Metabolic acceleration and the evolution of human brain size and life history.

Humans are distinguished from the other living apes in having larger brains and an unusual life history that combines high reproductive output with slow childhood growth and exceptional longevity. This suite of derived traits suggests major changes in energy expenditure and allocation in the human lineage, but direct measures of human and ape metabolism are needed to compare evolved energy strategies among hominoids. Here we used doubly labelled water measurements of total energy expenditure (TEE; kcal day(-1)) in humans, chimpanzees, bonobos, gorillas and orangutans to test the hypothesis that the human lineage has experienced an acceleration in metabolic rate, providing energy for larger brains and faster reproduction without sacrificing maintenance and longevity. In multivariate regressions including body size and physical activity, human TEE exceeded that of chimpanzees and bonobos, gorillas and orangutans by approximately 400, 635 and 820 kcal day(-1), respectively, readily accommodating the cost of humans' greater brain size and reproductive output. Much of the increase in TEE is attributable to humans' greater basal metabolic rate (kcal day(-1)), indicating increased organ metabolic activity. Humans also had the greatest body fat percentage. An increased metabolic rate, along with changes in energy allocation, was crucial in the evolution of human brain size and life history.

Endocrinological effects of social exclusion and inclusion: Experimental evidence for adaptive regulation of female fecundity.

When current conditions are probabilistically less suitable for successful reproduction than future conditions, females may prevent or delay reproduction until conditions improve. Throughout human evolution, social support was likely crucial to female reproductive success. Women may thus have evolved fertility regulation systems sensitive to cues from the social environment. However, current understanding of how psychological phenomena might affect female ovarian function is limited. In this study, we examined whether cues of reduced social support-social ostracism-impact women's hormone production. Following an in-lab group bonding task, women were randomly assigned to a social exclusion (n = 88) or social inclusion (n = 81) condition. After social exclusion, women with low background levels of social support experienced a decrease in estradiol relative to progesterone. In contrast, socially-included women with low background social support experienced an increase in estradiol relative to progesterone. Hormonal changes in both conditions occurred specifically when women were in their mid-to-late follicular phase, when baseline estradiol is high and progesterone is low. Follow-up analyses revealed that these changes were primarily driven by changes in progesterone, consistent with existing evidence for disruption of ovarian function following adrenal release of follicular-phase progesterone. Results offer support for a potential mechanism by which fecundity could respond adaptively to the loss or lack of social support.

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.

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.

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.

Associations between male testosterone and immune function in a pathogenically stressed forager-horticultural population.

OBJECTIVES: Despite well-known fitness advantages to males who produce and maintain high endogenous testosterone levels, such phenotypes may be costly if testosterone-mediated investment in reproductive effort trade-off against investment in somatic maintenance. Previous studies of androgen-mediated trade-offs in human immune function find mixed results, in part because most studies either focus on a few indicators of immunity, are confounded by phenotypic correlation, or are observational. Here the association between male endogenous testosterone and 13 circulating cytokines are examined before and after ex vivo antigen stimulation with phytohemagglutinin (PHA) and lipopolysaccharides (LPS) in a high pathogen population of Bolivian forager-horticulturalists. MATERIALS AND METHODS: A Milliplex 13-plex cytokine panel measured cytokine concentration in whole blood samples from 109 Tsimane men aged 40-89 (median = 50 years) before and after antigen stimulation with PHA and LPS. Urinary testosterone was measured via enzyme immunoassay, demographic, and anthropometric data were collected as part of the Tsimane Health and Life History Project. RESULTS: Higher endogenous testosterone was associated with down-regulated responses in all cytokines after PHA stimulation (but significantly in only 2/13 cytokines), controlling for age and body mass index. In contrast, testosterone was not significantly associated with down-regulation of cytokines after LPS stimulation. MANOVAs indicate that men with higher testosterone showed reduced cytokine responses to PHA compared with LPS (p = 0.0098). DISCUSSION: Endogenous testosterone appears to be immunomodulatory rather than immunosuppressive. Potentially costlier forms of immune activation like those induced by PHA (largely T-cell biased immune activation) are down-regulated in men with higher testosterone, but testosterone has less impact on potentially less costly immune activation following LPS stimulation (largely B-cell mediated immunity).

