Biology subjects

Archie, E.

Publications and source records attributed to Archie, E..

12 recordsLinked to original sources

bioRxiv2025

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↗

bioRxiv2025

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↗

bioRxiv2024

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↗

bioRxiv2024

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↗

bioRxiv2023

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↗

bioRxiv2023

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↗

bioRxiv2022

Seeing the future: a better way to model and test for adaptive developmental plasticity

In many species, individuals who experience harsh conditions during development often have poor health and fitness outcomes in adulthood relative to peers who do not. There are two classes of evolutionary hypotheses for the origins of these early life contributors to inequality in adulthood: developmental constraints (DC) models, which focus on the deleterious effects of low-quality early-life environments, and predictive adaptive response (PAR) hypotheses, which emphasize the cost of mismatches between early and adult environments. Distinguishing DC and PAR models empirically is difficult for both conceptual and analytical reasons. Here, we resolve this difficulty by providing explicit mathematical definitions for DC, PARs, and related concepts, and propose a novel, quadratic regression-based statistical test derived from these definitions. Simulations show that this approach improves the ability to discriminate between DC and PAR hypotheses relative to a common alternative based on testing for interaction effects between developmental and adult environments. Simulated data indicate that the interaction effects approach often conflates PARs with DC, while the quadratic regression approach yields high sensitivity and specificity for detecting PARs. Our results highlight the value of linking verbal and visual models to a formal mathematical treatment for understanding the developmental origins of inequitable adult outcomes.

evolutionary biology↗

bioRxiv2021

Synchrony and idiosyncrasy in the gut microbiome of wild primates

Human gut microbial dynamics are highly individualized, making it challenging to link microbiota to health and to design universal microbiome therapies. This individuality is typically attributed to variation in host genetics, diets, environments, and medications, but it could also emerge from fundamental ecological forces that shape microbiota more generally. Here we leverage extensive gut microbial time series from wild baboons--hosts who experience little interindividual dietary and environmental heterogeneity--to test whether gut microbial dynamics are synchronized across hosts or largely idiosyncratic. Despite their shared lifestyles, baboon microbiome dynamics were only weakly synchronized. The strongest synchrony occurred among baboons living in the same social group, likely because group members range over the same habitat and simultaneously encounter the same sources of food and water. However, this synchrony was modest compared to each hosts personalized dynamics. Indeed, host-specific factors, especially host identity, explained 10 times the deviance in longitudinal microbial dynamics, compared to factors shared across hosts. These results contribute to mounting evidence that highly idiosyncratic gut microbiomes are not an artifact of modern human environments, and that synchronizing forces in the gut microbiome (e.g., shared environments, diets, and microbial dispersal) are often not strong enough to overwhelm drivers of microbiome personalization, including host genetics, priority effects, horizontal gene transfer, and functional redundancy.

ecology↗

bioRxiv2020

Primate phageomes are structured by superhost phylogeny and environment

The evolutionary origins of human-associated bacteriophage communities are poorly understood. To address this question, we examined fecal phageomes of 23 wild non-human primate taxa, including multiple representatives of all the major primate radiations, and find relatives of the majority of human-associated phages. Primate taxa have distinct phageome compositions that exhibit a clear phylosymbiotic signal, and phage-superhost co-divergence is detected for 44 individual phages. Within species, neighboring social groups harbor evolutionarily and compositionally distinct phageomes, structured by superhost social behavior. However, captive non-human primate phageomes are more similar to humans than their wild counterparts, revealing replacement of wild-associated phages with human-associated ones. Together, our results suggest that potentially labile primate-phage associations persisted across millions of years of evolution, potentially facilitated by transmission between groupmates. One Sentence SummaryRelatives of human-associated phages in wild primates reveal ancient but dynamic superhost-phage associations shaped by social transmission.

microbiology↗

bioRxiv2020

The costs of competition: high social status males experience accelerated epigenetic aging in wild baboons

