Population genetic insights into the social organization of Guinea baboons (Papio papio): Evidence for female‐biased dispersal

Sex differences in philopatry and dispersal have important consequences on the genetic structure of populations, social groups, and social relationships within groups. Among mammals, male dispersal and female philopatry are most common and closely related taxa typically exhibit similar dispersal patterns. However, among four well‐studied species of baboons, only hamadryas baboons exhibit female dispersal, thus differing from their congenerics, which show female philopatry and close‐knit female social relationships. Until recently, knowledge of the Guinea baboon social system and dispersal pattern remained sparse. Previous observations suggested that the high degree of tolerance observed among male Guinea baboons could be due to kinship. This led us to hypothesize that this species exhibits male philopatry and female dispersal, conforming to the hamadryas pattern. We genotyped 165 individuals from five localities in the Niokolo‐Koba National Park, Senegal, at 14 autosomal microsatellite loci and sequenced a fragment of the mitochondrial hypervariable region I (HVRI) of 55 individuals. We found evidence for higher population structuring in males than in females, as expected if males are the more philopatric sex. A comparison of relatedness between male–male and female–female dyads within and among communities did not yield conclusive results. HVRI diversity within communities was high and did not differ between the sexes, also suggesting female gene flow. Our study is the first comprehensive analysis of the genetic population structure in Guinea baboons and provides evidence for female‐biased dispersal in this species. In conjunction with their multilevel social organization, this finding parallels the observations for human hunter‐gatherers and strengthens baboons as an intriguing model to elucidate the processes that shaped the highly cooperative societies of Homo. Am. J. Primatol. 77:878–889, 2015. © 2015 The Authors. American Journal of Primatology Published by Wiley Periodicals Inc.     

Female "dispersal" in hamadryas baboons: transfer among social units in a multilevel society

Unlike most cercopithecines, hamadryas baboons (Papio hamadryas hamadryas) are characterized by female-biased dispersal. To clarify this pattern within the context of their hierarchical social system (comprising one-male units, clans, bands, and troops), we report here 7 years of data on female transfers among social units in wild hamadryas baboons in Ethiopia. Female tenure in one-male units (OMUs) ranged from 1 to 2,556 days (N = 208) and survival analysis revealed a median tenure length of 1,217 days (40 months). Changes in OMU membership consisted almost exclusively of takeovers by males, not voluntary transfer. Of 130 takeovers, 67% occurred within the band and 33% across bands, and, of the 22 takeovers for which we have clan membership data, 77% occurred within, not between, clans. These results reinforce the notion that hamadryas female dispersal is not analogous to sex-biased dispersal in other taxa, because (1) at least in Ethiopian populations, females do not disperse voluntarily but are transferred, often forcibly, by males; (2) only dispersal between bands will promote gene flow, whereas females are most often rearranged within bands; (3) hamadryas females undergo social dispersal but not usually locational dispersal; and (4) while male hamadryas are far more philopatric than females, they have been observed to disperse. It thus appears that the ancestral baboon pattern of female philopatry and male dispersal has evolved into a system in which neither sex is motivated to disperse, but females are forcibly transferred by males, leading to female-mediated gene flow, and males more rarely disperse to find females.     

Genetic evidence for female-biased dispersal and gene flow in a polygynous primate

Many models of sex-biased dispersal predict that the direction of sex-bias depends upon a species' mating system. In agreement with this, almost all polygynous mammals show male-biased dispersal whereas largely monogamous birds show female-biased dispersal (FBD). The hamadryas baboon (Papio hamadryas hamadryas) is polygynous and so dispersal is predicted to be male biased, as is found in all other baboon subspecies, but there are conflicting field data showing both female and male dispersal. Using 19 autosomal genetic markers genotyped in baboons from four Saudi Arabian populations, we found strong evidence for FBD in post-dispersal adults but not, as expected, in pre-dispersal infants and young juveniles, when we compared male and female: population structure (F(st)), inbreeding (F(is)), relatedness (r), and the mean assignment index (mAIc). Furthermore, we found evidence for female-biased gene flow as population genetic structure (F(st)), was about four times higher for the paternally inherited Y, than for either autosomal markers or for maternally inherited mtDNA. These results contradict the direction of sex-bias predicted by the mating system and show that FBD has evolved recently from an ancestral state of male-biased dispersal. We suggest that the cost-benefit balance of dispersal to males and females is tightly linked to the unique hierarchical social structure of hamadryas baboons and that dispersal and social organization have coevolved.     

