Anne E Pusey

• Duke University

Conservation funding is currently limited; cost-effective conservation solutions are essential. We suggest that the thousands of field stations worldwide can play key roles at the frontline of biodiversity conservation and have high intrinsic value. We assessed field stations’ conservation return on investment and explored the impact of COVID-19. W...

Reproductive inequality, or reproductive skew, drives natural selection, but has been difficult to assess, particularly for males in species with promiscuous mating and slow life histories, such as bonobos (Pan paniscus) and chimpanzees (Pan troglodytes). Although bonobos are often portrayed as more egalitarian than chimpanzees, genetic studies hav...

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 le...

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 neverth...

Personality traits in many taxa correlate with fitness. Several models have been developed to try to explain how variation in these traits is maintained. One model proposes that variation persists because it is linked to trade-offs between current and future adaptive benefits. Tests of this model’s predictions, however, are scant in long-lived spec...

Chimpanzees (Pan troglodytes) harbor rich assemblages of malaria parasites, including three species closely related to P. falciparum (sub-genus Laverania), the most malignant human malaria parasite. Here, we characterize the ecology and epidemiology of malaria infection in wild chimpanzee reservoirs. We used molecular assays to screen chimpanzee fe...

A large body of literature demonstrates the adaptive benefits of social relationships between kin, including fitness and survival. Given that most social mammals are characterized by male-biased dispersal, the majority of research on kin selection and associated advantages focuses on social relationships between female kin. Meanwhile, research on s...

Objectives Energetics are widely recognized to influence timing of birth in humans and other eutherian mammals, yet considerable variation exists in the relationship between energetic constraints and gestation length. In humans, poor nutrition and short inter‐gestational intervals (IGIs) are associated with shorter gestations. In other mammals, low...

Significance Age-related changes in the capability to produce healthy young are common in humans and are increasingly well documented in nonhuman animals. However, differences among species in the nature of these age-related changes remain poorly understood. We compare patterns and consequences of age-related changes in female reproductive performa...

Group territory defence poses a collective action problem: individuals can free-ride, benefiting without paying the costs. Individual heterogeneity has been proposed to solve such problems, as individuals high in reproductive success, rank, fighting ability or motivation may benefit from defending territories even if others free-ride. To test this...

Although rare among group-living primates, infanticide by females has been reported in several chimpanzee, Pan troglodytes, populations. We examined 13 infanticidal attacks over 47 years at Gombe National Park, Tanzania to evaluate three adaptive hypotheses. (1) Exploitation of the infant as a food resource – by eating a vulnerable neonate, attacke...

In most male mammals, fitness is strongly shaped by competitive access to mates, a non-shareable resource. How, then, did selection favor the evolution of cooperative social bonds? We used behavioral and genetic data on wild chimpanzees (Pan troglodytes schweinfurthii) in Gombe National Park, Tanzania, to study the mechanisms by which male-male soc...

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 c...

Is it possible to slow the rate of ageing, or do biological constraints limit its plasticity? We test the ‘invariant rate of ageing’ hypothesis, which posits that the rate of ageing is relatively fixed within species, with a collection of 39 human and nonhuman primate datasets across seven genera. We first recapitulate, in nonhuman primates, the hi...

Vertebrates harbor gut microbial communities containing hundreds of bacterial species, most of which have never been cultivated or isolated in the laboratory. The lack of cultured representatives from vertebrate gut microbiotas limits the description and experimental interrogation of these communities. Here we show that representatives from >50% of...

Increased risk of pathogen transmission through proximity and contact is a well-documented cost of sociality. Affiliative social contact, however, is an integral part of primate group life and can benefit health. Despite its importance to the evolution and maintenance of sociality, the tradeoff between costs and benefits of social contact for group...

Male chimpanzees (Pan troglodytes) defend group territories and sometimes kill members of rival communities — a pattern often compared to human warfare1-3. Male chimpanzees also sometimes kill grown males from their own community4-9. Such within-community killings are puzzling, as they reduce the coalition strength needed to win inter-community con...

