Sex differences in early experience and the development of aggression in wild chimpanzees.

Sex differences in physical aggression occur across human cultures and are thought to be influenced by active sex role reinforcement. However, sex differences in aggression also exist in our close evolutionary relatives, chimpanzees, who do not engage in active teaching, but do exhibit long juvenile periods and complex social systems that allow differential experience to shape behavior. Here we ask whether early life exposure to aggression is sexually dimorphic in wild chimpanzees and, if so, whether other aspects of early sociality contribute to this difference. Using 13 y of all-occurrence aggression data collected from the Kanyawara community of chimpanzees (2005 to 2017), we determined that young male chimpanzees were victims of aggression more often than females by between 4 and 5 (i.e., early in juvenility). Combining long-term aggression data with data from a targeted study of social development (2015 to 2017), we found that two potential risk factors for aggression-time spent near adult males and time spent away from mothers-did not differ between young males and females. Instead, the major risk factor for receiving aggression was the amount of aggression that young chimpanzees displayed, which was higher for males than females throughout the juvenile period. In multivariate models, sex did not mediate this relationship, suggesting that other chimpanzees did not target young males specifically, but instead responded to individual behavior that differed by sex. Thus, social experience differed by sex even in the absence of explicit gender socialization, but experiential differences were shaped by early-emerging sex differences in behavior.

Wild chimpanzees exhibit humanlike aging of glucocorticoid regulation.

Cortisol, a key product of the stress response, has critical influences on degenerative aging in humans. In turn, cortisol production is affected by senescence of the hypothalamic-pituitary-adrenal (HPA) axis, leading to progressive dysregulation and increased cortisol exposure. These processes have been studied extensively in industrialized settings, but few comparative data are available from humans and closely related species living in natural environments, where stressors are very different. Here, we examine age-related changes in urinary cortisol in a 20-y longitudinal study of wild chimpanzees (n = 59 adults) in the Kanyawara community of Kibale National Park, Uganda. We tested for three key features of HPA aging identified in many human studies: increased average levels, a blunted diurnal rhythm, and enhanced response to stressors. Using linear mixed models, we found that aging was associated with a blunting of the diurnal rhythm and a significant linear increase in cortisol, even after controlling for changes in dominance rank. These effects did not differ by sex. Aging did not increase sensitivity to energetic stress or social status. Female chimpanzees experienced their highest levels of cortisol during cycling (versus lactation), and this effect increased with age. Male chimpanzees experienced their highest levels when exposed to sexually attractive females, but this effect was diminished by age. Our results indicate that chimpanzees share some key features of HPA aging with humans. These findings suggest that impairments of HPA regulation are intrinsic to the aging process in hominids and are side effects neither of extended human life span nor of atypical environments.

Female reproduction and viral infection in a long-lived mammal.

For energetically limited organisms, life-history theory predicts trade-offs between reproductive effort and somatic maintenance. This is especially true of female mammals, for whom reproduction presents multifarious energetic and physiological demands. Here, we examine longitudinal changes in the gut virome (viral community) with respect to reproductive status in wild mature female chimpanzees Pan troglodytes schweinfurthii from two communities, Kanyawara and Ngogo, in Kibale National Park, Uganda. We used metagenomic methods to characterize viromes of individual chimpanzees while they were cycling, pregnant and lactating. Females from Kanyawara, whose territory abuts the park's boundary, had higher viral richness and loads (relative quantity of viral sequences) than females from Ngogo, whose territory is more energetically rich and located farther from large human settlements. Viral richness (total number of distinct viruses per sample) was higher when females were lactating than when cycling or pregnant. In pregnant females, viral richness increased with estimated day of gestation. Richness did not vary with age, in contrast to prior research showing increased viral abundance in older males from these same communities. Our results provide evidence of short-term physiological trade-offs between reproduction and infection, which are often hypothesized to constrain health in long-lived species.

Viruses associated with ill health in wild chimpanzees.