A Papionin Multilevel Society as a Model for Hominin Social Evolution

Multilevel societies are unique in their ability to facilitate the maintenance of strong and consistent social bonds among some individuals while allowing separation among others, which may be especially important when social and sexual bonds carry significant and reliable benefits to individuals within social groups. Here we examine the importance of social and sexual bonds in the multilevel society of hamadryas baboons (Papio hamadryas) and apply these principles to social evolution in Plio-Pleistocene hominins. The behavior, adaptations, and socioecology of baboons (Papio spp.) have long been recognized as providing an important comparative sample to elucidate the processes of human evolution, and the social system of hamadryas baboons in particular shares even more similarities with humans than that of other baboons. Here we draw parallels between processes during the evolution of hamadryas social organization and those characterizing late Pliocene or early Pleistocene hominins, most likely Homo erectus. The higher costs of reproduction faced by female Homo erectus, exacerbated by an increased reliance on difficult to acquire, nutrient-dense foods, are commonly thought to have been alleviated by a strengthening of male–female bonds (via male provisioning and the evolution of monogamy) or by the assistance of older, postreproductive females (via grandmothering). We suggest that both of these social arrangements could have been present in Plio-Pleistocene hominins if we assume the development of a multilevel society such as that in hamadryas baboons. The evolution of a multilevel society thus underlies the adaptive potential for the complexity that we see in modern human social organization.     

Comparisons of Intraunit Relationships in Nonhuman Primates Living in Multilevel Social Systems

Multilevel social systems have evolved in several species of cercopithecoid primates and appear to be an effective means of changing group size amid variation in environmental conditions. Larger groupings of these species fission and fuse, making intraunit relationships essential to maintain the integrity of the smallest social units. We examine these intraunit relationships in four primates with multilevel social systems: proboscis monkeys (Nasalis larvatus), snub-nosed monkeys (Rhinopithecus roxellana), hamadryas baboons (Papio hamadryas), and geladas (Theropithecus gelada), using social network analysis. The proboscis monkeys and hamadryas baboons were wild and unprovisioned, whereas the snub-nosed monkeys and geladas were partly provisioned. Comparison of eigenvector centrality coefficients revealed a phylogenetic difference in the key individuals maintaining social networks between the colobines and the cercopithecines: females were more central in proboscis and snub-nosed monkeys, with males generally peripheral to social interaction, whereas males were more central than females in geladas and hamadryas. A comparison of sex differences in clustering coefficients, however, revealed a significant difference only in geladas, suggesting that one-male–multifemale units in this species become more unstable when females, but not males, are removed from social networks. Taken together, our results reveal the strongest differences between geladas, characterized by female philopatry and male dispersal, and the three species with bisexual dispersal. These results demonstrate the potential for social network analysis to reveal the social bonds most important for maintaining cohesion of the smallest units of primate multilevel societies. This, in turn, can serve as a proxy, in the absence of long-term data, for underlying patterns of sex-biased dispersal and philopatry.     

Group Composition of Guinea Baboons (<Emphasis Type="Italic">Papio papio</Emphasis>) at a Water Place Suggests a Fluid Social Organization