Significance Extensive care of offspring by mothers is a fundamental trait of all mammals, including humans, and the loss of a mother can be catastrophic for offspring. Here, we identify previously undocumented ways in which the death of a mother affects her offspring, using long-term, longitudinal data from seven primate species. First, females th...

Is it possible to slow the rate of aging, or do biological constraints limit its plasticity? We test this ‘invariant rate of aging’ hypothesis with an unprecedented collection of 39 human and nonhuman primate datasets across seven genera. We first recapitulate, in nonhuman primates, the highly regular relationship between life expectancy and lifesp...

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 challen...

The ability to generate genomic data from wild animal populations has the potential to give unprecedented insight into the population history and dynamics of species in their natural habitats. However, in the case of many species, it is impossible legally, ethically, or logistically to obtain tissues samples of high quality necessary for genomic an...

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 lifespan. Here we leverage data from eight wild primate populations (seven species) to examine two underappreciated pathways linking early maternal death a...

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 main...

The study of non-human primate thanatology has expanded dramatically in recent years as scientists seek to understand the evolutionary roots of human death concepts and practices. However, observations of how conspecifics respond to dead individuals are rare and highly variable. Mothers of several species of primate have been reported to carry and...

The study of non-human primate thanatology has expanded dramatically in recent years as scientists seek to understand the evolutionary roots of human death concepts and practices. However, observations of how conspecifics respond to dead individuals are rare and highly variable. Mothers of several species of primate have been reported to carry and...

The ability to generate genomic data from wild animal populations has the potential to give unprecedented insight into the population history and dynamics of species in their natural habitats. However, in the case of many species, it is impossible legally, ethically, or logistically to obtain tissues samples of high-quality necessary for genomic an...

The mother-offspring relationship is paramount in most mammals and infant survival often depends on maternal investment. In species with prolonged periods of development or co-residence, mothers may continue to influence their offspring’s outcomes beyond nutritional independence with benefits biased towards the philopatric sex. Chimpanzees (Pan tro...

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 P...

Historic calcified dental plaque (dental calculus) can provide a unique perspective into the health status of past human populations but currently no studies have focused on the oral microbial ecosystem of other primates, including our closest relatives, within the hominids. Here we use ancient DNA extraction methods, shotgun library preparation, a...

In many group-living mammals, mothers may increase the reproductive success of their daughters even after they are nutritionally independent and fully grown [1]. However, whether such maternal effects exist for adult sons is largely unknown. Here we show that males have higher paternity success when their mother is living in the group at the time o...

Disease surveillance in wildlife is rapidly expanding in scope and methodology, emphasizing the need for formal evaluations of system performance. We examined a syndromic surveillance system for respiratory disease detection in Gombe National Park, Tanzania, from 2004 to 2012, with respect to data quality, disease trends, and respiratory disease de...

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...

Syndromic surveillance is an incipient approach to early wildlife disease detection. Consequently, systematic assessments are needed for methodology validation in wildlife populations. We evaluated the sensitivity of a syndromic surveillance protocol for respiratory disease detection among chimpanzees in Gombe National Park, Tanzania. Empirical hea...

Breeding between relatives generally results in inbreeding depression—a reduction in the survival and fertility of offspring. Evolutionary adaptations that prevent inbreeding include sex‐biased dispersal (permanent movement of the members of one sex or the other from the natal group or area before breeding, which separates close kin); behavioral av...

Short tandem repeats (STRs), also known as microsatellites, are commonly used to noninvasively genotype wild‐living endangered species, including African apes. Until recently, capillary electrophoresis has been the method of choice to determine the length of polymorphic STR loci. However, this technique is labor intensive, difficult to compare acro...

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 behavi...

We present the first cross continental comparison of the flowering and fruiting phenology of tropical forests across Africa. Flowering events of 5,446 trees from 196 species across 12 sites, and fruiting events of 4,595 trees from 191 species, across 11 sites were monitored over periods of 6 to 29 years, and analysed to describe phenology at the co...

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 hypo...

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 informatio...

Social play is common among many group-living animals, but the benefits are not well understood. Proposed benefits include increased muscle coordination as the result of increased locomotor versatility and development, and strengthened social bonds through interactions with like-aged individuals. In this study, we used 33 years of long-term behavio...

