Aging In Chimpanzees Research Articles

Age-related physiological dysregulation progresses slowly in semi-free-ranging chimpanzees.

Lifestyle has widespread effects on human health and aging. Prior results from chimpanzees (Pan troglodytes), one of humans' closest evolutionary relatives, indicate that these lifestyle effects may also be shared with other species, as semi-free-ranging chimpanzees fed a naturalistic diet show healthier values in several specific health biomarkers, compared with their sedentary, captive counterparts. Here, we examined how lifestyle factors associated with different environments affect rates of physiological aging in closely related chimpanzees. We compared physiological dysregulation, an index of biological aging, in semi-free-ranging chimpanzees in an African sanctuary versus captive chimpanzees in US laboratories. If the rate of aging is accelerated by high-calorie diet and sedentism, we predicted greater age-related dysregulation in the laboratory populations. Conversely, if costs of a wild lifestyle accelerate aging, then semi-free-ranging chimpanzees at the sanctuary, whose environment better approximates the wild, should show greater age-related dysregulation. We further tested whether dysregulation differed based on sex or body system, as in humans. We found that semi-free-ranging chimpanzees showed lower overall dysregulation, as well as lower age-related change in dysregulation, than laboratory chimpanzees. Males experienced lower dysregulation than females in both contexts, and the two populations exhibited distinct aging patterns based on body system. Our results support the conclusion that naturalistic living conditions result in healthier aging in chimpanzees. These data provide support for the proposal that lifestyle effects on human health and aging are conserved from deeper into our evolutionary history.

Multimodal communication development in semiwild chimpanzees

Human language is characterized by the integration of multiple signal modalities, including speech, facial and gestural signals. While language likely has deep evolutionary roots that are shared with some of our closest living relatives, studies of great ape communication have largely focused on each modality separately, thus hindering insights into the origins of its multimodal nature. Studying when multimodal signals emerge during great ape ontogeny can inform about both the proximate and ultimate mechanisms underlying their communication systems, shedding light on potential evolutionary continuity between humans and other apes. To this end, the current study investigated developmental patterns of multimodal signal production by 28 semiwild chimpanzees, Pan troglodytes, ranging in age from infancy to early adolescence. We examined the production of facial expressions, gestures and vocalizations across a range of behavioural contexts, both when produced separately and as part of multimodal signal combinations (henceforth multimodal). Overall, we found that while unimodal signals were produced consistently more often than multimodal combinations across all ages and contexts, the frequency of multimodal combinations increased significantly in older individuals and most within the aggression and play contexts, where the costs of signalling ambiguity may be higher. Furthermore, older individuals were more likely to produce a multimodal than a unimodal signal and, again, especially in aggressive contexts. Variation in production of individual signal modalities across ages and contexts are also presented and discussed. Overall, evidence that multimodality increases with age in chimpanzees is consistent with patterns of developing communicative complexity in human infancy, revealing apparent evolutionary continuity. Findings from this study contribute novel insights into the evolution and development of multimodality and highlight the importance of adopting a multimodal approach in the comparative study of primate communication.

Face to face interactions in chimpanzee (Pan troglodytes) and human (Homo sapiens) mother-infant dyads.

Human mothers interact with their infants in different ways. In Western, educated, industrialized, rich and democratic (WEIRD) societies, face-to-face interactions and mutual gazes are especially frequent, yet little is known about their developmental trajectories and if they differ from those of other primates. Using a cross-species developmental approach, we compared mother-infant interactions in 10 dyads of urban humans from a WEIRD society (Homo sapiens) and 10 dyads of captive zoo-based chimpanzees (Pan troglodytes), when infants were one, six and 12 months old. Results showed that face-to-face interactions with mutual gaze events were common in both groups throughout the infant's first year of life. The developmental trajectories of maternal and infants' looks partially differed between species, but mutual gaze events were overall longer in humans than in chimpanzees. Mutual gazes were also more frequent in humans, peaking at six months in humans, while increasing with age in chimpanzees. The duration and frequency of mutual gazes varied across contexts in both groups, with mutual gazes being longer during caring/grooming and feeding contexts. These findings confirm that some aspects of early socio-cognitive development are shared by humans and other primates, and highlight the importance of combining developmental and cross-species approaches to better understand the evolutionary roots of parenting behaviour. This article is part of a discussion meeting issue 'Face2face: advancing the science of social interaction'.