Depression as sickness behavior? A test of the host defense hypothesis in a high pathogen population.

Sadness is an emotion universally recognized across cultures, suggesting it plays an important functional role in regulating human behavior. Numerous adaptive explanations of persistent sadness interfering with daily functioning (hereafter "depression") have been proposed, but most do not explain frequent bidirectional associations between depression and greater immune activation. Here we test several predictions of the host defense hypothesis, which posits that depression is part of a broader coordinated evolved response to infection or tissue injury (i.e. "sickness behavior") that promotes energy conservation and reallocation to facilitate immune activation. In a high pathogen population of lean and relatively egalitarian Bolivian forager-horticulturalists, we test whether depression and its symptoms are associated with greater baseline concentration of immune biomarkers reliably associated with depression in Western populations (i.e. tumor necrosis factor alpha [TNF-α], interleukin-1 beta [IL-1ß], interleukin-6 [IL-6], and C-reactive protein [CRP]). We also test whether greater pro-inflammatory cytokine responses to ex vivo antigen stimulation are associated with depression and its symptoms, which is expected if depression facilitates immune activation. These predictions are largely supported in a sample of older adult Tsimane (mean±SD age=53.2±11.0, range=34-85, n=649) after adjusting for potential confounders. Emotional, cognitive and somatic symptoms of depression are each associated with greater immune activation, both at baseline and in response to ex vivo stimulation. The association between depression and greater immune activation is therefore not unique to Western populations. While our findings are not predicted by other adaptive hypotheses of depression, they are not incompatible with those hypotheses and future research is necessary to isolate and test competing predictions.

Oxidative stress as an indicator of the costs of reproduction among free-ranging rhesus macaques.

Sex differences in longevity may reflect sex-specific costs of intra-sexual competition and reproductive effort. As male rhesus macaques experience greater intrasexual competition and die younger, we predicted that males would experience greater oxidative stress than females and that oxidative stress would reflect sex-specific measures of reproductive effort. Males, relative to females, had higher concentrations of 8-OHdG and malondialdehyde, which are markers of DNA oxidative damage and lipid peroxidation, respectively. Older macaques had lower 8-OHdG levels than younger ones, suggesting that oxidative stress decreases in parallel with known age-related declines in reproductive investment. Among males, a recent period of social instability affected oxidative status: males who attacked others at higher rates had higher 8-OHdG levels. Multiparous lactating females with daughters had higher 8-OHdG levels than those with sons. No differences in antioxidant capacity were found. These results lend initial support for the use of oxidative stress markers to assess trade-offs between reproductive effort and somatic maintenance in primates.

Testosterone and male cognitive performance in Tsimane forager-horticulturalists.

OBJECTIVE: Testosterone plays a vital role in brain function and behavior. Among humans, age-related decline in testosterone is associated with declining cognitive functioning, and aging men with higher testosterone maintain better cognitive performance. However, most research focuses on industrialized populations with widespread access to formal schooling, high testosterone, and low parasite and pathogen load. We examine whether men's testosterone is associated with cognitive performance among Tsimane forager-horticulturalists of Bolivia despite relatively lower levels of testosterone and higher immune burden. METHODS: Ninety-four Tsimane men aged 36-86 (median = 49) participated in a cognitive battery (assessing short- and long-term recall, digit span, semantic memory, and visual scan) and provided urine and blood samples to measure testosterone and markers of immune activation. Linear mixed effects regressions were used to model associations between cognitive performance and testosterone, controlling for age, years of schooling, Spanish fluency, and village residence. For a subset (n = 66) we included immune activation markers to examine mediator effects. RESULTS: Testosterone is positively associated with short- and long-term verbal memory (ß = 0.267, P = 0.018; ß = 0.326, P = 0.005 respectively) and visual scanning (ß = 0.306, P = 0.008) after controlling for potential confounders. Markers of immune activation were negatively associated with cognitive function, but did not change the associations between testosterone and cognitive performance. CONCLUSION: Tsimane men show positive associations between testosterone and cognitive performance, particularly for recall and visual scanning, despite higher immune burden. Testosterone may help motivate both physical and cognitive capacities that were essential for extracting the difficult-to-acquire, high-quality resources upon which humans relied over evolutionary history.