Researchers increasingly view animal personality traits as products of natural selection. We present data that describe the personalities of 128 eastern chimpanzees (Pan troglodytes schweinfurthii) currently living in or who lived their lives in the Kasekela and Mitumba communities of Gombe National Park, Tanzania. We obtained ratings on 24 items f...

Compared to great apes, humans maintain a relatively rapid reproductive pace despite long periods of dependency. This seemingly contradictory set of traits is made possible by weaning offspring before nutritional independence and alloparents who help provide care. In traditional societies, this help may be provided to mothers in part by their juven...

Among modern foraging societies, men hunt more than women, who mostly target relatively low-quality, reliable resources (i.e., plants). This difference has long been assumed to reflect human female reproductive constraints, particularly caring for and provisioning mates and offspring. Long-term studies of chimpanzees (Pan troglodytes) enable tests...

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 bec...

Inbreeding adversely affects fitness, whereas heterozygosity often augments it. Therefore, mechanisms to avoid inbreeding and increase genetic distance between mates should be advantageous in species where adult relatives reside together. Here we investigate mate choice for genetic dissimilarity in chimpanzees, a species in which many females avoid...

Electronic Supplementary Material - This single file contains detailed information on the paternity assignment procedure, including genbank numbers and a summary of paternity analyses. It also contains information on and checks of potential biases in our calculation of pairwise relatedness measures and compares our generated pairwise relatedness va...

Significance Public interest in social and economic equality is burgeoning. We examine a related phenomenon, lifespan equality, using data from charismatic primate populations and diverse human populations. Our study reveals three key findings. First, lifespan equality rises in lockstep with life expectancy, across primate species separated by mill...

Sexual selection theory predicts that because male reproductive success in mammals is limited by access to females, males will attempt to defend access to mates and exclude rivals from mating. In mammals, dominance rank is correlated with male reproductive success; however, the highestranking (alpha) male rarely monopolizes reproduction completely....

Promiscuous mating was traditionally thought to curtail paternal investment owing to the potential costs of providing care to unrelated infants. However, mounting evidence suggests that males in some promiscuous species can recognize offspring. In primates, evidence for paternal care exists in promiscuous Cercopithecines, but less is known about th...

Recent decades have seen rapid development of new analytical methods to investigate patterns of interspecific variation. Yet these cutting-edge statistical analyses often rely on data of questionable origin, varying accuracy, and weak comparability, which seem to have reduced the reproducibility of studies. It is time to improve the transparency of...

Dominance hierarchies are widespread in animal social groups and often have measureable effects on individual health and reproductive success. Dominance ranks are not static individual attributes, however, but instead are influenced by two independent processes: 1) changes in hierarchy membership and 2) successful challenges of higher-ranking indiv...

Human-microbiota coevolution The bacteria that make their home in the intestines of modern apes and humans arose from ancient bacteria that colonized the guts of our common ancestors. Moeller et al. have developed a method to compare rapidly evolving gyrB gene sequences in fecal samples from humans and wild chimpanzees, bonobos, and gorillas (see t...

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 ca...

Because body mass is correlated with many aspects of an animal’s ecology (Peters, 1983; Fleagle, 1985; McNab, 1990), predicting body mass in extinct or extant animals is a frequent goal of paleontologists and neontologists (Kay and Simons, 1980; Gingerich et al., 1982; Dagosto and Terranova, 1992; Mendoza et al., 2006; Yapuncich et al., 2015). Alth...

We provide male and female census count data, age-specific survivorship, and female age-specific fertility estimates for populations of seven wild primates that have been continuously monitored for at least 29 years: sifaka (Propithecus verreauxi) in Madagascar; muriqui (Brachyteles hypoxanthus) in Brazil; capuchin (Cebus capucinus) in Costa Rica;...

Chimpanzees (Pan troglodytes) compete aggressively for territory with their neighbors. Results from playback experiments and observations of naturally occurring intergroup interactions indicate that success in territorial competition depends mainly on the number of adult males on each side. Communities with more males are therefore expected to win...

