American Journal of

RESEARCH ARTICLE The Ties That Bind: Maternal Kin Bias in a Multilevel Primate Society Despite Natal Dispersal by Both Sexes

€ 1 2 2,3,4,5 1 VERONIKA STADELE *, MATHEW PINES , LARISSA SWEDELL , AND LINDA VIGILANT 1Department of Primatology, Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany 2Filoha Hamadryas Project, Awash National Park, Metahara, Ethiopia 3Department of Anthropology, Queens College, City University of New York, Flushing, New York 4New York Consortium in Evolutionary Primatology, New York, New York 5Department of Archaeology, University of Cape Town, Cape Town, South Africa In many social , individuals derive fitness benefits from close social bonds, which are often formed among kin of the philopatric sex. Hamadryas baboons, however, exhibit a hierarchical, multilevel social system where both sexes disperse from their natal one-male-unit (OMU). Although this would seem to hinder maintenance of kin ties, both sexes appear largely philopatric at the higher order band and clan levels, possibly allowing for bonds with same sex kin by both males and females. In order to investigate the possibility of kin bonds in hamadryas baboons, we identified kin dyads in a band without known pedigree information using a large panel of genetic markers: 1 Y-linked, 4 X-linked, and 23 autosomal microsatellites and part of the mitochondrial hypervariable region I. With these data, we performed a analysis while accounting for misclassification rates through simulations and determined kinship among two types of dyads: leader and follower males and female dyads within OMUs. Leader and follower males were maternal relatives more often than expected by chance, suggesting that kinship plays a role in the formation of these relationships. Moreover, maternal female relatives were found in the same OMU more often than expected by chance, indicating that females may be motivated to maintain post-dispersal contact with maternal female kin. Our results suggest that hamadryas baboons can recognize maternal kin and that has contributed to shaping their complex social system. This implies that an ancestral maternal kin bias has been retained in hamadryas society. Am. J. Primatol. © 2016 Wiley Periodicals, Inc.

Key words: kinship; hamadryas baboon; female choice; affiliation; kin selection

INTRODUCTION elephants, Archie et al., 2006; many rodents, review The causes and consequences of dispersal pat- by Silk, 2007; capuchins, Perry et al., 2008]. Such kin terns in social animals are important questions in associations may be adaptive, enhancing direct evolutionary biology because they determine the availability of social and reproductive partners and Contract grant sponsor: Max Planck Society; contract grant thereby shape opportunities for the effects of kin sponsor: The Leakey Foundation; contract grant sponsor: selection and other evolutionary processes to operate Wenner-Gren Foundation; contract grant sponsor: National Geographic Society; contract grant numbers: 6468-99, 8309-07; on social [Clutton-Brock & Lukas, 2012; contract grant sponsor: National Science Foundation; Greenwood, 1980; Lawson Handley & Perrin, 2007; contract grant number: 9629658; contract grant sponsor: Pusey, 1987]. Dispersal, the tendency of an individual PSC-CUNY Research Award Program funded jointly by the City University of New York and the Professional Staff to migrate out of its natal group, is male biased in most Congress species, whereas , the tendency of an individual to stay in its natal group, is often female Conflicts of interest: The authors declare no conflict of interest. biased [Greenwood, 1980; Pusey, 1987]. Female Correspondence to: Veronika Stadele€ and Linda Vigilant, philopatry leads to co-residence among female kin, Department of Primatology, Max Planck Institute for Evolu- who tend to exhibit preferential associations that may tionary Anthropology, Deutscher Platz 6, Leipzig, Germany. include overlapping home ranges, close proximity in a E-mail: [email protected]; [email protected] resting or feeding context, increased grooming or play, Received 15 October 2015; revised 2 February 2016; revision coalitions, communal nursing of offspring, or group accepted 2 February 2016 fissions and fusions along matrilines [, Pusey & DOI: 10.1002/ajp.22537 Packer, 1994; lemurs, Nakamichi & Koyama, 1997; Published online XX Month Year in Wiley Online Library hyenas, Smith et al., 2010; Wahaj et al., 2004; (wileyonlinelibrary.com).

