[show abstract][hide abstract] ABSTRACT: Women rarely give birth after ∼45 y of age, and they experience the cessation of reproductive cycles, menopause, at ∼50 y of age after a fertility decline lasting almost two decades. Such reproductive senescence in mid-lifespan is an evolutionary puzzle of enduring interest because it should be inherently disadvantageous. Furthermore, comparative data on reproductive senescence from other primates, or indeed other mammals, remains relatively rare. Here we carried out a unique detailed comparative study of reproductive senescence in seven species of nonhuman primates in natural populations, using long-term, individual-based data, and compared them to a population of humans experiencing natural fertility and mortality. In four of seven primate species we found that reproductive senescence occurred before death only in a small minority of individuals. In three primate species we found evidence of reproductive senescence that accelerated throughout adulthood; however, its initial rate was much lower than mortality, so that relatively few individuals experienced reproductive senescence before death. In contrast, the human population showed the predicted and well-known pattern in which reproductive senescence occurred before death for many women and its rate accelerated throughout adulthood. These results provide strong support for the hypothesis that reproductive senescence in midlife, although apparent in natural-fertility, natural-mortality populations of humans, is generally absent in other primates living in such populations.
Proceedings of the National Academy of Sciences 07/2013; · 9.74 Impact Factor
[show abstract][hide abstract] ABSTRACT: This article is part of a Special Issue "Puberty and Adolescence". The onset of reproduction is preceded by a host of organismal adjustments and transformations, involving morphological, physiological, and behavioral changes. In highly social mammals, including humans and most nonhuman primates, the timing and nature of maturational processes are affected by the animal's social milieu as well as its ecology. Here, we review a diverse set of findings on how maturation unfolds in wild baboons in the Amboseli basin of southern Kenya, and we place these findings in the context of other reports of maturational processes in primates and other mammals. First, we describe the series of events and processes that signal maturation in female and male baboons. Sex differences in age at both sexual maturity and first reproduction documented for this species are consistent with expectations of life history theory; males mature later than females and exhibit an adolescent growth spurt that is absent or minimal in females. Second, we summarize what we know about sources of variance in the timing of maturational processes including natal dispersal. In Amboseli, individuals in a food-enhanced group mature earlier than their wild-feeding counterparts, and offspring of high-ranking females mature earlier than offspring of low-ranking females. We also report on how genetic admixture, which occurs in Amboseli between two closely related baboon taxa, affects individual maturation schedules.
Hormones and Behavior 07/2013; 64(2):240-9. · 3.74 Impact Factor
[show abstract][hide abstract] ABSTRACT: Intraspecific competition is a key factor shaping space-use strategies and movement decisions in many species, yet how and when neighbors utilize shared areas while exhibiting active avoidance of one another is largely unknown. Here we investigated temporal landscape partitioning in a population of wild baboons (Papio cynocephalus). We used global positioning system (GPS) collars to synchronously record the hourly locations of 5 baboon social groups for ~900 days, and we used behavioral, demographic, and life history data to measure factors affecting use of overlap areas. Annual home ranges of neighboring groups overlapped substantially, as predicted (baboons are considered non-territorial), but home ranges overlapped less when space use was assessed over shorter time scales. Moreover, neighboring groups were in close spatial proximity to one another on fewer days than predicted by a null model, suggesting an avoidance-based spacing pattern. At all time scales examined (monthly, biweekly, and weekly), time spent in overlap areas was greater during time periods when groups fed on evenly dispersed, low-quality foods. The percent of fertile females in social groups was negatively correlated with time spent in overlap areas only during weekly time intervals. This suggests that broad temporal changes in ecological resources are a major predictor of how intensively overlap areas are used, and groups modify these ecologically driven spacing patterns at short time scales based on female reproductive status. Together these findings offer insight into the economics of territoriality by highlighting the dynamics of spacing patterns at differing time scales.
Behavioral Ecology and Sociobiology 06/2013; 67(6):875-884. · 2.75 Impact Factor
[show abstract][hide abstract] ABSTRACT: Highlights
► We assessed the relationship between grooming behaviour, tick load and tick-borne infection in wild yellow baboons. ► Grooming played a role in reducing tick loads. ► Older, low-ranking individuals and males were most vulnerable to high tick loads. ► We also found that tick load affected packed cell volume, an indicator of health in this baboon population.