Baboon social systems are among the most studied in primates. Solid knowledge of the hamadryas and savannah baboon systems has accumulated, leading to a dichotomic view of baboon social systems. Hamadryas baboons live in multilayered troops based on 1-male units whereas savannah baboons live in multimale multifemale groups based on a network of related females. Less attention has been paid to their West African congenerics, the Guinea baboons, Papio papio. To fill this gap, in 2007 we initiated a long-term study of a baboon troop ranging in the Niokolo Koba National Park in southeastern Senegal. Earlier studies suggested a tendency for a multilayered social system in Guinea baboons, similar to the hamadryas baboon organization. Therefore, as a first approach to analyzing variability in party size and composition, we observed members of the troop crossing an open area from a fixed point for 3 mo during the dry and wet seasons. We counted individuals and recorded changes in composition of both arriving and departing parties. Party size and composition were highly variable on both a daily and a seasonal basis; 45.9% of the arriving parties changed in composition while crossing the open area, either splitting into smaller parties or fusing into larger ones, suggesting a fluid organization. Our data support the existence of neither a hamadryas baboon-like multilayered social organization nor a stable medium-sized multimale multifemale group as in savannah baboons. In light of our data we may need to revise the dichotomic view of baboon social systems and include space for greater variability of their social systems.     

Mitochondrial evidence for the origin of hamadryas baboons

Baboons (Mammalia: Primates, Papio) are found primarily on the continent of Africa, but the range of hamadryas baboons (Papio hamadryas) extends to the Arabian Peninsula, and the origin of Arabian populations is unclear. To estimate the timing of the divergence between Arabian and African hamadryas populations we analyzed mitochondrial DNA (mtDNA) sequences from individuals of Arabian and African origin, and from representatives of the other major baboon taxa. The oldest hamadryas mitochondrial lineages in the Arabian Peninsula form an ancient trichotomy with the two major African lineages. This suggests that Arabia was colonized by hamadryas very soon after the appearance of the distinctive hamadryas phenotype, both events perhaps coinciding with a mid-Pleistocene stage of dry climate and low sea-level. The most closely related Arabian and African mtDNA haplotypes coalesce at approximately 35 ka, suggesting that no gene flow between African and Arabian baboons has occurred since the end of the last ice age, when a land bridge at the southern sill of the Red Sea was submerged. The mitochondrial paraphyly of Ethiopian hamadryas and anubis (P. anubis) baboons suggests an extensive and complex history of sex-specific introgression.     

Group Composition and Adult Sex-ratio of Hamadryas Baboons (Papio hamadryas hamadryas) in Central Eritrea

During a survey of the geographical distribution and abundance of hamadryas baboons (Papio hamadryas hamadryas) in central Eritrea, we collected detailed demographic data on six bands at four sites in different ecogeographical zones. The proportions of age-sex classes within the six bands differed only with respect to juveniles. The general social organization of the Eritrean hamadryas baboons is similar to that reported for Ethiopia and Saudi Arabia. Eritrean hamadryas baboons live in a nested fission-fusion system, with one-male units as the basic social entity. Although the baboons were not provisioned, as they are in many places in Saudi Arabia, and habitat quality in Eritrea is lower than that in Ethiopia, sex-ratios and group composition corresponded more to those found in the Saudi Arabian population. Sex-ratios within the study population, in bands and also in one-male units were significantly more female-biased than in Ethiopian ones, and one-male units tended to be larger. Data from Eritrea suggest that these differences are due to a combination of a heavily fluctuating rainfall pattern and differential maturation of the sexes.     

Distribution and Habitat Associations of Baboons (Papio hamadryas) in Central Eritrea

At least three diurnal primate taxa are still present in Eritrea, NE Africa: hamadryas baboons (Papio hamadryas hamadryas), olive baboons (Papio h. anubis) and grivet monkeys (Chlorocebus aethiops aethiops). However, information on status and distribution of primates and their habitats in Eritrea is outdated and incomplete. We conducted a primate survey, focussing on hamadryas baboons, to obtain data which will be integrated in a national wildlife management and conservation plan in Eritrea. We obtained information about the geographical distribution and abundance of baboons, their altitudinal range, habitat quality of their home-ranges, aggregation sizes at sleeping cliffs and predator presence. We described habitat quality via the Normalized Difference Vegetation Index (NDVI), a vegetation classification of Landsat MSS satellite data. Hamadryas and olive baboons are still present in Eritrea in ample numbers. Their geographical distributions in 1997 and 1998 did not deviate significantly from their historical distributions. An estimated 15,000 Papio hamadryas hamadryas lived in the 25,000-km² area of survey (0.58 baboons/km²). Population densities of hamadryas baboons in many parts of the survey area are higher than at Kummer's (1968) study site in Ethiopia. Hamadryas baboons live at all altitudes in four of five ecogeographical zones of Eritrea. Olive baboons replaced them in the western lowlands. Both baboon taxa tend to select better quality habitats, characterized by a higher normalized difference vegetation index (NDVI) than the average for the respective ecogeographical zones. Hamadryas baboons show a greater ecological plasticity than olive baboons, which are confined to riverbeds with extended gallery forest. By the end of 1999, a hybrid zone could not be confirmed.     