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fitness by increasing reproductive success via pro- of kin biases in male chimpanzees have found that longed survival or other means [lions, Packer et al., maternal brothers have particularly stable bonds 1991; voles, Lambin & Krebs, 1993; house mice, and maternal but not paternal brothers engage in Konig,€ 1994; marmots, Armitage & Schwartz, 2000; affiliative and cooperative behaviors more often than capuchins, Fedigan et al., 2008; ground squirrels, unrelated dyads [Langergraber et al., 2007; Mitani, Viblanc et al., 2010], whereas at the same time 2009]. However, close bonds can exist between providing inclusive fitness benefits by enhancing unrelated male chimpanzees as well [Gilby & reproductive success of relatives [Hamilton, 1964]. Wrangham, 2008; Langergraber et al., 2007]. In Particularly in some female-philopatric Old World contrast to chimpanzees, Guinea baboon males show monkeys, females may strongly bias their affiliative no evidence of a linear , engage behavior toward maternal female relatives [pig-tailed in affiliative interactions and display low levels of macaques, Massey, 1977; rhesus macaques, Kapsalis aggression, but these measures are not significantly & Berman, 1996; Japanese macaques, Chapais, 1997; correlated with genetic relatedness [Kopp et al., chacma baboons, Silk et al., 1999; yellow baboons, Silk 2015; Patzelt et al., 2014]. et al., 2006a,b; mandrills, Charpentier et al., 2007, Like the chimpanzee, the hamadryas baboon 2012; possibly geladas, Tinsley Johnson et al., 2013; (Papio hamadryas) is a primate species generally blue monkeys, Cords & Nikitopoulos, 2015] and may characterized by male philopatry and female dispersal engage in potentially costly support of maternal kin in [Hammond et al., 2006; Hapke et al., 2001; Stadele€ conflicts with other individuals [Kaplan, 1977; et al., 2015; Swedell et al., 2011]. Hamadryas baboons Kapsalis & Berman, 1996; Massey, 1977; Silk et al., live in a multilevel society with four distinct levels: 2004, 2010a; Wittig et al., 2007]. one-male units (OMUs), clans, bands, and troops. Maternal in may recognize OMUs consisting of a leader male, one or several adult one another through common familiarity and close and subadult females, and dependent offspring form association with the mother, an unlikely mechanism the first level. Males of particular OMUs, along with for paternal in most mammals due to extra-OMU bachelors called solitary males, associate the rarity of male parental care [Clutton-Brock, with each other to varying extents. Groups of 1991; Kleiman & Malcom, 1981]. Still, other mecha- preferentially associating OMUs and solitary males, nisms of paternal kin recognition have been sug- termed clans, form the second level of the society. The gested, such as phenotype matching or familiarity third level is the band, which comprises a social with same aged peers in groups with high male grouping of one or more clans in which males jointly reproductive skew [Holmes & Sherman, 1983; defend their females against males of other bands and Langergraber, 2012; Rendall, 2004]. Support for are visibly cohesive as a consistent social group the idea that at least some primate species may [Abegglen, 1984; Colmenares et al., 2006; Kummer, recognize paternal kin comes from recent findings 1968; Schreier & Swedell, 2009; Sigg et al., 1982]. that individuals may bias their affiliative and Different bands come together on sleeping cliffs at coalitionary behavior toward paternal kin over night to form a troop, which is likely not a true social unrelated individuals, although maternal kin are unit but an outcome of bands associating due to the typically preferred over paternal kin when both are limited availability of cliffs [Abegglen, 1984; Kummer, an option [Charpentier et al., 2007, 2012; Schulke€ 1968; Schreier & Swedell, 2009]. et al., 2013; Silk et al., 2006a,b; Smith et al., 2003; Although both sexes disperse from their natal Perry et al., 2008; Pfefferle et al., 2014; Watts, 1994; OMU to reproduce, hamadryas are characterized by Widdig et al., 2006, 2001]. female-biased dispersal at other levels of the social Although much is known about kin affiliations structure [Hammond et al., 2006; Stadele€ et al., and possible mechanisms for kin selection in many 2015]. In our study population in Filoha, Ethiopia, female-philopatric Old World monkey species, less is males are largely philopatric at the level of the band known about relationships among kin in male- and clan as indicated by higher average dyadic philopatric primates, which is surprising given relatedness within than across bands and clans and that the primate order contains many of the few clustering of Y-haplotypes within bands and clans male-philopatric species of mammals [Lawson [Stadele€ et al., 2015]. However, low levels of Handley & Perrin, 2007]. Howler monkeys, spider Y-haplotype sharing between bands and clans as monkeys, woolly monkeys, and muriquis show well as behavioral observations of at least temporary varying degrees of female-biased dispersal and dispersal of males into other bands point to some, accordingly, varying degrees of male cooperation albeit low, level of male-mediated flow and affiliative behaviors [reviewed in Di Fiore, 2009; [Phillips-Conroy et al., 1992; Sigg et al., 1982; Strier et al., 2015]. In western gorillas, although both Stadele€ et al., 2015]. Average dyadic relatedness sexes may disperse from their natal group, groups led and patterns of mtDNA sharing indicate that by related silverbacks often range in close proximity females are also largely philopatric at the level of to each other and inter-group encounters are the band, although to a lesser degree than males. A frequently peaceful [Bradley et al., 2004]. Studies behavioral study of the same population recorded