Viral infection is a major cause of ill health in wild chimpanzees (Pan troglodytes), but most evidence to date has come from conspicuous disease outbreaks with high morbidity and mortality. To examine the relationship between viral infection and ill health during periods not associated with disease outbreaks, we conducted a longitudinal study of wild eastern chimpanzees (P. t. schweinfurthii) in the Kanyawara and Ngogo communities of Kibale National Park, Uganda. We collected standardized, observational health data for 4 years and then used metagenomics to characterize gastrointestinal viromes (i.e., all viruses recovered from fecal samples) in individual chimpanzees before and during episodes of clinical disease. We restricted our analyses to viruses thought to infect mammals or primarily associated with mammals, discarding viruses associated with nonmammalian hosts. We found 18 viruses (nine of which were previously identified in this population) from at least five viral families. Viral richness (number of viruses per sample) did not vary by health status. By contrast, total viral load (normalized proportion of sequences mapping to viruses) was significantly higher in ill individuals compared with healthy individuals. Furthermore, when ill, Kanyawara chimpanzees exhibited higher viral loads than Ngogo chimpanzees, and males, but not females, exhibited higher infection rates with certain viruses and higher total viral loads as they aged. Post-hoc analyses, including the use of a machine-learning classification method, indicated that one virus, salivirus (Picornaviridae), was the main contributor to health-related and community-level variation in viral loads. Another virus, chimpanzee stool-associated virus (chisavirus; unclassified Picornavirales), was associated with ill health at Ngogo but not at Kanyawara. Chisavirus, chimpanzee adenovirus (Adenoviridae), and bufavirus (Parvoviridae) were also associated with increased age in males. Associations with sex and age are consistent with the hypothesis that nonlethal viral infections cumulatively reflect or contribute to senescence in long-lived species such as chimpanzees.

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.

Aggression, glucocorticoids, and the chronic costs of status competition for wild male chimpanzees.

Across vertebrates, high social status affords preferential access to resources, and is expected to correlate positively with health and longevity. Increasing evidence, however, suggests that although dominant females generally enjoy reduced exposure to physiological and psychosocial stressors, dominant males do not. Here we test the hypothesis that costly mating competition by high-ranking males results in chronic, potentially harmful elevations in glucocorticoid production. We examined urinary glucocorticoids (n = 8029 samples) in a 20-year longitudinal study of wild male chimpanzees (n = 20 adults) in the Kanyawara community of Kibale National Park, Uganda. We tested whether glucocorticoid production was associated with dominance rank in the long term, and with mating competition and dominance instability in the short term. Using mixed models, we found that both male aggression and glucocorticoid excretion increased when the dominance hierarchy was unstable, and when parous females were sexually available. Glucocorticoid excretion was positively associated with male rank in stable and unstable hierarchies, and in mating and non-mating contexts. Glucorticoids increased with both giving and receiving aggression, but giving aggression was the primary mechanism linking elevated glucocorticoids with high rank. Glucocorticoids also increased with age. Together these results show that investment in male-male competition increases cumulative exposure to glucocorticoids, suggesting a long-term tradeoff with health that may constrain the ability to maintain high status across the life course. Our data suggest that the relationship between social rank and glucocorticoid production often differs in males and females owing to sex differences in the operation of sexual selection.

Female-directed aggression by adolescent male chimpanzees primarily constitutes dominance striving, not sexual coercion.

OBJECTIVES: Chimpanzees (Pan troglodytes) are notable for exhibiting high levels of male-to-female aggression. Much of this aggression from adult males serves sexually coercive functions. Despite being smaller and lower-ranking than adult males, adolescent males also engage in regular aggression against adult females. Here, we test whether the primary function of this aggression is sexual coercion, as in adult males, or, alternatively, whether adolescent males use aggression to establish social dominance over females. MATERIALS AND METHODS: We analyzed 1771 copulations and 1812 instances of male-initiated aggression between adolescent males (aged nine through 14 years) and adult females across 21 years of observation of the Kanyawara chimpanzee community in Kibale National Park, Uganda. RESULTS: Our test of the sexual coercion hypothesis revealed that adolescent males did not selectively target cycling females for aggression, nor did aggression against cycling females predict rates of copulation with those females. Our test of the social dominance hypothesis showed that males succeeded in dominating all adult females before, or soon after, dominating their first adult male. Additionally, we found that adolescent males dominated females approximately in the order of the females' own ranks, from the bottom to the top of the female hierarchy. DISCUSSION: Our data illustrate that the establishment of social dominance was more important than sexual coercion in explaining patterns of adolescent male aggression toward females. In comparison, evidence for sexual coercion was clear and compelling in adult males. These findings highlight that the primary function of male-to-female aggression differs between adolescent and adult males.

