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Alberts, S. C.

Publications and source records attributed to Alberts, S. C..

At least 19 recordsLinked to original sources

Activity budgets, social behavior, and fitness outcomes associated with a baboon group fusion

Many primates exhibit female philopatry and live in stable, female-bonded groups, where females are seldom exposed to novel same-sex conspecifics. Permanent group fusions are unique in bringing unfamiliar female conspecifics together but are rarely documented in these populations. We present a case study on a fusion of two groups from a hybrid population of baboons (Papio cynocephalus x P. anubis ) living in the Amboseli basin of Kenya. We compared the behavior of eight adult females after the fusion to the behavior of females in groups that had not fused and compared pre- and post-fusion fitness outcomes. Following the fusion, the group's activity budget and patterns of agonistic interactions were typical for the study population. Females preferred familiar grooming partners for a short period following the fusion; however, after three months, female grooming patterns were comparable to other groups, indicating rapid social integration. Females from the smaller pre-fusion group were lower ranking than females from the larger group. The fusion occurred following increased human-induced mortality in one of the two groups. From our limited sample, we observed no detectable fitness-related costs of fusion in terms of birth rates or offspring survival, while adult female mortality was low following the fusion. These results demonstrate the flexibility of female baboons in navigating exposure to novel same-sex conspecifics despite a species-typic pattern of female philopatry. Our results support previous research indicating that group fusions most likely occur when groups are too small to retain adult males, defend against predators, or compete with other groups.

animal behavior and cognition↗

Social microbiome transmission predicts microbial specialization and host lifespan in a wild primate

Social interactions are proposed to provide reliable routes for microbial transmission between animals, facilitating animal-microbiome co-evolution. However, microbiome transmission remains challenging to measure in wild populations. Here we combine behavioral observations of wild baboons with repeated strain-resolved metagenomic profiling to identify individual gut microbial species that follow a dominant mode of social transmission. In an 18-year metagenomic time series from the same population, baboons with higher levels of socially transmitted species lived longer than those with lower levels of socially transmitted species. Socially transmitted species were also more stable and persistent within baboons, yet had narrower host ranges outside of baboons. Thus, social transmission is not only detectable in free-living primates, but may play a special role in both host and microbial fitness.

evolutionary biology↗

Real-time heart rate in the wild: remote collection of cardiac data in baboons using a low-power Bluetooth and LoRaWAN system

O_LICardiac rate and rhythm reveal how animals adapt physiologically to day-to-day challenges, with consequences for health and fitness. However, these data remain difficult to collect in wild animals, despite their relevance for individual health and fitness. C_LIO_LIHere, we present a system for collecting and transmitting long-term, fine-scaled physiological data in wild animals. We implanted Bluetooth-enabled cardiac and physiological monitor devices in three wild adult female baboons in the Amboseli ecosystem in Kenya and paired these devices with collars that enabled remote data downloads over long-range wide area network (LoRaWAN). C_LIO_LIThe system performed well over >10 months, providing the first long-term cardiac data in wild primates. The baboons showed strong circadian patterns in heart rate, heart rate variability, and activity. We also present data on one female who left her social group for unknown reasons; while alone she exhibited higher heart rate variability, lower activity, and evidence of disrupted sleep. C_LIO_LIIn sum, physiologgers paired with low-energy methods of remote data retrieval are powerful tools for investigating physiology in wild animals on timescales that extend over many months, with minimal disruption to their behavior. C_LI

zoology↗

Longitudinal changes in gut microbiota across reproductive states in wild baboons

