A missing piece of the Papio puzzle: Gorongosa baboon phenostructure and intrageneric relationships.

Most authors recognize six baboon species: hamadryas (Papio hamadryas), Guinea (Papio papio), olive (Papio anubis), yellow (Papio cynocephalus), chacma (Papio ursinus), and Kinda (Papio kindae). However, there is still debate regarding the taxonomic status, phylogenetic relationships, and the amount of gene flow occurring between species. Here, we present ongoing research on baboon morphological diversity in Gorongosa National Park (GNP), located in central Mozambique, south of the Zambezi River, at the southern end of the East African Rift System. The park exhibits outstanding ecological diversity and hosts more than 200 baboon troops. Gorongosa National Park baboons have previously been classified as chacma baboons (P. ursinus). In accordance with this, two mtDNA samples from the park have been placed in the same mtDNA clade as the northern chacma baboons. However, GNP baboons exhibit morphological features common in yellow baboons (e.g., yellow fur color), suggesting that parapatric gene flow between chacma and yellow baboons might have occurred in the past or could be ongoing. We investigated the phenostructure of the Gorongosa baboons using two approaches: 1) description of external phenotypic features, such as coloration and body size, and 2) 3D geometric morphometric analysis of 43 craniofacial landmarks on 11 specimens from Gorongosa compared to a pan-African sample of 352 baboons. The results show that Gorongosa baboons exhibit a mosaic of features shared with southern P. cynocephalus and P. ursinus griseipes. The GNP baboon phenotype fits within a geographic clinal pattern of replacing allotaxa. We put forward the hypothesis of either past and/or ongoing hybridization between the gray-footed chacma and southern yellow baboons in Gorongosa or an isolation-by-distance scenario in which the GNP baboons are geographically and morphologically intermediate. These two scenarios are not mutually exclusive. We highlight the potential of baboons as a useful model to understand speciation and hybridization in early human evolution.

Optimal group size in a highly social mammal.

Group size is an important trait of social animals, affecting how individuals allocate time and use space, and influencing both an individual's fitness and the collective, cooperative behaviors of the group as a whole. Here we tested predictions motivated by the ecological constraints model of group size, examining the effects of group size on ranging patterns and adult female glucocorticoid (stress hormone) concentrations in five social groups of wild baboons (Papio cynocephalus) over an 11-y period. Strikingly, we found evidence that intermediate-sized groups have energetically optimal space-use strategies; both large and small groups experience ranging disadvantages, in contrast to the commonly reported positive linear relationship between group size and home range area and daily travel distance, which depict a disadvantage only in large groups. Specifically, we observed a U-shaped relationship between group size and home range area, average daily distance traveled, evenness of space use within the home range, and glucocorticoid concentrations. We propose that a likely explanation for these U-shaped patterns is that large, socially dominant groups are constrained by within-group competition, whereas small, socially subordinate groups are constrained by between-group competition and predation pressures. Overall, our results provide testable hypotheses for evaluating group-size constraints in other group-living species, in which the costs of intra- and intergroup competition vary as a function of group size.

Variation in the nasal cavity of baboon hybrids with implications for late Pleistocene hominins.