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.

The Kibale Chimpanzee Project: Over thirty years of research, conservation, and change.

Long-term primate field research programs contribute to the protection of endangered primate species and their vanishing habitats by informing and fostering local and international conservation programs. The Kibale Chimpanzee Project (KCP) has studied the Kanyawara community of wild chimpanzees continuously since 1987, investigating a wide range of behavioral, ecological, and physiological questions. The study area includes the northwest boundary of Kibale National Park, Uganda, and has experienced habitat change driven by multiple causes, including forest regeneration, an increasingly warmer and wetter climate, and impacts from the neighboring human population. Here, we review the history of research on Kanyawara chimpanzees and examine how their demography, diet, and social behavior have changed over the last 30+ years. While Kanyawara chimpanzees were protected from the major threats of poaching and habitat loss, respiratory diseases of human origin were a major source of mortality. Many individuals were also injured by wire hunting snares. Nevertheless, the study community has grown modestly in size, individuals have become increasingly gregarious, and birth rates have increased. These results are likely attributable to improved habitat productivity that can be traced to decades-long efforts by wildlife authorities and the associated research and conservation programs in Kibale. Overall, research has contributed both to understanding interactions among nutritional ecology, social behavior, physiology, and health of an endangered species, and also to conservation activities in the Kibale community through direct interventions, positive economic impacts, and conservation education programs.

Human-like adrenal development in wild chimpanzees: A longitudinal study of urinary dehydroepiandrosterone-sulfate and cortisol.

The development of the adrenal cortex varies considerably across primates, being most conspicuous in humans, where a functional zona reticularis-the site of dehydroepiandrosterone-sulfate (DHEA/S) production-does not develop until middle childhood (5-8 years). Prior reports suggest that a human-like adrenarche, associated with a sharp prepubertal increase in DHEA/S, may only occur in the genus Pan. However, the timing and variability in adrenarche in chimpanzees remain poorly described, owing to the lack of longitudinal data, or data from wild populations. Here, we use urine samples from East African chimpanzees (Pan troglodytes schweinfurthii) collected over 20 years at Kanyawara in Kibale National Park, Uganda, to trace the developmental trajectories of DHEAS (n = 1,385 samples, 53 individuals) and cortisol (n = 12,726 samples, 68 individuals). We used generalized additive models (GAM) to investigate the relationship between age, sex, and hormone levels. Adrenarche began earlier in chimpanzees (~2-3 years) compared with what has been reported in humans (6-8 years) and, unlike humans, male and female chimpanzees did not differ significantly in the timing of adrenarche nor in DHEAS concentrations overall. Similar to what has been reported in humans, cortisol production decreased through early life, reaching a nadir around puberty (8-11 years), and a sex difference emerged with males exhibiting higher urinary cortisol levels compared with females by early adulthood (15-16 years). Our study establishes that wild chimpanzees exhibit a human-like pattern of cortisol production during development and corroborates prior reports from captive chimpanzees of a human-like adrenarche, accompanied by significant developmental increases in DHEAS. While the role of these developmental hormone shifts are as yet unclear, they have been implicated in stages of rapid behavioral development once thought unique to humans, especially in regard to explaining the divergence of female and male social behavior before pubertal increases in gonadal hormones.

Faster reproductive rates trade off against offspring growth in wild chimpanzees.