BackgroundIn humans and other mammals, female reproduction is linked to extensive changes in physiology, immunity, hormones, and behavior. These changes likely shape, and may be shaped by, the composition of gut microbial communities. Characterizing the dynamics of gut microbial change across reproductive states, including its relationship to female physiology, is important for understanding how the gut microbiota influences female and offspring health. ResultsHere we characterize longitudinal changes in gut microbiota across reproduction by combining 16S rRNA gene sequencing data from 4,462 stool samples (spanning 14 years of sample collection) with life history data on multiple reproductive events in 169 female baboons. These baboons were members of a well-studied, natural baboon population in Kenya where reproductive state (ovarian cycling, pregnancy, and postpartum amenorrhea) is tracked daily and microbiota data could be paired with measurements of fecal-derived estrogen, progesterone, and glucocorticoid levels. We found extensive changes in baboon gut microbiota as females transitioned between reproductive states. Pregnancy was linked to distinct patterns of ASV richness, community composition, and taxonomic abundances compared to postpartum amenorrhea and ovarian cycling. The most dramatic shifts occurred as females transitioned from the first to second trimester of pregnancy, with altered abundances of taxa that have been linked, in humans and model systems, to host immunity, weight gain, or hormone levels. Host identity was consistently the strongest predictor of gut microbiota composition across states, and this individual signature was strongest during pregnancy. Estrogen and progesterone levels had robust associations with the gut microbiota overall, but the microbial taxa involved in these associations were reproductive state-dependent. Glucocorticoid concentrations were not a major predictor of gut microbiota composition in any state. ConclusionsTogether, our results support the idea that gut microbiota contribute to the complex physiological changes necessary during pregnancy, but that microbial changes during pregnancy are somewhat unique to each female. Variation in steroid hormones is associated with some, but not all, of these relationships, emphasizing the importance of considering steroid hormone levels in studies of gut microbiota variation. Our results motivate future work on how gut microbiota contribute to reproductive outcomes, including both maternal and offspring health.

evolutionary biology↗

Group social conditions and environment predict foraging behavior in wild baboons

For group-living animals, conditions in the physical and social environments are closely linked to foraging outcomes, but the nature and causal direction of many aspects of these relationships remain unclear. Here, we use long-term data from a well-studied population of wild baboons in Amboseli, Kenya, to examine how group-level social traits (group size and social network density) and climate variables (rainfall and temperature) are linked to two types of foraging outcomes for adult female baboons: (i) foraging-related time budgets and (ii) diet composition (time spent on fallback foods, such as grass corms, versus high-energy foods). We find that rainfall and temperature interact to predict multiple foraging outcomes: more rainfall is associated with more time spent feeding, less time spent walking without feeding, and more feeding time spent on grass corms, but this influence is more pronounced in hotter years than in cooler years. Females in intermediate-sized groups spend more time walking without feeding than those in other groups, but group size does not significantly predict other foraging-related outcomes (i.e., time spent feeding or diet composition). We also find that females in groups with denser social networks spend less time feeding, and less time feeding on grass corms, than those in sparser networks. However, in a preliminary causal analysis meant to further explore this result, we find support for the hypothesis that this relationship is driven by effects of foraging on social behavior, as opposed to effects of network density on foraging: more time spent eating grass corms leads to lower social network density and more time spent feeding. Our results show how the social and the physical environments are linked to foraging outcomes, and highlight the importance of future studies of their pattern and mechanism.

ecology↗

Demographic, behavioral, and ecological data from a long-term field study of wild baboons in Amboseli, Kenya

Long-term data sets on individually recognized animals and their environments are critical to understanding animal behavior, evolution, and ecology. However, they are resource- and time-intensive and seldom made publicly available. The Amboseli Baboon Research Project (ABRP) is one of the longest-running studies of a wild mammal population in the world and has collected extensive data on the baboon population of the Amboseli ecosystem in Kenya since 1971. Here, we describe four ABRP data sets newly available to the evolutionary biology, behavioral ecology, and primatology communities: (1) the sizes and demographic compositions of 21 social groups from 1971-2023; (2) the activity budgets of adult females and immatures from 1984-2023; (3) behavioral data on diet for adult females and immatures from 1984-2023; and (4) weather data, including precipitation from 1976-2023 and temperature from 1976-2022. Data are aggregated annually and monthly to enable cross-data set analyses. These data offer a rare longitudinal perspective on behavioral and ecological change in a wild mammal population.

