High early lactational synchrony within baboon groups predicts increased infant mortality.

Social group composition can have fitness implications for group members by determining opportunities for affiliative and competitive interactions. Female-female competition may be particularly acute when many groupmates have young infants at the same time, with potential consequences for infant survival. Here, we used decades of data on wild baboons (Papio sp.) in Amboseli, Kenya, to examine the effects of 'early lactational synchrony' (here, 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 an energetically demanding time for mothers and a risky time for infants, we expected early lactational synchrony to produce intensified competition for food and/or male protectors, resulting in more frequent female-female agonistic interactions and high infant mortality. In support of these predictions, we found that the frequency of female-female agonistic interactions increased with increasing early lactational synchrony. Reproductive state affected this relationship: while females in all states (cycling, pregnant, and postpartum amenorrhea) initiated more agonistic interactions when early lactational synchrony was high, only females in postpartum amenorrhea (including, but not limited to, females in early lactation) received more agonistic interactions. Furthermore, while high early lactational synchrony was rare, it strongly predicted infant mortality. This association may result from both aggression among adult females and infanticidal behavior by peripubertal females. These findings provide novel evidence that social dynamics may shape reproductive phenology in a nonseasonal breeder. Specifically, both competition among reproductive females and harassment from nonreproductive females may select against synchronous reproduction.

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.

Social and environmental predictors of gut microbiome age in wild baboons.

Understanding why some individuals age faster than others is essential to evolutionary biology and geroscience, but measuring variation in biological age is difficult. One solution may lie in measuring gut microbiome composition because microbiota change with many age-related factors (e.g., immunity and behavior). Here we create 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 clock's predictions are linked to 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 high social status (both sexes). However, an individual's "microbiome age" does not predict the attainment of developmental milestones or lifespan. Hence, the microbiome clock accurately reflects age and some social and environmental conditions, but not the pace of development or mortality risk.

A female-biased gene expression signature of dominance in cooperatively breeding meerkats.

Dominance is a primary determinant of social dynamics and resource access in social animals. Recent studies show that dominance is also reflected in the gene regulatory profiles of peripheral immune cells. However, the strength and direction of this relationship differs across the species and sex combinations investigated, potentially due to variation in the predictors and energetic consequences of dominance status. Here, we investigated the association between social status and gene expression in the blood of wild meerkats (Suricata suricatta; n = 113 individuals), including in response to lipopolysaccharide, Gardiquimod (an agonist of TLR7, which detects single-stranded RNA in vivo) and glucocorticoid stimulation. Meerkats are cooperatively breeding social carnivores in which breeding females physically outcompete other females to suppress reproduction, resulting in high reproductive skew. They therefore present an opportunity to disentangle the effects of social dominance from those of sex per se. We identify a sex-specific signature of dominance, including 1045 differentially expressed genes in females but none in males. Dominant females exhibit elevated activity in innate immune pathways and a larger fold-change response to LPS challenge. Based on these results and a preliminary comparison to other mammals, we speculate that the gene regulatory signature of social status in the immune system depends on the determinants and energetic costs of social dominance, such that it is most pronounced in hierarchies where physical competition is important and reproductive skew is large. Such a pattern has the potential to mediate life history trade-offs between investment in reproduction versus somatic maintenance.

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. However, social microbiome transmission can be difficult to identify if social partners also have other traits in common or live in a shared environment. Strain-resolved metagenomics has been proposed as a solution for tracking microbial transmission. Using a fecal microbiota transplant dataset, we show that strain sharing can recapitulate true transmission networks under ideal settings when donor-recipient pairs are unambiguous. However, gut metagenomes from a wild baboon population, where social networks predict compositional similarity, show that strain sharing is also driven by demographic and environmental factors that can override signals of social interactions. 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 conclusions about the underlying mechanisms.

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 infant's 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.

Testing frameworks for early life effects: the developmental constraints and adaptive response hypotheses 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.

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.