Hybridization is increasingly proving to be an important force shaping human evolution. Comparisons of both ancient and modern genomes have provided support for a complex evolutionary scenario over the past million years, with evidence for multiple incidents of gene exchange. However, to date, genetic evidence is still limited in its ability to pinpoint the precise time and place of ancient admixture. For that we must rely on evidence of admixture from the skeleton. The research presented here builds on previous work on the crania of baboon hybrids, focusing on the nasal cavity of olive baboons, yellow baboons, and first generation (F1) hybrids. The nasal cavity is a particularly important anatomical region for study, given the clear differentiation of this feature in Neanderthals relative to their contemporaries, and therefore it is a feature that will likely differ in a distinctive manner in hybrids of these taxa. Metric data consist of 45 linear, area, and volume measurements taken from CT scans of known-pedigree baboon crania. Results indicate that there is clear evidence for differences among the nasal cavities of the parental taxa and their F1 hybrids, including a greater degree of sexual dimorphism in the hybrids. There is also some evidence for transgressive phenotypes in individual F1 animals. The greatest amount of shape variation occurs in the anterior bony cavity, the choana, and the mid-nasopharynx. Extrapolating our results to the fossil record, we would expect F1 hybrid fossils to have larger nasal cavities, on average, than either parental taxon, with overall nasal cavity shape showing the most profound changes in regions that are distinct between the parental taxa (e.g., anterior nasal cavity). We also expect size and shape differences to be more pronounced in male F1 hybrids than in females. Because of pronounced anterior nasal cavity differences between Neanderthals and their contemporaries, we suggest that this model might be effective for examining the fossil record of late Pleistocene contact.

Further evidence for phenotypic signatures of hybridization in descendant baboon populations.

Hybridization may have played a substantial role in shaping the diversity of our evolving lineage. Although recent genomic evidence has shown that hybridization occurred between anatomically modern humans (AMHS) and Neanderthals, it remains difficult to pin down precisely where and when this gene flow took place. Investigations of the hybrid phenotype in primates and other mammals are providing models for identifying signatures of hybridization in the fossil record. However, our understanding of intra- and inter-taxon variation in hybrids is still limited. Moreover, there is little evidence from these studies that is pertinent to the question of how long hybrid skeletal traits persist in descendants, and therefore it is not clear whether observed hybrid phenotypes are evidence of recent (e.g., F1) or much earlier hybridization events. Here, we present an analysis updating a previous study of cranial variation in pedigreed olive and yellow baboons and their hybrids. Results suggest that traits previously associated with hybrids in baboons and other mammalian species are also present in this expanded data set; many of these traits are highly heritable, confirming a genetic basis for their variation in this mixed population. While F1 animals - and especially F1 males - still have the highest number of dental anomalies, these and other atypical traits persist into later hybrid generations (such as F2 and B1). Moreover, non-F1 recombinants also show extremely rare trait variations, including reduced canines and rotated teeth. However, these results must be considered in light of the possibility that some founding individuals may have themselves been unrecognized hybrids. Despite this, the data are compelling, and indicate once again that further controlled research remains to be done on primates and other mammals in order to better understand variation in the hybrid phenotype.

Distinct gene regulatory signatures of dominance rank and social bond strength in wild baboons.

The social environment is a major determinant of morbidity, mortality and Darwinian fitness in social animals. Recent studies have begun to uncover the molecular processes associated with these relationships, but the degree to which they vary across different dimensions of the social environment remains unclear. Here, we draw on a long-term field study of wild baboons to compare the signatures of affiliative and competitive aspects of the social environment in white blood cell gene regulation, under both immune-stimulated and non-stimulated conditions. We find that the effects of dominance rank on gene expression are directionally opposite in males versus females, such that high-ranking males resemble low-ranking females, and vice versa. Among females, rank and social bond strength are both reflected in the activity of cellular metabolism and proliferation genes. However, while we observe pronounced rank-related differences in baseline immune gene activity, only bond strength predicts the fold-change response to immune (lipopolysaccharide) stimulation. Together, our results indicate that the directionality and magnitude of social effects on gene regulation depend on the aspect of the social environment under study. This heterogeneity may help explain why social environmental effects on health and longevity can also vary between measures. This article is part of the theme issue 'The centennial of the pecking order: current state and future prospects for the study of dominance hierarchies'.

Genetic ancestry predicts male-female affiliation in a natural baboon hybrid zone.