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.

When the economy falters, do people spend or save? Responses to resource scarcity depend on childhood environments.

Just as modern economies undergo periods of boom and bust, human ancestors experienced cycles of abundance and famine. Is the adaptive response when resources become scarce to save for the future or to spend money on immediate gains? Drawing on life-history theory, we propose that people's responses to resource scarcity depend on the harshness of their early-life environment, as reflected by childhood socioeconomic status (SES). In the three experiments reported here, we tested how people from different childhood environments responded to resource scarcity. We found that people who grew up in lower-SES environments were more impulsive, took more risks, and approached temptations more quickly. Conversely, people who grew up in higher-SES environments were less impulsive, took fewer risks, and approached temptations more slowly. Responses similarly diverged according to people's oxidative-stress levels-a urinary biomarker of cumulative stress exposure. Overall, whereas tendencies associated with early-life environments were dormant in benign conditions, they emerged under conditions of economic uncertainty.

Reproductive ecology of female chimpanzees.

An important adaptive problem for mammals in general, and primates in particular, is how females can manage the high costs of reproduction in the face of fluctuating energetic supplies. For many species, the best solution is to breed seasonally such that high costs are temporally coincident with predictable periods of resource abundance. This is an unreliable strategy for some primates, such as chimpanzees (Pan troglodytes), for which large body size forces an increase in dietary complexity and prolonged reproductive efforts. Here, I review data on reproductive function in chimpanzees, a species that demonstrates a risk-averse reproductive strategy wherein reproductive investment is allocated in accordance with maternal condition. Life history parameters for chimpanzees indicate that most females produce very few surviving offspring. However, comparisons between captive and wild populations and within wild populations illustrate that variation in resource access leads to highly variable reproductive success. Focused hormonal studies have demonstrated these effects at a proximate level, with energetic influences on female dispersal, receptivity, cycle quality, conception success, and lactational amenorrhea. Downstream of these effects, female reproductive function affects sexual attractiveness, and by virtue of males' own optimal reproductive strategies, can lead to coercive aggression and decreased foraging efficiency. Because of their extreme reproductive costs, female chimpanzees utilize a highly conservative reproductive strategy, one that minimizes the costs of ecological variation but makes them vulnerable to sexual conflict and costs of sociality.

Weak, but not strong, ties support coalition formation among wild female chimpanzees.

In social species, individuals may be able to overcome competitive constraints on cooperation by leveraging relationships with familiar, tolerant partners. While strong social ties have been linked to cooperation in several social mammals, it is unclear the extent to which weak social ties can support cooperation, particularly among non-kin. We tested the hypothesis that weakly affiliative social relationships support cooperative coalition formation using 10 years of behavioural data on wild female chimpanzees. Female chimpanzees typically disperse and reside with non-kin as adults. Their social relationships are differentiated but often relatively weak, with few dyads sharing strong bonds. Females occasionally form aggressive coalitions together. Three measures of relationship quality-party association, five-metre proximity and whether a dyad groomed-positively predicted coalitions, indicating that relationship quality influenced coalition partnerships. However, dyads that groomed frequently did not form more coalitions than dyads that groomed occasionally, and kin did not cooperate more than expected given their relationship quality. Thus, strong bonds and kinship did not bolster cooperation. We conclude that cooperative coalitions among female chimpanzees depend on social tolerance but do not require strong bonds. Our findings highlight social tolerance as a distinct pathway through which females can cultivate cooperative relationships. This article is part of the theme issue 'Cooperation among women: evolutionary and cross-cultural perspectives'.

Demographic and hormonal evidence for menopause in wild chimpanzees.

Among mammals, post-reproductive life spans are currently documented only in humans and a few species of toothed whales. Here we show that a post-reproductive life span exists among wild chimpanzees in the Ngogo community of Kibale National Park, Uganda. Post-reproductive representation was 0.195, indicating that a female who reached adulthood could expect to live about one-fifth of her adult life in a post-reproductive state, around half as long as human hunter-gatherers. Post-reproductive females exhibited hormonal signatures of menopause, including sharply increasing gonadotropins after age 50. We discuss whether post-reproductive life spans in wild chimpanzees occur only rarely, as a short-term response to favorable ecological conditions, or instead are an evolved species-typical trait as well as the implications of these alternatives for our understanding of the evolution of post-reproductive life spans.