[show abstract][hide abstract] ABSTRACT: Variation in the social environment can have profound effects on survival and reproduction in wild social mammals. However, we know little about the degree to which these effects are influenced by genetic differences among individuals, and conversely, the degree to which social environmental variation mediates genetic reaction norms. To better understand these relationships, we investigated the potential for dominance rank, social connectedness and group size to modify the effects of genetic variation on gene expression in the wild baboons of the Amboseli basin. We found evidence for a number of gene-environment interactions (GEIs) associated with variation in the social environment, encompassing social environments experienced in adulthood as well as persistent effects of early life social environment. Social connectedness, maternal dominance rank and group size all interacted with genotype to influence gene expression in at least one sex, and either in early life or in adulthood. These results suggest that social and behavioural variation, akin to other factors such as age and sex, can impact the genotype-phenotype relationship. We conclude that GEIs mediated by the social environment are important in the evolution and maintenance of individual differences in wild social mammals, including individual differences in responses to social stressors.
Philosophical Transactions of The Royal Society B Biological Sciences 01/2013; 368(1618):20120345. · 6.23 Impact Factor
[show abstract][hide abstract] ABSTRACT: Testosterone (T) is often positively associated with male sexual behavior and negatively associated with paternal care. These associations have primarily been demonstrated in species where investment in paternal care begins well after mating activity is complete, when offspring are hatched or born. Different patterns may emerge in studies of species where investment in mating and paternal care overlap temporally, for instance in non-seasonal breeders in which males mate with multiple females sequentially and may simultaneously have multiple offspring of different ages. In a 9-year data set on levels of T in male baboons, fecal concentrations of T (fT) were positively associated with both mate guarding ("consortship") - a measure of current reproductive activity - and with the number of immature offspring a male had in his social group - a measure of past reproductive activity and an indicator of likely paternal behavior. To further examine the relationship between T and potential paternal behavior, we next drew on an intensive 8-month study of male behavior, and found that fathers were more likely to be in close proximity to their offspring than expected by chance. Because male baboons are known to provide paternal care, and because time in proximity to offspring would facilitate such care, this suggests that T concentrations in wild male baboons may be associated with both current reproductive activity and with current paternal behavior. These results are consistent with the predicted positive association between T and mating effort but not with a negative association between T and paternal care; in male baboons, high levels of T occur in males that are differentially associating with their offspring.
Hormones and Behavior 11/2012; · 3.74 Impact Factor
[show abstract][hide abstract] ABSTRACT: In many social species, competition between groups is a major factor proximately affecting group-level movement patterns and space use and ultimately shaping the evolution of group living and complex sociality. Here we evaluated the factors influencing group-level dominance among 5 social groups of wild baboons (Papio cynocephalus), in particular focusing on the spatial determinants of dominance and the consequences of defeat. When direct conflict occurred between conspecific baboon groups, the winning group was predicted by differences in the number of adult males in each group and/or groups that had used the areas surrounding the encounter location more intensively than their opponent in the preceding 9 or 12 months. Relative intensity of space use over shorter timescales examined (3 and 6 months) was a poor predictor of the interaction's outcome. Losing groups but not winning groups experienced clear short-term costs. Losing groups used the area surrounding the interaction less following an agonistic encounter (relative to their intensity of use of the area prior to the interaction). These findings offer insight into the influences and consequences of intergroup competition on group-level patterns of space use.