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more movement of females among OMUs within 2015]. Leader males also benefit from follower rather than between clans and bands over a period of presence, which is associated with longer leader several years [Swedell et al., 2011]. In sum, these tenure lengths, more females, and higher reproduc- findings of a high degree of male as well as female tive output based on observational data [Chowdhury philopatry at the band and possibly clan level may be et al., 2015]. If followers and leaders are kin, then compatible with post-dispersal association of mater- both could also benefit via inclusive fitness [Abeg- nal and paternal kin dyads within each sex. glen, 1984; Chowdhury et al., 2015; Colmenares, The unique of hamadryas society, how- 1992; Pines et al., 2015]. ever, imposes constraints on how individuals may Unlike in other long-studied baboon species, associate with one another. Most notably, hama- where philopatric females benefit by close associa- dryas females are aggressively herded by their leader tion with same sex kin [Silk et al., 2003, 2009; but see males, who restrict female social activity to within Guinea baboons, Kopp et al., 2015], the primacy of the OMU [Abegglen, 1984; Kummer, 1968; Swedell & the bond with the leader male and the separation of Schreier, 2009]. Female transfer in hamadryas is in females from their maternal kin via successive fact an outcome of coercive behavior by males: leader takeovers would seem to preclude a hamadryas males of OMUs typically acquire females by taking female’s opportunity to choose same sex associates them over, one at a time, from other males, which can [Swedell et al., 2014]. However, although it may lead to females changing OMU membership several appear that OMU membership is determined by times in their lives (secondary dispersal) [Abegglen, male behavior alone, it has been suggested that 1984; Kummer, 1968; Swedell et al., 2011]. Take- females can influence the outcome of takeovers by overs can be aggressive, with males fighting over the subtly influencing male behavior or, more rarely, possession of females (challenge strategy); opportu- freely transferring between OMUs with little male nistic when females become separated from their resistance [Bachmann & Kummer, 1980; Swedell, leader males during intra- and inter-band conflicts or 2000, 2006; Swedell & Schreier, 2009]. We recently when the leader male is injured, ill or old, and weak found higher average dyadic relatedness of females and not capable of defending his females (opportu- within compared to among OMUs, suggesting a non- nistic strategy); or lead to the formation of initial random assortment of females into OMUs [Stadele€ units (IU strategy) when males acquire their et al., 2015]. Furthermore, an observational study first, usually sexually immature, female(s) specifically focused on female relationships found [Kummer, 1968; Pines et al., 2011]. In wild popula- that females interact with each other at least as tions, established leaders rarely challenge each much as with the leader male and noted that there is other’s possession of females and takeovers by great variability in the strength of these female leaders are mostly opportunistic [Abegglen, 1984; bonds among dyads, while females also occasionally Kummer, 1968; Kummer et al., 1974; Swedell, 2000, interact with each other across OMU boundaries 2006], with the IU and challenge strategies usually [Swedell, 2002]. It thus appears that hamadryas being employed by solitary and follower males who female relationships may be much more differenti- are first establishing their OMUs [Pines et al., 2011]. ated and important than previously appreciated. Solitary males reside in the band and are not Although bonds with kin should be harder to associated with any OMU in particular, whereas maintain for females due to takeovers by males, an follower males are seen in regular close association intrinsic motivation of females to maintain bonds with one or two OMUs and are usually tolerated in with female kin might be expected as it is the close proximity by the leader males [Colmenares, ancestral cercopithecine condition [Di Fiore & 1990, 1991; Kummer, 1968]. Follower and leader Rendall, 1994; Jolly, 2009; Strier, 1994; Swedell & males display ritualized greetings, called notifica- Plummer, 2012]. tions, in which one male presents to another, often In this study, we examine the potential for kin accompanied by lipsmacking, and the other male in bias in the dyadic associations of male and female return lipsmacks, mounts, and/or or touches the wild hamadryas baboons. In particular, we investi- genitals of the notifying male [Colmenares, 1991, gate whether pairs of leader and follower males are 1992; Kummer, 1968]. Followers will groom with the maternal or paternal kin more often than expected by OMU’s females, but rarely mount females [Swedell, chance. We then examine whether female maternal 2006]. Only follower males can form social relation- or paternal kin dyads are found in the same OMU ships with mature females of an OMU, and these more often than expected by chance and describe relationships can lead to peaceful transfers of those some observed illustrative circumstances that may females toward the end of the leader male’s tenure or allow females to associate with female kin in an OMU after the leader is deposed by another male (inheri- despite male herding. To achieve this, we conduct an tance strategy) [Kummer, 1968; Pines et al., 2011]. extensive kinship analysis using 23 autosomal, one Follower males apparently benefit from their status Y- and four X-linked microsatellites and mtDNA as followers in that they often acquire more of their haplotypes. By defining cut-off values for various leader’s females than other males [Pines et al., 2011, relatedness parameters as well as specifying

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conditions for haplotype sharing, we are able to to determine categorical kinship with genetic marker reliably distinguish among different kinds of kin data in the absence of pedigree information [Blouin, categories. This type of analysis allows us to 2003; Csillery et al., 2006; Van Horn et al., 2008]. determine the kinship of specific dyads as well as Approaches used need to take into account that the to distinguish between maternal and paternal kinship of a dyad can never be determined with kinship and, therefore, permits insights beyond absolute certainty and misclassifications are to be those that can be gained by assessing average expected and the extent of such error should be pairwise relatedness alone [cf. Stadele€ et al., 2015]. quantified [Blouin et al., 1996]. In order to identify related dyads in the absence of pedigree information, METHODS we devised an approach (Supporting Information, Fig. S1) inspired by analyses done in Langergraber fi Dyadic Relationship Classi cation et al. [2007, 2009]. In brief, we (i) performed a The genetic data used in this study derive from a parentage analysis (see Supporting Information) and recent analysis of the Filoha hamadryas study (ii) identified individuals that shared the same population in the Awash National Park, Ethiopia mother and/or father as full and half-siblings (see [Stadele€ et al., 2015]. In brief, we obtained genotypes Supporting Information, reconstruction of partial of 156 individuals of the habituated Band 1 and 88 pedigrees). We then (iii) used these known individuals from four unhabituated bands genotyped dyads to determine cut-off values for several param- at 23 autosomal, one Y-linked and four X-linked eters, that is, several log likelihood ratio values microsatellite loci and 364 bp of the mitochondrial (LODs) and the minimum dyadic relatedness coeffi- hypervariable region I. Two genotypes typed at less cient, for these kinship categories in our population than ten loci were excluded. Fecal samples were (Supporting Information, Tables SII and SIII). These collected from Band 1 between 2004 and 2011 and parameters were calculated in KINGROUP v2 from Bands 2 to 5 in 2010. In Band 1, individuals are [Konovalov et al., 2004]. The LOD score is the individually identified at an age at which they have natural logarithmic ratio of a dyad’s likelihood to typically left their natal OMU, so the vast majority of belong to a certain kinship category (primary individuals should be post-dispersal in the sense that hypothesis H) and the dyad’s likelihood to belong they are no longer in their natal OMU. Hamadryas to other kinship categories (null hypothesis H0). OMUs last only as long as an individual leader male Based on the cut-off values, we determined (iv) false maintains control of a number of females with their negative, misclassification (detailed below, Table I dependent offspring, which averages just under and Fig. 1) and false positive rates (detailed below, 6 years, so they are not permanent social units and Table II and Fig. 1) by simulation. Finally, we both males and females usually leave the units prior (v) applied the cut-off values determined in step 3 to to sexual maturity [Pines et al., 2015]. Due to the large our same-sex dyads of unknown kinship to assign the number of juveniles in this interim stage between the dyads to the categories of full siblings or paternal or natal OMU (and association with the mother) and a maternal second degree relatives or unclassified. reproductive OMU as a subadult or adult and the Paternal relatives are hereby defined as dyads difficulty of identifying juvenile individuals, we have related via a common male relative that is the father not been able to identify individuals consistently from of at least one of the dyad’s members and maternal infancy through adulthood and thus do not have relatives are defined as dyads related via a common pedigree information for any adult dyads. Additional female relative that is the mother of at least one of details on sample collection and completeness can be the dyad’s members. Second degree relatives consist found in Stadele€ et al. [2015]. of half-siblings, grandparent–grandoffspring, and Sampling procedures have been approved by the full avuncular relationships. Although many of these Institutional Care and Use Committee of second degree relatives are expected to be half- Queens College of the City University of New York. siblings, differentiating half-siblings from other This research was conducted with permission of and second degree relatives was not possible due to our following the guidelines of the Ethiopian Wildlife inability to clearly differentiate generations by age. Conservation Authority of Ethiopia and in accor- dance with the laws of Ethiopia. The research Misclassification and false negative rates adhered to the American Society of Primatologists In order to determine misclassification rates (ASP) Principles for the Ethical Treatment of Non- among the kinship categories and false negative Human Primates. Because our study exclusively rates for each kinship category, we generated ten sets relied on non-invasively collected samples and, of 500 pairs each of full siblings, maternal half therefore, did not involve animal handling or testing, siblings, paternal half siblings, and cousins in we did not violate any regulations of the Deutsches KINGROUP v2 based on our population Tierschutzgesetz. frequencies based on genotypes of individuals of all We used genetic data to assess kinship of dyads bands. Using the population haplotype frequencies, in our population. It is notoriously difficult to we randomly assigned mtDNA haplotypes to