Opposite-sex social relationships are important predictors of fitness in many animals, including several group-living mammals. Consequently, understanding sources of variance in the tendency to form opposite-sex relationships is important for understanding social evolution. Genetic contributions are of particular interest due to their importance in long-term evolutionary change, but little is known about genetic effects on male-female relationships in social mammals, especially outside of the mating context. Here, we investigate the effects of genetic ancestry on male-female affiliative behaviour in a hybrid zone between the yellow baboon, Papio cynocephalus, and the anubis baboon, Papio anubis, in a population in which male-female social bonds are known predictors of life span. We place our analysis within the context of other social and demographic predictors of affiliative behaviour in baboons. Genetic ancestry was the most consistent predictor of opposite-sex affiliative behaviour we observed, with the exception of strong effects of dominance rank. Our results show that increased anubis genetic ancestry is associated with a subtle, but significantly higher, probability of opposite-sex affiliative behaviour, in both males and females. Additionally, pairs of anubis-like males and anubis-like females were the most likely to socially affiliate, resulting in moderate assortativity in grooming and proximity behaviour as a function of genetic ancestry. Our findings indicate that opposite-sex affiliative behaviour partially diverged during baboon evolution to differentiate yellow and anubis baboons, despite overall similarities in their social structures and mating systems. Furthermore, they suggest that affiliative behaviour may simultaneously promote and constrain baboon admixture, through additive and assortative effects of ancestry, respectively.

Exaggerated sexual swellings and male mate choice in primates: testing the reliable indicator hypothesis in the Amboseli baboons.

The paradigm of competitive males vying to influence female mate choice has been repeatedly upheld, but, increasingly, studies also report competitive females and choosy males. One female trait that is commonly proposed to influence male mate choice is the exaggerated sexual swelling displayed by females of many Old World primate species. The reliable indicator hypothesis posits that females use the exaggerated swellings to compete for access to mates, and that the swellings advertise variation in female fitness. We tested the two main predictions of this hypothesis in a wild population of baboons (Papio cynocephalus). First, we examined the effect of swelling size on the probability of mate-guarding ('consortship') by the highest-ranking male and the behavior of those males that trailed consorshipts ('follower males'). Second, we asked whether a female's swelling size predicted several fitness measures. We found that high-ranking males do not prefer females with larger swellings (when controlling for cycle number and conception) and that females with larger swellings did not have higher reproductive success. Our study-the only complete test of the reliable indicator hypothesis in a primate population-rejects the idea that female baboons compete for mates by advertising heritable fitness differences. Furthermore, we found unambiguous evidence that males biased their mating decisions in favor of females who had experienced more sexual cycles since their most recent pregnancy. Thus, rather than tracking the potential differences in fitness between females, male baboons appear to track and target the potential for a given reproductive opportunity to result in fertilization.

Social networks predict gut microbiome composition in wild baboons.

Social relationships have profound effects on health in humans and other primates, but the mechanisms that explain this relationship are not well understood. Using shotgun metagenomic data from wild baboons, we found that social group membership and social network relationships predicted both the taxonomic structure of the gut microbiome and the structure of genes encoded by gut microbial species. Rates of interaction directly explained variation in the gut microbiome, even after controlling for diet, kinship, and shared environments. They therefore strongly implicate direct physical contact among social partners in the transmission of gut microbial species. We identified 51 socially structured taxa, which were significantly enriched for anaerobic and non-spore-forming lifestyles. Our results argue that social interactions are an important determinant of gut microbiome composition in natural animal populations-a relationship with important ramifications for understanding how social relationships influence health, as well as the evolution of group living.

The genetic architecture of gene expression levels in wild baboons.

Primate evolution has been argued to result, in part, from changes in how genes are regulated. However, we still know little about gene regulation in natural primate populations. We conducted an RNA sequencing (RNA-seq)-based study of baboons from an intensively studied wild population. We performed complementary expression quantitative trait locus (eQTL) mapping and allele-specific expression analyses, discovering substantial evidence for, and surprising power to detect, genetic effects on gene expression levels in the baboons. eQTL were most likely to be identified for lineage-specific, rapidly evolving genes; interestingly, genes with eQTL significantly overlapped between baboons and a comparable human eQTL data set. Our results suggest that genes vary in their tolerance of genetic perturbation, and that this property may be conserved across species. Further, they establish the feasibility of eQTL mapping using RNA-seq data alone, and represent an important step towards understanding the genetic architecture of gene expression in primates.

