Reproductive inequality in humans and other mammals.

To address claims of human exceptionalism, we determine where humans fit within the greater mammalian distribution of reproductive inequality. We show that humans exhibit lower reproductive skew (i.e., inequality in the number of surviving offspring) among males and smaller sex differences in reproductive skew than most other mammals, while nevertheless falling within the mammalian range. Additionally, female reproductive skew is higher in polygynous human populations than in polygynous nonhumans mammals on average. This patterning of skew can be attributed in part to the prevalence of monogamy in humans compared to the predominance of polygyny in nonhuman mammals, to the limited degree of polygyny in the human societies that practice it, and to the importance of unequally held rival resources to women's fitness. The muted reproductive inequality observed in humans appears to be linked to several unusual characteristics of our species-including high levels of cooperation among males, high dependence on unequally held rival resources, complementarities between maternal and paternal investment, as well as social and legal institutions that enforce monogamous norms.

Female reproductive aging in seven primate species: Patterns and consequences.

Age-related changes in fertility have increasingly been documented in wild animal populations: In many species the youngest and oldest reproducers are disadvantaged relative to prime adults. How do these effects evolve, and what explains their diversity across species? Tackling this question requires detailed data on patterns of age-related reproductive performance in multiple animal species. Here, we compare patterns and consequences of age-related changes in female reproductive performance in seven primate populations that have been subjects of long-term continuous study for 29 to 57 y. We document evidence of age effects on fertility and on offspring performance in most, but not all, of these primate species. Specifically, females of six species showed longer interbirth intervals in the oldest age classes, youngest age classes, or both, and the oldest females also showed relatively fewer completed interbirth intervals. In addition, five species showed markedly lower survival among offspring born to the oldest mothers, and two species showed reduced survival for offspring born to both the youngest and the oldest mothers. In contrast, we found mixed evidence that maternal age affects the age at which daughters first reproduce: Only in muriquis and to some extent in chimpanzees, the only two species with female-biased dispersal, did relatively young mothers produce daughters that tended to have earlier first reproduction. Our findings demonstrate shared patterns as well as contrasts in age-related changes in female fertility across species of nonhuman primates and highlight species-specific behavior and life-history patterns as possible explanations for species-level differences.

Maternal death and offspring fitness in multiple wild primates.

Primate offspring often depend on their mothers well beyond the age of weaning, and offspring that experience maternal death in early life can suffer substantial reductions in fitness across the life span. Here, we leverage data from eight wild primate populations (seven species) to examine two underappreciated pathways linking early maternal death and offspring fitness that are distinct from direct effects of orphaning on offspring survival. First, we show that, for five of the seven species, offspring face reduced survival during the years immediately preceding maternal death, while the mother is still alive. Second, we identify an intergenerational effect of early maternal loss in three species (muriquis, baboons, and blue monkeys), such that early maternal death experienced in one generation leads to reduced offspring survival in the next. Our results have important implications for the evolution of slow life histories in primates, as they suggest that maternal condition and survival are more important for offspring fitness than previously realized.

Barriers to chimpanzee gene flow at the south-east edge of their distribution.

Populations on the edge of a species' distribution may represent an important source of adaptive diversity, yet these populations tend to be more fragmented and are more likely to be geographically isolated. Lack of genetic exchanges between such populations, due to barriers to animal movement, can not only compromise adaptive potential but also lead to the fixation of deleterious alleles. The south-eastern edge of chimpanzee distribution is particularly fragmented, and conflicting hypotheses have been proposed about population connectivity and viability. To address this uncertainty, we generated both mitochondrial and MiSeq-based microsatellite genotypes for 290 individuals ranging across western Tanzania. While shared mitochondrial haplotypes confirmed historical gene flow, our microsatellite analyses revealed two distinct clusters, suggesting two populations currently isolated from one another. However, we found evidence of high levels of gene flow maintained within each of these clusters, one of which covers an 18,000 km2 ecosystem. Landscape genetic analyses confirmed the presence of barriers to gene flow with rivers and bare habitats highly restricting chimpanzee movement. Our study demonstrates how advances in sequencing technologies, combined with the development of landscape genetics approaches, can resolve ambiguities in the genetic history of critical populations and better inform conservation efforts of endangered species.

The Gombe Ecosystem Health Project: 16 years of program evolution and lessons learned.

