bioRxiv Science⌕ Search

Biology subjects

Tung, J.

Publications and source records attributed to Tung, J..

At least 19 recordsLinked to original sources

Accelerated Evolution of Context-Dependent Gene Expression in Primate Immune Cells

Regulatory variation is widely recognized as a driver of evolution within and between species, including in the primate lineage. Evidence for potentially adaptive regulatory evolution in primates comes from both sequence-based tests for selection and cross-species comparisons of gene expression. However, comparative studies of gene expression have tended to focus on baseline cellular states, despite growing evidence that context-dependent gene regulation is important. Here, we investigate the evolution of gene expression in lymphoblastoid cell lines (LCLs) from 6 primate lineages (humans, chimpanzees, bonobos, western gorillas, Sumatran orangutans, and rhesus macaques) using data from both control and 5 perturbed cellular conditions (n=22-25 individuals per condition). Analyzing baseline expression data, we find that genes involved in immunity often exhibit lineage-specific transcriptional shifts, and that these genes occur near regions with lineage-specific sequence acceleration and lineage-specific epigenomic states. However, the subset of genes that respond to in vitro perturbations have evolved at significantly higher rates than environmentally-insensitive genes, a finding we replicate in an independent four-species dataset of primary white blood cells (n=26). Together, our findings support the argument that focusing on baseline states alone provides a biased view of gene regulatory evolution, and suggest that studying gene regulation in dynamic contexts can enrich our understanding of primate evolution.

evolutionary biology↗

Genetic and behavioural repertoires support olfactory communication in wild capuchin monkeys

Olfaction is a key sense for many mammals, but its role in the social lives of anthropoid primates (monkeys, apes, humans) is poorly understood. Studies of chemosensory receptor genes and olfactory behaviours can provide insight into the evolution and function of olfaction across social contexts. Vomeronasal receptor (VR) genes are especially relevant to social behaviour as they are specialized for the detection of pheromones and other cues involved in social signaling, reproductive behaviour, and individual recognition in mammals. Here, we examined the population genetics and gene repertoires of VR genes in wild white-faced capuchin monkeys (Cebus imitator) from Costa Rica and Panama using DNA sourced through both host tissues and through noninvasive fluorescence-activated cell sorting of fecal samples (fecalFACS). We compared VR diversity relative to putatively neutral reference loci (NRs) to investigate evidence of selection and potential effects of demography. To complement the genetic analysis, we also conducted a detailed observational study of capuchin olfactory behaviours. Combined, we find evidence of intact VRs subject to evolutionary constraint in capuchins, providing novel evidence that members of this gene family are maintained by evolutionary constraint in wild monkeys. We further document a rich and varied ethogram of olfactory behaviours that have clear potential for communication. Overall, our study provides compelling evidence for a role of olfaction in the complex social lives of capuchin monkeys, motivating future research on the contributions of olfaction to social communication and evolution in primates and other mammals.

animal behavior and cognition↗

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↗

Adaptive immune responses to vaccination reflect social status at first exposure in female rhesus macaques

Social gradients are consistently associated with variation in health outcomes, including infectious disease. However, distinguishing between social gradients in antigen exposure versus social gradients in susceptibility remains challenging. Here, we use a nonhuman primate model for chronic social stress to investigate how social status affects the influenza vaccine-induced adaptive immune response. We first manipulated the social status of female rhesus macaques and then tested the response to influenza antigens in naive individuals and after secondary exposure. Higher social status at the time of first exposure, but not at the time of secondary exposure, predicted stronger antibody responses to both exposures. Social status also drove gene expression differences in adaptive immune pathways, and genes that predicted the magnitude of the antibody response overlapped with those linked to social status. Thus, social gradients shape the adaptive immune response in a temporally dependent manner, with particular sensitivity at the time of initial antigen exposure.

genomics↗

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↗

Lifetime fitness and annual survival are heritable and highly genetically correlated in a wild primate population

