21s2054 3 98.5 0.508 0.529 0.423 2.123 0.041 0.055 haviors (grooming time, and frequencies for both proximity and D3s1766 4 100 0.632 0.627 0.556 2.681 0.008 0.580 “approach”’) for 49 female–male dyads within the same units were D6s1050 4 98.5 0.642 0.654 0.581 2.888 0.018 0.424 calculated and are presented in Table 2. D6s493 5 97.1 0.712 0.765 0.729 4.246 0.069 0.347 D6s501 4 98.5 0.612 0.597 0.512 2.478 0.026 0.671 Genetic diversity D7s1804 4 91.2 0.226 0.245 0.229 1.324 0.078 0.371 D7s2204 5 100 0.677 0.714 0.669 3.496 0.053 0.333 We used 68 independent genetic samples (17 hair and 51 feces) for D7s820 5 98.5 0.672 0.719 0.672 3.560 0.066 0.721 microsatellite analysis (the sampling ratio was 95.8%). In order to D9s252 4 92.6 0.508 0.518 0.475 2.074 0.019 0.179 reliably estimate allele frequency, we sampled and genotyped more TPOX 4 95.6 0.569 0.610 0.542 2.565 0.067 0.498 adult individuals in the breeding band, which contained a total of 71 Average 3.95 96.8 0.578 0.582 0.518 2.562 0.009 adults. DNA extracts were amplified at 19 microsatellite loci. The characteristics of these loci are presented in Table 3. The number of Header row description: k is the number of alleles, T% is the genotyped per- alleles per locus ranged from 3 to 5, averaging 3.95. The observed centage, H and H are the observed and expected heterozygosities, PIC and O E heterozygosity ranged from 0.226 to 0.776, with an average of AR are the polymorphic information content and allelic richness, respectively, 0.578. The expected heterozygosity ranged from 0.245 to 0.765, P is the signiﬁcance of a HWE test. Downloaded from https://academic.oup.com/cz/article-abstract/64/4/441/3964668 by Ed 'DeepDyve' Gillespie user on 22 August 2018 Ren et al. Kinship and affiliative behaviors 445 females within an OMU are more closely related to each other OMUs in R. roxellana are common (Tan et al. 2003) and female al- than the overall level of relatedness between females within the liances are known to play an important role during such conflicts breeding band Figure 2. (Guo et al. 2007; Xi et al. 2008). This implies that kinship among fe- males makes a significant contribution to OMU cohesion, resulting in female kin alliances in R. roxellana. This may allow kinship- Kinship and behavior based alliances to compete more effectively for limited resources We found significant correlations between relatedness and affiliative (Guo et al. 2007) and defend a territory from other OMUs (Zhang behaviors (Table 4). For grooming there was a significant positive et al. 2006). Similar female–female alliances in other primate species correlation with the relatedness coefficient (partition Mantel test, with similar social systems have been shown to be important for ac- r¼ 0.359, P ¼ 0.004, Figure 3A). We also found a significant but cess to food and in conflicts with other OMUs, such as in geladas weaker positive trend between the relatedness coefficient and prox- (Dunbar 1993; Dunbar and Dunbar 1975; Kawai et al. 1983), alli- imity (partition Mantel test r ¼ 0.227, P< 0.05, Figure 3B). There ances that may have evolved via kin selection (Iwamoto 1993). was a marginally nonsignificant positive correlation between r and We also found that grooming and proximity behaviors occupied approach in adult female dyads (r¼ 0.197, P ¼ 0.057, Table 4, most of the times spent on social activities by adult females within Figure 3A-3C). an OMU, and these two types of affiliative behaviors occurred more frequently between closely related females than other females (Figure 3). These results are consistent with the predictions of kin- Discussion selection; the closer the genetic relationship between individuals, the higher the likelihood that affiliative behaviors will be exhibited. We examined the effects of kinship on grooming, proximity and ap- Similar patterns of the behavior are also present in ring-tailed lemurs proach behaviors in golden