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TABLE I. Classification Rates for Male and Female Kinship Categories

Actual relationship

Maternal second Paternal second Third degree Classified as Full siblings degree relatives degree relatives relatives

Female Full siblings 72.5 2.3 4.5 1.0 0.5 0.3 0.1 0.1 Maternal second degree relatives 7.7 0.7 40.8 2.2 5.3 1.0 2.4 0.4 Paternal second degree relatives ––43.0 2.1 15.3 2.0 False negative rate 19.8 2.3 54.7 2.4 51.2 2.5 – Male Full siblings 72.5 2.3 1.0 0.5 0.6 0.3 0.0 0.1 Maternal second degree relatives 7.7 0.7 40.8 2.2 5.5 1.1 1.3 0.6 Paternal second degree relatives ––42.8 1.8 4.2 1.0 False negative rate 19.8 2.3 58.1 2.3 51.1 2.5 –

True positive classification rates are in bold. Other rates are misclassification and false negative rates. Means were calculated from ten sets of each 500 full, half sibling and cousin dyads simulated in Kingroup v2. Second degree relatives are half siblings, full avuncular relatives, and grandparent–grand offspring. Third degree relatives are first cousins, half avuncular relatives, and great grandparent–great grand offspring. Rates in percent standard deviation. individuals of paternally related dyads, Y-haplotypes For dyads identified as female second degree to males in maternally related dyads, and Y- and relatives, we also determined whether they could mtDNA haplotypes to cousins in order to simulate potentially be paternal half-sisters as they would then the stochastic sharing of these haplotypes between necessarily share an allele at every X-chromosomal relatives of these kinship categories. We then applied . This was particularly useful for paternally our cut-off values and conditions on matching related female dyads because we expected that some haplotypes (see Supporting Information, Determin- third degree female relatives (cousins, half avuncular ing criteria for the classification of dyads) to each relationships, and great grandparent–great grand- set of a certain kinship category and calculated offspring) who do not share mtDNA haplotypes would what proportion of dyads would be misclassified be misidentified as paternal second degree relatives (misclassification rate), what proportion of dyads of (Table I). Likewise, we also expect that some third a certain kinship category would be categorized degree male relatives would be misidentified as as unclassified (false negative rates) and what paternal second degree relatives but our estimated proportion of dyads of a certain kinship category misclassification rate was one-third of that for females are correctly assigned to that category (true positive (Table I). rates). The misclassification, false negative, and true positive rates are shown in Table I and graphically Determining the false positive rate represented in Figure 1. In order to estimate a false positive rate (percent- It is important to note that all dyads not age of dyads that are truly unrelated but are categorized as relatives are categorized as unclassi- misclassified as kin by our criteria), we used fied. They cannot be classified as unrelated due to the KINGROUP v2 to generate a “null hypothesis” from high false negative rates and, therefore, include our set of 242 individuals of all bands by randomly many actually related dyads (Table I). Reducing the permuting at each locus between individuals. false negative rates would have the effect of increas- This simulates a set of unrelated individuals with the ing the false positive rates. In studies aiming to look allele frequencies of the real population. We then at the impact of kinship upon behavior, many fewer randomly assigned band membership and Y- and related than unrelated dyads are expected [Lukas mtDNA haplotypes drawn from our population et al., 2005] and it is important to set criteria so that haplotype frequencies to these new genotypes keeping the identified set of related dyads is accurate (low the number of individuals the same as in the real false positive rates) and behavioral preferences may bands. We created a set of unrelated male and female be observed, even if many related dyads are not X-chromosomal genotypes by permuting alleles identified (false negatives). Although we could have between individuals. We then randomly assigned an established criteria for classifying dyads as unre- X-chromosomal genotype to an autosomal genotype. lated, in this study, we do not explicitly compare We repeated this ten times and thus created ten related and unrelated dyads in subsequent analyses. simulated sets of 242 unrelated individuals (each of Having unclassified dyads is not problematic because 29,161 dyads) and proceeded to calculate all param- the ratio of true positives to false negatives is eters, conduct the parentage analysis and apply cut- expected to be the same in the observed data and off values as for the real set of individuals. The overall the permutations. false positive rate for male–male dyads was 0.5% and

