Natural disaster and immunological aging in a nonhuman primate.

Weather-related disasters are increasing in frequency and severity, leaving survivors to cope with ensuing mental, financial, and physical hardships. This adversity can exacerbate existing morbidities, trigger new ones, and increase the risk of mortality-features that are also characteristic of advanced age-inviting the hypothesis that extreme weather events may accelerate aging. To test this idea, we examined the impact of Hurricane Maria and its aftermath on immune cell gene expression in large, age-matched, cross-sectional samples from free-ranging rhesus macaques (Macaca mulatta) living on an isolated island. A cross section of macaques was sampled 1 to 4 y before (n = 435) and 1 y after (n = 108) the hurricane. Hurricane Maria was significantly associated with differential expression of 4% of immune-cell-expressed genes, and these effects were correlated with age-associated alterations in gene expression. We further found that individuals exposed to the hurricane had a gene expression profile that was, on average, 1.96 y older than individuals that were not-roughly equivalent to an increase in 7 to 8 y of a human life. Living through an intense hurricane and its aftermath was associated with expression of key immune genes, dysregulated proteostasis networks, and greater expression of inflammatory immune cell-specific marker genes. Together, our findings illuminate potential mechanisms through which the adversity unleashed by extreme weather and potentially other natural disasters might become biologically embedded, accelerate age-related molecular immune phenotypes, and ultimately contribute to earlier onset of disease and death.

Assessing Variance in Male Reproductive Skew Based on Long-Term Data in Free-Ranging Rhesus Macaques.

The unequal share in male reproduction (male reproductive skew) has been reported across primate species. To explain the distribution of male reproduction within groups various skew models have been applied to primates, however the "dynamic tug-of-war" model first accounted for the specifics of primate sociality. This model assumes that an increase in the number of competing males, a high degree of female cycle synchrony and their interaction will result in a lower degree of male reproductive skew. Here, we first tested the predictors of this model in rhesus macaques (Macaca mulatta) using long-term demographic and genetic data (up to 9 groups over 22 seasons) of the Cayo Santiago population (Puerto Rico). We also tested an extended version including group size and sex ratio and their interaction with female cycle synchrony. Finally, we investigated which male attributes determine the probability to become a top sire (highest paternity share per group and season). Confirming studies, male rhesus macaques exhibited low to medium degrees of reproductive skew based on the multinomial index, M. Unlike predicted, reproductive skew was higher in groups with more males. The extended analysis suggested that reproductive skew increased with group size in more male-biased groups, but decreased with group size in female-biased groups indicating that the numbers of male and female group members matter. We detected no effect of female cycle synchrony on the variance of reproductive skew. Finally, only maternal rank predicted the probability to become a top sire as long as males resided in their natal group. Together, our results did not support predictions by the dynamic skew model in rhesus macaques, but strengthen studies suggesting that other factors in addition to male-male competition predict male reproductive output in rhesus macaques. Future skew studies should consider female choice and alternative male mating strategies.

Higher offspring mortality with short interbirth intervals in free-ranging rhesus macaques.

Short birth intervals have long been linked to adverse child outcomes in humans. However, it remains unclear the extent to which the birth interval has a direct influence on offspring mortality, independent of the confounding effects of modern environments and human sociocultural practices on reproductive behavior. Outside of humans, the relationship between birth intervals and offspring mortality has been rarely tested, leaving an open question of how much the findings from humans imply evolutionarily conserved mechanisms. Here, using ∼9,000 birth records from ∼1,400 free-ranging rhesus macaque mothers, we show that short birth intervals preceding or succeeding the birth of an offspring are both associated with higher offspring mortality, after controlling for heterogeneity across mothers and birth cohorts. We clarify that the mortality risk of a short birth interval to an offspring is contingent on the survival of its older or younger sibling, the condition that reduces maternal resources for investment in the offspring. This finding suggests that life-history tradeoffs between offspring quantity (a short birth interval) and quality (offspring survival) form an evolutionary force shaping variation in birth intervals. Consistent with the well-known observation made in humans, we also found a nonlinear relationship between the preceding interbirth interval and infant mortality. The overall congruence with the findings from the human literature indicates a robust relationship between birth intervals and offspring mortality.

The observed pattern and hidden process of female reproductive trajectories across the life span in a non-human primate.