snub-nosed monkeys, and found that Lemur catta (Sbeglia et al. 2010), white-faced capuchin monkeys adult females within an OMU are more closely related than those of (Cebus capucinus)(Perry et al. 2008), and yellow baboons Papio the same age-sex class between OMUs (Figure 2). This suggests that cynocephalus (Silk et al. 2004, 2006). females with higher kinship are more likely to reside within the However, our data show that approach behavior was only weakly same OMU. Indeed, conflicts between the members of different associated with kinship among female R. roxellana (Figure 3). Kinship may thus be less important in determining approach behaviour than 0.15 *** for the other two affiliative behaviors that we measured. 0.10 Although grooming and proximity between individuals are both significantly positively correlated with kinship, their coefficients of 0.05 determination are small (Table 4), and the grooming times and proximity frequencies of two individuals varies greatly despite simi- 0.00 lar levels of kinship (Figure 3). Additionally, the relatedness coeffi- - 0.05 cients between individuals also vary, even though they exhibit similar affiliative behaviors. - 0.10 Table 4. The correlation coefﬁcients between relatedness and af- Dyad category ﬁliative behaviors in adult female dyads Figure 2. Mean value and standard error of relatedness for each dyad cat- 2 Behavior rR P b b 1 0 egory. The description of dyad categories are as follows: All denotes dyads between all kinds of individuals; MM denotes male–male dyads; FFW and Grooming 0.359 0.129 0.004 1.832 0.196 FFB denote female–female dyads within a same unit and between different Proximity 0.227 0.052 0.050 1.159 0.124 units; FMW and FMB denote female–male dyads within the same unit and be- Approach 0.197 0.039 0.057 1.030 0.161 tween different units, respectively. A B C 2 2 2 1 1 1 0 0 0 −1 −1 −1 −2 −2 −2 r = 0.359, P = 0.004 r = 0.227, P = 0.050 r = 0.197, P = 0.057 −0.2 0 0.2 0.4 0.6 −0.2 0 0.2 0.4 0.6 −0.2 0 0.2 0.4 0.6 Relatedness Relatedness Relatedness Figure 3. The relationship between r and each afﬁliative behavior in adult female dyads. The plots of the Z-scores of each of three afﬁliative behaviors, grooming, proximity and approach, versus the relatedness coefﬁcients are shown in the three subﬁgures. Each dot in the scatter plots denotes a dyad, and regression ana- lyses of those Z-scores on relatedness coefﬁcients were performed. The correlation coefﬁcient between independent and dependent variables and their signiﬁ- cance is shown in the bottom of each subﬁgure. The line in each subﬁgure shows the regression equation and the two curves denote the 95% conﬁdence interval of the estimated Z-score. Downloaded from https://academic.oup.com/cz/article-abstract/64/4/441/3964668 by Ed 'DeepDyve' Gillespie user on 22 August 2018 All MM FFW FFB FMW FMB Relatedness Grooming Proximity Approaching 446 Current Zoology, 2018, Vol. 64, No. 4 de Vladar HP, Szathm ary E, 2017. Beyond Hamilton’s rule. Science 356: These inconsistencies may be associated with at least three fac- 485–486. tors: 1) relatedness estimators are able to determine the degree of kin- Dunbar RIM, 1993. Social organization of the gelada. In: Jablonski NG, edi- ship but cannot identify maternal or paternal relatives. The social tor. Theropithecus: The Rise and Fall of A Primate Genus. Cambridge: structure of the golden snub-nosed monkey is based on a loose mater- Cambridge University Press. 425–439. nal, one-male and multiple-female multilevel society (Zhang et al. Dunbar RIM, Dunbar EP, 1975. Social Dynamics of Gelada Baboons. Basel: 2006). Maternal relatives tend to be involved in more social activities Karger. than nonmaternal relatives, and therefore have a more important so- Foster KR, Wenseleers T, Ratnieks FLW, 2006. Kin selection is the key to al- cial function than paternal relatives in a maternal society (Silk 2002); truism. Trends Ecol Evol 21:57–60. 