Age, adrenal steroids, and cognitive functioning in captive chimpanzees (Pan troglodytes).

Dehydroepiandrosterone-sulfate is the most abundant circulating androgen in humans and other catarrhines. It is involved in several biological functions, such as testosterone production, glucocorticoid antagonist actions, neurogenesis and neuroplasticty. Although the role of dehydroepiandrosterone-sulfate (DHEAS) in cognition remains elusive, the DHEAS/cortisol ratio has been positively associated with a slower cognitive age-decline and improved mood in humans. Whether this relationship is found in nonhuman primates remains unknown. We measured DHEAS and cortisol levels in serum of 107 adult chimpanzees to investigate the relationship between DHEAS levels and age. A subset of 21 chimpanzees was used to test the potential associations between DHEAS, cortisol, and DHEAS/cortisol ratio in cognitive function, taking into account age, sex, and their interactions. We tested for cognitive function using the primate cognitive test battery (PCTB) and principal component analyses to categorize cognition into three components: spatial relationship tasks, tool use and social communication tasks, and auditory-visual sensory perception tasks. DHEAS levels, but not the DHEAS/cortisol ratio, declined with age in chimpanzees. Our analyses for spatial relationships tasks revealed a significant, positive correlation with the DHEAS/cortisol ratio. Tool use and social communication had a negative relationship with age. Our data show that the DHEAS/cortisol ratio, but not DHEAS individually, is a promising predictor of spatial cognition in chimpanzees.

Age-related change in adult chimpanzee social network integration.

BackgroundSocial isolation is a key risk factor for the onset and progression of age-related disease and mortality in humans. Nevertheless, older people commonly have narrowing social networks, with influences from both cultural factors and the constraints of senescence. We evaluate evolutionarily grounded models by studying social aging in wild chimpanzees, a system where such influences are more easily separated than in humans, and where individuals are long-lived and decline physically with age.MethodologyWe applied social network analysis to examine age-related changes in social integration in a 7+ year mixed-longitudinal dataset on 38 wild adult chimpanzees (22 females, 16 males). Metrics of social integration included social attractivity and overt effort (directed degree and strength), social roles (betweenness and local transitivity) and embeddedness (eigenvector centrality) in grooming networks.ResultsBoth sexes reduced the strength of direct ties with age (males in-strength, females out-strength). However, males increased embeddedness with age, alongside cliquishness. These changes were independent of age-related changes in social and reproductive status. Both sexes maintained highly repeatable inter-individual differences in integration, particularly in mixed-sex networks.Conclusions and implicationsAs in humans, chimpanzees appear to experience senescence-related declines in social engagement. However, male social embeddedness and overall sex differences were patterned more similarly to humans in non-industrialized versus industrialized societies. Such comparisons suggest common evolutionary roots to ape social aging and that social isolation in older humans may hinge on novel cultural factors of many industrialized societies. Lastly, individual and sex differences are potentially important mediators of successful social aging in chimpanzees, as in humans. Lay summary: Few biological models explain why humans so commonly have narrowing social networks with age, despite the risk factor of social isolation that small networks pose. We use wild chimpanzees as a comparative system to evaluate models grounded in an evolutionary perspective, using social network analysis to examine changes in integration with age. Like humans in industrialized populations, chimpanzees had lower direct engagement with social partners as they aged. However, sex differences in integration and older males’ central positions within the community network were more like patterns of sociality in several non-industrialized human populations. Our results suggest common evolutionary roots to human and chimpanzee social aging, and that the risk of social isolation with age in industrialized populations stems from novel cultural factors.

Demography, life-history trade-offs, and the gastrointestinal virome of wild chimpanzees.