Infectious disease outbreaks pose a significant threat to the conservation of chimpanzees (Pan troglodytes) and all threatened nonhuman primates. Characterizing and mitigating these threats to support the sustainability and welfare of wild populations is of the highest priority. In an attempt to understand and mitigate the risk of disease for the chimpanzees of Gombe National Park, Tanzania, we initiated a long-term health-monitoring program in 2004. While the initial focus was to expand the ongoing behavioral research on chimpanzees to include standardized data on clinical signs of health, it soon became evident that the scope of the project would ideally include diagnostic surveillance of pathogens for all primates (including people) and domestic animals, both within and surrounding the National Park. Integration of these data, along with in-depth post-mortem examinations, have allowed us to establish baseline health indicators to inform outbreak response. Here, we describe the development and expansion of the Gombe Ecosystem Health project, review major findings from the research and summarize the challenges and lessons learned over the past 16 years. We also highlight future directions and present the opportunities and challenges that remain when implementing studies of ecosystem health in a complex, multispecies environment.

CD4 receptor diversity in chimpanzees protects against SIV infection.

Human and simian immunodeficiency viruses (HIV/SIVs) use CD4 as the primary receptor to enter target cells. Here, we show that the chimpanzee CD4 is highly polymorphic, with nine coding variants present in wild populations, and that this diversity interferes with SIV envelope (Env)-CD4 interactions. Testing the replication fitness of SIVcpz strains in CD4+ T cells from captive chimpanzees, we found that certain viruses were unable to infect cells from certain hosts. These differences were recapitulated in CD4 transfection assays, which revealed a strong association between CD4 genotypes and SIVcpz infection phenotypes. The most striking differences were observed for three substitutions (Q25R, Q40R, and P68T), with P68T generating a second N-linked glycosylation site (N66) in addition to an invariant N32 encoded by all chimpanzee CD4 alleles. In silico modeling and site-directed mutagenesis identified charged residues at the CD4-Env interface and clashes between CD4- and Env-encoded glycans as mechanisms of inhibition. CD4 polymorphisms also reduced Env-mediated cell entry of monkey SIVs, which was dependent on at least one D1 domain glycan. CD4 allele frequencies varied among wild chimpanzees, with high diversity in all but the western subspecies, which appeared to have undergone a selective sweep. One allele was associated with lower SIVcpz prevalence rates in the wild. These results indicate that substitutions in the D1 domain of the chimpanzee CD4 can prevent SIV cell entry. Although some SIVcpz strains have adapted to utilize these variants, CD4 diversity is maintained, protecting chimpanzees against infection with SIVcpz and other SIVs to which they are exposed.

Sexual dimorphism in chimpanzee (Pan troglodytes schweinfurthii) and human age-specific fertility.

Across vertebrates, species with intense male mating competition and high levels of sexual dimorphism in body size generally exhibit dimorphism in age-specific fertility. Compared with females, males show later ages at first reproduction and earlier reproductive senescence because they take longer to attain adult body size and musculature, and maintain peak condition for a limited time. This normally yields a shorter male duration of effective breeding, but this reduction might be attenuated in species that frequently use coalitionary aggression. Here, we present comparative genetic and demographic data on chimpanzees from three long-term study communities (Kanyawara: Kibale National Park, Uganda; Mitumba and Kasekela: Gombe National Park, Tanzania), comprising 581 male risk years and 112 infants, to characterize male age-specific fertility. For comparison, we update estimates from female chimpanzees in the same sites and append a sample of human foragers (the Tanzanian Hadza). Consistent with the idea that aggressive mating competition favors youth, chimpanzee males attained a higher maximum fertility than females, followed by a steeper decline with age. Males did not show a delay in reproduction compared with females, however, as adolescents in both sites successfully reproduced by targeting young, subfecund females, who were less attractive to adults. Gombe males showed earlier reproductive senescence and a shorter duration of effective breeding than Gombe females. By contrast, older males in Kanyawara generally continued to reproduce, apparently by forming coalitions with the alpha. Hadza foragers showed a distinct pattern of sexual dimorphism in age-specific fertility as, compared with women, men gained conceptions later but continued reproducing longer. In sum, both humans and chimpanzees showed sexual dimorphism in age-specific fertility that deviated from predictions drawn from primates with more extreme body size dimorphism, suggesting altered dynamics of male-male competition in the two lineages. In both species, coalitions appear important for extending male reproductive careers.

Lethal aggression in Pan is better explained by adaptive strategies than human impacts.

