Wild Baboons Research Articles

Baboons, bacteria, and biological clocks address an age-old question.

Studying the fecal microbiota of wild baboons helps provide new insight into the factors that influence biological aging.

Shared environments complicate the use of strain-resolved metagenomics to infer microbiome transmission.

In humans and other social animals, social partners have more similar microbiomes than expected by chance, suggesting that social contact transfers microorganisms. Yet, social microbiome transmission can be difficult to identify based on compositional data alone. To overcome this challenge, recent studies have used information about microbial strain sharing (i.e., the shared presence of highly similar microbial sequences) to infer transmission. However, the degree to which strain sharing is influenced by shared traits and environments among social partners, rather than transmission per se , is not well understood. Here, we first use a fecal microbiota transplant dataset to show that strain sharing can recapitulate true transmission networks under ideal settings when donor-recipient pairs are unambiguous and recipients are sampled shortly after transmission. In contrast, in gut metagenomes from a wild baboon population, we find that demographic and environmental factors can override signals of strain sharing among social partners. We conclude that strain-level analyses provide useful information about microbiome similarity, but other facets of study design, especially longitudinal sampling and careful consideration of host characteristics, are essential for inferring the underlying mechanisms.

Linking energy availability, movement and sociality in a wild primate (Papio ursinus).

Proximate mechanisms of 'social ageing', i.e. shifts in social activity and narrowing of social networks, are understudied. It is proposed that energetic deficiencies (which are often seen in older individuals) may restrict movement and, in turn, sociality, but empirical tests of these intermediary mechanisms are lacking. Here, we study wild chacma baboons (Papio ursinus), combining measures of faecal triiodothyronine (fT3), a non-invasive proxy for energy availability, high-resolution GPS data (movement and social proximity) and accelerometry (social grooming durations). Higher (individual mean-centred) fT3 was associated with increased residency time (i.e. remaining in the same area longer), which, in turn, was positively related to social opportunities (i.e. close physical proximity). Individuals with more frequent social opportunities received more grooming, whereas for grooming given, fT3 moderated this effect, suggesting an energetic cost of giving grooming. While our results support the spirit of the energetic deficiencies hypothesis, the directionality of the relationship between energy availability and movement is unexpected and suggests that lower-energy individuals may use strategies to reduce the costs of intermittent locomotion. Thus, future work should consider whether age-related declines in sociality may be a by-product of a strategy to conserve energy.This article is part of the discussion meeting issue 'Understanding age and society using natural populations'.

High early lactational synchrony within baboon groups predicts increased infant mortality.

Social group composition can have fitness implications for group members by determining opportunities for affiliative and competitive interactions. Female-female competition may be particularly acute when many groupmates have young infants at the same time, with potential consequences for infant survival. Here, we used decades of data on wild baboons (Papio sp.) in Amboseli, Kenya, to examine the effects of 'early lactational synchrony' (here, the proportion of females in a group with an infant <90 days old) on female-female agonistic interactions and infant survival. Because early lactation is an energetically demanding time for mothers and a risky time for infants, we expected early lactational synchrony to produce intensified competition for food and/or male protectors, resulting in more frequent female-female agonistic interactions and high infant mortality. In support of these predictions, we found that the frequency of female-female agonistic interactions increased with increasing early lactational synchrony. Reproductive state affected this relationship: while females in all states (cycling, pregnant, and postpartum amenorrhea) initiated more agonistic interactions when early lactational synchrony was high, only females in postpartum amenorrhea (including, but not limited to, females in early lactation) received more agonistic interactions. Furthermore, while high early lactational synchrony was rare, it strongly predicted infant mortality. This association may result from both aggression among adult females and infanticidal behavior by peripubertal females. These findings provide novel evidence that social dynamics may shape reproductive phenology in a nonseasonal breeder. Specifically, both competition among reproductive females and harassment from nonreproductive females may select against synchronous reproduction.

No Evidence for a Link Between Dominance Rank, Unit Size, and Faecal Glucocorticoid Levels in a Small Sample of Wild female Guinea Baboons (Papio papio)

No Evidence for a Link Between Dominance Rank, Unit Size, and Faecal Glucocorticoid Levels in a Small Sample of Wild female Guinea Baboons (Papio papio)

Re-evaluating the relationship between female social bonds and infant survival in wild baboons.