In humans, senescence increases susceptibility to viral infection. However, comparative data on viral infection in free-living non-human primates-even in our closest living relatives, chimpanzees and bonobos (Pan troglodytes and P. paniscus)-are relatively scarce, thereby constraining an evolutionary understanding of age-related patterns of viral infection. We investigated a population of wild eastern chimpanzees (P. t. schweinfurthii), using metagenomics to characterize viromes (full viral communities) in the faeces of 42 sexually mature chimpanzees (22 males, 20 females) from the Kanyawara and Ngogo communities of Kibale National Park, Uganda. We identified 12 viruses from at least four viral families possessing genomes of both single-stranded RNA and single-stranded DNA. Faecal viromes of both sexes varied with chimpanzee age, but viral richness increased with age only in males. This effect was largely due to three viruses, salivirus, porprismacovirus and chimpanzee stool-associated RNA virus (chisavirus), which occurred most frequently in samples from older males. This finding is consistent with the hypothesis that selection on males for early-life reproduction compromises investment in somatic maintenance, which has delayed consequences for health later in life, in this case reflected in viral infection and/or shedding. Faecal viromes are therefore useful for studying processes related to the divergent reproductive strategies of males and females, ageing, and sex differences in longevity. This article is part of the theme issue 'Evolution of the primate ageing process'.

Astrocytic changes with aging and Alzheimer's disease-type pathology in chimpanzees.

Astrocytes are the main homeostatic cell of the central nervous system. In addition, astrocytes mediate an inflammatory response when reactive to injury or disease known as astrogliosis. Astrogliosis is marked by an increased expression of glial fibrillary acidic protein (GFAP) and cellular hypertrophy. Some degree of astrogliosis is associated with normal aging and degenerative conditions such as Alzheimer's disease (AD) and other dementing illnesses in humans. The recent observation of pathological markers of AD (amyloid plaques and neurofibrillary tangles) in aged chimpanzee brains provided an opportunity to examine the relationships among aging, AD-type pathology, and astrocyte activation in our closest living relatives. Stereologic methods were used to quantify GFAP-immunoreactive astrocyte density and soma volume in layers I, III, and V of the prefrontal and middle temporal cortex, as well as in hippocampal fields CA1 and CA3. We found that the patterns of astrocyte activation in the aged chimpanzee brain are distinct from humans. GFAP expression does not increase with age in chimpanzees, possibly indicative of lower oxidative stress loads. Similar to humans, chimpanzee layer I astrocytes in the prefrontal cortex are susceptible to AD-like changes. Both prefrontal cortex layer I and hippocampal astrocytes exhibit a high degree of astrogliosis that is positively correlated with accumulation of amyloid beta and tau proteins. However, unlike humans, chimpanzees do not display astrogliosis in other cortical layers. These results demonstrate a unique pattern of cortical aging in chimpanzees and suggest that inflammatory processes may differ between humans and chimpanzees in response to pathology.

Age-related decline in cognitive flexibility in female chimpanzees.

Data on cognitive aging in chimpanzees are extremely sparse, yet can provide an invaluable phylogenetic perspective, especially because Alzheimer disease (AD)-like neuropathology has recently been described in the oldest chimpanzee brains. This finding underscores the importance of data on cognitive aging in this fellow hominin, our closest biological relative. We tested 30 female chimpanzees, 12-56years old, on a computerized analog of the Wisconsin Card Sort test. This test assesses cognitive flexibility, which is severely impaired in normal aging and AD. Subjects selected stimuli according to color or shape; the rewarded dimension (i.e., color or shape) switched without warning and the chimpanzee had to adapt her responses accordingly. We found that increasing age was associated with an increased number of perseverative errors and an increased number of trials to reach criterion in each switching dimension. The number of aborted trials was similar across age groups. These data show that similar to humans, chimpanzees show a clear age-related decline in cognitive flexibility that is already observed at middleage.

Estimation of chimpanzee age based on DNA methylation

In wild animal conservation, knowing the age of an individual animal is extremely beneficial. However, estimating the age is difficult for many species. Recently, epigenetics-based methods of estimating age have been reported. These studies were predominantly on humans with few reports on other animals, especially wild animals. In the present study, a chimpanzee (Pan troglodytes) age prediction model was developed based on the ELOVL2, CCDC102B, and ZNF423 genes that may also have application in human age prediction. Pyrosequencing was used to measure methylation in 20 chimpanzee blood samples and correlation between age and methylation status was calculated. Age and methylation of sites in ELOVL2 and CCDC102B were significantly correlated and an age prediction model was created using these genes. In the regression equation using only ELOVL2, the highest correlation coefficient was 0.741, with a mean absolute deviation (MAD) of 5.41, compared with the combination of ELOVL2 and CCDC102B, where the highest correlation coefficient was 0.742 and the MAD was 5.41. Although larger MADs were observed in chimpanzees than in humans based on these genes, the results indicate the feasibility of estimating chimpanzee age using DNA methylation, and can have implications in understanding the ecology of chimpanzees and chimpanzee conservation.