Age-specific fertility trajectories are fundamental to understanding population structure and the evolutionary ecology of diverse life histories. However, characterizing reproductive ageing has been difficult with cross-sectional data, where senescence especially late in life can be confounded by selective disappearance. Addressing such challenge requires longitudinal data tracking the reproductive life span of known individuals, but such data are rare, especially for very long-lived species such as primates. We analyse the entire life span trajectory of annual fertility, from reproductive maturity to death, for 673 free-ranging female rhesus macaques, Macaca mulatta, on Cayo Santiago, Puerto Rico. Using generalized linear mixed-effects models (GLMMs), we first tested if time to death explains the ageing pattern independently of and additionally to chronological age, and if so, whether there is interaction between them. While GLMM captures the patterns in the data well, it is not a generative model. For example, given the GLMM and an individual's reproductive trajectory up to a given age, we cannot directly predict the probability of reproduction or death in the next year. For this reason, we further fitted a hidden Markov chain model (HMM) which allows just such a prediction, and additionally helps infer the process underlying the observed trajectory. We show that, after accounting for individual differences in fertility, reproductive ageing exhibits both age-dependent decline and also an abrupt terminal decline independently of age at death. We infer from the HMM that the underlying process of reproductive trajectory is where individuals cycle between reproductive bouts until they enter an irreversible frail condition that constrains fertility. The findings provide valuable insights into the longitudinal progression of reproductive trajectories in primates, by revealing both age-dependent and age-independent patterns and processes of ageing, and contribute to a growing body of literature on reproductive ageing and senescence across animal taxa.

Las trayectorias de fertilidad específicas de la edad son pieza clave en los estudios que pretenden entender la estructura de la población y la ecología evolutiva de las diversas historias de vida. Sin embargo, la caracterización del envejecimiento reproductivo ha sido difícil con datos transversales, en los que los patrones asociados a la edad avanzada, como la senescencia, pueden verse confundidos por la desaparición selectiva. Los datos longitudinales que rastrean la vida reproductiva de individuos específicos son fundamentales, pero tales datos son escasos, especialmente para especies muy longevas como los primates. En este estudio analizamos la trayectoria completa de la fertilidad anual, desde la madurez reproductiva hasta la muerte, de 673 macaco rhesus (Macaca mulatta) hembras que habitan libremente la isla de Cayo Santiago, Puerto Rico. Mostramos que, después de tener en cuenta las diferencias individuales en la fertilidad, el envejecimiento reproductivo exhibe tanto un declive dependiente de la edad, como un declive terminal abrupto independiente de la edad al morir. Aplicando un modelo de cadena de Markov oculta, caracterizamos además el proceso reproductivo subyacente, en el que los individuos pasan por ciclos reproductivos hasta que entran en una condición de fragilidad irreversible que limita la fertilidad. Los resultados proporcionan una valiosa visión de la progresión longitudinal de las trayectorias reproductivas en los primates, al revelar patrones y procesos de senescencia dependientes e independientes de la edad, y contribuyen a un creciente cuerpo de literatura sobre el envejecimiento reproductivo en todos los taxones animales.

Deconstructing sociality: the types of social connections that predict longevity in a group-living primate.

Many species use social interactions to cope with challenges in their environment and a growing number of studies show that individuals which are well-connected to their group have higher fitness than socially isolated individuals. However, there are many ways to be 'well-connected' and it is unclear which aspects of sociality drive fitness benefits. Being well-connected can be conceptualized in four main ways: individuals can be socially integrated by engaging in a high rate of social behaviour or having many partners; they can have strong and stable connections to favoured partners; they can indirectly connect to the broader group structure; or directly engage in a high rate of beneficial behaviours, such as grooming. In this study, we use survival models and long-term data in adult female rhesus macaques (Macaca mulatta) to compare the fitness outcomes of multiple measures of social connectedness. Females that maintained strong connections to favoured partners had the highest relative survival probability, as did females well-integrated owing to forming many weak connections. We found no survival benefits to being structurally well-connected or engaging in high rates of grooming. Being well-connected to favoured partners could provide fitness benefits by, for example, increasing the efficacy of coordinated or mutualistic behaviours.

Discovery of a secular trend in Cayo Santiago macaque reproduction.