[show abstract][hide abstract] ABSTRACT: Mating behavior has profound consequences for two phenomena--individual reproductive success and the maintenance of species boundaries--that contribute to evolutionary processes. Studies of mating behavior in relation to individual reproductive success are common in many species, but studies of mating behavior in relation to genetic variation and species boundaries are less commonly conducted in socially complex species. Here we leveraged extensive observations of a wild yellow baboon (Papio cynocephalus) population that has experienced recent gene flow from a close sister taxon, the anubis baboon (Papio anubis), to examine how admixture-related genetic background affects mating behavior. We identified novel effects of genetic background on mating patterns, including an advantage accruing to anubis-like males and assortative mating among both yellow-like and anubis-like pairs. These genetic effects acted alongside social dominance rank, inbreeding avoidance, and age to produce highly nonrandom mating patterns. Our results suggest that this population may be undergoing admixture-related evolutionary change, driven in part by nonrandom mating. However, the strength of the genetic effect is mediated by behavioral plasticity and social interactions, emphasizing the strong influence of social context on mating behavior in socially complex species.
The American Naturalist 07/2012; 180(1):113-29. · 4.55 Impact Factor
[show abstract][hide abstract] ABSTRACT: In a wide range of taxa, including baboons, close social bonds seem to help animals cope with stress and enhance long-term reproductive success and longevity. Current evidence suggests that female baboons may benefit from establishing and maintaining highly individuated relationships with a relatively small number of partners. Here, we extend previous work on the stability of female baboons' social relationships in three different ways. First, we assess the stability of females' social relationships in two distinct and geographically distant sites using the same method. Second, we conduct simulations to determine whether females' social relationships were more stable than expected by chance. Third, we examine demographic sources of variance in the stability of close social bonds. At both sites, females' relationships with their most preferred partners were significantly more stable than expected by chance. In contrast, their relationships with less preferred partners were more ephemeral, often changing from year to year. While nearly all females experienced some change in their top partners across time, many maintained relationships with top partners for several years. Females that lived in smaller groups and had more close kin available had more stable social relationships than those that lived in larger groups and had fewer close kin available.
[show abstract][hide abstract] ABSTRACT: Social status can have striking effects on health in humans and other animals, but the causes often are unknown. In male vertebrates, status-related differences in health may be influenced by correlates of male social status that suppress immune responses. Immunosuppressive correlates of low social status may include chronic social stress, poor physical condition, and old age; the immunosuppressive correlates of high status may include high testosterone and energetic costs of reproduction. Here we test whether these correlates could create status-related differences in immune function by measuring the incidence of illness and injury and then examining healing rates in a 27-y data set of natural injuries and illnesses in wild baboon males. We found no evidence that the high testosterone and intense reproductive effort associated with high rank suppress immune responses. Instead, high-ranking males were less likely to become ill, and they recovered more quickly than low-ranking males, even controlling for differences in age. Notably, alpha males, who experience high glucocorticoids, as well as the highest testosterone and reproductive effort, healed significantly faster than other males, even other high-ranking males. We discuss why alpha males seem to escape from the immunosuppressive costs of glucocorticoids but low-ranking males do not, including the idea that glucocorticoids' effects depend on an individual's physiological and social context.
Proceedings of the National Academy of Sciences 05/2012; 109(23):9017-22. · 9.74 Impact Factor
[show abstract][hide abstract] ABSTRACT: Highlights
► We studied causes of variability in the mother–neonate relationship in wild baboons. ► The more experience a mother had, the more initiative her newborn infant exhibited. ► At each level of maternal experience, sons exhibited more initiative than daughters. ► Suckling by daughters was predicted from maternal rank and prenatal oestrogens. ► Our results suggest sex differences in primate life history emerge early in infancy.
[show abstract][hide abstract] ABSTRACT: In immature wild savannah baboons (Papio cynocephalus), we observed symptoms consistent with copper (Cu) deficiency and, more specifically, with a disorder referred to as white monkey syndrome (WMS) in laboratory primates. The objectives of this study were to characterize this pathology, and test three hypotheses that (1) Cu deficiency may have been induced by zinc (Zn) toxicity, (2) it may have been induced by molybdenum (Mo) toxicity, and (3) cumulative rainfall during the perinatal period and particularly during gestation is an ecological factor distinguishing infants afflicted with WMS from non-WMS infants. During 2001-2009, we observed 22 instances of WMS out of a total 377 live births in the study population. Visible symptoms exhibited by WMS infants included whitening of the animal's fur and/or impaired mobility characterized by an apparent "stiffening" of the hindlimbs. Occurrence of WMS did not vary significantly by gender. However, among individuals that survived at least 180 days, WMS males had a significantly lower survivorship probability than non-WMS males. Zn/Cu ratios assessed from hair samples of adult female baboons were higher in females who had produced at least one WMS offspring relative to females who had not had a WMS offspring. This was true even when the hair sample was collected long after the birth of the female's afflicted infant. We consider this potentially indicative of a robust tendency for low Cu levels induced by elevated Zn intake in some individuals. No significant differences of Mo/Cu ratios were observed. Cumulative rainfall during gestation (∼179 days) was 50% lower for WMS infants relative to non-WMS infants. In contrast, rainfall for the two classes of infants did not differ in the 180 days before conception or in the 180 days following birth. This finding highlights the importance of prenatal ecological conditions in healthy fetal development with regard to WMS.