Life history theory predicts a trade-off between offspring quality and quantity. Among large-bodied mammals, prolonged lactation and infant dependence suggest particularly strong potential for a quality-quantity trade-off to exist. Humans are one of the only such species to have been examined, providing mixed evidence under a peculiar set of circumstances, including extensive nutritional provisioning by nonmothers and extrasomatic wealth transmission. Here, we examine trade-offs between reproductive rate and one aspect of offspring quality (body size) in wild chimpanzees (Pan troglodytes schweinfurthii), a species with long periods of infant dependence and little direct provisioning. Juvenile lean body mass, estimated using urinary creatinine excretion, was positively associated with the interval to the next sibling's birth. These effects persisted into adolescence and were not moderated by maternal identity. Maternal depletion could not explain poor offspring growth, as older mothers had larger offspring, and low maternal energy balance during lactation predicted larger, not smaller, juvenile size. Instead, our data suggest that offspring growth suffers when mothers wean early to invest in new reproductive efforts. These findings indicate that chimpanzee mothers with the resources to do so prioritize production of new offspring over prolonged investment in current offspring.

Lethal Respiratory Disease Associated with Human Rhinovirus C in Wild Chimpanzees, Uganda, 2013.

We describe a lethal respiratory outbreak among wild chimpanzees in Uganda in 2013 for which molecular and epidemiologic analyses implicate human rhinovirus C as the cause. Postmortem samples from an infant chimpanzee yielded near-complete genome sequences throughout the respiratory tract; other pathogens were absent. Epidemiologic modeling estimated the basic reproductive number (R0) for the epidemic as 1.83, consistent with the common cold in humans. Genotyping of 41 chimpanzees and examination of 24 published chimpanzee genomes from subspecies across Africa showed universal homozygosity for the cadherin-related family member 3 CDHR3-Y529 allele, which increases risk for rhinovirus C infection and asthma in human children. These results indicate that chimpanzees exhibit a species-wide genetic susceptibility to rhinovirus C and that this virus, heretofore considered a uniquely human pathogen, can cross primate species barriers and threatens wild apes. We advocate engineering interventions and prevention strategies for rhinovirus infections for both humans and wild apes.

The development of feeding behavior in wild chimpanzees (Pan troglodytes schweinfurthii).

OBJECTIVES: Primates have an extended period of juvenility before adulthood. Although dietary complexity plays a prominent role in hypotheses regarding the evolution of extended juvenility, the development of feeding behavior is still poorly understood. Indeed, few studies have investigated the timing and nature of feeding transitions in apes, including chimpanzees. We describe general patterns of feeding development in wild chimpanzees and evaluate predictions of the needing-to-learn hypothesis. MATERIALS AND METHODS: We analyzed 4 years of behavioral data (2010-2013) from 26 immature chimpanzees and 31 adult chimpanzees of the Kanyawara community in Kibale National Park, Uganda. Specifically, we examined milestones of nutritional independence (first consumption of solid food and cessation of suckling) as well as developmental changes in feeding time, diet composition, diet breadth, and ingestion rates. RESULTS: Chimpanzees first fed on solid food at 5.1 months and, on average, suckled until 4.8 years. Daily feeding time of immature individuals reached adult levels between 4 and 6 years, while diet composition showed minor changes with age. By juvenility (5-10 years), individuals had a complete adult diet breadth. Ingestion rates for five ripe fruit species remained below adult levels until juvenility but continued to show absolute increases into adolescence. DISCUSSION: Chimpanzees acquired adult-like patterns on all feeding measures by infancy or juvenility. These data are inconsistent with the needing-to-learn hypothesis; moreover, where delays exist, alternatives hypotheses make similar predictions but implicate physical constraints rather than learning as causal factors. We outline predictions for how future studies might distinguish between hypotheses for the evolution of extended juvenility.

Predation by female chimpanzees: Toward an understanding of sex differences in meat acquisition in the last common ancestor of Pan and Homo.