The ecological determinants of baboon troop movements at local and continental scales.

BACKGROUND: How an animal moves through its environment directly impacts its survival, reproduction, and thus biological fitness. A basic measure describing how an individual (or group) travels through its environment is Day Path Length (DPL), i.e., the distance travelled in a 24-hour period. Here, we investigate the ecological determinants of baboon (Papio spp.) troop DPL and movements at local and continental scales. RESULTS: At the continental scale we explore the ecological determinants of annual mean DPL for 47 baboon troops across 23 different populations, updating a classic study by Dunbar (Behav Ecol Sociobiol 31: 35-49, 1992). We find that variation in baboon DPLs is predicted by ecological dissimilarity across the genus range. Troops that experience higher average monthly rainfall and anthropogenic influences have significantly shorter DPL, whilst troops that live in areas with higher average annual temperatures have significantly longer DPL. We then explore DPLs and movement characteristics (the speed and distribution of turning angles) for yellow baboons (Papio cynocephalus) at a local scale, in the Issa Valley of western Tanzania. We show that our continental-scale model is a good predictor of DPL in Issa baboons, and that troops move significantly slower, and over shorter distances, on warmer days. We do not find any effect of season or the abundance of fruit resources on the movement characteristics or DPL of Issa baboons, but find that baboons moved less during periods of high fruit availability. CONCLUSION: Overall, this study emphasises the ability of baboons to adapt their ranging behaviour to a range of ecological conditions and highlights how investigations of movement patterns at different spatial scales can provide a more thorough understanding of the ecological determinants of movement.

Body mass and growth rates in a wild primate population.

We obtined data on body mass and growth rates for the immature members of two groups of wild baboons in Amboseli National Park, Kenya. Data were collected without feeding, trapping, or handling. The data were separated into cross-sectional and longitudinal components, allowing both the examination of body mass-age relationships and the calculation of growth rates for individuals. For animals less than three years old, body mass was wellperedicted from age by a linear model. Differences based on social group membership were small but consistent, and their origins are discussed. We detected no differences in body mass based on sex or on maternal dominance rank. For older juveniles, those three to seven years of age, a better fit was obtained from log of mass than by mass in a linear model. This was also true for the cross-sectional data set over the whole age range (zero to seven years). For older juveniles, samples were too small for quantitative analysis of differences based on sex, rank, or group membership, but trends in the data are indicated. Growth rates derived from repeat measures of body mass for 38 animals are presented and discussed.The growth rate values obtained in this study are consistent with data from cross-sectional studies of other wild baboon populations; these values for wild baboons are consistently one-half to one-third lower than growth rate values for well-provisioned captive baboons and equivalent to captive baboons fed a low-protein diet. Comparisons between primates and other mammals in the primate size range raise questions concerning ecological and behavioral constraints on primate growth rates; some possible mechanisms of constraint are suggested.

Fatal intragroup kidnapping in yellow baboons.

The fatal kidnapping of a 5-day-old baboon (Papio cynocephalus) in Amboseli National Park, Kenya, is described. Although pulling and rough handling of primate infants by nonmothers are frequently observed, records of fatal intragroup kidnappings are rare. In the instance described here, the mother, a healthy, primiparous female, did not retrieve the infant from the kidnapper, a higher-ranking juvenile female of the same group, until he died 3 days later, presumably from starvation or dehydration. This incident is compared with other fatal intragroup kidnappings in nonhuman primates and related to adaptive interpretations.

Yellow baboon labor and parturition at the Tana River National Primate Reserve, Kenya.