Reproductive synchrony and the consequent clustering of births are hypothesized to be regulated by seasonal changes in rainfall and food availability. Such climate-related seasonality is, however, questionable in tropical populations occupying temporally invariant habitats year round. Using the long-term data of the Cayo Santiago rhesus macaques from 1973 to 2013, this study distinguishes synchrony (a greater than chance clustering of births) from seasonality (a cluster of births during a period of the year when abiotic conditions are favorable) and shows that females are highly synchronized (>72% of births in a 3-month period) but the effects of environmental zeitgebers on reproduction are overridden by biological factors. Specifically, biotic and abiotic factors including (i) loss of immature offspring; (ii) population density; (iii) age at delivery; (iv) rainfall; and (v) changes in colony management were modeled in relation to the annual onset of births and the median birth date. Females experiencing loss of immature offspring had an interbirth interval of <365 days in average and the proportion of these females increased up to 48% due to changes in colony management overtime, although reproductive synchrony increased with increasing population density. A secular trend in both the onset of births and the median date of birth is documented and the model predicts that the median birth date will advance across all calendar-based seasons by 2050. The secular trend in reproduction appears to be triggered by changes in the age at delivery of females, the absence of physiological constraints from maternal investment due to offspring loss, shorter interbirth interval, and a higher degree of coordination due to increasing population density. This study challenges the reproductive phenology previously described for rhesus macaques highlighting the importance of long-term studies in addressing the ultimate causes of reproductive synchrony.

Managing the Cayo Santiago rhesus macaque population: The role of density.

Cayo Santiago is the oldest continuously operating free-ranging rhesus monkey colony in the world. Population control of this colony has historically been carried out by periodic live capture and removal of animals. However, the effect of such a strategy on the size, growth rate, age structure, and sex ratio of the population has not been analyzed. This study reviews past removal data and uses a population projection model to simulate the effects of different removal schemes based on Cayo Santiago demographic data from 2000-2012. The model incorporates negative density-dependence in female fertility, as well as male and female survival rates, to determine the population-level effects of selective removal by age and sex. Modeling revealed that removal of sexually immature individuals has negligible effects on the population dynamics explaining why with an initial population of 1309 in 2000 and annual removals of immature monkeys a mean annual population growth rate of 12% and a final population size of ∼1,435 individuals by 2012 (∼0.009 animal/m(2) ) was observed. With no removals, the population is expected to exhibit dampened oscillations until reaching equilibrium at ∼1,690 individuals (∼0.0111 animal/m(2) ) in 2,100. In contrast, removal of adult females (≥4 yrs) would significantly reduce the population size, but would also promote an increase in population growth rate due to density feedback. A maximum annual production of 275 births is expected when 550 adult females are present in the population. Sensitivity analyses showed that removing females, in contrast to controlling their fertility through invasive treatments would contribute the most to changes in population growth rate. Given the density compensation on fertility, stabilizing the population would require removing ∼80% of the current population of adult females. This study highlights the importance of addressing the population-level density effects, as well as sensitivity analyses, to optimize management strategies.

Female rhesus macaques discriminate unfamiliar paternal sisters in playback experiments: support for acoustic phenotype matching.

Widespread evidence exists that when relatives live together, kinship plays a central role in shaping the evolution of social behaviour. Previous studies showed that female rhesus macaques (Macaca mulatta) recognize familiar maternal kin using vocal cues. Recognizing paternal kin might, however, be more difficult as rhesus females mate promiscuously during the possible conception period, most probably concealing paternity. Behavioural observations indicate that semi free-ranging female rhesus macaques prefer to associate with their paternal half-sisters in comparison to unrelated females within the same group, particularly when born within the same age cohort. However, the cues and mechanism/s used in paternal kin discrimination remain under debate. Here, we investigated whether female rhesus macaques use the acoustic modality to discriminate between paternal half-sisters and non-kin, and tested familiarity and phenotype matching as the underlying mechanisms. We found that test females responded more often to calls of paternal half-sisters compared with calls of unrelated females, and that this discrimination ability was independent of the level of familiarity between callers and test females, which provides, to our knowledge, the first evidence for acoustic phenotype matching. Our study strengthens the evidence that female rhesus macaques can recognize their paternal kin, and that vocalizations are used as a cue.

Sexually selected skin colour is heritable and related to fecundity in a non-human primate.

Sexual selection promotes the prevalence of heritable traits that increase an individual's reproductive rate. Despite theoretically strong directional selection, sexually selected traits can show inter-individual variation. Here, we investigate whether red skin ornamentation, a rare example of a male mammalian trait involved in mate attraction, influences fecundity and is heritable in rhesus macaques (Macaca mulatta), and explore the mechanisms that are involved in maintaining trait variation. Interestingly, the trait is expressed by and is attractive to both sexes. We collected facial images of 266 free-ranging individuals and modelled skin redness and darkness to rhesus macaque vision. We used 20 years of genetic parentage data to calculate selection gradients on the trait and perform heritability analyses. Results show that males who were both darkly coloured and high-ranking enjoyed higher fecundity. Female skin redness was positively linked to fecundity, although it remains unclear whether this influences male selectiveness. Heritability explained 10-15% of the variation in redness and darkness, and up to 30% for skin darkness when sexes are considered separately, suggesting sex-influenced inheritance. Our results suggest that inter-individual variation is maintained through condition-dependence, with an added effect of balancing selection on male skin darkness, providing rare evidence for a mammalian trait selected through inter-sexual selection.