Over the past few decades studies have provided strong evidence that the robust links between the social environment, health, and survival found in humans also extend to non-human social animals. A number of these studies emphasize the early life origins of these effects. For example, in several social mammals, more socially engaged mothers have infants with higher rates of survival compared to less socially engaged mothers, suggesting that positive maternal social relationships causally improve offspring survival. Here we show that the relationship between infant survival and maternal sociality is confounded by previously underappreciated variation in female social behavior linked to changes in reproductive state and the presence of a live infant. Using data from a population of wild baboons living in the Amboseli basin of Kenya - a population where high levels of maternal sociality have previously been linked to improved infant survival - we find that infant- and reproductive state-dependent changes in female social behavior drive a statistically significant relationship between maternal sociality and infant survival. After accounting for these state-dependent changes in social behavior, maternal sociality is no longer positively associated with infant survival in this population. Our results emphasize the importance of considering multiple explanatory pathways-including third-variable effects-when studying the social determinants of health in natural populations.

Social and environmental predictors of gut microbiome age in wild baboons.

Understanding why some individuals age faster than others is essential to evolutionary biology and geroscience, but measuring variation in biological age is difficult. One solution may lie in measuring gut microbiome composition because microbiota change with many age-related factors (e.g., immunity and behavior). Here we create a microbiome-based age predictor using 13,563 gut microbial profiles from 479 wild baboons collected over 14 years. The resulting "microbiome clock" predicts host chronological age. Deviations from the clock's predictions are linked to demographic and socio-environmental factors that predict baboon health and survival: animals who appear old-for-age tend to be male, sampled in the dry season (for females), and high social status (both sexes). However, an individual's "microbiome age" does not predict the attainment of developmental milestones or lifespan. Hence, the microbiome clock accurately reflects age and some social and environmental conditions, but not the pace of development or mortality risk.

More allogrooming is followed by higher physiological stress in wild female baboons.

Social bonds increase fitness in a range of mammals. One pathway by which social bonds may increase fitness is by reducing the exposure to physiological stress, i.e. glucocorticoid (GC) hormones, that can be detrimental to health and survival. This is achieved through downregulating hypothalamic-pituitary-adrenal (HPA)-axis activity. Indeed, long-term measures of social (grooming) bonds are often negatively correlated with HPA-axis activity. However, the proximate role of physical touch through allogrooming remains an open question in the sociality-health-fitness debate. Demonstrating the potential anxiolytic benefits of grooming in the wild is hindered by methodological limitations. Here, we match accelerometer-identified grooming in wild female chacma baboons (Papio ursinus) to non-invasive faecal GC metabolite concentrations (fGCs). Consistent with previous work, we found a negative (but statistically non-significant) overall relationship between individual averaged fGCs and grooming rates. However, when time-matching grooming to fGCs, we found that both more giving and receiving grooming were followed by higher fGCs. This upregulation of HPA-axis activity suggests that maintaining social bonds (and its ultimate fitness benefits) may come at a shorter-term physiological cost. This finding sheds new light on a ubiquitous social behaviour typically considered 'relaxing' and suggests that sociopositive contact can trigger physiological stress.

Using non-invasive behavioral and physiological data to measure biological age in wild baboons

Biological aging is near-ubiquitous in the animal kingdom, but its timing and pace vary between individuals and over lifespans. Prospective, individual-based studies of wild animals—especially non-human primates—help identify the social and environmental drivers of this variation by indicating the conditions and exposure windows that affect aging processes. However, measuring individual biological age in wild primates is challenging because several of the most promising methods require invasive sampling. Here, we leverage observational data on behavior and physiology, collected non-invasively from 319 wild female baboons across 2402 female-years of study, to develop a composite predictor of age: the non-invasive physiology and behavior (NPB) clock. We found that age predictions from the NPB clock explained 51% of the variation in females’ known ages. Further, deviations from the clock’s age predictions predicted female survival: females predicted to be older than their known ages had higher adult mortality. Finally, females who experienced harsh early-life conditions were predicted to be about 6 months older than those who grew up in more benign conditions. While the relationship between early adversity and NPB age is noisy, this estimate translates to a predicted 2–3 year reduction in mean adult lifespan in our model. A constraint of our clock is that it is tailored to data collection approaches implemented in our study population. However, many of the clock’s components have analogs in other populations, suggesting that non-invasive data can provide broadly applicable insight into heterogeneity in biological age in natural populations.

Wild Baboons Groom Objects with Fur: Implications for Infant Corpse Carrying in Primates?