Vocal convergence in a multi-level primate society: insights into the evolution of vocal learning

The extent to which nonhuman primate vocalizations are amenable to modification through experience is relevant for understanding the substrate from which human speech evolved. We examined the vocal behaviour of Guinea baboons, Papio papio, ranging in the Niokolo Koba National Park in Senegal. Guinea baboons live in a multi-level society, with units nested within parties nested within gangs. We investigated whether the acoustic structure of grunts of 27 male baboons of two gangs varied with party/gang membership and genetic relatedness. Males in this species are philopatric, resulting in increased male relatedness within gangs and parties. Grunts of males that were members of the same social levels were more similar than those of males in different social levels (N = 351 dyads for comparison within and between gangs, and N = 169 dyads within and between parties), but the effect sizes were small. Yet, acoustic similarity did not correlate with genetic relatedness, suggesting that higher amounts of social interactions rather than genetic relatedness promote the observed vocal convergence. We consider this convergence a result of sensory–motor integration and suggest this to be an implicit form of vocal learning shared with humans, in contrast to the goal-directed and intentional explicit form of vocal learning unique to human speech acquisition.     

Early sexual maturity in male hamadryas baboons (Papio hamadryas hamadryas) and its reproductive implications

We present data on sexual maturity in young hamadryas baboon males (Papio hamadryas hamadryas) and its reproductive consequences in a large captive baboon colony. Hamadryas baboons live in a multilevel social system, with one-male units (OMUs) as the smallest social entity. Male leaders of OMUs are believed to monopolize matings within their OMUs; hence mating is believed to be polygynous and monandrous. In a captive colony of hamadryas baboons, we found evidence that young males less than 4 years old fathered at least 2.5% of 121 offspring born subsequent to vasectomy of all adult males, and males aged 4-5 years fathered at least 16.5% of the offspring. Additional evidence that these young males are able to sire offspring came from a morphological comparison of sperm from hamadryas males of different ages. The sperm of a 48-month-old hamadryas baboon were morphologically indistinguishable from viable sperm from adult males, whereas sperm from a 45-month-old male showed some aberrations. If successful copulations by adolescent males constitute a regular pattern even in free-ranging hamadryas baboons, a hamadryas male's chances to reproduce would not be limited to his role as an OMU leader as previously assumed, and a male's reproductive career would consist of two phases: the adolescent phase, and the OMU leader male phase.     

Greeting movements among adult males in a colony of baboons:Papio hamadryas,P. cynocephalus and their hybrids

Seven greeting movements performed by four adult males belonging to a colony of baboons (Papio hamadryas, P. cynocephalus and their hybrids) were described. The hamadryas male has more number and more refined repertoire of movements than the yellow baboons, what would mean that the greeting movements possess a species-specific nature. This characteristic is expressed also by the existence of some inappropriate responses of the yellow baboons to the greeting of the hamadryas male. The differences in the greeting movements between both species would be explained as characteristic consequences of their social system organization. The hybrid male, having acquired a system organization similar to that of the hamadryas male, has acquired the same signal code, too, according to this system. The hybridization tendency would be adaptive in those colonies or troops with mixed species.     