Facial and genital color ornamentation, testosterone, and reproductive output in high-ranking male rhesus macaques.

Males in many vertebrate species have colorful ornaments that evolved by sexual selection. The role of androgens in the genesis and maintenance of these signals is unclear. We studied 21 adult high-ranking male rhesus macaques from nine social groups in the free-ranging population on Cayo Santiago, Puerto Rico, and analyzed facial and genital skin luminance and redness, fecal androgens, rates of mating behaviors, and offspring sired. Facial and genital coloration varied in relation to age, mating behavior, reproductive success, and testosterone concentration. Our results indicate that skin coloration in high-ranking male rhesus macaques is a sexually-selected trait mediated by androgens. These results add to the growing literature on the proximate and ultimate causes of male sexual signals and highlight the need to examine how these characteristics change with age in other species.

Socioecological drivers of injuries in female and male rhesus macaques (Macaca mulatta).

Competition over access to resources, such as food and mates, is believed to be one of the major costs associated with group living. Two socioecological factors suggested to predict the intensity of competition are group size and the relative abundance of sexually active individuals. However, empirical evidence linking these factors to injuries and survival costs is scarce. Here, we leveraged 10 years of data from free-ranging rhesus macaques where injuries inflicted by conspecifics are associated with a high mortality risk. We tested if group size and adult sex ratio predicted the occurrence of injuries and used data on physical aggression to contextualise these results. We found that males were less likely to be injured when living in larger groups, potentially due to advantages in intergroup encounters. Females, instead, had higher injury risk when living in larger groups but this was not explained by within-group aggression among females. Further, male-biased sex ratios predicted a weak increase in injury risk in females and were positively related to male-female aggression, indicating that male coercion during mating competition may be a cause of injuries in females. Overall, our results provide insights into sex differences in the fitness-related costs of competition and empirical evidence for long-standing predictions on the evolution of group living.

Taking identity-by-descent analysis into the wild: Estimating realized relatedness in free-ranging macaques.

Biological relatedness is a key consideration in studies of behavior, population structure, and trait evolution. Except for parent-offspring dyads, pedigrees capture relatedness imperfectly. The number and length of DNA segments that are identical-by-descent (IBD) yield the most precise estimates of relatedness. Here, we leverage novel methods for estimating locus-specific IBD from low coverage whole genome resequencing data to demonstrate the feasibility and value of resolving fine-scaled gradients of relatedness in free-living animals. Using primarily 4-6× coverage data from a rhesus macaque (Macaca mulatta) population with available long-term pedigree data, we show that we can call the number and length of IBD segments across the genome with high accuracy even at 0.5× coverage. The resulting estimates demonstrate substantial variation in genetic relatedness within kin classes, leading to overlapping distributions between kin classes. They identify cryptic genetic relatives that are not represented in the pedigree and reveal elevated recombination rates in females relative to males, which allows us to discriminate maternal and paternal kin using genotype data alone. Our findings represent a breakthrough in the ability to understand the predictors and consequences of genetic relatedness in natural populations, contributing to our understanding of a fundamental component of population structure in the wild.

Early life adversity has sex-dependent effects on survival across the lifespan in rhesus macaques.

Exposure to early life adversity is linked to detrimental fitness outcomes across taxa. Owing to the challenges of collecting longitudinal data, direct evidence for long-term fitness effects of early life adversity from long-lived species remains relatively scarce. Here, we test the effects of early life adversity on male and female longevity in a free-ranging population of rhesus macaques (Macaca mulatta) on Cayo Santiago, Puerto Rico. We leveraged six decades of data to quantify the relative importance of 10 forms of early life adversity for 6599 macaques. Individuals that experienced more early life adversity died earlier than those that experienced less adversity. Mortality risk was highest during early life, defined as birth to 4 years old, but heightened mortality risk was also present in macaques that survived to adulthood. Females and males were affected differently by some forms of adversity, and these differences might be driven by varying energetic demands and dispersal patterns. Our results show that the fitness consequences of early life adversity are not uniform across individuals but vary as a function of the type of adversity, timing and social context, and thus contribute to our limited but growing understanding of the evolution of early life sensitivities.This article is part of the discussion meeting issue 'Understanding age and society using natural populations'.