Observations of chimpanzees (Pan troglodytes) and bonobos (Pan paniscus) provide valuable comparative data for understanding the significance of conspecific killing. Two kinds of hypothesis have been proposed. Lethal violence is sometimes concluded to be the result of adaptive strategies, such that killers ultimately gain fitness benefits by increasing their access to resources such as food or mates. Alternatively, it could be a non-adaptive result of human impacts, such as habitat change or food provisioning. To discriminate between these hypotheses we compiled information from 18 chimpanzee communities and 4 bonobo communities studied over five decades. Our data include 152 killings (n = 58 observed, 41 inferred, and 53 suspected killings) by chimpanzees in 15 communities and one suspected killing by bonobos. We found that males were the most frequent attackers (92% of participants) and victims (73%); most killings (66%) involved intercommunity attacks; and attackers greatly outnumbered their victims (median 8:1 ratio). Variation in killing rates was unrelated to measures of human impacts. Our results are compatible with previously proposed adaptive explanations for killing by chimpanzees, whereas the human impact hypothesis is not supported.

Sources of variation in weaned age among wild chimpanzees in Gombe National Park, Tanzania.

OBJECTIVES: A key feature of human life history evolution is that modern humans wean their infants 2-4 years earlier on average than African apes. However, our understanding of weaning variation in apes remains limited. Here we provide the first such report in chimpanzees by examining weaned age variation using long-term data from Gombe National Park, Tanzania. MATERIAL AND METHODS: We analyzed 41 years of observational behavioral data from 65 offspring of 29 mothers to examine the relationships between weaned age (defined as cessation of suckling) in wild chimpanzees and maternal age, dominance rank and parity, and offspring sex. We used Cox proportional hazards regression with mixed effects to model time to weaning and to examine potential sources of variation in offspring weaned age. RESULTS: We found that male offspring were less likely than female offspring to wean by a given age and that weaned age of males varied more than weaned age of females. In addition, maternal dominance rank interacted with offspring age, such that low-ranking mothers were less likely to wean offspring early, but this effect decreased with offspring age. DISCUSSION: We found that male offspring and offspring of low-ranking females were less likely to wean early, but did not find evidence for variable weaning according to maternal age or parity. As more data accumulate, we will be better able to disentangle the effects of maternal dominance rank, age and parity. Such studies will not only provide a richer understanding of living ape life history characteristics, but will also provide an important framework for understanding the evolution of early weaning in humans.

Research and Conservation in the Greater Gombe Ecosystem: Challenges and Opportunities.

The study of chimpanzees in Gombe National Park, Tanzania, started by Jane Goodall in 1960, provided pioneering accounts of chimpanzee behavior and ecology. With funding from multiple sources, including the Jane Goodall Institute (JGI) and grants from private foundations and federal programs, the project has continued for sixty years, providing a wealth of information about our evolutionary cousins. These chimpanzees face two main challenges to their survival: infectious disease - including simian immunodeficiency virus (SIVcpz), which can cause Acquired Immune Deficiency Syndrome (AIDS) in chimpanzees - and the deforestation of land outside the park. A health monitoring program has increased understanding of the pathogens affecting chimpanzees and has promoted measures to characterize and reduce disease risk. Deforestation reduces connections between Gombe and other chimpanzee populations, which can cause loss of genetic diversity. To promote habitat restoration, JGI facilitated participatory village land use planning, in which communities voluntarily allocated land to a network of Village Land Forest Reserves. Expected benefits to people include stabilizing watersheds, improving water supplies, and ensuring a supply of forest resources. Surveys and genetic analyses confirm that chimpanzees persist on village lands and remain connected to the Gombe population. Many challenges remain, but the regeneration of natural forest on previously degraded lands provides hope that conservation solutions can be found that benefit both people and wildlife. Conservation work in the Greater Gombe Ecosystem has helped promote broader efforts to plan and work for conservation elsewhere in Tanzania and across Africa.

Great ape genetic diversity and population history.