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Fig. 1. Graphical representation of dyads in a two- and three-dimensional parameter space. Exemplary sets of 500 dyads of each full siblings (black), half siblings (red), and unrelated dyads (green) simulated from the population allele frequencies in KINGROUP v2. Borders of rectangles and boxes represent the cut-off values beyond which dyads get assigned to a certain kinship category, second degree relatives (2nd), full siblings (fs), or unclassified kinship status. For maternal siblings and full siblings and paternally related males and full brothers, respectively, sharing of mtDNA and/or Y-haplotypes was also required and represents a fourth or fifth dimension not shown. Axes are three genetic parameters calculated from autosomal microsatellite genotypes: coef., coefficient; LOD, natural logarithm of the likelihood ratio of the corresponding parameter; LOD 2, H: full siblings versus H0: parent–offspring, half siblings, unrelated (autosomal microsatellites; H, hypothesis; H0, null hypothesis); LOD 3, H: half siblings versus H0: parent–offspring, full siblings, unrelated (autosomal microsatellites).

1.7% for female–female dyads (Table II). For pater- second order relationships), 61 of which were same- nally related second degree female relatives, the rate sex dyads and 52 of which were cross-sex dyads. should be somewhat lower if only potential paternal Given that a large proportion of both sexes stay in sisters are concerned because they are also required to their natal band, finding many related cross-sex share at least one allele at every locus of the dyads is expected. As we were only interested in X-chromosome. It is important to note that from these same-sex dyads, we then applied the cut-off values to rates, we cannot calculate the number of false positive all same-sex dyads of Band 1 of still unknown kinship dyads we would expect to find in the final set of related (5,970 dyads). For paternally related second degree dyads because the actual number of unrelated dyads female relatives detected in this way, we also checked in the dataset is unknown. whether they shared at least one allele at every X-linked locus (parameter 7: P-value < 1; Table SIV). Classification of dyads of unknown kinship If females did not share one allele at every X-linked The parentage analysis for individuals of Band 1 locus, they could not be paternal sisters and were and the partial pedigree reconstruction led to the rather full avuncular relatives, grandparent– assignment of 113 dyads to categories of known grandoffspring, or third degree relatives that were kinship (57 parent–offspring, 28 full siblings, 28 misclassified as second degree relatives (Table II). All

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TABLE II. False Positive Rates per Kinship Category comparison to the observed number of related dyads. in Simulated Data of Unrelated Individuals In some cases, a leader male had two followers or a follower followed two leader males, so in order to Mean expected false SD avoid pseudoreplication, we chose 20 random subsets Kinship positive rate (%) (%) of the data in which each male was included in only Parent–offspring 0.0 0.0 one dyad and the other dyads it was included in were Full siblings discarded for each subset. We then ran a set of Female–female 0.0 0.0 permutations for each of the subsets. This meant that Male–male 0.0 0.0 subsets contained fewer leader–follower dyads than Second degree relatives the total number of genotyped dyads (n ¼ 24) and Paternally related, 1.5 0.2 also varying numbers of leader–follower dyads female–female (n ¼ 15–17). P-values are the mean P-value of the Maternally related, 0.2 0.0 – 20 subsets and the standard deviation. The expected female female number of dyads is the mean of the 20 permutation Paternally related, 0.3 0.1 male–male means and the standard deviation. In order to Maternally related, 0.2 0.1 investigate whether female relatives were found male–male within OMUs more often than expected by chance we limited this analysis to May 2010, the month in The false positive rate is the percentage of truly unrelated dyads that are which most females were genotyped (67 females, 65% falsely classified as kin. Means were calculated from ten datasets of 242 unrelated individuals simulated in Kingroup v2. Second degree relatives of individually identified females; 52 within-OMU are half siblings, full avuncular relatives, and grandparent–grand dyads, 41% of all within-OMU dyads; 35 OMUs). We offspring relationships. SD, standard deviation. randomly permuted females among OMUs 9,999 times while keeping the numbers and sizes of the OMUs the same as in the original dataset. In order to dyads not assigned to a kinship category were obtain a P-value, we counted how often the number of considered unclassified, not unrelated, due to the female related dyads within OMUs in the permuta- large expected proportion of false negatives given our tions was larger than or equal to the observed value. cut-off values (Table I).

RESULTS Tests for Non-Random Association Dyadic Relationship Classification We programmed a permutation test in R 3.0.2. fi – [R Development Core Team, 2013] in order to We identi ed 149 male male and 238 – fi determine whether females within OMUs and female female rst and second degree relatives leader–follower male dyads were relatives more among the 156 individuals of Band 1. The number fi often than expected by chance. In order to determine of related dyads identi ed per kinship category is whether leader–follower male dyads were relatives shown in Table III. more often than expected by chance, we limited this analysis to the year 2009 because this was the year in – which the largest number of leader–follower male Leader Follower Dyads dyads were genotyped (n ¼ 24, 89% of all individually Of the 34 leader–follower male dyads identified identified leader–follower male dyads). We included between 2004 and 2011 for which genotypes all leader males that did not have a follower male or were available, 15 (44%) were relatives (one whose follower male was not genotyped in the parent–offspring dyad, one full sibling dyad, ten permutations (n ¼ 18). We then randomly permuted maternal and three paternal second degree rela- followers among leader males 9,999 times. In order to tives). The status of eight dyads (24%) was obtain a P-value, we checked how often we found unclassified, with one dyad sharing an mtDNA more related dyads in the permutations in haplotype but not a Y-haplotype and seven dyads

TABLE III. Same-Sex Dyads of Kin Identified in Band 1

Parent–offspring Full siblings Maternal second degree Paternal second degree

Male–male dyads 7 11 40 91 Female–female dyads 18 11 47 162 (73)

Second degree relatives are half-siblings, full avuncular relatives, or grandparent–grandoffspring. Paternally related dyads are related via a common male relative that is the father of one of the dyad’s members and maternally related dyads are related via a common female relative that is the mother of one of the dyad’s members. The number of paternally related female dyads among all paternal second degree relatives who could potentially be paternal sisters as they share at least one allele at every locus of the X-chromosome is shown in brackets.

