Within-individual changes reveal increasing social selectivity with age in rhesus macaques.

Accumulating evidence in humans and other mammals suggests older individuals tend to have smaller social networks. Uncovering the cause of these declines can inform how changes in social relationships with age affect health and fitness in later life. While age-based declines in social networks have been thought to be detrimental, physical and physiological limitations associated with age may lead older individuals to adjust their social behavior and be more selective in partner choice. Greater selectivity with age has been shown in humans, but the extent to which this phenomenon occurs across the animal kingdom remains an open question. Using longitudinal data from a population of rhesus macaques on Cayo Santiago, we provide compelling evidence in a nonhuman animal for within-individual increases in social selectivity with age. Our analyses revealed that adult female macaques actively reduced the size of their networks as they aged and focused on partners previously linked to fitness benefits, including kin and partners to whom they were strongly and consistently connected earlier in life. Females spent similar amounts of time socializing as they aged, suggesting that network shrinkage does not result from lack of motivation or ability to engage, nor was this narrowing driven by the deaths of social partners. Furthermore, females remained attractive companions and were not isolated by withdrawal of social partners. Taken together, our results provide rare empirical evidence for social selectivity in nonhumans, suggesting that patterns of increasing selectivity with age may be deeply rooted in primate evolution.

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.

Immune gene regulation is associated with age and environmental adversity in a nonhuman primate.

Phenotypic aging is ubiquitous across mammalian species, suggesting shared underlying mechanisms of aging. Aging is linked to molecular changes to DNA methylation and gene expression, and environmental factors, such as severe external challenges or adversities, can moderate these age-related changes. Yet, it remains unclear whether environmental adversities affect gene regulation via the same molecular pathways as chronological, or 'primary', aging. Investigating molecular aging in naturalistic animal populations can fill this gap by providing insight into shared molecular mechanisms of aging and the effects of a greater diversity of environmental adversities - particularly those that can be challenging to study in humans or laboratory organisms. Here, we characterised molecular aging - specifically, CpG methylation - in a sample of free-ranging rhesus macaques living off the coast of Puerto Rico (n samples = 571, n individuals = 499), which endured a major hurricane during our study. Age was associated with methylation at 78,661 sites (31% of all sites tested). Age-associated hypermethylation occurred more frequently in areas of active gene regulation, while hypomethylation was enriched in regions that show less activity in immune cells, suggesting these regions may become de-repressed in older individuals. Age-associated hypomethylation also co-occurred with increased chromatin accessibility while hypermethylation showed the opposite trend, hinting at a coordinated, multi-level loss of epigenetic stability during aging. We detected 32,048 CpG sites significantly associated with exposure to a hurricane, and these sites overlapped age-associated sites, most strongly in regulatory regions and most weakly in quiescent regions. Together, our results suggest that environmental adversity may contribute to aging-related molecular phenotypes in regions of active gene transcription, but that primary aging has specific signatures in non-regulatory regions.

Social ageing: exploring the drivers of late-life changes in social behaviour in mammals.

Social interactions help group-living organisms cope with socio-environmental challenges and are central to survival and reproductive success. Recent research has shown that social behaviour and relationships can change across the lifespan, a phenomenon referred to as 'social ageing'. Given the importance of social integration for health and well-being, age-dependent changes in social behaviour can modulate how fitness changes with age and may be an important source of unexplained variation in individual patterns of senescence. However, integrating social behaviour into ageing research requires a deeper understanding of the causes and consequences of age-based changes in social behaviour. Here, we provide an overview of the drivers of late-life changes in sociality. We suggest that explanations for social ageing can be categorized into three groups: changes in sociality that (a) occur as a result of senescence; (b) result from adaptations to ameliorate the negative effects of senescence; and/or (c) result from positive effects of age and demographic changes. Quantifying the relative contribution of these processes to late-life changes in sociality will allow us to move towards a more holistic understanding of how and why these patterns emerge and will provide important insights into the potential for social ageing to delay or accelerate other patterns of senescence.

Reduced older male presence linked to increased rates of aggression to non-conspecific targets in male elephants.