Human–hamadryas baboon (Papio hamadryas) conflict in the Wonchit Valley,South Wollo,Ethiopia

Understanding the extent of human–primate conflict is crucial to the development of conservation and management strategies. We carried out this study in an unprotected area of central Ethiopia to examine the magnitude of human–hamadryas baboon (Papio hamadryas) conflict and to assess the attitude of local farmers towards baboons in Wonchit Valley. In 2014, we interviewed 119 adult respondents using a structured questionnaire. Local farmers considered hamadryas baboons to be the major pest in the area. All respondents reported that hamadryas baboons caused crop raiding and small livestock predation in the region. Respondents reported that a shortage of fruit producing wild trees and ready availability of crops were the main causes of conflict between farmers and hamadryas baboons. We found that hamadryas baboons damaged cereal crops at dusk and dawn during full moonlight, and most (89.9%) respondents claimed that they were not interested in hamadryas baboon conservation. Our results indicate that human–hamadryas baboon conflict has a strongly negative impact on both baboon conservation and local farmers. We suggest that to mitigate the human–hamadryas baboon conflict, job opportunities such as beekeeping should be introduced in the region.     

Crossing the Red Sea: phylogeography of the hamadryas baboon, Papio hamadryas hamadryas

The hamadryas baboon (Papio hamadryas hamadryas) is found both in East Africa and western Arabia and is the only free-ranging nonhuman primate in Arabia. It has been hypothesized that hamadryas baboons colonized Arabia in the recent past and were possibly even transported there by humans. We investigated the phylogeography of hamadryas baboons by sequencing a portion of the control region of mtDNA in 107 baboons from four Saudi Arabian populations and combing these data with published data from Eritrean (African) P. h. hamadryas. Analysis grouped sequences into three distinct clades, with clade 1 found only in Arabia, clade 3 found only in Africa, but clade 2 found in both Arabian and African P. h. hamadryas and also in the olive baboon, P. h. anubis. Patterns of variation within Arabia are neither compatible with the recent colonization of Arabia, implying that baboons were not transported there by humans, nor with a northerly route of colonization of Arabia. We propose that hamadryas baboons reached Arabia via land bridges that have formed periodically during glacial maxima at the straits of Bab el Mandab in the southern Red Sea. We suggest that the genetic differentiation of Arabian from African populations suggests that Arabian populations have a higher conservation status than recognized previously.     

Reconciliation in hamadryas baboons, Papio hamadryas: testing the relationships quality hypothesis

Post-conflict interactions between former opponents were investigated in a troop of hamadryas baboons, Papio hamadryas. This species is known for it's multilevel structure with evidently expressed hierarchy between males and females. Due to this fact hamadryas baboons represent an ideal object for testing the "relationship quality" hypothesis. The analyses were done on 436 PC-MC pairs of animals, which represented different social classes (harem male-female pairs, harem females, relatives, females from different harems. Male-male pairs, and female-subadult pairs). Reconciliation was practiced in different social classes of individuals: harem male-female pairs, harem female-female pairs, kin-kin pairs, male-male pairs, female-subadult pairs. Significant differences in the rate of reconciliatory tendency for different categories of interacting animals were found. Interactions between former opponents were highly selective. These may be interpreted as an indicator of the influence of the relation quality on the probability of reconciliation in hamadryas baboons.     

Mitochondrial phylogeny and systematics of baboons (Papio)

Baboons (Papio, s.s.) comprise a series of parapatric allotaxa (subspecies or closely related species) widely distributed in sub-Saharan Africa. Despite extensive studies of their ecology, morphology, and behavior, disagreement about their phylogenetic relationships continues, as expressed in the current coexistence of at least three major, competing taxonomic treatments. To help resolve this situation, we sequenced approximately 900 bases of mitochondrial DNA of 40 individuals from five of the widely recognized "major" allotaxa. Total sequence diversity (>5%) is high compared to most primate species. Major mitochondrial clades correspond to recognized allotaxa, with the important exception that haplotypes from yellow and olive baboons form a single, monophyletic clade within which the two allotaxa do not comprise mutually exclusive clusters. The major clades fall unambiguously into the pattern: (chacma (Guinea (hamadryas (yellow + olive)))). This phylogeny does not support taxonomies that oppose hamadryas to all other baboons ("desert" vs. "savanna"), but is compatible with the view that all definable allotaxa should be recognized as coordinates, either as "phylogenetic" species or "biological" subspecies. The close relationship and unsegregated distribution of haplotypes from Kenyan and Tanzanian yellow and olive baboons are unexplained, but may reflect introgression across the documented hybrid zone. The overall phylogeny, when combined with paleontological data, suggests a southern African origin for extant Papio baboons, with all extant lineages sharing a common mitochondrial ancestor at approximately 1.8 Ma.     

