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.     

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.     

Ecological determinism in the life histories of baboons

An evolutionary model is presented for the covariation of parameters in ecology, behavior, morphology and social organization observed in interpopulational comparisons of baboons. Ecological determinants, in particular rainfall, shape the optimal life history strategies of individuals within a local population, in terms of the distribution of time and energy for reproductive effort, growth and maintenance. The results are adaptations in body mass, sexual dimorphism and aggression among baboons that are significantly correlated with rainfall. The three common types of baboon social organization, one-male units, multi-male troops and age-graded groups, are discussed as the consequences of male and female life history strategies, and in turn as social environments generating their own selection pressures.     

Proboscis monkey (Nasalis larvatus) social organization: Intergroup patterns of association

Proboscis monkey (Nasalis larvatus) social organization was studied at the Natai Lengkuas station, Tanjung Puting National Park in Kalimantan Tengah, Indonesia. Data were collected on ten one-male groups and two all-male groups using scan sampling and event sampling during follows, and through evening census surveys. Proboscis monkeys were found to form stable one-male groups. Specific groups associated at their sleeping sites, in a manner similar to the fission-fusion pattern described for hamadryas and gelada baboons. Analyses performed on these associations indicated that the groups formed two separate bands. These separate bands appear to be a secondary level of organization, distinct from the primary level of organization, the one-male and all-male groups. This is the first evidence for such a two-tiered system of organization in an arboreal colobine species. Proboscis monkeys closely resemble gelada baboons in their organizational pattern. In both species, adult females direct the majority of their affiliative behavior towards their offspring and other adult females, males do not engage in active herding, all-male groups are present, and one-male groups do spend time apart from other groups. Home ranges of both groups and of bands of proboscis monkeys overlapped extensively; temporal avoidance between bands may have been mediated by early morning vocalizations and branch shaking displays.     

Group housing of hamadryas baboons: a new cage design based upon field studies of social organization

The hamadryas subspecies, which is utilized extensively for laboratory research, has a social structure unique among baboons. Field studies have shown that small one male units are the basic grouping in a complex multi-level social system. A housing design for a research colony of hamadryas baboons was conceived to reflect this unique social organization and related behavioral patterns. The outcome of combining such ethological considerations with practical dictates for housing large laboratory primates has been assessed in terms of reproductive performance, animal health and utilization for research. Various benefits of this approach to cage design for hamadryas baboons are identified in this report.     

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.     

The Influence of Social Systems on Patterns of Mitochondrial DNA Variation in Baboons

Behavior is influenced by genes but can also shape the genetic structure of natural populations. Investigating this link is of great importance because behavioral processes can alter the genetic diversity on which selection acts. Gene flow is one of the main determinants of the genetic structure of a population and dispersal is the behavior that mediates gene flow. Baboons (genus Papio) are among the most intensely studied primate species and serve as a model system to investigate the evolution of social systems using a comparative approach. The general mammalian pattern of male dispersal and female philopatry has thus far been found in baboons, with the exception of hamadryas baboons (Papio hamadryas). As yet, the lack of data on Guinea baboons (Papio papio) creates a taxonomic gap in genus-wide comparative analyses. In our study we investigated the sex-biased dispersal pattern of Guinea baboons in comparison to hamadryas, olive, yellow, and chacma baboons using sequences of the maternally transmitted mitochondrial hypervariable region I. Analyzing whole-range georeferenced samples (N = 777), we found strong evidence for female-biased gene flow in Guinea baboons and confirmed this pattern for hamadryas baboons, as shown by a lack of genetic-geographic structuring. In addition, most genetic variation was found within and not among demes, in sharp contrast to the pattern observed in matrilocal primates including the other baboon taxa. Our results corroborate the notion that the Guinea baboons’ social system shares some important features with that of hamadryas baboons, suggesting similar evolutionary forces have acted to distinguish them from all other baboons.     

The rehabilitation of captive baboons

Eleven baboons who had been singly housed indoors for an average of 5 years were moved to outdoor social groups in an attempt to provide a more species-typical environment and reduce high levels of abnormal behavior. Nine of the baboons were observed while in single housing and, over a 6-month period, while housed outdoors socially to document long-term changes in behavior. Abnormal behavior decreased significantly from an average of 14% of the observation time in the single cages to 3% in the sixth month of social housing. Cage manipulation and self-directed behaviors also significantly decreased, while social behavior, enrichment-directed behavior, and locomotion increased in social housing. Baboons that had been in long-term indoor single housing were able to reproduce and form stable social groups without injury. This study provides evidence that even behaviorally disturbed nonhuman primates can be successfully rehabilitated to live in social groups.     