Am. J. Primatol. 8/Stadele€ et al.

sharing a Y-haplotype but not an mtDNA haplotype. time with the most individually identified and Eleven dyads (32%) could not possibly have been genotyped leader–follower male dyads, ten dyads close relatives because they shared neither Y- nor were relatives (42% of 24 genotyped leader–follower mtDNA haplotypes. For five (45%) of the follower dyads). These dyads were maternal relatives signifi- males in these apparently unrelated dyads, at least cantly more often than expected by chance (P < 0.001 one maternal or paternal second degree relative in all subsets; mean observed number of related leader male would have been present in Band 1 at the dyads in subsets ¼ 6.0 SD 0.7; mean expected time they started being follower males. In other number¼0.4 SD 0.0; see Methods section). At words, they started following a non-relative leader that time, leader–follower male dyads were not male despite the fact that a related leader male was paternal relatives more often than expected by chance present in Band 1 at the time. There were no obvious (P ¼ 0.221 SD 0.15; observed number ¼ 1.7 SD differences in the number of females or presence of 0.5; mean expected number ¼ 0.6 SD 0.1). other followers between the OMUs they followed and the OMUs of the related leader males. Only in one case was the leader the father of the follower and the Female Relatives in OMUs follower’s mother was a female in the OMU, so the In order to assess whether females typically have male likely started following his natal OMU. This access to female relatives, we investigated how often dyad was not included in the following analysis female relatives were found in the same OMU. We because the follower disappeared in 2008. In general, examined data on the composition of OMUs between followers are usually older than the average male 2004 and 2010. The number of OMUs in which tenure length of 5–6 years. In all other 14 cases, the females were individually identified increased over leader male could not have been the follower’s father. the years as the number of identifications improved. For the 11 leader–follower dyads deemed not closely For example, in January 2004, 55 females in 20 OMUs related, one might argue that the follower was were individually identified and we obtained geno- attached to the natal OMU containing his mother types for 28 (51%) of these females, whereas in and was not related to the leader due to a change in May 2010, 103 females in 38 OMUs were individually leadership. However, we found that in 8 out of 11 identified and we obtained genotypes for 67 (65%) of cases, the follower’s mother was either in a different these females. For the period between 2004 and 2010, OMU (n ¼ 4) or none of the OMU females could have there were ten instances in which we found 11 been the follower’s mother. Only in the three different dyads of female relatives in the same remaining cases were the follower’s mother unknown OMU (8% of 137 different genotyped within-OMU and the followed OMUs incompletely genotyped, so dyads) (Fig. 2). These were four mother–daughter that an untyped female could have theoretically been dyads, one dyad of full sisters, one dyad of maternal the follower’s mother. It is, therefore, unlikely that sisters, three dyads of potential paternal half-sisters, the assessment of kinship among leaders and and two dyads of paternally related second degree followers was strongly biased due to followers having relatives. In May 2010, the month with the best not yet dispersed from their natal OMU. In 2009, the sampling of females, seven of these dyads were found

Fig. 2. Transfer of females into one-male-units containing relatives. Females are depicted as ovals below the names of their leader males. Only transferring females and females having a relative in their one-male-unit (OMU) are shown. Solid arrows indicate a female’s change of OMU membership. Shared colors indicate a dyad’s kin relationship within an OMU (green, mother–daughter; orange, maternal sisters; gray, full sisters; blue, paternal second degree relatives). Paternal second degree relatives are half-sisters, full avuncular relatives, or grandmother–granddaughter where dyads are related via a common male relative that is the father of one of the dyad’s members. Dashed arrows indicate the dissolution of an OMU due to death (†) or old age of the leader male (X). ?Leader male unknown. I is sick and Herb stops herding her. S changes OMU membership and her daughter Li follows 4 days later.