Nonhuman primates demonstrate great behavioral diversity in their responses to death, yet the most prevalent of these—infant corpse carrying—remains poorly understood. While mothers are the most frequent carriers, corpse carrying can be performed by non-mothers, and heterospecifics’ corpses are also carried. We propose a new hypothesis to explain, in part, non-maternal corpse carrying, the ‘mammalian cues hypothesis,’ and experimentally test it in a population of wild baboons. The mammalian-cues hypothesis argues that evolutionary pressures on maternal responsiveness have created a generalized attraction towards mammalian-typical traits in mammals of both sexes. This attraction may drive interest in inanimate objects (including corpses) that display mammalian cues. To test this, we presented objects that varied in mammalian traits to wild chacma baboons (Papio ursinus) and recorded their behavioral responses. Contrary to our hypothesis, baboons handled all objects (i.e., with or without mammalian traits) for similar lengths of time. However, in partial support of our hypothesis, baboons groomed the objects with fur—even those without any other mammalian traits—and explored them in a less destructive manner. We caution that infant corpse grooming by non-mothers in primates may be indicative of the visual and tactile stimuli the corpse presents rather than an interest in death or a reflection of social bonds.

DNA methylation signatures of early-life adversity are exposure-dependent in wild baboons

The early-life environment can profoundly shape the trajectory of an animal's life, even years or decades later. One mechanism proposed to contribute to these early-life effects is DNA methylation. However, the frequency and functional importance of DNA methylation in shaping early-life effects on adult outcomes is poorly understood, especially in natural populations. Here, we integrate prospectively collected data on fitness-associated variation in the early environment with DNA methylation estimates at 477,270 CpG sites in 256 wild baboons. We find highly heterogeneous relationships between the early-life environment and DNA methylation in adulthood: aspects of the environment linked to resource limitation (e.g., low-quality habitat, early-life drought) are associated with many more CpG sites than other types of environmental stressors (e.g., low maternal social status). Sites associated with early resource limitation are enriched in gene bodies and putative enhancers, suggesting they are functionally relevant. Indeed, by deploying a baboon-specific, massively parallel reporter assay, we show that a subset of windows containing these sites are capable of regulatory activity, and that, for 88% of early drought-associated sites in these regulatory windows, enhancer activity is DNA methylation-dependent. Together, our results support the idea that DNA methylation patterns contain a persistent signature of the early-life environment. However, they also indicate that not all environmental exposures leave an equivalent mark and suggest that socioenvironmental variation at the time of sampling is more likely to be functionally important. Thus, multiple mechanisms must converge to explain early-life effects on fitness-related traits.

Gut microbiota variations in wild yellow baboons (Papio cynocephalus) are associated with sex and habitat disturbance

Although male and female mammals differ in biological traits and functional needs, the contribution of this sexual dimorphism to variations in gut bacteria and fungi (gut microbiota) in relation to habitat type has not been fully examined. To understand whether the combination of sex and habitat affects gut microbiota variation, we analyzed 40 fecal samples of wild yellow baboons (Papio cynocephalus) living in contrasting habitat types (intact, well-protected vs. fragmented, less protected forests) in the Udzungwa Mountains of Tanzania. Sex determination was performed using the marker genes SRY (Sex-determining Region Y) and DDX3X-DDX3Y (DEAD-Box Helicase 3). Samples were attributed to 34 individuals (19 females and 15 males) belonging to five social groups. Combining the results of sex determination with two amplicon sequencing datasets on bacterial (V1–V3 region of the 16S rRNA gene) and fungal (ITS2) gut communities, we found that overall, baboon females had a significantly higher gut bacterial richness compared to males. Beta diversity estimates indicated that bacterial composition was significantly different between males and females, and this was true for individuals from both well- and less protected forests. Our results highlight the combined role of sex and habitat type in shaping variation in gut microbial communities in wild non-human primates.

STRESS AND DEATH: GLUCOCORTICOIDS AND SURVIVAL IN A WILD PRIMATE MODEL OF AGING

Abstract Chronic exposure to stressors has been linked with a wide range of detrimental effects on health in humans, laboratory animals, and a few wild animal populations. Glucocorticoids (GCs) mediate stress responses, and consequently GC levels are regularly measured in humans and other animals as biological markers of stress. However, no tests in humans or in natural populations of animals have yet established clear connections between environmental stressors, chronically elevated GCs, and shortened lifespan. To fill this gap, we used longitudinal data on wild female baboons to investigate the relationship between GC levels and survival—the single greatest determinant of variation in evolutionary fitness among female baboons. Using 14,173 GC measurements from 242 wild adult female baboons over 1634 female years, we document a powerful link between GCs and survival: females with relatively high current GCs or high lifelong cumulative GCs face an elevated risk of death. A hypothetical female who maintained GCs in the top 90% for her age across adulthood would be expected to lose 5.4 years of life relative to a female who maintained GCs in the bottom 10% for her age. Hence, differences among individuals in HPA axis activity provide valuable prognostic information about disparities in lifespan. Together, our results both support the value of GCs as a window into health, fitness, and aging and suggest that they may mechanistically contribute to the established link between sociality and lifespan.

