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.

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.

Insights into the genetic foundation of aggression in Papio and the evolution of two length-polymorphisms in the promoter regions of serotonin-related genes (5-HTTLPR and MAOALPR) in Papionini.

BACKGROUND: Aggressive behaviors are an integral part of competitive interactions. There is considerable variation in aggressiveness among individuals both within and among species. Aggressiveness is a quantitative trait that is highly heritable. In modern humans and macaques (Macaca spp.), variation in aggressiveness among individuals is associated with polymorphisms in the serotonergic (5-HT) neurotransmitter system. To further investigate the genetics underlying interspecific variation in aggressiveness, 123 wild individuals from five baboon species (Papio papio, P. hamadryas, P. anubis, P. cynocephalus, and P. ursinus) were screened for two polymorphisms in promoter regions of genes relevant for the 5-HT system (5-HTTLPR and MAOALPR). RESULTS: Surprisingly, despite considerable interspecific variation in aggressiveness, baboons are monomorphic in 5-HTTLPR, except for P. hamadryas, which carries one additional allele. Accordingly, this locus cannot be linked to behavioral variation among species. A comparison among 19 papionin species, including nine species of macaques, shows that the most common baboon allele is similar to the one described for Barbary macaques (Macaca sylvanus), probably representing the ancestral allele in this tribe. It should be noted that (almost) all baboons live in Africa, but within Macaca only M. sylvanus lives on this continent. Baboons are, however, highly polymorphic in the so-called 'warrior gene' MAOALPR, carrying three alleles. Due to considerable variation in allele frequencies among populations of the same species, this genotype cannot be invoked to explain variation in aggressiveness at the species level. CONCLUSIONS: This study provides another indication that 5-HTTLPR is not related to aggressiveness in primates per se, but may have been under differential selective pressures among taxa and potentially among populations in different geographic regions. The results on MAOALPR alleles in Papio indicate that variation in the metabolism of monoamine neurotransmitters and associated behaviors is more important among populations than among species. We, therefore, propose to compile behavioral data from additional populations of Papio to obtain further insight into the genetics underlying behavioral differences among primate species.

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.

Out of Africa, but how and when? The case of hamadryas baboons (Papio hamadryas).

Many species of Arabian mammals are considered to be of Afrotropical origin and for most of them the Red Sea has constituted an obstacle for dispersal since the Miocene-Pliocene transition. There are two possible routes, the 'northern' and the 'southern', for terrestrial mammals (including humans) to move between Africa and Arabia. The 'northern route', crossing the Sinai Peninsula, is confirmed for several taxa by an extensive fossil record, especially from northern Egypt and the Levant, whereas the 'southern route', across the Bab-el-Mandab Strait, which links the Red Sea with the Gulf of Aden, is more controversial, although post-Pliocene terrestrial crossings of the Red Sea might have been possible during glacial maxima when sea levels were low. Hamadryas baboons (Papio hamadryas) are the only baboon taxon to disperse out of Africa and still inhabit Arabia. In this study, we investigate the origin of Arabian hamadryas baboons using mitochondrial sequence data from 294 samples collected in Arabia and Northeast Africa. Through the analysis of the geographic distribution of genetic diversity, the timing of population expansions, and divergence time estimates combined with palaeoecological data, we test: (i) if Arabian and African hamadryas baboons are genetically distinct; (ii) if Arabian baboons exhibit population substructure; and (iii) when, and via which route, baboons colonized Arabia. Our results suggest that hamadryas baboons colonized Arabia during the Late Pleistocene (130-12 kya [thousands of years ago]) and also moved back to Africa. We reject the hypothesis that hamadryas baboons were introduced to Arabia by humans, because the initial colonization considerably predates the earliest records of human seafaring in this region. Our results strongly suggest that the 'southern route' from Africa to Arabia could have been used by hamadryas baboons during the same time period as proposed for modern humans.

A Comprehensive Overview of Baboon Phylogenetic History.

Baboons (genus Papio) are an intriguing study system to investigate complex evolutionary processes and the evolution of social systems. An increasing number of studies over the last 20 years has shown that considerable incongruences exist between phylogenies based on morphology, mitochondrial, and nuclear sequence data of modern baboons, and hybridization and introgression have been suggested as the main drivers of these patterns. Baboons, therefore, present an excellent opportunity to study these phenomena and their impact on speciation. Advances both in geographic and genomic coverage provide increasing details on the complexity of the phylogeography of baboons. Here, we compile the georeferenced genetic data of baboons and review the current knowledge on baboon phylogeny, discuss the evolutionary processes that may have shaped the patterns that we observe today, and propose future avenues for research.

Adulis and the transshipment of baboons during classical antiquity.