Long bone cross-sectional properties reflect changes in locomotor behavior in developing chimpanzees.

Recent studies indicate that the locomotor behavior of wild chimpanzees changes during development. Before transitioning to quadrupedal knuckle-walking in adulthood, young chimpanzees engage in a significant amount of upper limb loading suspensory behavior. We investigated whether these dramatic changes in locomotion influence the strength and shape of chimpanzee long bones. We examined changes in chimpanzee arboreal locomotion over the course of development using behavioral data collected on wild chimpanzees. We measured the midshaft geometric properties of femora and humeri of wild-caught individuals housed in museum collections using micro computed tomographic scans. Chimpanzees spent less time moving arboreally as they aged. Femoral/humeral strength ratios also increased with age, as predicted by the changing loading environment during development. Additional analyses revealed that femoral shape, but not humeral shape, varied across chimpanzee age classes. Adult femora were more elliptical compared with those of infants. This change in adult femora is consistent with the observation that adult chimpanzees spend most of their time moving terrestrially and consequently experience a less variable loading environment than do infants. Taken together, these findings contribute to our understanding of how ontogenetic changes in function affect form. As similar changes may have characterized the behavioral and skeletal ontogeny of extinct hominoids including hominins, these findings furnish a potential means to make inferences about the behavior of fossil taxa based on the structural properties of their bones.

How much more would KNM-WT 15000 have grown?

Because of its completeness, the juvenile Homo ergaster/erectus KNM-WT 15000 has played an important role in studies of the evolution of body form in Homo. Early attempts to estimate his adult body size used modern human growth models. However, more recent evidence, particularly from the dentition, suggests that he may have had a more chimpanzee-like growth trajectory. Here we re-estimate his adult stature and body mass using ontogenetic data derived from four African ape taxa: Pan troglodytes troglodytes, Pan troglodytes schweinfurthii, Pan paniscus, and Gorilla gorilla gorilla. The average percentage change in femoral and tibial lengths and femoral head breadth between individuals at the same stage of dental development as KNM-WT 15000 – eruption of M2s but not M3s – and adult individuals with fully fused long bone epiphyses, was determined. Results were then applied to KNM-WT 15000, and his adult size estimated from skeletal dimensions using modern human prediction formulae. Using this approach, adult stature best estimates of 176–180 cm and body mass best estimates of 80–83 kg were obtained. These estimates are close to those estimated directly from longitudinal changes in body length and body mass between 8 and 12 years of age in chimpanzees, the suggested chronological equivalent to KNM-WT 15000's remaining growth period. Thus, even using an African ape growth model, it is likely that KNM-WT 15000 would have attained close to 180 cm in stature (without a slight reduction for his lower cranial height) and 80 kg in body mass as an adult. Other evidence from the East African Early Pleistocene indicates that KNM-WT 15000 was not unusually large-bodied for his time period.

Cognitive and motor aging in female chimpanzees

We present the first longitudinal data on cognitive and motor aging in the chimpanzee (Pan troglodytes). Thirty-eight adult female chimpanzees (10–54 years old) were studied. The apes were tested longitudinally for 3 years in a modified Primate Cognition Test Battery, which comprised 12 tests of physical and social cognition. The chimpanzees were also administered a fine motor task requiring them to remove a steel nut from rods of various complexity. There was little evidence for an age-related decline in tasks of Physical Cognition: for most tasks, performance was either stable or improved with repeated testing across age groups. An exception was Spatial Memory, for which 4 individuals more than 50 years old experienced a significant performance decline across the 3 years of testing. Poorer performance with age was found in 2 tasks of Social Cognition, an attention-getting task and a gaze-following task. A slight motor impairment was also observed, with old chimpanzees improving less than younger animals with repeated testing on the simplest rod. Hormonal status effects were restricted to spatial memory, with non-cycling females outperforming cycling females independently of age. Unexpectedly, older chimpanzees were better than younger individuals in understanding causality relationships based on sound.