American Journal of Primatology 09/2011; 73(11):1160-8. · 2.46 Impact Factor
[show abstract][hide abstract] ABSTRACT: In social hierarchies, dominant individuals experience reproductive and health benefits, but the costs of social dominance remain a topic of debate. Prevailing hypotheses predict that higher-ranking males experience higher testosterone and glucocorticoid (stress hormone) levels than lower-ranking males when hierarchies are unstable but not otherwise. In this long-term study of rank-related stress in a natural population of savannah baboons (Papio cynocephalus), high-ranking males had higher testosterone and lower glucocorticoid levels than other males, regardless of hierarchy stability. The singular exception was for the highest-ranking (alpha) males, who exhibited both high testosterone and high glucocorticoid levels. In particular, alpha males exhibited much higher stress hormone levels than second-ranking (beta) males, suggesting that being at the very top may be more costly than previously thought.
[show abstract][hide abstract] ABSTRACT: Human senescence patterns-late onset of mortality increase, slow mortality acceleration, and exceptional longevity-are often described as unique in the animal world. Using an individual-based data set from longitudinal studies of wild populations of seven primate species, we show that contrary to assumptions of human uniqueness, human senescence falls within the primate continuum of aging; the tendency for males to have shorter life spans and higher age-specific mortality than females throughout much of adulthood is a common feature in many, but not all, primates; and the aging profiles of primate species do not reflect phylogenetic position. These findings suggest that mortality patterns in primates are shaped by local selective forces rather than phylogenetic history.
[show abstract][hide abstract] ABSTRACT: In conditions characterized by energetic constraints, such as in periods of low food availability, some trade-offs between reproduction and self-maintenance may be necessary; even year-round breeders may then be forced to exhibit some reproductive seasonality. Prior research has largely focused on female reproduction and physiology, and few studies have evaluated the impact of environmental factors on males. Here we assessed the effects of season and ambient temperatures on fecal glucocorticoid (fGC) and testosterone (fT) levels in male baboons in Amboseli, Kenya. The Amboseli basin is a highly challenging, semiarid tropical habitat that is characterized by strongly seasonal patterns of rainfall and by high ambient temperatures. We previously reported that female baboons were impacted by these challenging environmental conditions. We ask here whether male baboons in the same environment and groups as females exhibit similar physiological effects. We found that after accounting for male age and individual variability, males exhibited higher fGC levels and lower fT levels during the dry season than during the wet season. Furthermore, fT but not fGC levels were lower in months of high average daily maximum temperatures, suggesting a direct impact of heat on testes. Our results demonstrate that male baboons, like females, experience ecological stress that alters their reproductive physiology. The impact of the environment on male reproduction deserves more attention both in its own right and because alteration in male physiology may contribute to the reduction in female fertility observed inchallenging environments.