Adulis, located on the Red Sea coast in present-day Eritrea, was a bustling trading centre between the first and seventh centuries CE. Several classical geographers-Agatharchides of Cnidus, Pliny the Elder, Strabo-noted the value of Adulis to Greco-Roman Egypt, particularly as an emporium for living animals, including baboons (Papio spp.). Though fragmentary, these accounts predict the Adulite origins of mummified baboons in Ptolemaic catacombs, while inviting questions on the geoprovenance of older (Late Period) baboons recovered from Gabbanat el-Qurud ('Valley of the Monkeys'), Egypt. Dated to ca. 800-540 BCE, these animals could extend the antiquity of Egyptian-Adulite trade by as much as five centuries. Previously, Dominy et al. (2020) used stable isotope analysis to show that two New Kingdom specimens of Papio hamadryas originate from the Horn of Africa. Here, we report the complete mitochondrial genomes from a mummified baboon from Gabbanat el-Qurud and 14 museum specimens with known provenance together with published georeferenced mitochondrial sequence data. Phylogenetic assignment connects the mummified baboon to modern populations of P. hamadryas in Eritrea, Ethiopia, and eastern Sudan. This result, assuming geographical stability of phylogenetic clades, corroborates Greco-Roman historiographies by pointing toward present-day Eritrea, and by extension Adulis, as a source of baboons for Late Period Egyptians. It also establishes geographic continuity with baboons from the fabled Land of Punt (Dominy et al., 2020), giving weight to speculation that Punt and Adulis were essentially the same trading centres separated by a thousand years of history.

Insights into the evolution of social systems and species from baboon studies.

Baboons, members of the genus Papio, comprise six closely related species distributed throughout sub-Saharan Africa and southwest Arabia. The species exhibit more ecological flexibility and a wider range of social systems than many other primates. This article summarizes our current knowledge of the natural history of baboons and highlights directions for future research. We suggest that baboons can serve as a valuable model for complex evolutionary processes, such as speciation and hybridization. The evolution of baboons has been heavily shaped by climatic changes and population expansion and fragmentation in the African savanna environment, similar to the processes that acted during human evolution. With accumulating long-term data, and new data from previously understudied species, baboons are ideally suited for investigating the links between sociality, health, longevity and reproductive success. To achieve these aims, we propose a closer integration of studies at the proximate level, including functional genomics, with behavioral and ecological studies.

The comparative genomics and complex population history of Papio baboons.

Recent studies suggest that closely related species can accumulate substantial genetic and phenotypic differences despite ongoing gene flow, thus challenging traditional ideas regarding the genetics of speciation. Baboons (genus Papio) are Old World monkeys consisting of six readily distinguishable species. Baboon species hybridize in the wild, and prior data imply a complex history of differentiation and introgression. We produced a reference genome assembly for the olive baboon (Papio anubis) and whole-genome sequence data for all six extant species. We document multiple episodes of admixture and introgression during the radiation of Papio baboons, thus demonstrating their value as a model of complex evolutionary divergence, hybridization, and reticulation. These results help inform our understanding of similar cases, including modern humans, Neanderthals, Denisovans, and other ancient hominins.

Disrupted dispersal and its genetic consequences: Comparing protected and threatened baboon populations (Papio papio) in West Africa.

Dispersal is a demographic process that can potentially counterbalance the negative impacts of anthropogenic habitat fragmentation. However, mechanisms of dispersal may become modified in populations living in human-dominated habitats. Here, we investigated dispersal in Guinea baboons (Papio papio) in areas with contrasting levels of anthropogenic fragmentation, as a case study. Using molecular data, we compared the direction and extent of sex-biased gene flow in two baboon populations: from Guinea-Bissau (GB, fragmented distribution, human-dominated habitat) and Senegal (SEN, continuous distribution, protected area). Individual-based Bayesian clustering, spatial autocorrelation, assignment tests and migrant identification suggested female-mediated gene flow at a large spatial scale for GB with evidence of contact between genetically differentiated males at one locality, which could be interpreted as male-mediated gene flow in southern GB. Gene flow was also found to be female-biased in SEN for a smaller scale. However, in the southwest coastal part of GB, at the same geographic scale as SEN, no sex-biased dispersal was detected and a modest or recent restriction in GB female dispersal seems to have occurred. This population-specific variation in dispersal is attributed to behavioural responses to human activity in GB. Our study highlights the importance of considering the genetic consequences of disrupted dispersal patterns as an additional impact of anthropogenic habitat fragmentation and is potentially relevant to the conservation of many species inhabiting human-dominated environments.

Correction: Disrupted dispersal and its genetic consequences: Comparing protected and threatened baboon populations (Papio papio) in West Africa.

[This corrects the article DOI: 10.1371/journal.pone.0194189.].

Efficient Genome-Wide Sequencing and Low-Coverage Pedigree Analysis from Noninvasively Collected Samples.

Research on the genetics of natural populations was revolutionized in the 1990s by methods for genotyping noninvasively collected samples. However, these methods have remained largely unchanged for the past 20 years and lag far behind the genomics era. To close this gap, here we report an optimized laboratory protocol for genome-wide capture of endogenous DNA from noninvasively collected samples, coupled with a novel computational approach to reconstruct pedigree links from the resulting low-coverage data. We validated both methods using fecal samples from 62 wild baboons, including 48 from an independently constructed extended pedigree. We enriched fecal-derived DNA samples up to 40-fold for endogenous baboon DNA and reconstructed near-perfect pedigree relationships even with extremely low-coverage sequencing. We anticipate that these methods will be broadly applicable to the many research systems for which only noninvasive samples are available. The lab protocol and software ("WHODAD") are freely available at www.tung-lab.org/protocols-and-software.html and www.xzlab.org/software.html, respectively.