Brain aging in humans, chimpanzees (Pan troglodytes), and rhesus macaques (Macaca mulatta): magnetic resonance imaging studies of macro- and microstructural changes

Among primates, humans are uniquely vulnerable to many age-related neurodegenerative disorders. We used structural and diffusion magnetic resonance imaging (MRI) to examine the brains of chimpanzees and rhesus monkeys across each species' adult lifespan, and compared these results with published findings in humans. As in humans, gray matter volume decreased with age in chimpanzees and rhesus monkeys. Also like humans, chimpanzees showed a trend for decreased white matter volume with age, but this decrease occurred proportionally later in the chimpanzee lifespan than in humans. Diffusion MRI revealed widespread age-related decreases in fractional anisotropy and increases in radial diffusivity in chimpanzees and macaques. However, both the fractional anisotropy decline and the radial diffusivity increase started at a proportionally earlier age in humans than in chimpanzees. Thus, even though overall patterns of gray and white matter aging are similar in humans and chimpanzees, the longer lifespan of humans provides more time for white matter to deteriorate before death, with the result that some neurological effects of aging may be exacerbated in our species.

Menopause occurs late in life in the captive chimpanzee (Pan troglodytes).

Menopause in women occurs at mid-life. Chimpanzees, in contrast, continue to display cycles of menstrual bleeding and genital swelling, suggestive of ovulation, until near their maximum life span of about 60 years. Because ovulation was not confirmed hormonally, however, the age at which chimpanzees experience menopause has remained uncertain. In the present study, we provide hormonal data from urine samples collected from 30 female chimpanzees, of which 9 were old (>30 years), including 2 above the age of 50 years. Eight old chimpanzees showed clear endocrine evidence of ovulation, as well as cycles of genital swelling that correlated closely with measured endocrine changes. Endocrine evidence thus confirms prior observations (cyclic anogenital swelling) that menopause is a late-life event in the chimpanzee. We also unexpectedly discovered an idiopathic anovulation in some young and middle-aged chimpanzees; this merits further study. Because our results on old chimpanzees validate the use of anogenital swelling as a surrogate index of ovulation, we were able to combine data on swelling and urinary hormones to provide the first estimates of age-specific rates of menopause in chimpanzees. We conclude that menopause occurs near 50 years of age in chimpanzees as it does in women. Our finding identifies a basic difference between the human and chimpanzee aging processes: female chimpanzees can remain reproductively viable for a greater proportion of their life span than women. Thus, while menopause marks the end of the chimpanzee's life span, women may thrive for decades more.

“Reproductive aging in captive and wild common chimpanzees: factors influencing the rate of follicular depletion,” by S. Atsalis and E. Videan, American Journal of Primatology 71, 271–282 (2009)