An observation of the birth of a feral yellow baboon (Papio cynocephalus cynocephalus) is reported. Over an approximate 45-min period, the late stages of labor, parturition, cleaning of the infant, and consumption of the placenta were observed. The labor and parturition occurred in the late afternoon/early evening hours, and within 5 m of the observer. A review of the literature on feral births suggests that selection may have favored both the timing and the location of births. © 1994 Wiley-Liss, Inc.

Correlates of agonistic and competitive interactions in pregnant baboons.

Maternal condition during pregnancy is known to influence fetal viability. Recently, primatologists have suggested that certain characteristics of the fetus may influence maternal condition as well. For example, among captive pigtailed macaques (Macaca nemestrina) mothers of female infants may be at greater risk of injury during their pregnancies than mothers of male infants. Analysis of the rates of aggression, submission, competition, and wounding among free-ranging pregnant baboons (Papio cynocephalus) in Amboseli National Park generally fail to support these findings, but several other factors such as maternal dominance rank, environmental conditions during pregnancy, maternal parity, and fetal age correlate with aggression, submission, competition, and injuries sustained by pregnant female baboons.

Predation on a yellow baboon (Papio cynocephalus cynocephalus) by a lioness in the Tana River National Primate Reserve, Kenya.

Predation on an adult female yellow baboon (Papio cynocephalus cynocephalus) by a lioness is reported. This predation occurred in full daylight within 10 m of the observer. The high incidence of disappearances of adult females from the study troop during a one-year period is reported and the potential long-term demographic effects upon the troop resulting from this one year's high number of disappearances discussed. These disappearances may be due to predation. We suggest that lion predation upon baboons, and baboon deaths and disappearances in general, in the Tana Reserve, may be inversely related to rainfall. We also report that there does not appear to be a long-term sex difference in vulnerability to death or disappearance. © 1994 Wiley-Liss, Inc.

Radioimmunoassay of somatomedin-C in the baboon (Papio cynocephalus): A comparison of multiple techniques of measurement.

This study was undertaken to assess the nature of somatomedin-C (SM-C) in baboon (Papio cynocephalus) blood and to compare various methods for estimating SM-C concentrations. Parallel dose-response curves were obtained with normal baboon serum, normal human serum, and purified SM-C. Recovery of purified SM-C added to baboon serum over a wide dosage range (n = 17) was 111 ± 12%, with slightly better recovery at higher potencies. Chromatography of normal baboon serum on Sephadex G-200 at neutral pH produced a profile similar to that observed in the human, as did samples chromatographed on Sephadex G-50 in acid. Although the SM-C content in acid chromatographed plasma was approximately 2.5 times higher than in native unprocessed plasma, there was excellent correlation between the values (r = 0.9143, p < 0.0001). The SM-C in baboon plasma which had been preincubated with glycine HCl was approximately twice that of unprocessed plasma, but the correlation between the two methods was excellent (r = 0.9593, p < 0.0001). The correlation between values obtained after simple acid-ethanol extraction and those observed in unextracted plasma were also significant (r = 0.7689, p < 0.0001). Following a series of four injections of human growth hormone (hGH) to a normal baboon, plasma SM-C rose approximately sevenfold above the initial concentration and returned to basal levels five days after the final injection. These studies show that although the radioimmunoassay (RIA) for SM-C in unprocessed baboon plasma does not measure all of the SM-C present, it provides a reliable index of the total SM-C concentration and reflects GH status in the baboon.

Scratching, dominance, tension, and displacement in male baboons.