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 of hypotheses about the possible origins of human sex differences in hunting, prior to pair-bonding and regular provisioning. We studied two eastern chimpanzee communities (Kasekela, Mitumba) in Gombe, Tanzania and one (Kanyawara) in Kibale, Uganda. Relative to males, females had low hunting rates in all three communities, even where they encountered red colobus monkeys (the primary prey of chimpanzees) as often as males did. There was no evidence that clinging offspring hampered female hunting. Instead, consistent with the hypothesis that females should be more risk-averse than males, females at all three sites specialized in low-cost prey (terrestrial/sedentary prey at Gombe; black and white colobus monkeys at Kanyawara). Female dominance rank was positively correlated with red colobus hunting probability only at Kasekela, suggesting that those in good physical condition were less sensitive to the costs of possible failure. Finally, the potential for carcass appropriation by males deterred females at Kasekela (but not Kanyawara or Mitumba) from hunting in parties containing many adult males. Although chimpanzees are not direct analogs of the last common ancestor (LCA) of Pan and Homo, these results suggest that before the emergence of social obligations regarding sharing and provisioning, constraints on hunting by LCA females did not necessarily stem from maternal care. Instead, they suggest that a risk-averse foraging strategy and the potential for losing prey to males limited female predation on vertebrates. Sex differences in hunting behavior would likely have preceded the evolution of the sexual division of labor among modern humans.

Testosterone and reproductive effort in male primates.

Considerable evidence suggests that the steroid hormone testosterone mediates major life-history trade-offs in vertebrates, promoting mating effort at the expense of parenting effort or survival. Observations from a range of wild primates support the "Challenge Hypothesis," which posits that variation in male testosterone is more closely associated with aggressive mating competition than with reproductive physiology. In both seasonally and non-seasonally breeding species, males increase testosterone production primarily when competing for fecund females. In species where males compete to maintain long-term access to females, testosterone increases when males are threatened with losing access to females, rather than during mating periods. And when male status is linked to mating success, and dependent on aggression, high-ranking males normally maintain higher testosterone levels than subordinates, particularly when dominance hierarchies are unstable. Trade-offs between parenting effort and mating effort appear to be weak in most primates, because direct investment in the form of infant transport and provisioning is rare. Instead, infant protection is the primary form of paternal investment in the order. Testosterone does not inhibit this form of investment, which relies on male aggression. Testosterone has a wide range of effects in primates that plausibly function to support male competitive behavior. These include psychological effects related to dominance striving, analgesic effects, and effects on the development and maintenance of the armaments and adornments that males employ in mating competition.

Origin of the human malaria parasite Plasmodium falciparum in gorillas.

Plasmodium falciparum is the most prevalent and lethal of the malaria parasites infecting humans, yet the origin and evolutionary history of this important pathogen remain controversial. Here we develop a single-genome amplification strategy to identify and characterize Plasmodium spp. DNA sequences in faecal samples from wild-living apes. Among nearly 3,000 specimens collected from field sites throughout central Africa, we found Plasmodium infection in chimpanzees (Pan troglodytes) and western gorillas (Gorilla gorilla), but not in eastern gorillas (Gorilla beringei) or bonobos (Pan paniscus). Ape plasmodial infections were highly prevalent, widely distributed and almost always made up of mixed parasite species. Analysis of more than 1,100 mitochondrial, apicoplast and nuclear gene sequences from chimpanzees and gorillas revealed that 99% grouped within one of six host-specific lineages representing distinct Plasmodium species within the subgenus Laverania. One of these from western gorillas comprised parasites that were nearly identical to P. falciparum. In phylogenetic analyses of full-length mitochondrial sequences, human P. falciparum formed a monophyletic lineage within the gorilla parasite radiation. These findings indicate that P. falciparum is of gorilla origin and not of chimpanzee, bonobo or ancient human origin.

First molar eruption, weaning, and life history in living wild chimpanzees.