Most great ape genetic variation remains uncharacterized; however, its study is critical for understanding population history, recombination, selection and susceptibility to disease. Here we sequence to high coverage a total of 79 wild- and captive-born individuals representing all six great ape species and seven subspecies and report 88.8 million single nucleotide polymorphisms. Our analysis provides support for genetically distinct populations within each species, signals of gene flow, and the split of common chimpanzees into two distinct groups: Nigeria-Cameroon/western and central/eastern populations. We find extensive inbreeding in almost all wild populations, with eastern gorillas being the most extreme. Inferred effective population sizes have varied radically over time in different lineages and this appears to have a profound effect on the genetic diversity at, or close to, genes in almost all species. We discover and assign 1,982 loss-of-function variants throughout the human and great ape lineages, determining that the rate of gene loss has not been different in the human branch compared to other internal branches in the great ape phylogeny. This comprehensive catalogue of great ape genome diversity provides a framework for understanding evolution and a resource for more effective management of wild and captive great ape populations.

The emergence of longevous populations.

The human lifespan has traversed a long evolutionary and historical path, from short-lived primate ancestors to contemporary Japan, Sweden, and other longevity frontrunners. Analyzing this trajectory is crucial for understanding biological and sociocultural processes that determine the span of life. Here we reveal a fundamental regularity. Two straight lines describe the joint rise of life expectancy and lifespan equality: one for primates and the second one over the full range of human experience from average lifespans as low as 2 y during mortality crises to more than 87 y for Japanese women today. Across the primate order and across human populations, the lives of females tend to be longer and less variable than the lives of males, suggesting deep evolutionary roots to the male disadvantage. Our findings cast fresh light on primate evolution and human history, opening directions for research on inequality, sociality, and aging.

Maturation is prolonged and variable in female chimpanzees.

Chimpanzees are important referential models for the study of life history in hominin evolution. Age at sexual maturity and first reproduction are key life history milestones that mark the diversion of energy from growth to reproduction and are essential in comparing life history trajectories between chimpanzees and humans. Yet, accurate information on ages at these milestones in wild chimpanzees is difficult to obtain because most females transfer before breeding. Precise age at first birth is only known from a relatively small number of non-dispersing individuals. Moreover, due to small sample sizes, the degree to which age at maturation milestones varies is unknown. Here we report maturation milestones and explore sources of variance for 36 wild female chimpanzees of known age, including eight dispersing females born in Gombe National Park, Tanzania. Using Kaplan-Meier survival analysis, including censored intervals, we find an average age of 11.5 years (range 8.5-13.9) at sexual maturity and 14.9 years (range 11.1-22.1) at first birth. These values exceed previously published averages for wild chimpanzees by one or more years. Even in this larger sample, age at first birth is likely underestimated due to the disproportionate number of non-dispersing females, which, on average, give birth two years earlier than dispersing females. Model selection using Cox Proportional Hazards models shows that age at sexual maturity is delayed in females orphaned before age eight years and those born to low-ranking mothers. Age at first birth is most delayed in dispersing females and those orphaned before age eight years. These data provide improved estimates of maturation milestones in a population of wild female chimpanzees and indicate the importance of maternal factors in development.

Signature Patterns of MHC Diversity in Three Gombe Communities of Wild Chimpanzees Reflect Fitness in Reproduction and Immune Defense against SIVcpz.

Major histocompatibility complex (MHC) class I molecules determine immune responses to viral infections. These polymorphic cell-surface glycoproteins bind peptide antigens, forming ligands for cytotoxic T and natural killer cell receptors. Under pressure from rapidly evolving viruses, hominoid MHC class I molecules also evolve rapidly, becoming diverse and species-specific. Little is known of the impact of infectious disease epidemics on MHC class I variant distributions in human populations, a context in which the chimpanzee is the superior animal model. Population dynamics of the chimpanzees inhabiting Gombe National Park, Tanzania have been studied for over 50 years. This population is infected with SIVcpz, the precursor of human HIV-1. Because HLA-B is the most polymorphic human MHC class I molecule and correlates strongly with HIV-1 progression, we determined sequences for its ortholog, Patr-B, in 125 Gombe chimpanzees. Eleven Patr-B variants were defined, as were their frequencies in Gombe's three communities, changes in frequency with time, and effect of SIVcpz infection. The growing populations of the northern and central communities, where SIVcpz is less prevalent, have stable distributions comprising a majority of low-frequency Patr-B variants and a few high-frequency variants. Driving the latter to high frequency has been the fecundity of immigrants to the northern community, whereas in the central community, it has been the fecundity of socially dominant individuals. In the declining population of the southern community, where greater SIVcpz prevalence is associated with mortality and emigration, Patr-B variant distributions have been changing. Enriched in this community are Patr-B variants that engage with natural killer cell receptors. Elevated among SIVcpz-infected chimpanzees, the Patr-B*06:03 variant has striking structural and functional similarities to HLA-B*57, the human allotype most strongly associated with delayed HIV-1 progression. Like HLA-B*57, Patr-B*06:03 correlates with reduced viral load, as assessed by detection of SIVcpz RNA in feces.