Males in many large mammal species spend a considerable portion of their lives in all-male groups segregated from females. In long-lived species, these all-male groups may contain individuals of vastly different ages, providing the possibility that behaviours such as aggression vary with the age demographic of the social environment, as well as an individual's own age. Here, we explore social factors affecting aggression and fear behaviours in non-musth male African elephants (Loxodonta africana) aggregating in an all-male area. Adolescent males had greater probabilities of directing aggressive and fearful behaviours to non-elephant targets when alone compared to when with other males. All males, regardless of age, were less aggressive towards non-elephant targets (e.g. vehicles and non-elephant animals) when larger numbers of males from the oldest age cohort were present. The presence of older males did not influence the probability that other males were aggressive to conspecifics or expressed fearful behaviours towards non-elephant targets. Older bulls may police aggression directed towards non-elephant targets or may lower elephants' perception of their current threat level. Our results suggest male elephants may pose an enhanced threat to humans and livestock when adolescents are socially isolated, and when fewer older bulls are nearby.

Comparing measures of social complexity: larger mountain gorilla groups do not have a greater diversity of relationships.

Social complexity reflects the intricate patterns of social interactions in societies. Understanding social complexity is fundamental for studying the evolution of diverse social systems and the cognitive innovations used to cope with the demands of social life. Social complexity has been predominantly quantified by social unit size, but newer measures of social complexity reflect the diversity of relationships. However, the association between these two sets of measures remains unclear. We used 12 years of data on 13 gorilla groups to investigate how measures of social complexity relate to each other. We found that group size was a poor proxy for relationship diversity and that the social complexity individuals experienced within the same group varied greatly. Our findings demonstrate two fundamental takeaways: first, that the number of relationships and the diversity of those relationships represent separate components of social complexity, both of which should be accounted for; and second, that social complexity measured at the group level may not represent the social complexity experienced by individuals in those groups. These findings suggest that comprehensive studies of social complexity, particularly those relating to the social demands faced by individuals, may require fine-scale social data to allow accurate comparisons across populations and species.

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.

Weak effects of common genetic variation in oxytocin and vasopressin receptor genes on rhesus macaque social behavior.

The neuropeptides oxytocin (OT) and arginine vasopressin (AVP) influence pair bonding, attachment, and sociality, as well as anxiety and stress responses in humans and other mammals. The effects of these peptides are mediated by genetic variability in their associated receptors, OXTR and the AVPR gene family. However, the role of these genes in regulating social behaviors in non-human primates is not well understood. To address this question, we examined whether genetic variation in the OT receptor gene OXTR and the AVP receptor genes AVPR1A and AVPR1B influence naturally-occurring social behavior in free-ranging rhesus macaques-gregarious primates that share many features of their biology and social behavior with humans. We assessed rates of social behavior across 3,250 hr of observational behavioral data from 201 free-ranging rhesus macaques on Cayo Santiago island in Puerto Rico, and used genetic sequence data to identify 25 OXTR, AVPR1A, and AVPR1B single-nucleotide variants (SNVs) in the population. We used an animal model to estimate the effects of 12 SNVs (n = 3 OXTR; n = 5 AVPR1A; n = 4 AVPR1B) on rates of grooming, approaches, passive contact, contact aggression, and non-contact aggression, given and received. Though we found evidence for modest heritability of these behaviors, estimates of effect sizes of the selected SNVs were close to zero, indicating that common OXTR and AVPR variation contributed little to social behavior in these animals. Our results are consistent with recent findings in human genetics that the effects of individual common genetic variants on complex phenotypes are generally small.

Indirectly connected: simple social differences can explain the causes and apparent consequences of complex social network positions.

Animal societies are often structurally complex. How individuals are positioned within the wider social network (i.e. their indirect social connections) has been shown to be repeatable, heritable and related to key life-history variables. Yet, there remains a general lack of understanding surrounding how complex network positions arise, whether they indicate active multifaceted social decisions by individuals, and how natural selection could act on this variation. We use simulations to assess how variation in simple social association rules between individuals can determine their positions within emerging social networks. Our results show that metrics of individuals' indirect connections can be more strongly related to underlying simple social differences than metrics of their dyadic connections. External influences causing network noise (typical of animal social networks) generally inflated these differences. The findings demonstrate that relationships between complex network positions and other behaviours or fitness components do not provide sufficient evidence for the presence, or importance, of complex social behaviours, even if direct network metrics provide less explanatory power than indirect ones. Interestingly however, a plausible and straightforward heritable basis for complex network positions can arise from simple social differences, which in turn creates potential for selection to act on indirect connections.