animal behavior and cognition↗

Admixture influences the genetic architecture of DNA methylation in a wild primate hybrid zone

BackgroundHybrid zones play a central role in evolutionary biology because they serve as natural laboratories for studying how traits and taxa diverge. Changes in gene regulation make important contributions to this process. However, the degree to which admixture shapes gene regulatory variation in hybrid populations remains poorly understood. Here, we combine genome-wide resequencing and DNA methylation data from 295 hybrid baboons--members of a single, intensively studied natural population--to investigate how admixture affects the genetic architecture of this important epigenetic mark. ResultsWe find that local genetic ancestry frequently predicts DNA methylation levels and recapitulates differences between the parent species. By performing methylation quantitative trait locus (meQTL) mapping, we show that these differences predominantly arise due to evolved differences in allele frequencies. Thus, admixture in the hybrid population increases variance in DNA methylation, including by introducing meQTL that would otherwise be invariant. Finally, we integrate massively parallel reporter assay data to show that admixture-derived variation in DNA methylation alters enhancer activity and gene expression. ConclusionsTogether, these results demonstrate how admixture can meaningfully alter the genetic architecture of gene regulatory traits in natural hybrid zones. They also suggest that the genetic architecture of DNA methylation is conserved across closely related primates, suggesting that genetic effects on gene regulation may remain stable over timescales that range into the millions of years.

evolutionary biology↗

Disparate social structures are underpinned by distinct social rules across a primate radiation

Over six decades of research on wild baboons and their close relatives (collectively, the African papionins) have uncovered substantial variation in their behavior and social systems. While most papionins form discrete social groups (single-level societies), a few others form small social units that are nested within larger supergroups (multi-level societies). These two systems are generally thought to be qualitatively distinct, but data from wild populations increasingly suggest that there may be areas of overlap. To quantify this potential gradient in social structure, a more systematic, comparative analysis is needed. Here, we constructed a database of behavioral and demographic records spanning 135 group-years, 28 social groups, 13 long-term field studies, and 11 species to quantify variation in grooming network structure, and identify the individual and dyadic properties (e.g., kinship and social status effects) that underlie this variation. Consistent with accumulating observations in the field, the single-level species could be divided into two categories: cohesive and cliquish. Cohesive single-level networks were dense, kin-biased, and moderately rank-structured, while cliquish single-level networks were more differentiated, slightly more kin-biased, and strongly rank-structured. As expected, multi-level networks were very modular and shaped by females ties to specific dominant males but varied in their kin biases. Taken together, these data suggest that (i) kin and rank biases are widespread but vary in their strength; (ii) male-centered subgroups are exclusive to multi-level systems; and (iii) increases in network modularity can emerge in response to heightened nepotism and male-centered clustering. SIGNIFICANCE STATEMENTWhat forces explain variation in primate societies? While kinship and dominance shape the social lives of many of our close relatives, it is unclear how their effects differ across species. Using a new database comprising decades of field research, we found that baboons and their close relatives fell into three general patterns: one in which groups were cohesive, kin-biased, and moderately rank-biased, another in which groups were more cliquish and nepotistic, and a third in which groups were divided into clusters centered on dominant males. Distinct primate societies may thus reflect differences in the strength of females nepotistic biases and the degree of males social influence.