This paper reports a study designed to test the hypothesis that a relationship exists among dominance rank, tension, and scratch behaviors in anubis baboons (Papio cynocephalus anubis). Our study was conducted on two groups of male baboons, each containing eight unrelated individuals who were approximately 6 years of age and who shared common rearing histories. Focal animal sampling was used to collect behavioral data. Hand scratching, foot scratching, avoid, tension, allogrooming, autogrooming, and manipulation were measured as acts performed per hour of sampling. Dominance matrices were constructed based on net difference of avoid behavior performed and received (adjusted for time sampled). Individual status ranks were grouped into two status classes, high and low. Analysis of variance models demonstrated significant differences in the performance rate of scratching behaviors by dominance rank class, as well as differences in scratching performance by tension class. Individuals in the high status class had significantly higher rates of total scratching, hand scratching, foot scratching, and tension behavior performance than their counterparts in the low status class. No significant difference was found between status classes or tension classes for performance rate of allogrooming, autogrooming, or manipulation behavior. The frequency of scratching and general level of activity were not significantly correlated. The results are interpreted to indicate the possibility that scratching may function as a displacement behavior, which subjectively appears to communicate heightened frustration, anxiety, or arousal.

Demography of Amboseli baboons, 1963-1983.

Repeated censuses of a population of yellow baboons (Papio cynocephalus) in Amboseli National Park, Kenya, revealed a decrease from over 2,500 animals in 1963-1964 to 123 individuals in 1979, or from a density of about 73 to 1.8 baboons per km2 over a 15-year period. Median group size decreased from 43 in 1964 to 27 in 1979. The largest and smallest groups declined the most; groups near the median have maintained fairly stable size and age distributions. The population seemed to have stabilized by 1983 at approximately 150 animals in six groups (median group size 28; density 2.2/km2). Although baboon population and group size appeared to be stable during 1963-1964, the age distribution and demographic parameters (age-specific mortality and natality for one social group) during that year indicate that the population decline had already started. The rate of population decline was greatest in the 1964-1969 period and remained appreciable during the next 5 years. The decline of the baboon population was paralleled by that of other Amboseli savannah woodland mammalian species and took place during a period of very high mortality of fever trees (Acacia xanthophloea) and extensive invasion of the area by halophytes, a transition brought on by rising ground water and consequent elevation of the soil salinity zone. In this and several other primate populations, mortality of infants and juveniles appears to be the demographic variable most sensitive to environmental change.

An intergroup encounter with fatal consequences in yellow baboons (Papio cynocephalus).

This paper describes the fatal wounding of an infant yellow baboon (Papio cynocephalus) and the severe injury of its mother during an encounter between two baboon groups with overlapping home ranges in Amboseli National Park, Kenya. Also, a description is given of the apparent use of the infant as an agonistic buffer by an adult male in fights with other males.

Fecal steroid analysis of ovarian cycles in free-ranging baboons.

This paper reports field and laboratory tests of serial sampling, solid phase extraction, and microradioimmunoassay methods for the collection, preservation, and analysis of fecal steroids. The field study was conducted in a troop of 87 yellow baboons (Papio cynocephalus) in the Tana River Primate Reserve, Kenya. Serial samples of four focal females and opportunistic sampling of 18 additional females over 22 days of sampling yielded a total of 62 samples, X = 3.1 ± 0.4/day, demonstrating the feasibility of regular field collection and extraction. Estradiol and progesterone concentrations in the field-extracted samples exhibited high recovery and statistically significant correlations (P < 0.05) with concentrations in the lab-extracted samples, suggesting that solid phase extraction could provide a useful alternative to freezing in sites where electricity or liquid nitrogen is not available. Tests of microradioimmunoassays demonstrated that these assays were sensitive, accurate, and precise when applied to the assay of fecal extracts, providing estimates of ovarian steroids that varied significantly with reproductive state. The demonstration that testosterone could be accurately and reliably assayed in fecal extracts suggests that these techniques also could be applied to the study of male reproductive function. Parallels between fecal profiles of cycling and pregnant baboons with patterns reported for serum steroids in baboons suggest that fecal steroids might be useful in distinguishing amenorrhea from early pregnancy in free-ranging baboons as well as in species lacking external indices of reproductive state. © 1995 Wiley-Liss, Inc.