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

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

Thyroid hormone concentrations in female baboons: Metabolic consequences of living in a highly seasonal environment.

How female mammals adapt metabolically in response to environmental variation remains understudied in the wild, because direct measures of metabolic activity are difficult to obtain in wild populations. However, recent advances in the non-invasive measurement of fecal thyroid hormones, triiodothyronine (T3), an important regulator of metabolism, provide an opportunity to understand how female baboons living in the harsh Amboseli ecosystem in southern Kenya adapt to environmental variability and escape strict reproductive seasonality. Specifically, we assessed how a female's activity budget, diet, and concentrations of fecal T3 metabolites (mT3) changed over the course of the year and between years. We then tested which of several environmental variables (season, rainfall, and temperature) and behavioral variables (female activity budget and diet) best predicted mT3 concentrations. Finally, we determined if two important reproductive events - onset of ovarian cycling and conception of an offspring - were preceded by changes in female mT3 concentrations. We found female baboons' mT3 concentrations varied markedly across the year and between years as a function of environmental conditions. Further, changes in a female's behavior and diet only partially mediated the metabolic response to the environment. Finally, mT3 concentrations increased in the weeks prior to menarche and cycling resumption, regardless of the month or season in which cycling started. This pattern indicates that metabolic activation may be an indicator of reproductive readiness in female baboons as their energy balance is restored.

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

AbstractOver the past 50 years, a wealth of testable, often conflicting hypotheses have been generated about the evolution of offspring sex ratio manipulation by mothers. Several of these hypotheses have received support in studies of invertebrates and some vertebrate taxa. However, their success in explaining sex ratios in mammalian taxa-especially in primates-has been mixed. Here, we assess the predictions of four different hypotheses about the evolution of biased offspring sex ratios in the baboons of the Amboseli basin in Kenya: the Trivers-Willard, female rank enhancement, local resource competition, and local resource enhancement hypotheses. Using the largest sample size ever analyzed in a primate population (n=1,372 offspring), we test the predictions of each hypothesis. Overall, we find no support for adaptive biasing of sex ratios. Offspring sex is not consistently related to maternal dominance rank or biased toward the dispersing sex, nor is it predicted by group size, population growth rates, or their interaction with maternal rank. Because our sample size confers power to detect even subtle biases in sex ratio, including modulation by environmental heterogeneity, these results suggest that adaptive biasing of offspring sex does not occur in this population.

Selection against admixture and gene regulatory divergence in a long-term primate field study.

Genetic admixture is central to primate evolution. We combined 50 years of field observations of immigration and group demography with genomic data from ~9 generations of hybrid baboons to investigate the consequences of admixture in the wild. Despite no obvious fitness costs to hybrids, we found signatures of selection against admixture similar to those described for archaic hominins. These patterns were concentrated near genes where ancestry is strongly associated with gene expression. Our analyses also show that introgression is partially predictable across the genome. This study demonstrates the value of integrating genomic and field data for revealing how "genomic signatures of selection" (e.g., reduced introgression in low-recombination regions) manifest in nature; moreover, it underscores the importance of other primates as living models for human evolution.

Mechanisms of inbreeding avoidance in a wild primate.

Inbreeding often imposes net fitness costs,1-5 leading to the expectation that animals will engage in inbreeding avoidance when the costs of doing so are not prohibitive.4-9 However, one recent meta-analysis indicates that animals of many species do not avoid mating with kin in experimental settings,6 and another reports that behavioral inbreeding avoidance generally evolves only when kin regularly encounter each other and inbreeding costs are high.9 These results raise questions about the processes that separate kin, how these processes depend on kin class and context, and whether kin classes differ in how effectively they avoid inbreeding via mate choice-in turn, demanding detailed demographic and behavioral data within individual populations. Here, we address these questions in a wild mammal population, the baboons of the Amboseli ecosystem in Kenya. We find that death and dispersal are very effective at separating opposite-sex pairs of close adult kin. Nonetheless, adult kin pairs do sometimes co-reside, and we find strong evidence for inbreeding avoidance via mate choice in kin classes with relatedness ≥0.25. Notably, maternal kin avoid inbreeding more effectively than paternal kin despite having identical coefficients of relatedness, pointing to kin discrimination as a potential constraint on effective inbreeding avoidance. Overall, demographic and behavioral processes ensure that inbred offspring are rare in undisturbed social groups (1% of offspring). However, in an anthropogenically disturbed social group with reduced male dispersal, we find inbreeding rates 10× higher. Our study reinforces the importance of demographic and behavioral contexts for understanding the evolution of inbreeding avoidance.9.

Gut microbiome heritability is nearly universal but environmentally contingent.

Relatives have more similar gut microbiomes than nonrelatives, but the degree to which this similarity results from shared genotypes versus shared environments has been controversial. Here, we leveraged 16,234 gut microbiome profiles, collected over 14 years from 585 wild baboons, to reveal that host genetic effects on the gut microbiome are nearly universal. Controlling for diet, age, and socioecological variation, 97% of microbiome phenotypes were significantly heritable, including several reported as heritable in humans. Heritability was typically low (mean = 0.068) but was systematically greater in the dry season, with low diet diversity, and in older hosts. We show that longitudinal profiles and large sample sizes are crucial to quantifying microbiome heritability, and indicate scope for selection on microbiome characteristics as a host phenotype.

Higher dominance rank is associated with lower glucocorticoids in wild female baboons: A rank metric comparison.

In vertebrates, glucocorticoid secretion occurs in response to energetic and psychosocial stressors that trigger the hypothalamic-pituitary-adrenal (HPA) axis. Measuring glucocorticoid concentrations can therefore shed light on the stressors associated with different social and environmental variables, including dominance rank. Using 14,172 fecal samples from 237 wild female baboons, we test the hypothesis that high-ranking females experience fewer psychosocial and/or energetic stressors than lower-ranking females. We predicted that high-ranking females would have lower fecal glucocorticoid (fGC) concentrations than low-ranking females. Because dominance rank can be measured in multiple ways, we employ an information theoretic approach to compare 5 different measures of rank as predictors of fGC concentrations: ordinal rank; proportional rank; Elo rating; and two approaches to categorical ranking (alpha vs non-alpha and high-middle-low). Our hypothesis was supported, but it was also too simplistic. We found that alpha females exhibited substantially lower fGCs than other females (typical reduction = 8.2%). If we used proportional rank instead of alpha versus non-alpha status in the model, we observed a weak effect of rank such that fGCs rose 4.2% from the highest- to lowest-ranking female in the hierarchy. Models using ordinal rank, Elo rating, or high-middle-low categories alone failed to explain variation in female fGCs. Our findings shed new light on the association between dominance rank and the stress response, the competitive landscape of female baboons as compared to males, and the assumptions inherent in a researcher's choice of rank metric.