The additive genetic variance (VA) of fitness quantifies the expected response to selection; lifetime breeding success (LBS) is an effective metric of fitness in animal populations. However, data on LBS are relatively rare for wild populations of long-lived species, while time-limited metrics such as annual survival or fertility are more readily available. The magnitude of VA for these time-limited metrics, and the degree to which they are genetically correlated with LBS, remains unclear in most cases. Here we estimated the VA and heritability (h2) of LBS and four time-limited fitness metrics in wild female baboons in Kenya. The most highly heritable metrics were LBS (h2=0.25) and annual survival (h2=0.23). Notably, all the VA for LBS was attributable to survival to first successful reproduction. Furthermore, all fitness metrics examined were highly genetically correlated with each other, supporting the potential use of time-limited metrics where LBS data are limited. Our analyses predicted faster phenotypic evolution than we observed, raising the possibility that environmental effects have masked responses to selection ("cryptic evolution") or that social effects inflate estimated VA. Together, our findings reveal a substantial genetic contribution to variation in survival, and in turn, to fitness and contemporary evolution in a long-lived animal.

evolutionary biology↗

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↗

A structural basis for chaperone repression of stress signalling from the endoplasmic reticulum

The endoplasmic reticulum (ER) unfolded protein response (UPR) is tuned by the balance between unfolded proteins and chaperones. While reserve chaperones are known to suppress the UPR transducers via their stress-sensing luminal domains, the underlying structural mechanisms remain unclear. Cellular and biophysical analyses established that the ER chaperone AGR2 forms a repressive complex with the luminal domain of the UPR transducer IRE1{beta}. Structural prediction, X-ray crystallography and NMR spectroscopy identify critical interactions between an AGR2 monomer and a regulatory loop in IRE1{beta}s luminal domain. However, in the repressive complex it is an AGR2 dimer that binds IRE1{beta}. Cryo-EM reconstruction reveals a mechanism of unanticipated simplicity: one AGR2 protomer engages the regulatory loop, while the second asymmetrically binds IRE1{beta}s luminal domains C-terminus, blocking IRE1{beta}-activating dimerization. Molecular dynamic simulations indicate that the second, disruptive AGR2 protomer exploits rare fluctuations in the IRE1{beta} dimer that expose its binding site. Thus, AGR2 actively disrupts IRE1{beta} dimers to suppress the UPR, while chaperone clients compete for AGR2 to trigger UPR signalling

biochemistry↗

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↗

Enhancing student comprehension of paternity assignment in molecular primatology: a pilot study using a Shiny web application in Kenya

Kinship is a major determinant of affiliative and mating behavior in primates. In field studies, identifying kin typically relies in part on genetic analysis, especially for discriminating paternal relationships. Such analyses assume knowledge of Mendelian inheritance, genotyping technologies, and basic statistical inference. Consequently, they can be difficult for students to grasp, particularly through traditional lecture formats. Here, we investigate whether integrating an additional active learning approach--interaction with a Shiny web application, DadApp, which implements a popular paternity inference approach in an accessible graphical user interface--improves student understanding of genetic kinship analysis in molecular primatology. We do so in the context of a non-traditional learning environment in Kenya, a developing nation in which students have limited access to technology, and where the efficacy of educational Shiny apps has never been assessed. Twenty-eight (28) participants with diverse educational backgrounds attended an introductory lecture on genetics and paternity inference, completed a pre-test, interacted with DadApp via a structured set of exercises and questions, and then completed a post-test and survey about their experience and subjective understanding. Post-test scores significantly improved relative to pre-test scores (p-value=3.75 x 10-6 . Further, student interest and confidence in the subject matter significantly increased after the practical session with DadApp. Our results suggest that Shiny web app-based active learning approaches have potential benefits in communicating complex topics in molecular primatology, including in resource-limited settings where such methods have not yet experienced high penetrance. Graphical Abstract*Images in the graphical abstract are courtesy of publicdomainpictures.net O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=111 SRC="FIGDIR/small/610690v1_ufig1.gif" ALT="Figure 1"> View larger version (19K): org.highwire.dtl.DTLVardef@5ce036org.highwire.dtl.DTLVardef@18429a0org.highwire.dtl.DTLVardef@1c8d997org.highwire.dtl.DTLVardef@1456624_HPS_FORMAT_FIGEXP M_FIG C_FIG

scientific communication and education↗

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↗