Charting the neglected West: The social system of Guinea baboons.

OBJECTIVES: Primate social systems are remarkably diverse, and thus play a central role in understanding social evolution, including the biological origin of human societies. Although baboons have been prominently featured in this context, historically little was known about the westernmost member of the genus, the Guinea baboon (Papio papio). MATERIAL AND METHODS: Here, we summarize the findings from the first years of observations at the field site CRP Simenti in the Niokolo Koba National Park in Senegal. RESULTS: Guinea baboons reveal a nested multi-level social organization, with reproductive units comprising one "primary" male, one to several females, young, and occasionally "secondary" males at the base of the society. Three to five units form "parties," which team up with other parties to form a "gang." Different gangs have largely overlapping home ranges and agonistic interactions between different parties or gangs are rare. Some but not all strongly socially bonded males are highly related, and population genetic and behavioral evidence indicate female-biased dispersal. Females play an important role in intersexual bond formation and maintenance, and female tenure length varies between a few weeks to several years. DISCUSSION: While the social organization resembles that of hamadryas baboons (P. hamadryas), the social structure differs considerably, specifically in terms of low male aggressiveness and female freedom. Despite substantial differences in social organization and social structure, the acoustic structure of Guinea baboon vocalizations does not differ substantially from that of other baboon taxa. With its multi-level organization, stable bonds between males and females, as well as a high-degree of male-male cooperation and tolerance, Guinea baboons constitute an intriguing model for reconstructing human social evolution.

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.

Male tolerance and male-male bonds in a multilevel primate society.

Male relationships in most species of mammals generally are characterized by intense intrasexual competition, with little bonding among unrelated individuals. In contrast, human societies are characterized by high levels of cooperation and strong bonds among both related and unrelated males. The emergence of cooperative male-male relationships has been linked to the multilevel structure of traditional human societies. Based on an analysis of the patterns of spatial and social interaction in combination with genetic relatedness data of wild Guinea baboons (Papio papio), we show that this species exhibits a multilevel social organization in which males maintain strong bonds and are highly tolerant of each other. Several "units" of males with their associated females form "parties," which team up as "gangs." Several gangs of the same "community" use the same home range. Males formed strong bonds predominantly within parties; however, these bonds were not correlated with genetic relatedness. Agonistic interactions were relatively rare and were restricted to a few dyads. Although the social organization of Guinea baboons resembles that of hamadryas baboons, we found stronger male-male affiliation and more elaborate greeting rituals among male Guinea baboons and less aggression toward females. Thus, the social relationships of male Guinea baboons differ markedly from those of other members of the genus, adding valuable comparative data to test hypotheses regarding social evolution. We suggest that this species constitutes an intriguing model to study the predictors and fitness benefits of male bonds, thus contributing to a better understanding of the evolution of this important facet of human social behavior.

Social monitoring in a multilevel society: a playback study with male Guinea baboons.

Keeping track of social interactions among conspecifics is a driving force for the evolution of social cognition. How social cognition, such as social knowledge, ties in with a species' social organization is, however, largely unexplored. We investigated the social knowledge of wild Guinea baboons (Papio papio) ranging in Senegal, a species that lives in a fluid multilevel society with overlapping habitat use. Using playback experiments, we tested how adult males differentiate between subjects from their own vs. a neighboring or a stranger social unit ("gang") and assessed ranging patterns with Global Positioning System (GPS) data. While territorial species usually differentiate between group and nongroup members and often respond more strongly to strangers than neighbors (the "dear enemy" effect), subjects in this highly tolerant species should largely ignore other unit members and mainly attend to subjects from their own unit. Males responded strongly after playback of calls recorded from members of their own gang, while they attended only briefly to neighbor or stranger calls. Apparently, males benefit from monitoring the social maneuvers in their own social unit, while it remains to be resolved whether they are unmotivated or unable to keep track of the identities and actions of individuals outside their own gang. The study highlights how the allocation of social attention is tuned to the specifics of a species' social organization, while a complex social organization does not necessarily translate into the need for more elaborate social knowledge.

Group Composition of Guinea Baboons (Papio papio) 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.

Orienting asymmetries and lateralized processing of sounds in humans.

BACKGROUND: Lateralized processing of speech is a well studied phenomenon in humans. Both anatomical and neurophysiological studies support the view that nonhuman primates and other animal species also reveal hemispheric differences in areas involved in sound processing. In recent years, an increasing number of studies on a range of taxa have employed an orienting paradigm to investigate lateralized acoustic processing. In this paradigm, sounds are played directly from behind and the direction of turn is recorded. This assay rests on the assumption that a hemispheric asymmetry in processing is coupled to an orienting bias towards the contralateral side. To examine this largely untested assumption, speech stimuli as well as artificial sounds were presented to 224 right-handed human subjects shopping in supermarkets in Germany and in the UK. To verify the lateralized processing of the speech stimuli, we additionally assessed the brain activation in response to presentation of the different stimuli using functional magnetic resonance imaging (fMRI). RESULTS: In the naturalistic behavioural experiments, there was no difference in orienting behaviour in relation to the stimulus material (speech, artificial sounds). Contrary to our predictions, subjects revealed a significant left bias, irrespective of the sound category. This left bias was slightly but not significantly stronger in German subjects. The fMRI experiments confirmed that the speech stimuli evoked a significant left lateralized activation in BA44 compared to the artificial sounds. CONCLUSION: These findings suggest that in adult humans, orienting biases are not necessarily coupled with lateralized processing of acoustic stimuli. Our results -- as well as the inconsistent orienting biases found in different animal species -- suggest that the orienting assay should be used with caution. Apparently, attention biases, experience, and experimental conditions may all affect head turning responses. Because of the complexity of the interaction of factors, the use of the orienting assay to determine lateralized processing of sound stimuli is discouraged.