2) age differences exists among adult females, and in primates social Gagneux P, Boesch C, Woodruff DS, 1999. Female reproductive strategies, pa- ties among individuals within the same age class are tighter than ternity and community structure in wild West African chimpanzees. Anim. Behav 57:19–32. those between different age classes (Mitani et al. 2002; Widdig et al. Guo ST, Huang K, Ji WH, Garber PA, Li BG, 2015. The role of kinship in the 2002); and 3) a biological market may have influenced partner selec- formation of a primate multilevel society. Am J Phys Anthropol 156: tion and affected social interactions among females (Wei et al. 2012). 606–613. For example, females without infants prefer to groom the females Guo ST, Li BG, Watanabe K, 2007. Diet and activity budget of Rhinopithecus with infants to gain access to infants (Wei et al. 2013). Thus, even roxellana in the Qinling Mountains, China. Primates 48:268–276. though kin selection plays an important role in social evolution, close Guy AJ, Schuerch FS, Heffernan S, Thomson PC, O’brien JK et al. 2008. The ef- kinship is not always necessary to explain social behavior (de Vladar fect of medroxyprogesterone acetate on behavioural responses of captive fe- and Szathm ary 2017). A multitude of factors may are likely to affect male hamadryas baboons Papio hamadryas. Anim Reprod Sci 108:412–424. social behavior in species such as R. roxellana in addition to those Hamilton WD, 1964. The genetical evolution of social behaviour. II. J Theor we mentioned previously, e.g., social structure (Silk 2002), rank Biol 7:1–16. Huang K, Guo ST, Cushman SA, Dunn DW, Qi XG et al. 2016a. Population (Bentley-Condit and Smith 1999), and physiological condition (Guy structure of the golden snub-nosed monkey Rhinopithecus roxellana in the et al. 2008). It is thus necessary to carry out further studies on kin- Qinling Mountains, central China. Integr Zool 11:350–360. ship and affiliative behaviors in this species. Huang K, Ritland K, Dunn DW, Qi X, Guo S et al. 2016b. Estimating related- In conclusion, we show that closely related R. roxellana females ness in the presence of null alleles. Genetics 202:247–260. are more likely to reside in the same OMU than less related females. Iwamoto T, 1993. The ecology of Theropithecus gelada. In: Jablonski NG, Females with higher genetic relatedness between groomed each other editor. Theropithecus: The Rise and Fall of A Primate Genus. Cambridge: more frequently, were in closer proximity, than more distantly Cambridge University Press. 441–453. related females. We suggest that female kinship plays an important Kalinowski ST, Taper ML, 2006. Maximum likelihood estimation of the fre- role in the maintenance and organization of the R. roxellana social quency of null alleles at microsatellite loci. Conserv Genet 7:991–995. system. Additional studies are needed to measure the benefits to adult Kalinowski ST, Taper ML, Marshall TC, 2007. Revising how the computer program cervus accommodates genotyping error increases success in pater- females that reside in the same OMU and preferentially make social nity assignment. Mol Ecol 16:1099–1106. affiliations with close kin, and to clarify if kinship-based social asso- Kawai M, Dunbar RIM, Ohsawa H, Mori U, 1983. Social organization of gel- ciations result in increased inclusive fitness for adult females. ada baboons: social units and deﬁnitions. Primates 24:13–24. Li BG, Chen C, Ji WH, Ren BP, 2000. Seasonal home range changes of the Sichuan snub-nosed monkey Rhinopithecus roxellana in the Qinling Mountains of China. Folia Primatol 71:375–386. Acknowledgments Li BG, Jia ZY, Pan RL, Ren BP, 2003. Changes in distribution of the snub-nosed monkey in China. In: Marsh LK, editor. Primates in Fragments: Ecology and We thank the Northwest University students W. Wei, L.L. Wu, and H.Y. Conservation. New York: Kluwer Academic/Plenum Press. 