The timing and causes of a unique chimpanzee community fission preceding Gombe's "Four-Year War".

OBJECTIVES: While permanent group fissions are documented in humans and other primate species, they are relatively rare in male philopatric primates. One of the few apparent cases occurred in 1973 in Gombe National Park, Tanzania, when a community of chimpanzees split into two separate groups, preceding the famous "Four-Year War." We tested the hypothesis that the original group was a single cohesive community that experienced permanent fission, and investigated several potential catalysts. MATERIALS AND METHODS: We calculated association, grooming, and ranging metrics from historical data and used community detection algorithms and matrix permutation tests to determine the timing, dynamics, and causes of changes in social network subgrouping structure. RESULTS: We found that the two communities indeed split from one cohesive community, albeit one with incipient subgrouping. The degree of subgrouping in grooming and association networks increased sharply in 1971 and 1972, a period characterized by a dominance struggle between three high-ranking males and unusually high male:female sex ratios. Finally, we found a relationship between post-split community membership and previous association, grooming and ranging patterns in most periods of analysis, one that became more pronounced as the fission approached. DISCUSSION: Our analysis suggests that the community began to split during a time of an unusually male-biased sex ratio and a protracted dominance struggle, and that adult males remained with those with whom they had preferentially associated prior to the split. We discuss the costs and benefits of group membership in chimpanzees and contrast these results with group fissions in humans and other taxa.

Destabilization of the gut microbiome marks the end-stage of simian immunodeficiency virus infection in wild chimpanzees.

Enteric dysbiosis is a characteristic feature of progressive human immunodeficiency virus type 1 (HIV-1) infection but has not been observed in simian immunodeficiency virus (SIVmac)-infected macaques, including in animals with end-stage disease. This has raised questions concerning the mechanisms underlying the HIV-1 associated enteropathy, with factors other than virus infection, such as lifestyle and antibiotic use, implicated as playing possible causal roles. Simian immunodeficiency virus of chimpanzees (SIVcpz) is also associated with increased mortality in wild-living communities, and like HIV-1 and SIVmac, can cause CD4+ T cell depletion and immunodeficiency in infected individuals. Given the central role of the intestinal microbiome in mammalian health, we asked whether gut microbial constituents could be identified that are indicative of SIVcpz status and/or disease progression. Here, we characterized the gut microbiome of SIVcpz-infected and -uninfected chimpanzees in Gombe National Park, Tanzania. Subjecting a small number of fecal samples (N = 9) to metagenomic (shotgun) sequencing, we found bacteria of the family Prevotellaceae to be enriched in SIVcpz-infected chimpanzees. However, 16S rRNA gene sequencing of a larger number of samples (N = 123) failed to show significant differences in both the composition and diversity (alpha and beta) of gut bacterial communities between infected (N = 24) and uninfected (N = 26) chimpanzees. Similarly, chimpanzee stool-associated circular virus (Chi-SCV) and chimpanzee adenovirus (ChAdV) identified by metagenomic sequencing were neither more prevalent nor more abundant in SIVcpz-infected individuals. However, fecal samples collected from SIVcpz-infected chimpanzees within 5 months before their AIDS-related death exhibited significant compositional changes in their gut bacteriome. These data indicate that SIVcpz-infected chimpanzees retain a stable gut microbiome throughout much of their natural infection course, with a significant destabilization of bacterial (but not viral) communities observed only in individuals with known immunodeficiency within the last several months before their death. Am. J. Primatol. 80:e22515, 2018. © 2015 Wiley Periodicals, Inc.

Socioecological correlates of clinical signs in two communities of wild chimpanzees (Pan troglodytes) at Gombe National Park, Tanzania.