Immune cell composition varies by age, sex and exposure to social adversity in free-ranging Rhesus Macaques.

Increasing age is associated with dysregulated immune function and increased inflammation-patterns that are also observed in individuals exposed to chronic social adversity. Yet we still know little about how social adversity impacts the immune system and how it might promote age-related diseases. Here, we investigated how immune cell diversity varied with age, sex and social adversity (operationalized as low social status) in free-ranging rhesus macaques. We found age-related signatures of immunosenescence, including lower proportions of CD20 + B cells, CD20 + /CD3 + ratio, and CD4 + /CD8 + T cell ratio - all signs of diminished antibody production. Age was associated with higher proportions of CD3 + /CD8 + Cytotoxic T cells, CD16 + /CD3- Natural Killer cells, CD3 + /CD4 + /CD25 + and CD3 + /CD8 + /CD25 + T cells, and CD14 + /CD16 + /HLA-DR + intermediate monocytes, and lower levels of CD14 + /CD16-/HLA-DR + classical monocytes, indicating greater amounts of inflammation and immune dysregulation. We also found a sex-dependent effect of exposure to social adversity (i.e., low social status). High-status males, relative to females, had higher CD20 + /CD3 + ratios and CD16 + /CD3 Natural Killer cell proportions, and lower proportions of CD8 + Cytotoxic T cells. Further, low-status females had higher proportions of cytotoxic T cells than high-status females, while the opposite was observed in males. High-status males had higher CD20 + /CD3 + ratios than low-status males. Together, our study identifies the strong age and sex-dependent effects of social adversity on immune cell proportions in a human-relevant primate model. Thus, these results provide novel insights into the combined effects of demography and social adversity on immunity and their potential contribution to age-related diseases in humans and other animals.

Evolutionary and biomedical implications of sex differences in the primate brain transcriptome.

Humans exhibit sex differences in the prevalence of many neurodevelopmental disorders and neurodegenerative diseases. Here, we generated one of the largest multi-brain-region bulk transcriptional datasets for the rhesus macaque and characterized sex-biased gene expression patterns to investigate the translatability of this species for sex-biased neurological conditions. We identify patterns similar to those in humans, which are associated with overlapping regulatory mechanisms, biological processes, and genes implicated in sex-biased human disorders, including autism. We also show that sex-biased genes exhibit greater genetic variance for expression and more tissue-specific expression patterns, which may facilitate rapid evolution of sex-biased genes. Our findings provide insights into the biological mechanisms underlying sex-biased disease and support the rhesus macaque model for the translational study of these conditions.

Demographic variability and density-dependent dynamics of a free-ranging rhesus macaque population.

Density-dependence is hypothesized as the major mechanism of population regulation. However, the lack of long-term demographic data has hampered the use of density-dependent models in nonhuman primates. In this study, we make use of the long-term demographic data from Cayo Santiago's rhesus macaques to parameterize and analyze both a density-independent and a density-dependent population matrix model, and compare their projections with the observed population changes. We also employ a retrospective analysis to determine how variance in vital rates, and covariance among them, contributed to the observed variation in long-term fitness across different levels of population density. The population exhibited negative density-dependence in fertility and the model incorporating this relationship accounted for 98% of the observed population dynamics. Variation in survival and fertility of sexually active individuals contributed the most to the variation in long-term fitness, while vital rates displaying high temporal variability exhibited lower sensitivities. Our findings are novel in describing density-dependent dynamics in a provisioned primate population, and in suggesting that selection is acting to lower the variance in the population growth rate by minimizing the variation in adult survival at high density. Because density-dependent mechanisms may become stronger in wild primate populations due to increasing habitat loss and food scarcity, our study demonstrates that it is important to incorporate variation in population size, as well as demographic variability into population viability analyses for a better understanding of the mechanisms regulating the growth of primate populations.

Yearly variation coupled with social interactions shape the skin microbiome in free-ranging rhesus macaques.