Atsalis and Videan [2009] conclude that the ‘‘occurrence of a postreproductive life span [is] more evident in some species of captive populations that can live for a long time beyond what is foreseen by the follicular store.’’ Specifically, they contend that captivity causes chimpanzees to undergo more ovulations than do chimpanzees in the wild, so that they experience menopause earlier. Central to this contention is the premise that ‘‘despite the increased longevity generally observed in captive populations reproductive life span is shortened.’’ We point out in this commentary that most published evidence on the timing of menopause in chimpanzees, including our own work, contradicts this premise, instead suggesting that menopause occurs late in the life span of the captive chimpanzee. The authors cite Emery Thompson et al. [2007] as support for their claim that chimpanzees reproduce into their 40s in the wild. The conclusion that menopause has occurred by age 40 in captive chimpanzees is based upon a study by Videan et al. [2006], which claimed that menopause occurs at 35–40 years of age in the chimpanzees. This conclusion was not based upon observation of menses or cycles of ovulation, but rather upon determination of gonadotrophin levels in two samples each year obtained from 14 female chimpanzees, 3 of which were over the age of 40. The criterion for menopause was the presence of FSH levels greater than 14 IU/ mL. The conclusion that menopause is reached between 35 and 40 years of age was based upon mean FSH in each age group. Studies using other methods have reached different conclusions. The first published study on reproductive aging in captive chimpanzees [Graham, 1979] examined ten female chimpanzees aged 35–48 years old at the Yerkes National Primate Research Center (YNPRC). At least one menstrual cycle was observed within 1 year of death in each of these individuals. In a subsequent study, also conducted at the YNPRC, Gould et al. [1981] observed two common chimpanzees and one bonobo over the age of 40. They concluded that the bonobo (Pan paniscus) was menopausal, based on cessation of menses and anogenital swelling, elevated gonadotropins and ovarian histology. Unfortunately, the precise age of this individual was unknown. Importantly, the two common chimpanzees (Pan troglodytes) continued to experience menstrual cyclicity at ages 48 and 50. Our larger study of menstrual cycles in 89 chimpanzees at the YNPRC [Lacreuse et al., 2008] confirms the findings of Gould et al. [1981] and contradicts the findings of the Videan et al. [2006]. Our study was based upon observations of cycles of menstrual bleeding and included observations of 20 individuals past the age of 40 years; all 20 of these individuals displayed menstrual cycles after the age of 40; one chimpanzee gave birth at the age of 42, two years past the age suggested as the age of menopause for captive chimpanzees. Since this birth occured in the same year (1997) that the US moratorium on chimpanzee breeding was begun, we do not know whether births may have occurred at even later maternal ages. Indeed, a recent paper reports that a chimpanzee in a zoo in Switzerland gave birth to a healthy infant at a documented age of 49 years; this chimpanzee’s only other infant (to date!) was born when the mother was 42 [Puschmann & Federer, 2008]. This late fertility is consistent with our population at YNPRC, where

Brief communication: Methods of sequence heterochrony for describing modular developmental changes in human evolution

Interest in the developmental changes leading to apomorphic features of human anatomy is longstanding. Although most research has focused on quantitative measures of size and shape, additional information may be available in the sequence of events in development, including aspects of phenotypic integration. I apply two recently proposed techniques for analyzing developmental sequences to literature data on human and chimpanzee age of limb element ossification center appearance in radiographs. The event-pair cracking method of Jeffery et al. (Syst Biol 51 [2002] 478-491) offers little additional insight on sequence differences in this data set than a simpler difference of ranks. Both reveal shifts in timing that are likely related to locomotor differences between the two species. Poe's (Evolution 58 [2004] 1852-1855) test for modularity in a sequence identifies the ankle, wrist, and hind limb as developmental modules, which may correspond to localized combinations of developmental genes. Ossification patterns of the rays of the hand and foot show little modularity. Integrating these and other methods of sequence analysis with traditional metrics of size and shape remains an underdeveloped area of inquiry.

Effects of aging on hematology and serum clinical chemistry in chimpanzees (Pan troglodytes)

A number of age-related changes in physiological functions have been identified in macaques and humans. However, few studies have examined physiological aging in chimpanzees, despite the increasing age of the chimpanzee population. We documented age-related changes in seven hematology and 17 clinical chemistry parameters in 49 adult chimpanzees (17 males, 32 females) as a comparative viewpoint with human and macaque aging. Longitudinal data were analyzed using weighted linear and quadratic mixed effects regression models. Male chimpanzees exhibited a significant age-related increase in anemia risk, based on significant decreases in hemoglobin (F(1,49)=12.45, P=0.0009) and hematocrit (F(1,49)=15.42, P=0.0003). Both sexes exhibited significant age-related decreases in both kidney and liver function. Decreases in kidney function were noted by significant increases in blood urea nitrogen (F(1,45)=3.92, P=0.036) and creatinine (F(1,50)=5.63, P=0.022) as well as changes in electrolyte (i.e., sodium, potassium, phosphorous, chloride) balance. Declining liver function was based on significant increases in globulin (F(1,46)=32.34, P<0.0001) and decreases in albumin (F(1,48)=23.42, P<0.0001). These changes were most evident beginning at 25-30 years of age in males and 30-35 years of age in females. We recommend amending chimpanzee age classes to categorize males over 25 years and females over 30 years as aged.