Disease and other health hazards pose serious threats to the persistence of wild ape populations. The total chimpanzee population at Gombe National Park, Tanzania, has declined from an estimated 120 to 150 individuals in the 1960's to around 100 individuals by the end of 2013, with death associated with observable signs of disease as the leading cause of mortality. In 2004, we began a non-invasive health-monitoring program in the two habituated communities in the park (Kasekela and Mitumba) with the aim of understanding the prevalence of health issues in the population, and identifying the presence and impacts of various pathogens. Here we present prospectively collected data on clinical signs (observable changes in health) in the chimpanzees of the Kasekela (n = 81) and Mitumba (n = 32) communities over an 8-year period (2005-2012). First, we take a population approach and analyze prevalence of clinical signs in five different categories: gastrointestinal system (diarrhea), body condition (estimated weight loss), respiratory system (coughing, sneezing etc.), wounds/lameness, and dermatologic issues by year, month, and community membership. Mean monthly prevalence of each clinical sign per community varied, but typically affected <10% of observed individuals. Secondly, we analyze the presence of clinical signs in these categories as they relate to individual demographic and social factors (age, sex, and dominance rank) and simian immunodeficiency virus (SIVcpz) infection status. Adults have higher odds of being observed with diarrhea, loss of body condition, and wounds or lameness when compared to immatures, while males have a higher probability of being observed with wounds or lameness than females. In contrast, signs of respiratory illness appear not to be related to chimpanzee-specific factors and skin abnormalities are very rare. For a subset of known-rank individuals, dominance rank predicts the probability of wounding/lameness in adult males, but does not predict any adverse clinical signs in adult females. Instead, adult females with SIVcpz infection are more likely to be observed with diarrhea, a finding that warrants further investigation. Comparable data are needed from other sites to determine whether the prevalence of clinical signs we observe are relatively high or low, as well as to more fully understand the factors influencing health of wild apes at both the population and individual level. Am. J. Primatol. 80:e22562, 2018. © 2016 Wiley Periodicals, Inc.

Morphological Identification of Hair Recovered from Feces for Detection of Cannibalism in Eastern Chimpanzees.

Chimpanzees (Pan troglodytes) are primarily frugivorous but consume a variable amount of meat from a variety of organisms, including other chimpanzees. Cannibalism is rare, usually follows lethal aggression, and does not occur following natural deaths. While chimpanzee cannibalism has been documented at multiple sites, many instances of this behavior go unrecorded. Identification of chimpanzee remains in feces, however, can provide indirect evidence of cannibalism. Hair, in particular, typically passes through the gastrointestinal tract undamaged and is commonly used for purposes of identification in wildlife forensics. Here we test the hypothesis that eastern chimpanzee (Pan troglodytes schweinfurthii) guard hair morphology can be reliably distinguished from the hairs of their most common prey species. Methods and results are presented in the context of a case study involving a suspected chimpanzee infanticide from Gombe, Tanzania. We find that chimpanzee guard hair morphology is unique among tested mammals and that the presence of abundant chimpanzee hair in feces is likely the result of cannibalism and not incidental ingestion from grooming or other means. Accordingly, morphological analysis of guard hairs from feces is a promising, cost-effective tool for the determination of cannibalistic acts in chimpanzees.

Does climate variability influence the demography of wild primates? Evidence from long-term life-history data in seven species.

Earth's rapidly changing climate creates a growing need to understand how demographic processes in natural populations are affected by climate variability, particularly among organisms threatened by extinction. Long-term, large-scale, and cross-taxon studies of vital rate variation in relation to climate variability can be particularly valuable because they can reveal environmental drivers that affect multiple species over extensive regions. Few such data exist for animals with slow life histories, particularly in the tropics, where climate variation over large-scale space is asynchronous. As our closest relatives, nonhuman primates are especially valuable as a resource to understand the roles of climate variability and climate change in human evolutionary history. Here, we provide the first comprehensive investigation of vital rate variation in relation to climate variability among wild primates. We ask whether primates are sensitive to global changes that are universal (e.g., higher temperature, large-scale climate oscillations) or whether they are more sensitive to global change effects that are local (e.g., more rain in some places), which would complicate predictions of how primates in general will respond to climate change. To address these questions, we use a database of long-term life-history data for natural populations of seven primate species that have been studied for 29-52 years to investigate associations between vital rate variation, local climate variability, and global climate oscillations. Associations between vital rates and climate variability varied among species and depended on the time windows considered, highlighting the importance of temporal scale in detection of such effects. We found strong climate signals in the fertility rates of three species. However, survival, which has a greater impact on population growth, was little affected by climate variability. Thus, we found evidence for demographic buffering of life histories, but also evidence of mechanisms by which climate change could affect the fates of wild primates.