Understanding dental development in chimpanzees, our closest living relatives, is of fundamental importance for reconstructing the evolution of human development. Most early hominin species are believed to show rapid ape-like patterns of development, implying that a prolonged modern human childhood evolved quite recently. However, chimpanzee developmental standards are uncertain because they have never been based on living wild individuals. Furthermore, although it is well established that first molar tooth emergence (movement into the mouth) is correlated with the scheduling of growth and reproduction across primates broadly, its precise relation to solid food consumption, nursing behavior, or maternal life history is unknown. To address these concerns we conducted a photographic study of subadult chimpanzees (Pan troglodytes schweinfurthii) in Kanyawara, Kibale National Park, Uganda. Five healthy infants emerged their lower first molars (M1s) by or before 3.3 y of age, nearly identical to captive chimpanzee mean ages (∼3.2 y, n = 53). First molar emergence in these chimpanzees does not directly or consistently predict the introduction of solid foods, resumption of maternal estrous cycling, cessation of nursing, or maternal interbirth intervals. Kanyawara chimpanzees showed adult patterns of solid food consumption by the time M1 reached functional occlusion, spent a greater amount of time on the nipple while M1 was erupting than in the preceding year, and continued to suckle during the following year. Estimates of M1 emergence age in australopiths are remarkably similar to the Kanyawara chimpanzees, and recent reconstructions of their life histories should be reconsidered in light of these findings.

The Paternal Provisioning Hypothesis: effects of workload and testosterone production on men's musculature.

OBJECTIVES: Testosterone supports male reproduction through a broad range of behavioral and physiological effects, including the maintenance of sexually dimorphic muscle used in male-male competition. Although it is often assumed that a persistent relationship exists between men's testosterone production and musculature, most studies either fail to find evidence for such a relationship, or document very weak associations. In nonhuman primates, by contrast, correlations between testosterone and muscle mass are higher. Here, we propose the "Paternal Provisioning Hypothesis," which predicts that men's skeletal muscle is less dependent on the effects of androgens than that of other primates, and more sensitive to the physical demands of men's work. This permits human fathers to downregulate testosterone, which has negative impacts on pair-bonding and parenting effort, but without sacrificing the strength and musculature necessary to provision mates and offspring. METHODS: We tested predictions of the Paternal Provisioning Hypothesis by assessing parental status, salivary testosterone levels, anthropometry, and strength among 122 men (ages 18-78) at the Mogielica Human Ecology Study Site in rural Poland. We chose this population because men practice subsistence agriculture, regularly engaging in physically demanding labor. Grip and chest strength were assessed using a dynamometer, and upper-body musculature was estimated from arm muscle circumference. RESULTS: In this population, testosterone showed no association with measures of strength or musculature, and was lower in older men and pair-bonded fathers. Marital and parental status and workload, by contrast, were positive predictors of muscle mass and strength measures. DISCUSSION: These findings offer support for the Paternal Provisioning Hypothesis.

Screening wild and semi-free ranging great apes for putative sexually transmitted diseases: Evidence of Trichomonadidae infections.

Sexually transmitted diseases (STDs) can persist endemically, are known to cause sterility and infant mortality in humans, and could have similar impacts in wildlife populations. African apes (i.e., chimpanzees, bonobos, and to a lesser extent gorillas) show multi-male mating behavior that could offer opportunities for STD transmission, yet little is known about the prevalence and impact of STDs in this endangered primate group. We used serology and PCR-based detection methods to screen biological samples from wild and orphaned eastern chimpanzees and gorillas (N = 172 individuals, including adults, and juveniles) for four classes of pathogens that either commonly cause human STDs or were previously detected in captive apes: trichomonads, Chlamydia spp., Treponema pallidum (syphilis and yaws), and papillomaviruses. Based on results from prior modeling and comparative research, we expected STD prevalence to be highest in females versus males and in sexually mature versus immature individuals. All samples were negative for Chlamydia, Treponema pallidum, and papillomaviruses; however, a high percentage of wild chimpanzee urine and fecal samples showed evidence of trichomonads (protozoa). Analysis revealed that females were more likely than males to have positive urine-but not fecal-samples; however, there was no evidence of age (sexual maturity) differences in infection status. Sequence analysis of chimpanzee trichomonad samples revealed a close relationship to previously described trichomonads within the genus Tetratrichomonas. Phylogenetic comparisons to archived sequences from multiple vertebrate hosts suggests that many of the chimpanzee parasites from our study are likely transmitted via fecal-oral contact, but the transmission of some Tetratrichomonas sequence-types remains unknown and could include sexual contact. Our work emphasizes that only a fraction of infectious agents affecting wild apes are presently known to science, and that further work on great ape STDs could offer insights for the management of endangered great apes and for understanding human STD origins.