BIODEMOGRAPHY OF AGING, CELEBRATING JAMES W. VAUPEL, PHD

Abstract James W. Vaupel, PhD (1945 – 2022), was an international leader in demography and aging research and a pioneer in the field of biodemography. He was a highly creative researcher and very entrepreneurial in the development of new interdisciplinary research environments. This symposium highlights a few of the biodemographic research areas that Dr. Vaupel has been a catalyst for. Denmark was Dr. Vaupel’s home country during the last third of his life, and Dr. Christensen reports on findings from Danish nationwide genetic-epidemiological studies on twins and the oldest old: familial influence on aging phenotypes, cohort differences in health among the oldest old, associations of early life events with late life health, as well as tongue-in-cheek research on perceived age and teeth. Dr. Alberts discusses the ‘invariant rate of aging’ hypothesis that was developed by Vaupel and others. She presents comparative analyses from multiple nonhuman primate populations showing that, while life expectancy can continue to improve, we probably can’t slow the demographic rate of aging. Dr. Campos presents evidence from a wild baboon population in Kenya that glucocorticoid levels—biological markers of stress responses—are strong prognostic indicators of survival and may be key explanations of life span disparities. Dr. Carey presents key discoveries from large-scale studies involving the Mediterranean fruit fly. These include the slowing of mortality at older ages, context-specific sex mortality differentials, a behavioral biomarker for morbidity, dietary conditions for maximizing lifespan versus reproduction and a stationary population identity whereby life lived equals life left.

Environmental, sex-specific and genetic determinants of infant social behaviour in a wild primate.

Affiliative social bonds are linked to fitness components in many social mammals. However, despite their importance, little is known about how the tendency to form social bonds develops in young animals, or if the timing of development is heritable and thus can evolve. Using four decades of longitudinal observational data from a wild baboon population, we assessed the environmental determinants of an important social developmental milestone in baboons-the age at which a young animal first grooms a conspecific-and we assessed how the rates at which offspring groom their mothers develops during the juvenile period. We found that grooming development differs between the sexes: female infants groom at an earlier age and reach equal rates of grooming with their mother earlier than males. We also found that age at first grooming for both sexes is weakly heritable (h2 = 0.043, 95% CI: 0.002-0.110). These results show that sex differences in grooming emerge at a young age; that strong, equitable social relationships between mothers and daughters begin very early in life; and that age at first grooming is heritable and therefore can be shaped by natural selection.

Estimating individual exposure to predation risk in group-living baboons, Papio anubis.

In environments with multiple predators, vulnerabilities associated with the spatial positions of group-living prey are non-uniform and depend on the hunting styles of the predators. Theoretically, coursing predators follow their prey over long distances and attack open areas, exposing individuals at the edge of the group to predation risk more than those at the center (marginal predation). In contrast, ambush predators lurk unnoticed by their prey and appear randomly anywhere in the group; therefore, isolated individuals in the group would be more vulnerable to predators. These positions of vulnerability to predation are expected to be taken by larger-bodied males. Moreover, dominant males presumably occupy the center of the safe group. However, identifying individuals at higher predation risk requires both simultaneous recording of predator location and direct observation of predation events; empirical observations leave ambiguity as to who is at risk. Instead, several theoretical methods (predation risk proxies) have been proposed to assess predation risk: (1) the size of the individual 'unlimited domain of danger' based on Voronoi tessellation, (2) the size of the 'limited domain of danger' based on predator detection distance, (3) peripheral/center position in the group (minimum convex polygon), (4) the number and direction of others in the vicinity (surroundedness), and (5) dyadic distances. We explored the age-sex distribution of individuals in at-risk positions within a wild baboon group facing predation risk from leopards, lions, and hyenas, using Global Positioning System collars. Our analysis of the location data from 26 baboons revealed that adult males were consistently isolated at the edge of the group in all predation risk proxies. Empirical evidence from previous studies indicates that adult male baboons are the most frequently preyed upon, and our results highlights the importance of spatial positioning in this.

Cycle length flexibility: is the duration of sexual receptivity associated with changes in social pressures?