Am. J. Primatol. Maternal Kin Bias in Hamadryas Baboons /9

in the same OMU (13% of 52 genotyped within- In this study, leader and follower male dyads OMU dyads). We found that in May 2010, maternally were maternal but not paternal relatives more often related dyads were found within OMUs more than expected by chance, suggesting that maternal often than expected by chance (P ¼ 0.016; observed kinship may play a role in the formation of number of dyads ¼ 4; expected number of dyads ¼ 1.0 leader–follower relationships. This is consistent SD 1.0), but paternally related dyads were with previous research on captive hamadryas-like not (P ¼ 0.36; observed number of dyads ¼ 2; hamadryas–cynocephalus hybrids, which found that expected number of dyads ¼ 1.3 SD 1.1; only poten- maternally related leader–follower dyads (either tial paternal half-sisters were considered paternally maternal or full brothers) occurred more often than related, see Misclassification and false negative rates expected by chance while leader–follower dyads were section). paternal brothers less often than expected by chance We can use observational data to examine the [Colmenares, 1992]. Leaders who are at the end of circumstances under which related females ended up their reproductive career and not likely to sire more in the same OMU. In nine of the ten instances in offspring could gain indirect fitness benefits by which female relatives were found in the same OMU, peacefully surrendering mature females to closely these relatives were not together in the same OMU related males. Kummer [1968] suggested that old when they were originally individually identified, leaders tend to gradually release females from their but rather one of the females subsequently trans- control. If the females were then taken over by a ferred into the OMU of a female relative (Fig. 2). This related follower or ex-follower of the leader, the means that these relatives were not in the same outcome of this process would be behaviorally similar OMU simply because neither had yet left their natal to levirate or widow inheritance in humans in which OMU. In three of these cases, the OMU of origin of a brother marries his deceased sibling’s wife, which is the transferring female could not be determined, but practiced in roughly 50% of human societies in six cases, the transferring females came from [Murdock, 1949]. Only follower males are in a OMUs in which the leader died or was ill or old and position to employ such an inheritance strategy had begun losing females to other males, which tends and peacefully and non-opportunistically acquire to happen relatively quickly near the end of a male’s mature females from other leaders [Pines et al., 2011, tenure as leader [Kummer 1968; Pines et al., 2015]. 2015]. We do not know the strategy behind the In the one remaining case, the transferring female takeovers for enough dyads of known kinship to test was visibly ill and her leader male had stopped whether followers that are related to leaders are herding her (Herb; Fig. 2). In one instance, a mother more likely to inherit adult females than unrelated and her daughter transferred together into an OMU followers. Nevertheless, it has recently been shown containing another daughter of that mother after that OMUs with one or more followers produce three their leader male fell off a cliff and died (Redface; times as many offspring as OMUs without followers Fig. 2). Another female from this OMU transferred due to prolonged leader and female tenures and the into her daughter’s OMU, where they remained acquisition by leaders of twice as many females together for approximately 8 months (Fig. 2). during their tenure [Chowdhury et al., 2015]. Thus, When the new OMU eventually started to dissolve, assuming, as behavioral evidence suggests, near probably due to old age of the leader male, the exclusive paternity certainty for leader males, the mother transferred into another OMU and the presence of followers appears to increase a leader’s daughter followed 4 days later when the leader direct fitness and consequentially a related follower’s male died (Len; Fig. 2). On average, females would indirect fitness [Chowdhury et al., 2015]. have been expected to end up by chance in an Follower males are in fact unlikely sires of OMU with a maternal relative with a likelihood of offspring as only 3% of copulations involve fol- 0.11 SD 0.08. lowers and copulations between followers and reproductively mature females are usually incom- plete [Kummer 1968; Nitsch et al., 2011; Swedell & DISCUSSION Saunders, 2006; Swedell unpublished data]. How- Our analysis of patterns of kinship in a band of ever, a low probability of paternity may be part of the wild hamadryas baboons suggests that two impor- reason why followers follow even if they are not tant elements of hamadryas society, the relation- closely related to the leader. Followers form social ships among females within an OMU and the bonds with their leader’s females and it is likely relationships between leader males and their easier for a follower to take over a female that has a followers, are non-random associations of same sex predisposition to join him [Pines et al., 2011]. kin. These associations may result from motivations Generally, followers and ex-followers are more on the part of both sexes to establish and maintain successful in taking over females from their leader relationships with maternal kin. If so, then kin or ex-leader than are leader or solitary males [Pines selection may play a greater role in hamadryas social et al., 2011, 2015]. Overall, our finding that at least organization than previously thought. one-third of assessed leader–follower dyads in this

Am. J. Primatol. 10 / Stadele€ et al.