While skin microbes are known to mediate human health and disease, there has been minimal research on the interactions between skin microbiota, social behavior, and year-to-year effects in non-human primates-important animal models for translational biomedical research. To examine these relationships, we analyzed skin microbes from 78 rhesus macaques living on Cayo Santiago Island, Puerto Rico. We considered age, sex, and social group membership, and characterized social behavior by assessing dominance rank and patterns of grooming as compared to nonsocial behaviors. To measure the effects of a shifting environment, we sampled skin microbiota (based on sequence analysis of the 16S rRNA V4 region) and assessed weather across sampling periods between 2013 and 2015. We hypothesized that, first, monkeys with similar social behavior and/or in the same social group would possess similar skin microbial composition due, in part, to physical contact, and, second, microbial diversity would differ across sampling periods. We found significant phylum-level differences between social groups in the core microbiome as well as an association between total grooming rates and alpha diversity in the complete microbiome, but no association between microbial diversity and measures of rank or other nonsocial behaviors. We also identified alpha and beta diversity differences in microbiota and differential taxa abundance across two sampling periods. Our findings indicate that social dynamics interact with yearly environmental changes to shape the skin microbiota in rhesus macaques, with potential implications for understanding the factors affecting the microbiome in humans, which share many biological and social characteristics with these animals. IMPORTANCE Primate studies are valuable for translational and evolutionary insights into the human microbiome. The majority of primate microbiome studies focus on the gut, so less is known about the factors impacting the microbes on skin and how their links affect health and behavior. Here, we probe the impact of social interactions and the yearly environmental changes on food-provisioned, free-ranging monkeys living on a small island. We expected animals that lived together and groomed each other would have more similar microbes on their skin, but surprisingly found that the external environment was a stronger influence on skin microbiome composition. These findings have implications for our understanding of the human skin microbiome, including potential manipulations to improve health and treat disease.

Early life adversity has sex-dependent effects on survival across the lifespan in rhesus macaques.

Exposure to adversity during early life is linked to lasting detrimental effects on evolutionary fitness across many taxa. However, due to the challenges of collecting longitudinal data, especially in species where one sex disperses, direct evidence from long-lived species remains relatively scarce. Here we test the effects of early life adversity on male and female longevity in a free-ranging population of rhesus macaques (Macaca mulatta) at Cayo Santiago, Puerto Rico. We leveraged six decades of data to quantify the relative importance of ten forms of early life adversity for 6,599 macaques (3,230 male, 3,369 female), with a smaller sample size (N=299) for one form of adversity (maternal social isolation) which required high-resolution behavioral data. We found that individuals who experienced more early life adversity died earlier than those who experienced less adversity. Mortality risk was highest during early life, defined as birth to four years old, suggesting acute survival effects of adversity, but heightened mortality risk was also present in macaques who survived to adulthood. Females and males were affected differently by some forms of adversity, and these differences might be driven by varying energetic demands, female philopatry, and male dispersal. By leveraging data on thousands of macaques collected over decades, our results show that the fitness consequences of early life adversity are not uniform across individuals but vary as a function of the type of adversity, timing, and social context, and thus contribute to our limited but growing understanding of the evolution of early life sensitivities in long-lived species.

Reduced injury risk links sociality to survival in a group-living primate.

Sociality has been linked to a longer lifespan in many mammals, including humans. Yet, how sociality results in survival benefits remains unclear. Using 10 years of data and over 1,000 recorded injuries in rhesus macaques (Macaca mulatta), we tested two injury-related mechanisms by which social status and affiliative partners might influence survival. Injuries increased individual risk of death by 3-fold in this dataset. We found that sociality can affect individuals' survival by reducing their risk of injury but had no effect on the probability of injured individuals dying. Both males and females of high social status (measured as female matrilineal rank and male group tenure) and females with more affiliative partners (estimated using the number of female relatives) experienced fewer injuries and thus were less likely to die. Collectively, our results offer rare insights into one mechanism that can mediate the well-known benefits of sociality on an individual's fitness.

Multiregion transcriptomic profiling of the primate brain reveals signatures of aging and the social environment.

Aging is accompanied by a host of social and biological changes that correlate with behavior, cognitive health and susceptibility to neurodegenerative disease. To understand trajectories of brain aging in a primate, we generated a multiregion bulk (N = 527 samples) and single-nucleus (N = 24 samples) brain transcriptional dataset encompassing 15 brain regions and both sexes in a unique population of free-ranging, behaviorally phenotyped rhesus macaques. We demonstrate that age-related changes in the level and variance of gene expression occur in genes associated with neural functions and neurological diseases, including Alzheimer's disease. Further, we show that higher social status in females is associated with younger relative transcriptional ages, providing a link between the social environment and aging in the brain. Our findings lend insight into biological mechanisms underlying brain aging in a nonhuman primate model of human behavior, cognition and health.