Research in social mammals has revealed the complexity of strategies females use in response to female-female reproductive competition and sexual conflict. One point at which competition and conflict manifests acutely is during sexual receptivity, indicated by swellings in some primates. Whether females can adjust their sexual receptivity from cycle to cycle to decrease reproductive competition and sexual conflict in response to social pressures has not been tested. As a first step, this study explores whether sexual receptivity duration is predicted by social pressures in wild female chacma baboons (Papio ursinus). Given that female baboons face intense reproductive competition and sexual coercion, we predicted that: females could shorten the duration of their sexual receptive period to reduce female-female aggression and male coercion or increase it to access multiple or their preferred male(s). We quantified 157 ovulatory cycles from 46 wild females living in central Namibia recorded over 15 years. We found no support for our hypothesis; however, our analyses revealed a negative correlation between maximal-swelling duration and group size, a proxy of within-group competition. This study provides further evidence that swelling is costly as well as a testable framework for future investigations of 'cycle length manipulation'.

Early life drought predicts components of adult body size in wild female baboons.

In many taxa, adverse early-life environments are associated with reduced growth and smaller body size in adulthood. However, in wild primates, we know very little about whether, where, and to what degree trajectories are influenced by early adversity, or which types of early adversity matter most. Here, we use parallel-laser photogrammetry to assess inter-individual predictors of three measures of body size (leg length, forearm length, and shoulder-rump length) in a population of wild female baboons studied since birth. Using >2000 photogrammetric measurements of 127 females, we present a cross-sectional growth curve of wild female baboons (Papio cynocephalus) from juvenescence through adulthood. We then test whether females exposed to several important sources of early-life adversity-drought, maternal loss, low maternal rank, or a cumulative measure of adversity-were smaller for their age than females who experienced less adversity. Using the "animal model," we also test whether body size is heritable in this study population. Prolonged early-life drought predicted shorter limbs but not shorter torsos (i.e., shoulder-rump lengths). Our other measures of early-life adversity did not predict variation in body size. Heritability estimates for body size measures were 36%-67%. Maternal effects accounted for 13%-17% of the variance in leg and forearm length, but no variance in torso length. Our results suggest that baboon limbs, but not torsos, grow plastically in response to maternal effects and energetic early-life stress. Our results also reveal considerable heritability for all three body size measures in this study population.

Five Decades of Data Yield No Support for Adaptive Biasing of Offspring Sex Ratio in Wild Baboons (Papio cynocephalus).

AbstractOver the past 50 years, a wealth of testable, often conflicting hypotheses have been generated about the evolution of offspring sex ratio manipulation by mothers. Several of these hypotheses have received support in studies of invertebrates and some vertebrate taxa. However, their success in explaining sex ratios in mammalian taxa-especially in primates-has been mixed. Here, we assess the predictions of four different hypotheses about the evolution of biased offspring sex ratios in the baboons of the Amboseli basin in Kenya: the Trivers-Willard, female rank enhancement, local resource competition, and local resource enhancement hypotheses. Using the largest sample size ever analyzed in a primate population ( offspring), we test the predictions of each hypothesis. Overall, we find no support for adaptive biasing of sex ratios. Offspring sex is not consistently related to maternal dominance rank or biased toward the dispersing sex, nor is it predicted by group size, population growth rates, or their interaction with maternal rank. Because our sample size confers power to detect even subtle biases in sex ratio, including modulation by environmental heterogeneity, these results suggest that adaptive biasing of offspring sex does not occur in this population.

Human-influenced diets affect the gut microbiome of wild baboons

Industrialized diets that incorporate processed foods and are often high in simple sugars and fats and low in fiber have myriad health impacts, many of which may operate via impacts on the gut microbiota. Examining how these diets affect the gut microbiota can be challenging given that lab animal models experience altered environmental contexts, and human studies include a suite of co-varying cultural and environmental factors that are likely to shape the gut microbiota alongside diet. To complement these approaches, we compare the microbiomes of wild populations of olive baboons (Papio anubis) with differential access to human trash high in processed foods, simple sugars, and fats in Rwanda’s Akagera National Park. Baboons are a good model system since their microbiomes are compositionally similar to those of humans. Additionally, this population inhabits a common environment with different social groups consuming qualitatively different amounts of human trash, limiting variation in non-dietary factors. Using 16S rRNA gene amplicon sequencing we find that baboons with unlimited access to human trash have reduced microbial alpha diversity and reduced relative abundances of fiber-degrading taxa such as Ruminococcaceae, Prevotellaceae, and Lachnospiraceae. In contrast, baboons with limited access to human trash have a microbiome more similar to that of baboons with no access to human trash. Our results suggest that while a human-influenced diet high in processed foods, simple sugars, and fats is sufficient to alter the microbiome in wild baboons, there is a minimum threshold of dietary alteration that must occur before the microbiome is substantially altered. We recommend that data from wild primate populations such as these be used to complement ongoing research on diet-microbiome-health interactions in humans and lab animal models.