29–51. Zhang for their ﬁeldwork and experimental assistance. We also thank the Li BG, Pan RL, Oxnard CE, 2002. Extinction of snub-nosed monkeys in management of Zhouzhi National Nature Reserve for permission to conduct China during the past 400 years. Int J Primatol 23:1227–1244. this study, which was supported by the National Nature Science Foundation Lynch M, Ritland K, 1999. Estimation of pairwise relatedness with molecular of China (31672301, 31501872, 31572278 31472014), National Key markers. Genetics 152:1753–1766. Program of Research and Development, Ministry of Science and Technology Mantel N, 1976. Fundamental carcinogenic processes and their implications of China (2016YFC0503202), Science and Technology Foundation of for low-dose risk assessment. Cancer Res 36:1835–1838. Shaanxi Academy of Sciences, China (2013 K-04, 2017 K-06 2016K-20; 2017K-09), Science and technology development project of Shaanxi Province, Martin P, Patrick B, 2006. Measuring Behaviour: An introductory Guide. 2nd China (2017NY-181; 2016NY-126) and Natural Science Basic Research Plan edn. Cambridge: Cambridge University Press. in Shaanxi Province of China (2016JZ009 2016JM3016). Mateo JM, 2002. Kin-recognition abilities and nepotism as a function of soci- ality. Proc R Soc Lond B Biol Sci 269:323–325. Matsumura S, Okamoto K, 1997. Factors affecting proximity among members References of a wild group of moor macaques during feeding, moving, and resting. Int. J. Primatol 18:929–940. Allen M, Engstro ¨ m AS, Meyers S, Handt O, Saldeen T et al. 1998. Mitani JC, Watts DP, 2010. Why do chimpanzees hunt and share meat? Anim Mitochondrial DNA sequencing of shed hairs and saliva on robbery caps: Behav 61:915–924. sensitivity and matching probabilities. J. Forensic Sci 43:453–466. Mitani JC, Watts DP, Pepper JW, Merriwether DA, 2002. Demographic and Altmann J, 1974. Observational study of behavior: sampling methods. social constraints on male chimpanzee behaviour. Anim Behav 64:727–737. Behaviour 49:227–267. Morin PA, Goldberg TL, 2004. Determination of genealogical relationships Bentley-Condit VK, Smith EO, 1999. Female dominance and female social re- from genetic data: a review of methods and applications. In: Chapais B, lationships among yellow baboons Papio hamadryas cynocephalus. Am J Berman CM, editors. Kinship and Behavior in Primates. Oxford: Oxford Primatol 47:321–334. University Press. 15–45. Blaustein AR, Waldman B, 1992. Kin recognition in anuran amphibians. Nam KB, Simeoni M, Sharp SP, Hatchwell BJ, 2010. Kinship affects invest- Anim Behav 44:207–221. ment by helpers in a cooperatively breeding bird. Proc R Soc Lond B Biol Davis AR, 2012. Kin presence drives philopatry and social aggregation in ju- Sci 277:3299–3306. venile desert night lizards Xantusia vigilis. Behav Ecol 23:18–24. Downloaded from https://academic.oup.com/cz/article-abstract/64/4/441/3964668 by Ed 'DeepDyve' Gillespie user on 22 August 2018 Ren et al. Kinship and affiliative behaviors 447 Perry S, Manson JH, Muniz L, Gros-Louis J, Vigilant L, 2008. Kin-biased so- Sussman RW, Garber PA, Cheverud JM, 2005. Importance of cooperation cial behaviour in wild adult female white-faced capuchins, Cebus capucinus. and afﬁliation in the evolution of primate sociality. Am J Phys Anthropol Anim Behav 76:187–199. 128:84–97. Pope TR, 2000. Reproductive success increases with degree of kinship in co- Taberlet P, Grifﬁn S, Goossens B, Questiau S, Manceau V et al. 1996. Reliable operative coalitions of female red howler monkeys Alouatta seniculus. genotyping of samples with very low DNA quantities using PCR. Nucleic Behav Ecol Sociobiol 48:253–267. Acids Res 24: 3189–3194. Qi XG, Garber PA, Ji W, Huang ZP, Huang K et al. 2014. Satellite telemetry Tan CL, Zhang P, Li BG, Watanabe K, Wada K, 2003. A preliminary study on and social modeling offer new insights into the origin of primate multilevel the social organization of Sichuan snub-nosed monkeys Rhinopithecus rox- societies. Nat Commun 5:5296–5296. ellana in Qinling, China. Am J Primatol 60:144. Qi XG, Li BG, Garber PA, Ji WH, Watanabe K, 2009. Social dy- van Oosterhout C, Hutchinson WF, Wills DP, Shipley P, 2004. namics of the golden snub-nosed monkey Rhinopithecus roxellana: MICRO-CHECKER: software for identifying and correcting genotyping female transfer and one-male unit succession. Am J Primatol 71: errors in microsatellite data. Mol Ecol Notes 4:535–538. 