Chimpanzees (Pan troglodytes) compete aggressively for territory with their neighbors. Results from playback experiments and observations of naturally occurring intergroup interactions indicate that success in territorial competition depends mainly on the number of adult males on each side. Communities with more males are therefore expected to win...

An increase in faunivory is a consistent component of human evolutionary models. Animal matter is energy- and nutrient-dense and can provide macronutrients, minerals, and vitamins that are limited or absent in plant foods. For female humans and other omnivorous primates, faunivory may be of particular importance during the costly periods of pregnan...

The distribution and abundance of food resources are among the most important factors that influence animal behavioral strategies. Yet, spatial variation in feeding habitat quality is often difficult to assess with traditional methods that rely on extrapolation from plot survey data or remote sensing. Here, we show that maximum entropy species dist...

Animal sociality facilitates the transmission of pathogenic microorganisms among hosts, but the extent to which sociality enables animals' beneficial microbial associations is poorly understood. The question is critical because microbial communities, particularly those in the gut, are key regulators of host health. We show evidence that chimpanzee...

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 f...

Even when hunting in groups is mutually beneficial, it is unclear how communal hunts are initiated. If it is costly to be the only hunter, individuals should be reluctant to hunt unless others already are.We used 70 years of data from three communities to examine how male chimpanzees ‘solve’ this apparent collective action problem. The ‘impact hunt...

Leadership is an active area of research in both the biological and social sciences. This review provides a transdisciplinary synthesis of biological and social-science views of leadership from an evolutionary perspective, and examines patterns of leadership in a set of small-scale human and non-human mammalian societies. We review empirical and th...

Studies of chimpanzee vocal communication provide valuable insights into the evolution of communication in complex societies, and also comparative data for understanding the evolution of human language. One particularly valuable dataset of recordings from free-living chimpanzees was collected by Frans X. Plooij and the late Hetty van de Rijt-Plooij...

In most primate societies, strong and enduring social bonds form preferentially among kin, who benefit from cooperation through direct and indirect fitness gains. Chimpanzees, Pan troglodytes, differ from most species by showing consistent female-biased dispersal and strict male philopatry. In most East African populations, females tend to forage a...

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 div...

For many long-lived mammalian species, extended maternal investment has a profound effect on offspring integration in complex social environments. One component of this investment may be aiding young in aggressive interactions, which can set the stage for offspring social position later in life. Here we examined maternal effects on dyadic aggressiv...

In sexually reproducing animals, male and female reproduc-tive strategies often conflict [1]. In some species, males use aggression to overcome female choice [2, 3], but debate persists over the extent to which this strategy is successful. Previous studies of male aggression toward females among wild chimpanzees have yielded contradictory results a...

Significance Early social experience is critical to developing appropriate adult behavior. Mothers are particularly important social partners but may also facilitate or restrict access to others. Studies investigating human parental facilitation are limited and confounded by culture. Comparative studies therefore provide invaluable insight into how...

Significance Human lifestyles profoundly influence the communities of microorganisms that inhabit the body, that is, the microbiome; however, how the microbiomes of humans have diverged from those found within wild-living hominids is not clear. To establish how the gut microbiome has changed since the diversification of human and ape species, we ch...

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 fit-ness benefits by incre...

Many researchers are interested in chimpanzee vocal communication, both as an important aspect of chimpanzee social behavior and as a source of insights into the evolution of human language. Nonetheless, very little is known about how chimpanzee vocal communication develops from infancy to adulthood. The largest dataset of audiorecordings from free...

Parental investment theory predicts that maternal resources are finite and allocated among offspring based on factors including maternal age and condition, and offspring sex and parity. Among humans, firstborn children are often considered to have an advantage and receive greater investment than their younger siblings. However, conflicting evidence...

Plasmodium vivax is the leading cause of human malaria in Asia and Latin America but is absent from most of central Africa due to the near fixation of a mutation that inhibits the expression of its receptor, the Duffy antigen, on human erythrocytes. The emergence of this protective allele is not understood because P. vivax is believed to have origi...