Aging, for virtually all life, is inescapable. However, within populations, biological aging rates vary. Understanding sources of variation in this process is central to understanding the biodemography of natural populations. We constructed a DNA methylation-based age predictor for an intensively studied wild baboon population in Kenya. Consistent with findings in humans, the resulting "epigenetic clock" closely tracks chronological age, but individuals are predicted to be somewhat older or younger than their known ages. Surprisingly, these deviations are not explained by the strongest predictors of lifespan in this population, early adversity and social integration. Instead, they are best predicted by male dominance rank: high-ranking males are predicted to be older than their true ages, and epigenetic age tracks changes in rank over time. Our results argue that achieving high rank for male baboons--the best predictor of reproductive success--imposes costs consistent with a "live fast, die young" life history strategy.

genomics↗

bioRxiv2018

Vertical transmission of sponge microbiota is weak and inconsistent

Classic coevolutionary theory predicts that if beneficial microbial symbionts improve host fitness, they should be faithfully transmitted to offspring. More recently, the hologenome theory of evolution predicts resemblance between parent and offspring microbiomes and high partner fidelity between host species and their vertically transmitted microbes. Here, we test these ideas for the first time in multiple coexisting host species with highly diverse microbiota, leveraging known parent-offspring pairs sampled from eight species of wild marine sponges (Porifera). We found that the processes governing vertical transmission were both neutral and selective. A neutral model explained 66% of the variance in larval microbiota, which was higher than the variance this model explained for adult sponge microbiota (R2 = 27%). However, microbes that are enriched above neutral expectations in adults were disproportionately transferred to offspring. Patterns of vertical transmission were, however, incomplete: larval sponges shared, on average, 44.8% of microbes with their parents, which was not higher than the fraction they shared with nearby non-parental adults. Vertical transmission was also inconsistent across siblings, as larval sponges from the same parent only shared 17% of microbes. Finally, we found no evidence that vertically transmitted microbes are faithful to a single sponge host species. Surprisingly, larvae were just as likely to share vertically transmitted microbes with larvae from other sponge species as they were with their own species. Our study demonstrates that common predictions of vertical transmission that stem from species-poor systems are not necessarily true when scaling up to diverse and complex microbiomes.

ecology↗

bioRxiv2018

Dominance rank-associated immune gene expression is widespread, sex-specific, and a precursor to high social status in wild male baboons

In humans and other hierarchical species, social status is tightly linked to variation in health and fitness-related traits. Experimental manipulations of social status in female rhesus macaques suggest that this relationship is partially explained by status effects on immune gene regulation. However, social hierarchies are established and maintained in different ways across species: while some are based on kin-directed nepotism, others emerge from direct physical competition. We investigated how this variation influences the relationship between social status and immune gene regulation in wild baboons, where hierarchies in males are based on fighting ability but female hierarchies are nepotistic. We measured rank-related variation in gene expression levels in adult baboons of both sexes at baseline and in response to ex vivo stimulation with the bacterial endotoxin lipopolysaccharide (LPS). We identified >2000 rank- associated genes in males, an order of magnitude more than in females. In males, high status predicted increased expression of genes involved in innate immunity and preferential activation of the NFkB-mediated pro-inflammatory pathway, a pattern previously associated with low status in female rhesus macaques. Using Mendelian randomization, we reconcile these observations by demonstrating that high status-associated gene expression patterns are precursors, not consequences, of high social status in males, in support of the idea that physiological condition determines who attains high rank. Together, our work provides the first test of the relationship between social status and immune gene regulation in wild primates. It also emphasizes the importance of social context in shaping the relationship between social status and immune function.\n\nSIGNIFICANCESocial status predicts fitness outcomes in social animals, motivating efforts to understand its physiological causes and consequences. We investigated the relationship between social status and immune gene expression in wild baboons, where female status is determined by kinship but male status is determined by fighting ability. We uncover pervasive status-gene expression associations in males, but not females. High status males exhibit high levels of pro-inflammatory gene expression, in contrast to previous findings in hierarchies that are not competitively determined. Using Mendelian randomization, we show that this status-associated variation precedes dominance rank attainment: males who compete successfully for high status are already immunologically distinct. The nature of social hierarchies thus fundamentally shapes the relationship between social status and immune function.

evolutionary biology↗