study were unrelated suggests that such relation- preferentially join OMUs containing maternal rela- ships are not wholly determined by kinship between tives. Some degree of female choice in OMU member- the males. In part, the tolerance of leader males ship has previously been suggested [Swedell, 2000, toward followers may be explained by disinterest of 2006], a notion supported by observations of pairs of the leader male in immature natal females who are females, including mother–daughter dyads, interact- his probable daughters. Indeed, leader males rarely ing across OMUs [Abegglen, 1984; Swedell, 2002] as intervene in interactions between immature females well as transfers of females who had previously been and non-leader males [Abegglen, 1984]. in an OMU together into the same new OMU directly avoidance could, therefore, partly account for the after one or more changes of OMU membership gradual and mostly non-aggressive formations of [Chaylan et al., 1994; Sigg et al., 1982; Swedell, 2000]. initial units with immature females by followers. We An examination of the instances of female transfer do not know whether solitary males and unrelated into OMUs containing female kin in this study followers are more likely to be tolerated when natal revealed that in all instances in which the OMU of juvenile females are present, but this possibility is origin was known these transfers occurred in certain supported by the finding of a correlation between the circumstances: either the leader died, the female was number of followers and the number of pregnant and sick and the leader stopped herding her, or the OMU immature females in an OMU [Swedell, 2006]. dissolved during or shortly after the transfer of the We conclude that leader and follower males may female because the leader male lost one female both gain direct fitness from their relationship, relatively soon after another (which tends to happen although the reproductive benefits to followers are to older or ill leader males who cannot effectively herd delayed rather than immediate. This is comple- or defend their females). This suggests that under mented by a gain of indirect fitness for both if certain conditions females may be able and motivated followers and leaders are related. Whether a male to choose membership in an OMU containing female becomes a follower and which leader he follows kin and that some opportunistic takeovers may rather probably depends on various factors such as kinship be opportunistic voluntary transfers. Although these to the leader, age, and reproductive state of the circumstances arise stochastically and many females OMU’s females or the age and physical condition of may never be found in an OMU with a female relative, himself and the leader males in his clan. females remaining in their natal band in particular The second set of results from these analyses should have the opportunity to transfer with or be suggests a role of kinship in relationships among reunited with a female relative in the same OMU at hamadryas females. Traditionally classified as a “non- some point in their lives and occasional interactions female-bonded” taxon because females disperse across OMUs might represent an additional way of among social units and show a lower degree of maintaining contact with female kin. Taken as a female–female affiliation than in other baboons, whole, our results suggest that hamadryas baboon hamadryas females have traditionally been thought females may have retained an ancestral tendency to to not reside with their kin nor have any motivation to preferentially associate with maternal female kin and do so. Hamadryas differ from most other female- so instances of female philopatry may not simply be a dispersing taxa, however, in that females are usually consequence of a tendency of males to take over forcibly moved between social units by leader males females within their band or clan. and do not generally appear to be inherently Chapais [2001] noted that kin selection might not motivated to leave their natal units [Abegglen, be the only ultimate driving force behind primate 1984; Swedell, 2002, 2006; Swedell et al., 2011]. matrilineal nepotism. He suggested that the proxim- Behavioral data from Filoha, in fact, show that adult ity correlate, the fact that proximity often correlates females of the same OMU interact affiliatively (i.e., with matrilineal kinship in female philopatric species, groom and sit within 10 cm) with each other on can create matrilineal nepotism in the absence of kin average at least as much as each does with her leader selection. Under the assumption of a proximity male, and that female dyads vary greatly in the correlate, proximity among all kinds of maternal strength of these affiliative behaviors, possibly relatives is mediated through the special bonds of reflecting differences in kinship among dyads mothers and daughters and not through an attraction [Swedell, 2002, 2006]. The fact that some of other kinds of maternal kin to each other. Nepotistic female–female dyads within the hamadryas OMUs behavior among these kin could then be driven by in this study are maternal kin raises the potential for rather than kin selection. The kinship and nepotism to play a role in shaping female hamadryas social system lacks the proximity corre- social interactions. In this study, for the year 2010, the late due to takeovers of females and, therefore, year with our best sample of females, we found presents an ideal system for further investigation of maternally but not paternally related females in the these ideas. Our current sample size does not allow us same OMU more often than expected by chance. This to test whether females transfer into OMUs contain- non-random association of maternal female relatives ing non-mother–daughter relatives at a similar rate in OMUs is best explained by a tendency of females to as into OMUs containing a mother or daughter. If this

Am. J. Primatol. Maternal Kin Bias in Hamadryas Baboons /11

were the case and hamadryas females actually kin results in inclusive fitness benefits for individu- displayed nepotistic behaviors, kin selection rather als and, if so, which proximate mechanisms are than natural selection acting on individuals in close involved. Furthermore, the tendency of females to proximity would explain matrilineal nepotism. Fur- join OMUs containing female kin when possible thermore, this means that matrilineal nepotism indicates that female bonds, although not immedi- would likely also be driven by kin selection in other ately apparent, may also be important for hamadryas baboon species. Four out of the five transfers that led females. These results corroborate previous hypoth- to maternal female relatives’ being found in the same eses suggesting that hamadryas baboons occupy an OMU involved mother–daughter dyads. Studies in extreme position along a Papionin behavioral contin- other baboons and rhesus macaques have indeed uum [Alberts & Altmann, 2006; Henzi & Barrett, found that mothers and daughters form particularly 2003]. stronger and more equitable bonds than other female maternal relatives [Schulke€ et al., 2013; Seyfarth et al., 2013; Silk et al., 2006a]. ACKNOWLEDGMENTS Ultimately, future research is needed to extend these results beyond mere presence of kin We thank Anthony Di Fiore and two anonymous inthesamesocialunitsoastoexamineifandto reviewers for helpful comments on the manuscript. what extent hamadryas females bias affiliative This project was funded by the Max Planck Society, social behavior toward related maternal females the Leakey Foundation through grants awarded to over unrelated females, as well as whether such L. V. (2011) and L. S. (1998, 2007, 2012), the Wenner- biases are adaptive in terms of inclusive fitness Gren Foundation (1996, 2009, and 2012 to L.S.), the benefits in addition to possible direct fitness National Geographic Society (6468-99 and 8309-07 to benefits gained through close social bonds [Silk, L.S.), the National Science Foundation (9629658 to 2007]. Research in other cercopithecines has L.S.), the PSC-CUNY Research Award Program linked strong social bonds among female baboons funded jointly by the City University of New York and mandrills to a younger age at first reproduc- and the Professional Staff Congress (to L.S.). The fi tion, enhanced offspring survival, and increased eldwork portion of this project would not be possible longevity, and such bonds are preferentially without the permission of the Ethiopian Wildlife fi formed with maternal kin [Charpentier et al., Conservation Authority (EWCA) and af liation and 2012; Silk et al., 2009, 2010b]. assistance from the Awash National Park Baboon Our findings of a non-random association of Research Project (ANPBRP). In addition, we thank maternal but not paternal dyadic kin, both with Vanessa van Doren for collecting samples and regard to female dyads and leader–follower male initiating lab work, Julian Saunders, Amy Schreier, dyads, is notable considering that the lengthy tenure Brittany Davis, and Teklu Tesfaye for collecting of leader males combined with seemingly high samples that contributed to this data set; Teklu paternity certainty would appear to facilitate recog- Tesfaye, Demekech Woldearegay, Tariku Woldear- nition of paternal siblings as well as of father egay, and the employees of the Awash National Park and offspring. Additionally, we previously found for logistical support; and Alexis Amann and Y-haplotypes to cluster within clans suggesting Shahrina Chowdhury for assistance with sample that clans consist of patrilineally related males transport and data management. [Stadele€ et al., 2015]. 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