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Archie, E. A.

Publications and source records attributed to Archie, E. A..

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↗

Using insertable cardiac monitors to test determinants of heart rate and activity in captive baboons

BackgroundInsertable cardiac monitors (ICMs) provide fine-grained, continuous data on cardiac activity. These data have great potential to reveal individual physiology, energetics, and stress responses, with implications for animal health, cognition, welfare, and conservation. However, these devices must be tested for safety, accuracy, and biological validity before being deployed in new species. Here we do so for the Reveal LINQTM ICM (Medtronic, Minneapolis, MN USA) over an 8-month period in 10 adult female baboons (Papio anubis and P. cynocephalus) at the Kenya Institute of Primate Research in Kenya. We also report data on heart rate, physical activity, and body temperature in unrestrained, conscious, captive baboons during their normal activities. Finally, we test how heart rate and activity levels are predicted by baboon species, body mass, time of day, ambient temperature, social dominance rank, and ovarian cycle phase. ResultsThe baboons had no adverse reactions to the Reveal LINQTM ICM. Their mean daytime heart rates (HRs) ranged from 89.6 to 128.0 beats per minute (bpm), and their resting HRs ranged from 74.4 to 98.2 bpm. The fastest observed R-wave interval validated by electrocardiogram (ECG) was 230 milliseconds (ms) (260 bpm), and the slowest was 1270 ms (47.4 bpm). In terms of predictors of HR and activity, HR was highly individualized, while activity level was not: baboon identity explained 41% of the variation in HR, but identity only 2% of variation in activity levels. HR was positively correlated with physical activity and HR was highest during daylight hours when the baboons were more active. Dominant baboons had higher HRs controlling for activity and were more active than low ranking individuals. In terms of ovarian cycle phase, HR was higher when individuals were in the periovulatory and luteal phases of the ovarian cycle compared to the follicular phase. ConclusionsOur findings support the future use of ICMs to investigate physiological responses in baboons. These devices safety and validity represent the plausibility of understanding inter-individual and inter-species variation in heart rate and activity in response to variation in the external environment and in individual internal state.

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↗

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↗

When is microbial strain sharing evidence for 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.

microbiology↗

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↗

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↗

Early life adversity and adult social relationships have independent effects on survival in a wild animal model of aging

Does social isolation in adulthood predict survival because socially isolated individuals are already unhealthy due to adversity earlier in life (health selection)? Or do adult social environments directly cause poor health and increased mortality risk ("social causation")? These alternative hypotheses are difficult to disentangle in humans because prospective data on survival and the environment for both early life and adulthood are rarely available. Using data from the baboon population of Amboseli, Kenya, a model for human behavior and aging, we show that early adversity and adult social isolation contribute independently to reduced adult survival, in support of both health selection and social causation. Further, strong social bonds and high social status can buffer some negative effects of early adversity on survival. These results support a growing change in perspective, away from "either-or" hypotheses and towards a multi-causal perspective that points to multiple opportunities to mitigate the effects of social adversity. TeaserEarly life environments and adult social bonds have strong, but largely independent effects on survival in wild baboons.

animal behavior and cognition↗

Ecology and age, but not genetic ancestry, predict fetal loss in a wild baboon hybrid zone

ObjectivesPregnancy failure and fetal loss represent a major fitness cost for any mammal, particularly those with slow life histories such as primates. Here, we quantified the risk of fetal loss in wild hybrid baboons, including genetic, ecological, and demographic sources of variance. We were particularly interested in testing the hypothesis that hybridization imposes a cost by increasing fetal loss rates. Such an effect would help explain how baboons maintain taxonomic integrity despite interspecific gene flow. Materials and MethodsWe analyzed pregnancy outcomes for 1,020 pregnancies observed over 46 years in a natural yellow baboon-anubis baboon hybrid zone. Fetal losses and live births were scored based on near-daily records of female reproductive state and the appearance of live neonates. We modeled the probability of fetal loss as a function of a females genetic ancestry (based on whole-genome resequencing data), age, number of previous fetal losses, dominance rank, group size, climate, and habitat quality using binomial mixed effects models. ResultsFemale genetic ancestry did not predict the likelihood of fetal loss. Instead, the risk of fetal loss is elevated for very young and very old females. Fetal loss is most robustly predicted by ecological factors, including poor habitat quality and extreme heat during pregnancy. DiscussionOur results suggest that gene flow between yellow baboons and anubis baboons is not impeded by an increased risk of fetal loss for hybrid females. Instead, ecological conditions and female age are key determinants of this component of female reproductive success. Research HighlightsO_LIFemale baboons do not experience fetal loss as a cost of hybridization. C_LIO_LIHeat stress, poor habitat quality, and young and old age elevate the risk of fetal loss, emphasizing roles for ecology and life history in determining birth outcomes. C_LI Graphical Abstract O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=124 SRC="FIGDIR/small/505836v1_ufig1.gif" ALT="Figure 1"> View larger version (23K): org.highwire.dtl.DTLVardef@74dd64org.highwire.dtl.DTLVardef@7301b5org.highwire.dtl.DTLVardef@751e9dorg.highwire.dtl.DTLVardef@12ce924_HPS_FORMAT_FIGEXP M_FIG Neonate drawings by Emily Nonnamaker. C_FIG

evolutionary biology↗

Genetic variance and indirect genetic effects for affiliative social behavior in a wild primate

Affiliative social behaviors are linked to fitness components in multiple species. However, the role of genetic variance in shaping affiliative social behaviors remains largely unknown, limiting our understanding of how these behaviors can respond to natural selection. Here, we employed the animal model to estimate both environmental and genetic sources of variance and covariance in grooming behavior in the well-studied Amboseli baboon population in Kenya. We found that grooming given, grooming received, and total grooming all are similarly heritable (h2=0.22, h2=0.16, and h2=0.26 respectively), and that rank and the presence of kin contribute to environmental variance. We detected small but measurable indirect genetic effects of partner identity on the amount of grooming given within dyadic grooming partnerships. The genetic correlation between grooming given and grooming received was exceptionally strong and positive (R=0.94 {+/-} 0.12), and the indirect and direct genetic effects for grooming given were also strongly positively correlated (R=0.86 {+/-} 0.06). Our results provide insight into the evolvability of affiliative behavior in wild animals, including the possibility for correlations between direct and indirect genetic effects to accelerate the response to selection. As such they provide novel information about the genetic architecture of social behavior in nature, with important implications for the evolution of cooperation and reciprocity.

evolutionary biology↗