Affiliation Among Females in Wild Hamadryas Baboons (Papio hamadryas hamadryas)

Previous researchers of hamadryas baboons have described a star-shaped sociogram, whereby the strongest social bonds within hamadryas one-male units are between a leader male and his females and bonds among females are weak by comparison. This type of social organization is also known as cross-bonding to distinguish it from the female-bonding found in most papionin monkeys. Models of female primate socioecology suggest that hamadryas baboons lack female bonding due to their reliance on scarce, widely-dispersed food resources. Here, I report observational data from a wild population of hamadryas baboons in Ethiopia indicating that, while females varied widely in their frequency of social interaction with other females, most females spent about as much social time with other females as they did with the leader male and some females even crossed unit boundaries to interact with one another. The size of a unit was positively correlated with the tendency of its females to interact with other females and was negatively correlated with the tendency of its females to interact with the leader male. Females were equally likely to spend social time with other females whether or not the leader male was available for social interaction at the time. Overall, this study suggests that a star-shaped sociogram does not characterize all hamadryas baboons and that female hamadryas may be, to some extent, female-bonded as well as cross-bonded. The lack of more pronounced female bonding in hamadryas is probably due to the behavior of males rather than to ecological factors.     

Kin Selection in Primate Groups

Altruism poses a problem for evolutionary biologists because natural selection is not expected to favor behaviors that are beneficial to recipients, but costly to actors. The theory of kin selection, first articulated by Hamilton (1964), provides a solution to the problem. Hamilton's well-known rule (br > c) provides a simple algorithm for the evolution of altruism via kin selection. Because kin recognition is a crucial requirement of kin selection, it is important to know whether and how primates can recognize their relatives. While conventional wisdom has been that primates can recognize maternal kin, but not paternal kin, this view is being challenged by new findings. The ability to recognize kin implies that kin selection may shape altruistic behavior in primate groups. I focus on two cases in which kin selection is tightly woven into the fabric of social life. For female baboons, macaques, and vervets maternal kinship is an important axis of social networks, coalitionary activity, and dominance relationships. Detailed studies of the patterning of altruistic interactions within these species illustrate the extent and limits of nepotism in their social lives. Carefully integrated analyses of behavior, demography, and genetics among red howlers provide an independent example of how kin selection shapes social organization and behavior. In red howlers, kin bonds shape the life histories and reproductive performance of both males and female. The two cases demonstrate that kin selection can be a powerful source of altruistic activity within primate groups. However, to fully assess the role of kin selection in primate groups, we need more information about the effects of kinship on the patterning of behavior across the Primates and accurate information about paternal kin relationships.     

How should a clever baboon choose and move rocks?

Chacma baboons (Papio ursinus) intentionally overturn rocks to feed on the invertebrates beneath. However, baboons do not move all the rocks they encounter, with this presumably reflecting cost–benefit (or effort–reward) trade‐offs in their foraging behavior. We ask, how do “clever baboons” choose rock sizes and shapes and move these rocks? Using optimal foraging theory, we predicted that baboons would prefer to move medium‐sized rocks, a trade‐off between moving larger rocks that might require more effort to move, and smaller rocks that likely do not provide enough prey (the reward) to make the effort worthwhile. We also expected baboons to prefer rounded rocks as these will require less energy to move by rolling (rather than being flipped as for flat rocks) and that the effort of rock movement might be offset by moving rocks along the shortest axis. We show that baboons have clear preferences for specific rock sizes (medium‐sized) and shapes (angular and flat when these were medium‐sized), and the way in which rocks are moved (along the shortest axis). Prey occurred infrequently under rocks. The low predictability of prey beneath rocks suggests that such prey, when encountered, is of considerable value to baboons for them to expend the search effort, and also explains the extensive nature of rock movement by baboons in the landscape. Our study provides a novel application of the optimal foraging theory concept and has important implications for understanding and predicting how animals choose to move rocks.     

Progressions of adult male chacma baboons (Papio ursinus) in the moremi wildlife reserve

It has been suggested that the sociospatial organization of baboon progressions has a protective function in which the most physically powerful troop members, the adult males, play a key role. This theory implies regularities in adult male progression order for different species of savannah baboons with similar social systems. Quantitative progression data are available from two such similar baboon species, olive and yellow, but not from the third, chacma. The order of movement of 15 adult male chacma baboons was determined from 40 progressions observed at the Moremi Wildlife Reserve, Botswana. The chacma males were most often found in the front sixth of progressions, next most often in the second sixth, and about equally often from there to the rear. As expected from the protection theory, this frontal positioning is consistent with available quantitative data from other species of savannah baboons.     

Effect of stressor factors on the behavior of monkeys. III. The behavior of rhesus macaques during immobilization stress

The three-hour immobilizational stress in two groups of males of rhesus monkeys at the age of 7-8 and 10-12 years has been investigated. The reaction on the stress has been established to depend on the age of animals. The young males bear the stress easier, their behaviour after it is practically normal. The normal behaviour of the elder animals restores during 24 hours after immobilization. A comparative analysis of hamadryas baboons and rhesus monkeys behaviour during this type of stress has been carried out. These species differ by their reaction on stress: Papio hamadryas serve as a model of hard depressive stress, the rhesus monkeys--a model of slight-stimulative stress. The peculiarities of stress bearing depend on the selected species, age of the animal, the type of social organization and individual features of behaviour.     