Testicular Size,Mating System,and Maturation Schedules in Wild Anubis and Hamadryas Baboons

We report body mass and testicular size in 258 anubis (Papio anubis or P. hamadryas anubis) and 59 hamadryas (P. hamadryas or P. h. hamadryas) baboons, live-trapped in Ethiopia. As predicted by theories of sexual selection by sperm competition, among hamadryas baboons, which are monandrous, fully adult males have absolutely and relatively smaller testes than those of comparable males among anubis baboons, which are polyandrous. Male hamadryas are also ca. 10% smaller in bodily mass as adults. The intertaxonal difference in adults is due entirely to the fact that in male anubis baboons, testicular and bodily mass continue to grow up to full adulthood–the age at which most males emigrate from their natal troop and initiate a confrontational breeding strategy among unrelated animals. By contrast, male hamadryas baboons, which are usually philopatric, attain adult body mass and testicular size as subadults. In both species, juveniles experience rapid testicular growth peaking in rate at ca. 12kg body mass, but testicular descent and growth starts earlier in hamadryas than in anubis baboons. Juvenile hamadryas baboons have relatively larger testes than their anubis equivalents, perhaps because male philopatry allows the mating strategy of male hamadryas baboons to be initiated during juvenile life and therefore permits some sperm competition between juveniles and adults.     

One-male harems and female social dynamics in Guinea baboons

Little is known about the mating system and social organization of Guinea baboons. This study investigated whether Guinea baboons have a harem-based mating system similar to that of hamadryas and gelada baboons and whether one-male mating units also correspond to social units. Ten adult females in a captive multi-male multi-female group of Guinea baboons were focally observed 2 h per week for 12 weeks, and all observed copulations within the group were recorded. Some males copulated with a single female while others had harems of 2-4 females. All females copulated with a single male except 1 female that switched harems early in the study. The focal females had higher rates of social interaction with their harem members, especially their harem male, than with individuals outside the harem. Females appeared to be subordinate to the harem male but little or no physical aggression or herding behavior from the male was observed. Variation in female social interactions within the harem was not accounted for by their sexual interactions with the male or their genetic relatedness with the females. Females, however, appeared to maintain social relationships with their female relatives in other harems. Taken together, the results of this study show that both mating and affiliative interactions in Guinea baboons are concentrated within one-male units and that the social dynamics within and between these units share some similarities as well as differences with those of hamadryas and gelada baboons.     

Behavioral variation and reproductive success of male baboons (Papio anubis x Papio hamadryas) in a hybrid social group

We take advantage of an array of hybrid baboons (Papio anubis x Papio hamadryas) living in the same social group to explore the causes and consequences of different male mating strategies. Male hamadryas hold one-male units and exhibit a sustained, intense interest in adult females, regardless of the latter's reproductive state. Anubis baboons, by contrast, live in multi-male, multi-female groups where males compete for females only when the latter are estrous. These two taxa interbreed to form a hybrid zone in the Awash National Park, Ethiopia, where previous work has suggested that hybrid males have intermediate and ineffective behavior. Here, we first examine male mating strategies with respect to morphological and genetic measures of ancestry. We found significant relationships between behavioral measures and morphology; males with more hamadryas-like morphology had more hamadryas-like behavior. However, genetic ancestry was not related to behavior, and in both cases intermediates displayed a previously unreported level of behavioral variation. Furthermore, male behavior was unrelated to natal group. Second, we evaluated reproductive success by microsatellite-based paternity testing. The highest reproductive success was found for individuals exhibiting intermediate behaviors. Moreover, over nine years, some genetically and morphologically intermediate males had high reproductive success. We conclude that the behavior of hybrid males is therefore unlikely to be an absolute barrier to admixture in the region.