American Journal of Physical Anthropology 02/2011; 144(2):169-76. · 2.48 Impact Factor
[show abstract][hide abstract] ABSTRACT: Natural populations hold enormous potential for evolutionary genetic studies, especially when phenotypic, genetic and environmental data are all available on the same individuals. However, untangling the genotype-phenotype relationship in natural populations remains a major challenge. Here, we describe results of an investigation of one class of phenotype, allele-specific gene expression (ASGE), in the well-studied natural population of baboons of the Amboseli basin, Kenya. ASGE measurements identify cases in which one allele of a gene is overexpressed relative to the alternative allele of the same gene, within individuals, thus providing a control for background genetic and environmental effects. Here, we characterize the incidence of ASGE in the Amboseli baboon population, focusing on the genetic and environmental contributions to ASGE in a set of eleven genes involved in immunity and defence. Within this set, we identify evidence for common ASGE in four genes. We also present examples of two relationships between cis-regulatory genetic variants and the ASGE phenotype. Finally, we identify one case in which this relationship is influenced by a novel gene-environment interaction. Specifically, the dominance rank of an individual's mother during its early life (an aspect of that individual's social environment) influences the expression of the gene CCL5 via an interaction with cis-regulatory genetic variation. These results illustrate how environmental and ecological data can be integrated into evolutionary genetic studies of functional variation in natural populations. They also highlight the potential importance of early life environmental variation in shaping the genetic architecture of complex traits in wild mammals.
[show abstract][hide abstract] ABSTRACT: Teeth represent an essential component of the foraging apparatus for any mammal, and tooth wear can have significant implications for survival and reproduction. This study focuses on tooth wear in wild baboons in Amboseli, southern Kenya. We obtained mandibular and maxillary tooth impressions from 95 baboons and analyzed digital images of replicas made from these impressions. We measured tooth wear as the percent dentine exposure (PDE, the percent of the occlusal surface on which dentine was exposed), and we examined the relationship of PDE to age, behavior, and life history variables. We found that PDE increased significantly with age for both sexes in all three molar types. In females, we also tested the hypotheses that long-term patterns of feeding behavior, social dominance rank, and one measure of maternal investment (the cumulative number of months that a female had dependent infants during her lifetime) would predict tooth wear when we controlled for age. The hypothesis that feeding behavior predicted tooth wear was supported. The percent of feeding time spent consuming grass corms predicted PDE when controlling for age. However, PDE was not associated with social dominance rank or maternal investment.
American Journal of Physical Anthropology 01/2011; 144(1):51-9. · 2.48 Impact Factor
[show abstract][hide abstract] ABSTRACT: In a stochastic environment, long-term fitness can be influenced by variation, covariation, and serial correlation in vital rates (survival and fertility). Yet no study of an animal population has parsed the contributions of these three aspects of variability to long-term fitness. We do so using a unique database that includes complete life-history information for wild-living individuals of seven primate species that have been the subjects of long-term (22-45 years) behavioral studies. Overall, the estimated levels of vital rate variation had only minor effects on long-term fitness, and the effects of vital rate covariation and serial correlation were even weaker. To explore why, we compared estimated variances of adult survival in primates with values for other vertebrates in the literature and found that adult survival is significantly less variable in primates than it is in the other vertebrates. Finally, we tested the prediction that adult survival, because it more strongly influences fitness in a constant environment, will be less variable than newborn survival, and we found only mixed support for the prediction. Our results suggest that wild primates may be buffered against detrimental fitness effects of environmental stochasticity by their highly developed cognitive abilities, social networks, and broad, flexible diets.
The American Naturalist 01/2011; 177(1):E14-28. · 4.55 Impact Factor
[show abstract][hide abstract] ABSTRACT: The pace of reproductive aging has been of considerable interest, especially in regard to the long postreproductive period in modern women. Here we use data for both sexes from a 37-year longitudinal study of a wild baboon population to place reproductive aging within a life history context for this species, a primate relative of humans that evolved in the same savannah habitat as humans did. We examine the patterns and pace of reproductive aging, including birth rates and reproductive hormones for both sexes, and compare reproductive aging to age-related changes in several other traits. Reproductive senescence occurs later in baboon females than males. Delayed senescence in females relative to males is also found in several other traits, such as dominance status and body condition, but not in molar wear or glucocorticoid profiles. Survival, health, and well-being are the product of risk factors in morphological, physiological, and behavioral traits that differ in rate of senescence and in dependence on social or ecological conditions; some will be very sensitive to differences in circumstances and others less so.
Annals of the New York Academy of Sciences 08/2010; 1204:127-38. · 4.38 Impact Factor