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.     

The social contingency model and olive baboons

A theoretical and illustrative analysis of sequences of actions between pairs of olive baboons (Papio cynocephals anubis) is carried out using the social contingency model originally suggested by Jones and Gerard (1967) in social psychology. The model provides the basis for a step-by-step analysis and a typology. Signals from body postures, facial expressions, and vocalizations are subject to close study by using the model, in a similar fashion to its use in social skills analysis (Argyle, 1988). Sequences are categorized according to individual and joint strategies. Examples are given of three categories of contingency, reactive, mutual, and asymmetrical, which are adapted from their social psychological usage. The model is extended by a new category for competitive relationships between baboons: a conflictive category. The contingencies, as they are shown graphically, have a superficial resemblance to Tinbergen's (1951) zigzag diagrams, but their purpose is distinct in focusing on the detail of both infrequent and repeated interactions. The overall aim of the contingencies is to improve the analysis of social behavior at the proximate level and the model is potentially applicable to observation records at a level of detail that is often not utilized in reporting field studies.     

The Socioecology of Network Scaling Ratios in the Multilevel Society of Hamadryas Baboons (Papio hamadryas hamadryas)

Multilevel or modular societies characterize a range of mammalian taxa, allowing social groups to fission and fuse in response to ecological factors. The modular society of hamadryas baboons has previously been shown to consist of 4 levels: troop, band, clan, and one-male unit (OMU). A recent study by Hill et al. (Biology Letters 4:748–751, 2008) revealed a mean scaling ratio across successive levels of multilevel societies of ca. 3; this was consistent across elephants, orca, geladas, and hamadryas baboons. Here we reanalyze the scaling ratio for hamadryas baboons with previously unavailable data from Filoha. Our analysis revealed a mean scaling ratio for hamadryas of 3.28 without data on the hamadryas clan layer of organization at Filoha, but a ratio of 6.17 with these data included. This discrepancy is due to the large clan and band sizes at Filoha yielding a larger than average gap between the OMU and the clan. Further analysis revealed subsets of OMUs within clans, suggesting a 5th level of society in this population. When this 5th layer of social structure is included in the analysis, the scaling ratio at Filoha is consistent with that of other hamadryas populations and other taxa. These results suggest that a consistent mammalian scaling ratio can be used to detect previously hidden levels of organization within societies and to predict their sizes in taxa for which detailed behavioral data are not available.     

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.     

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.     

Thermal effects on movement patterns of yellow baboons

This paper examines the effect of thermal environment on movement patterns of free-ranging yellow baboons (Papio cynocephalus). For Amboseli baboons, one source of potential thermal stress is intense midday heat, and a plausible thermoregulatory response is for animals to simply move into the shade. I therefore examined the hypothesis that baboons would choose quadrats with higher shade availability (as measured by vegetation cover) in response to increasing midday heat loads (as measured by air temperature and solar radiation). Surprisingly, this was not the case—neither ambient air temperature, ambient solar radiation, nor quadrat plant species composition had a significant effect on shade availability of quadrat selected. Instead, thermal conditions affected a different aspect of baboon movements; namely, spatial displacement rates. At high air temperatures, baboons as a group traversed woodland habitats more slowly, and bare pans more quickly, than at lower air temperatures. I surmised that this relationship might reflect thermal effects on movement patterns at a smaller scale: if individuals exposed to high heat loads spent more time resting in shade under clumps of vegetation, they would thereby traverse densely-vegetated (hence shaded) quadrats more slowly. To address this question directly, I obtained focal sample data on activity and microhabitat budgets of individual baboons in relation to environmental temperature. The frequency of most combinations of activity state (e.g., grooming, social behavior) and microenvironment state (e.g., elevation, proximity to vegetation) did not vary monotonically with air temperature. However, baboons in shaded locations (but not those in unshaded locations) spent more time resting and less time moving at high air temperatures than low. In other words, baboon activity budgets depended on both microclimate and microhabitat—animals reduced their activity, particularly movement, when they encountered shade under hot conditions. This pattern of microhabitat choice in turn led to temperature-dependent changes in travel rate at the habitat level. These observational studies of movement patterns suggest that Amboseli baboons employ opportunistic thermoregulation—they do not seek out densely-shaded habitats or individual patches of shade at high air temperatures. Instead, they respond to environmental heat loads by resting, and thereby slowing down, when they happen to encounter plant shade. Aspects of baboon ecology that favor such an opportunistic mode of thermoregulation include large body size and non-thermal constraints on movement patterns.