animal behavior and cognition↗

Early-life paternal relationships predict adult female survival in wild baboons

Parent-offspring relationships can have profound effects on offspring behavior, health, and fitness in adulthood. These effects are strong when parents make heavy investments in offspring care. However, in some mammals, including several species of carnivores, rodents, and primates, fathers live and socialize with offspring, but paternal care per se is subtle or indirect. Do these limited father-offspring relationships also affect later-life outcomes for offspring? Working in a well-studied baboon population where males contribute little direct offspring care, we found that juvenile female baboons who had stronger paternal relationships, or who resided longer with their fathers, led adult lives that were 2-4 years longer than females with weak or short paternal relationships. This pattern did not differ between females who experienced high versus low levels of early-life adversity; hence, paternal relationships were equally protective in both harsh and benign early environments. Males relationships were strongest with juvenile females they were most likely to have sired and when males had few mating opportunities. Hence, father-daughter relationships may be constrained by male mating effort. Because survival predicts female fitness, fathers and their daughters may experience selection to engage socially and stay close in daughters early lives.

evolutionary biology↗

Eukaryotic composition across seasons and social groups in the gut microbiota of wild baboons

BackgroundAnimals coexist with complex microbiota, including bacteria, viruses, and eukaryotes (e.g., fungi, protists, and helminths). While the composition of bacterial and viral components of animal microbiota are increasingly well understood, eukaryotic composition remains neglected. Here we characterized eukaryotic diversity in the microbiomes in wild baboons and tested the degree to which eukaryotic community composition was predicted by host social group membership, sex, age, and season of sample collection. ResultsWe analyzed a total of 75 fecal samples collected between 2012 and 2014 from 73 wild baboons in the Amboseli ecosystem in Kenya. DNA from these samples was subjected to shotgun metagenomic sequencing, revealing members of the kingdoms Protista, Chromista, and Fungi in 90.7%, 46.7%, and 20.3% of samples, respectively. Social group membership explained 11.2% of the global diversity in gut eukaryotic species composition, but we did not detect statistically significant effect of season, host age, and host sex. Across samples, the most prevalent protists were Entamoeba coli (74.66% of samples), Enteromonas hominis (53.33% of samples), and Blastocystis subtype 3 (38.66% of samples), while the most prevalent fungi included Pichia manshurica (14.66% of samples), and Ogataea naganishii (6.66% of samples). ConclusionsProtista, Chromista, and Fungi are common members of the gut microbiome of wild baboons. More work on eukaryotic members of primate gut microbiota is essential for primate health monitoring and management strategies.

microbiology↗

High early lactational synchrony within baboon groups predicts increased infant mortality

Female-female competition may be particularly acute when many females in the same social group have dependent young at the same time, with potential negative consequences for offspring survival. Here, we used more than four decades of data on wild baboons (Papio sp.) in Amboseli, Kenya, to examine the effects of early lactational synchrony (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 energetically demanding for mothers and high-risk for infants, we expected early lactational synchrony to intensify both female-female aggression and maternal association with males, who can buffer infants from conspecific harassment. In support of these predictions, when early lactational synchrony was high, new mothers initiated more agonistic contests. Further, high-ranking females increased their time associating with adult males, which may limit the ability of low-ranking females to receive male protective services and may have downstream consequences for female foraging efficiency. Finally, high early lactational synchrony strongly predicted infant mortality. This association may result from both aggression among adult females and infanticidal behavior by peripubertal females. Our findings provide evidence that synchronous reproduction alters competitive regimes and compromises reproductive outcomes even in nonseasonal breeders.

animal behavior and cognition↗

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.

animal behavior and cognition↗

Social and environmental predictors of gut microbiome age in wild baboons

Mammalian gut microbiomes are highly dynamic communities that shape and are shaped by host aging, including age-related changes to host immunity, metabolism, and behavior. As such, gut microbial composition may provide valuable information on host biological age. Here we test this idea by creating 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 clocks predictions are linked to some 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 have high social status (both sexes). However, an individuals "microbiome age" does not predict the attainment of developmental milestones or lifespan. Hence, in our host population, gut microbiome age largely reflects current, as opposed to past, social and environmental conditions, and does not predict the pace of host development or host mortality risk. We add to a growing understanding of how age is reflected in different host phenotypes and what forces modify biological age in primates.