670–679. Wei W, Qi XG, Garber PA, Guo ST, Zhang P et al. 2013. Supply and demand Rousset F, 2008. GENEPOP ’007: a complete re-implementation of the determine the market value of access to infants in the golden snub-nosed genepop software for Windows and Linux. MolEcolResour 8: monkey Rhinopithecus roxellana. PLoS ONE 8: e65962., 103–106. Wei W, Qi XG, Guo ST, Zhao DP, Zhang P et al. 2012. Market powers pre- Sbeglia GC, Tang-Martinez Z, Sussman RW, 2010. Effects of food, proximity, dict reciprocal grooming in golden snub-nosed monkeys Rhinopithecus rox- and kinship on social behavior in ringtailed lemurs. Am J Primatol 72: ellana. PLoS ONE 7:e36802. 981–991. Widdig A, Nu ¨ rnberg P, Krawczak M, Streich WJ, Bercovitch F, 2002. Silk JB, 2002. Kin selection in primate groups. Int J Primatol 23:849–875. Afﬁliation and aggression among adult female rhesus macaques: a genetic Silk JB, Alberts SC, Altmann J, 2004. Patterns of coalition formation by adult analysis of paternal cohorts. Behaviour 139:371–391. female baboons in Amboseli, Kenya. Anim Behav 67:573–582. Xi WZ, Li BG, Zhao DP, Ji WH, Zhang P, 2008. Beneﬁts to female helpers in Silk JB, Altmann J, Alberts SC, 2006. Social relationships among adult female wild Rhinopithecus roxellana. Int J Primatol 29:593–600. baboons Papio cynocephalus. I. Variation in the strength of social bonds. Zhang P, Watanabe K, Li BG, Qi XG, 2008. Dominance relationships among Behav Ecol Sociobiol 61:183–195. one-male units in a provisioned free-ranging band of the Sichuan Strayer FF, Harris PJ, 1979. Social cohesion among captive squirrel monkeys snub-nosed monkeys Rhinopithecus roxellana in the Qinling Mountains, Saimiri sciureus. Behav Ecol Sociobiol 5:93–110. China. Am J Primatol 70:634–641. Surbeck M, Hohmann G, 2011. Mothers matter! Maternal support, domin- Zhang P, Watanabe K, Li BG, Tan CL, 2006. Social organization of Sichuan ance status and mating success in male bonobos Pan paniscus. Proc R Soc snub-nosed monkeys Rhinopithecus roxellana in the Qinling Mountains, Lond B Biol Sci 278:590–598. Central China. Primates 47:374–382. Downloaded from https://academic.oup.com/cz/article-abstract/64/4/441/3964668 by Ed 'DeepDyve' Gillespie user on 22 August 2018
Current Zoology – Oxford University Press
Published: Aug 1, 2018
It’s your single place to instantly
discover and read the research
that matters to you.
Enjoy affordable access to
over 18 million articles from more than
15,000 peer-reviewed journals.
All for just $49/month
Query the DeepDyve database, plus search all of PubMed and Google Scholar seamlessly
Save any article or search result from DeepDyve, PubMed, and Google Scholar... all in one place.
Get unlimited, online access to over 18 million full-text articles from more than 15,000 scientific journals.
Read from thousands of the leading scholarly journals from SpringerNature, Wiley-Blackwell, Oxford University Press and more.
All the latest content is available, no embargo periods.
“Hi guys, I cannot tell you how much I love this resource. Incredible. I really believe you've hit the nail on the head with this site in regards to solving the research-purchase issue.”Daniel C.
“Whoa! It’s like Spotify but for academic articles.”@Phil_Robichaud
“I must say, @deepdyve is a fabulous solution to the independent researcher's problem of #access to #information.”@deepthiw
“My last article couldn't be possible without the platform @deepdyve that makes journal papers cheaper.”@JoseServera