Vocal signals facilitate cooperative hunting in wild chimpanzees.

Cooperation and communication likely coevolved in humans. However, the evolutionary roots of this interdependence remain unclear. We address this issue by investigating the role of vocal signals in facilitating a group cooperative behavior in an ape species: hunting in wild chimpanzees. First, we show that bark vocalizations produced before hunt initiation are reliable signals of behavioral motivation, with barkers being most likely to participate in the hunt. Next, we find that barks are associated with greater hunter recruitment and more effective hunting, with shorter latencies to hunting initiation and prey capture. Our results indicate that the coevolutionary relationship between vocal communication and group-level cooperation is not unique to humans in the ape lineage and is likely to have been present in our last common ancestor with chimpanzees.

Under threat of social exclusion, females exclude more than males.

Theoretical analyses and studies with children suggest that females are more likely than males to respond to threats of social exclusion with exclusion. Here we present a series of studies using a modified version of a computerized competitive game that participants play against two fictitious opponents. In previous studies, females and males have typically made identical strategy choices when playing this game. We show that when players are told that the two fictitious opponents may form an exclusionary alliance against them, females modify their competitive strategies by forming more preventive exclusionary alliances than males do. These results support the idea that adult females are more likely than males to form preventive exclusionary alliances when faced with a social threat. The results further suggest that females and males compete in different ways.

Testosterone and romance: the association of testosterone with relationship commitment and satisfaction in heterosexual men and women.

OBJECTIVES: The current study extends previous research on testosterone (T) and mating effort by examining whether relationship commitment and satisfaction explain variance in T beyond relationship status alone. METHODS: Salivary testosterone and self-reported assessments of relationship commitment and satisfaction were assessed among 90 heterosexual men and women (age M = 23.57) in a cross-sectional community sample. RESULTS: Relationship commitment was significantly related to T among men (P < 0.01), with increasing levels of commitment predicting lower T, even among paired men (P < 0.05). In contrast, relationship commitment was not related to women's T (P > 0.05). Controlling for relationship commitment, satisfaction did not predict T levels in men or women (P's > 0.18). CONCLUSIONS: The association of increasing relationship commitment with reduced T levels in men confirms and extends prior research linking T with mating effort. Together with previous research, this study suggests that T does not vary with relationship commitment or quality in monogamous, heterosexual women.

Primate Reproduction: When Timing Is Everything.

In species with intense male competition, reproducing at the wrong time can have dire consequences for females. A new study of wild gelada monkeys finds that females delay or accelerate puberty to moderate the risks of inbreeding and infanticide.

Evolution of water conservation in humans.

To sustain life, humans and other terrestrial animals must maintain a tight balance of water gain and water loss each day.1-3 However, the evolution of human water balance physiology is poorly understood due to the absence of comparative measures from other hominoids. While humans drink daily to maintain water balance, rainforest-living great apes typically obtain adequate water from their food and can go days or weeks without drinking4-6. Here, we compare isotope-depletion measures of water turnover (L/d) in zoo- and rainforest-sanctuary-housed apes (chimpanzees, bonobos, gorillas, and orangutans) with 5 diverse human populations, including a hunter-gatherer community in a semi-arid savannah. Across the entire sample, water turnover was strongly related to total energy expenditure (TEE, kcal/d), physical activity, climate (ambient temperature and humidity), and fat free mass. In analyses controlling for those factors, water turnover was 30% to 50% lower in humans than in other apes despite humans' greater sweating capacity. Water turnover in zoo and sanctuary apes was similar to estimated turnover in wild populations, as was the ratio of water intake to dietary energy intake (∼2.8 mL/kcal). However, zoo and sanctuary apes ingested a greater ratio of water to dry matter of food, which might contribute to digestive problems in captivity. Compared to apes, humans appear to target a lower ratio of water/energy intake (∼1.5 mL/kcal). Water stress due to changes in climate, diet, and behavior apparently led to previously unknown water conservation adaptations in hominin physiology.