evolutionary biology↗

Testing frameworks for early life effects: the developmental constraints and adaptive responsehypotheses do not explain key fertility outcomes in wild female baboons

In evolutionary ecology, two classes of explanations are frequently invoked to explain "early life effects" on adult outcomes. Developmental constraints (DC) explanations contend that costs of early adversity arise from limitations adversity places on optimal development. Adaptive response (AR) hypotheses propose that later life outcomes will be worse when early and adult environments are poorly "matched." Here, we use recently proposed mathematical definitions for these hypotheses and a quadratic-regression based approach to test the long-term consequences of variation in developmental environments on fertility in wild baboons. We evaluate whether low rainfall and/or dominance rank during development predict three female fertility measures in adulthood, and whether any observed relationships are consistent with DC and/or AR. Neither rainfall during development nor the difference between rainfall in development and adulthood predicted any fertility measures. Females who were low-ranking during development had an elevated risk of losing infants later in life, and greater change in rank between development and adulthood predicted greater risk of infant loss. However, both effects were statistically marginal and consistent with alternative explanations, including adult environmental quality effects. Consequently, our data do not provide compelling support for either of these common explanations for the evolution of early life effects.

evolutionary biology↗

Infant spatial relationships with adult males in a wild primate: males as mitigators or magnifiers of intergenerational effects of early adversity?

Adult male mammals can provide infants with protection and enhance their access to resources. They can also pose a risk to infants, either directly through infanticide or other aggression, or indirectly by placing infants at increased risk of conspecific or heterospecific conflict. Both benefits and costs may be especially important for offspring born to mothers in poor condition. Here we present the most detailed analysis to date of the influence of adult non-human primate males on a wide range of infant behaviors, and a description of the predictors of individual infants proximity to adult males. We show that the number of adult males near an infant predicts many infant behavioral traits, including aspects of the mother-infant relationship, infant activity budgets, and the frequency of social interactions with non-mothers. Infant exposure to adult males is statistically significantly repeatable over time (R = 0.16). This repeatability is partially explained by whether the infants mother experienced early life adversity: offspring of high-adversity mothers spent time in close proximity to more males during the first months of life. Our results are consistent with the possibility that the effects of maternal early life adversity can be mitigated or magnified by relationships with adult males.

ecology↗

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

The early life environment can profoundly shape the trajectory of an animals 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. Significance statementThe environment animals face when young can affect how they function throughout life. Long-lasting changes in DNA methylation--a chemical mark deposited on DNA that can affect gene activity--have been hypothesized to contribute to early life effects. But evidence for persistent, early environment-associated differences in DNA methylation is lacking in wild animals. Here, we show that early life adversity in wild baboons predicts DNA methylation levels in adulthood, especially for animals born in low resource environments and drought conditions. We also show that some of the changes we observe in DNA methylation have the capacity to influence gene activity levels. Together, our results support the idea that early experiences can become biologically embedded in the genomes of wild animals.

genomics↗

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

ObjectivesIn 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. Materials and MethodsUsing >2,000 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 three important sources of early-life adversity - drought, maternal loss, 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. ResultsProlonged early-life drought predicted shorter limbs but not shorter torsos (i.e., shoulder-rump lengths). Our other two measures of early-life adversity did not predict any variation in body size. Heritability estimates for body size measures were 36%-58%. Maternal effects accounted for 13%-22% of the variance in leg and forearm length, but no variance in torso length. DiscussionOur 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.

ecology↗

Heritable and sex-specific variation in the development of social behavior 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 development of social behavior 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 mother-offspring grooming reciprocity develops during the juvenile period. We found that grooming development differs between the sexes: female infants groom at an earlier age and reach reciprocity in grooming with their mother earlier than males. Using the quantitative genetic animal model, we also found that age at first grooming behavior for both sexes is weakly heritable (h2 = 4.3%). These results show that sex differences in grooming emerge at a young age; that strong, reciprocal 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.

animal behavior and cognition↗