The evolution of self-control.

Cognition presents evolutionary research with one of its greatest challenges. Cognitive evolution has been explained at the proximate level by shifts in absolute and relative brain volume and at the ultimate level by differences in social and dietary complexity. However, no study has integrated the experimental and phylogenetic approach at the scale required to rigorously test these explanations. Instead, previous research has largely relied on various measures of brain size as proxies for cognitive abilities. We experimentally evaluated these major evolutionary explanations by quantitatively comparing the cognitive performance of 567 individuals representing 36 species on two problem-solving tasks measuring self-control. Phylogenetic analysis revealed that absolute brain volume best predicted performance across species and accounted for considerably more variance than brain volume controlling for body mass. This result corroborates recent advances in evolutionary neurobiology and illustrates the cognitive consequences of cortical reorganization through increases in brain volume. Within primates, dietary breadth but not social group size was a strong predictor of species differences in self-control. Our results implicate robust evolutionary relationships between dietary breadth, absolute brain volume, and self-control. These findings provide a significant first step toward quantifying the primate cognitive phenome and explaining the process of cognitive evolution.

Neuroethology of primate social behavior.

A neuroethological approach to human and nonhuman primate behavior and cognition predicts biological specializations for social life. Evidence reviewed here indicates that ancestral mechanisms are often duplicated, repurposed, and differentially regulated to support social behavior. Focusing on recent research from nonhuman primates, we describe how the primate brain might implement social functions by coopting and extending preexisting mechanisms that previously supported nonsocial functions. This approach reveals that highly specialized mechanisms have evolved to decipher the immediate social context, and parallel circuits have evolved to translate social perceptual signals and nonsocial perceptual signals into partially integrated social and nonsocial motivational signals, which together inform general-purpose mechanisms that command behavior. Differences in social behavior between species, as well as between individuals within a species, result in part from neuromodulatory regulation of these neural circuits, which itself appears to be under partial genetic control. Ultimately, intraspecific variation in social behavior has differential fitness consequences, providing fundamental building blocks of natural selection. Our review suggests that the neuroethological approach to primate behavior may provide unique insights into human psychopathology.

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.

Understanding age and society using natural populations.

Ageing affects almost all aspects of life and therefore is an important process across societies, human and non-human animal alike. This article introduces new research exploring the complex interplay between individual-level ageing and demography, and the consequences this interplay holds for the structure and functioning of societies across various natural populations. We discuss how this Special Issue provides a foundation for integrating perspectives from evolutionary biology, behavioural ecology and demography to provide new insights into how ageing shapes individuals' social behaviour and social associations, and how this in turn impacts social networks, social processes (such as disease or information transfer) and fitness. Through examining these topics across taxa, from invertebrates to birds and mammals, we outline how contemporary studies are using natural populations to advance our understanding of the relationship between age and society in innovative ways. We highlight key emerging research themes from this Special Issue, such as how sociality affects lifespan and health, the genetic and ecological underpinnings of social ageing and the adaptive strategies employed by different species. We conclude that this Special Issue underscores the importance of studying social ageing using diverse systems and interdisciplinary approaches for advancing evolutionary and ecological insights into both ageing and sociality more generally.This article is part of the discussion meeting issue 'Understanding age and society using natural populations '.

Social ageing can protect against infectious disease in a group-living primate.

The benefits of social living are well established, but sociality also comes with costs, including infectious disease risk. This cost-benefit ratio of sociality is expected to change across individuals' lifespans, which may drive changes in social behaviour with age. To explore this idea, we combine data from a group-living primate for which social ageing has been described with epidemiological models to show that having lower social connectedness when older can protect against the costs of a hypothetical, directly transmitted endemic pathogen. Assuming no age differences in epidemiological characteristics (susceptibility to, severity and duration of infection), older individuals suffered lower infection costs, which was explained largely because they were less connected in their social networks than younger individuals. This benefit of 'social ageing' depended on epidemiological characteristics and was greatest when infection severity increased with age. When infection duration increased with age, social ageing was beneficial only when pathogen transmissibility was low. Older individuals benefited most from having a lower frequency of interactions (strength) and network embeddedness (closeness) and benefited less from having fewer social partners (degree). Our study provides a first examination of the epidemiology of social ageing, demonstrating the potential for pathogens to influence the evolutionary dynamics of social ageing in natural populations.This article is part of the discussion meeting issue 'Understanding age and society using natural populations'.