Depletion of Ovarian Follicles with Age in Chimpanzees: Similarities to Humans1

We retrieved ovarian sections taken from necropsies of 19 captive chimpanzees (Pan troglodytes) aged 0-47 yr, counted the number of primordial follicles in each, and compared the rate of decline in numbers to declines previously documented in humans. The follicular depletion rate in this sample was indistinguishable from that shown across the same ages in classic human data sets. This result supports earlier suggestions that ovarian senescence occurs at the same ages in chimpanzees and humans, implying that the influence of declining ovarian function on other physiologic systems may be distinctively buffered in humans.

Comparing maternal styles in bonobos (Pan paniscus) and chimpanzees (Pan troglodytes)

Studies on Cercopithecine primate maternal styles, using factor analysis on a set of maternal behaviors, commonly render two factors that describe separate dimensions of maternal behavior: protectiveness and rejection. The aims of this study were to 1) investigate whether this method for determining maternal styles in Cercopithecine species can be applied to bonobos (Pan paniscus) and chimpanzees (Pan troglodytes), 2) determine whether they follow the same pattern, and 3) assess whether species differences in maternal style are apparent. We performed a factor analysis on nine maternal behaviors using data on eight mother-infant pairs of each species. This resulted in three factors: protectiveness, distance, and refusal. Protectiveness is positively correlated with time spent in ventral contact, making contact, approaching, and restraining. Distance is positively related with breaking contact and leaving. Refusal is positively correlated with rejecting and nipple-rejecting. The pattern of protectiveness corresponds with the pattern found in Cercopithecine species, suggesting a high consistency of this dimension across species and higher taxa. The retention of the other two factors indicates that in the Pan species, breaking contact and leaving represent another dimension, apart from rejecting and nipple-rejecting, which usually fall under one dimension in Cercopithecine species. An interspecific comparison of the factor scores for each dimension of maternal behavior reveals that, on average, bonobos and chimpanzees score equally on protectiveness. Scores on distance increase positively with infant age in chimpanzees, and negatively in bonobos, and on average bonobos have higher scores on refusal. These interspecies differences in maternal style are discussed in the light of interspecies differences in infant development, infant vulnerability to aggression, interbirth intervals, and female sociality.

Strategy for identifying biomarkers of aging in long-lived species.

If effective anti-aging interventions are to be identified for human application, then the development of reliable and valid biomarkers of aging are essential for this progress. Despite the apparent demand for such gerotechnology, biomarker research has become a controversial pursuit. Much of the controversy has emerged from a lack of consensus on terminology and standards for evaluating the reliability and validity of candidate biomarkers. The initiation of longitudinal studies of aging in long-lived non-human primates has provided an opportunity for establishing the reliability and validity of biomarkers of aging potentially suitable for human studies. From the primate study initiated in 1987 at the National Institute on Aging (NIA), the following criteria for defining a biomarker of aging have been offered: (1) significant cross-sectional correlation with age; (2) significant longitudinal change in the same direction as the cross-sectional correlation; (3) significant stability of individual differences over time. These criteria relate to both reliability and validity. However, the process of validating a candidate biomarker requires a greater standard of proof. Ideally, the rate of change in a biomarker of aging should be predictive of lifespan. In short-lived species, such as rodents, populations differing in lifespan can be identified, such as different strains of rodents or groups on different diets, such as those subjected to calorie restriction (CR), which live markedly longer. However, in the NIA primate study, the objective is to demonstrate that CR retards the rate of aging and increases lifespan. In the absence of lifespan data associated with CR in primates, validation of biomarkers of aging must rely on other strategies of proof. With this challenge, we have offered the following strategy: If a candidate biomarker is a valid measure of the rate of aging, then the rate of age-related change in the biomarker should be proportional to differences in lifespan among related species. Thus, for example, the rate of change in a candidate biomarker of aging in chimpanzees should be twice that of humans (60 vs 120 years maximum lifespan); in rhesus monkeys three times that of humans (40 vs 120 years maximum lifespan). The realization of this strategy will be aided by developing a primate aging database, a project that was recently launched in cooperation with the NIA, the National Center for Research Resources, and the University of Wisconsin Regional Primate Research Center.