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.

Social ageing can protect against infectious disease in a group-living primate.

The benefits of social living are well established, but sociality also comes with costs, including infectious disease risk. This cost-benefit ratio of sociality is expected to change across individuals' lifespans, which may drive changes in social behaviour with age. To explore this idea, we combine data from a group-living primate for which social ageing has been described with epidemiological models to show that having lower social connectedness when older can protect against the costs of a hypothetical, directly transmitted endemic pathogen. Assuming no age differences in epidemiological characteristics (susceptibility to, severity, and duration of infection), older individuals suffered lower infection costs, which was explained largely because they were less connected in their social networks than younger individuals. This benefit of 'social ageing' depended on epidemiological characteristics and was greatest when infection severity increased with age. When infection duration increased with age, social ageing was beneficial only when pathogen transmissibility was low. Older individuals benefited most from having a lower frequency of interactions (strength) and network embeddedness (closeness) and benefited less from having fewer social partners (degree). Our study provides a first examination of the epidemiology of social ageing, demonstrating the potential for pathogens to influence evolutionary dynamics of social ageing in natural populations.

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'.

Relationship between dominance hierarchy steepness and rank-relatedness of benefits in primates.

In animal social groups, the extent to which individuals consistently win agonistic interactions and their ability to monopolize resources represent 2 core aspects of their competitive regime. However, whether these two aspects are closely correlated within groups has rarely been studied. Here, we tested the hypothesis that hierarchy steepness, which is generally used to represent power differentials between group members, predicts the variation in the distribution of fitness-related benefits (i.e. fecundity, infant survival, mating success, and feeding success) in relation to individual dominance ranks. We tested this hypothesis in primate groups using comparative phylogenetic meta-analytical techniques. Specifically, we reviewed published and unpublished studies to extract data on individual dominance ranks, their access to fitness-related benefits, and hierarchy steepness. We collected and included in our analysis a total of 153 data points, representing 27 species (including 2 chimpanzee sub-species). From these, we used 4 common methods to measure individual dominance ranks and hierarchy steepness, i.e. D ij -based normalized David's scores, randomized Elo-ratings, and David's scores and Elo-ratings estimated in Bayesian frameworks. We found that hierarchy steepness had no effect on the strength of the relationship between dominance rank and access to fitness-related benefits. Our results suggest that hierarchy steepness does not reflect between-group variation in the extent to which individual dominance affects the acquisition of fitness-related benefits in primates. Although the ability to win agonistic encounters is essential, we speculate that other behavioral strategies adopted by individuals may play crucial roles in resource acquisition in animal competitive regimes.

Quantifying the relationship between bone and soft tissue measures within the rhesus macaques of Cayo Santiago.

OBJECTIVES: Interpretations of the primate and human fossil record often rely on the estimation of somatic dimensions from bony measures. Both somatic and skeletal variation have been used to assess how primates respond to environmental change. However, it is unclear how well skeletal variation matches and predicts soft tissue. Here, we empirically test the relationship between tissues by comparing somatic and skeletal measures using paired measures of pre- and post-mortem rhesus macaques from Cayo Santiago, Puerto Rico. MATERIALS AND METHODS: Somatic measurements were matched with skeletal dimensions from 105 rhesus macaque individuals to investigate paired signals of variation (i.e., coefficients of variation, sexual dimorphism) and bivariate codependence (reduced major axis regression) in measures of: (1) limb length; (2) joint breadth; and (3) limb circumference. Predictive models for the estimation of soft tissue dimensions from skeletons were built from Ordinary Least Squares regressions. RESULTS: Somatic and skeletal measurements showed statistically equivalent coefficients of variation and sexual dimorphism as well as high epiphyses-present ordinary least square (OLS) correlations in limb lengths (R2 >0.78, 0.82), joint breadths (R2 >0.74, 0.83) and, to a lesser extent, limb circumference (R2 >0.53, 0.68). CONCLUSION: Skeletal measurements are good substitutions for somatic values based on population signals of variation. OLS regressions indicate that skeletal correlates are highly predictive of somatic dimensions. The protocols and regression equations established here provide a basis for reliable reconstruction of somatic dimension from catarrhine fossils and validate our ability to compare or combine results of studies based on population data of either hard or soft tissue proxies.

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.