[Show abstract][Hide abstract] ABSTRACT: Linear dominance hierarchies, which are common in social animals, can profoundly influence access to limited resources, reproductive opportunities and health. In spite of their importance, the mechanisms that govern the dynamics of such hierarchies remain unclear. Two hypotheses explain how linear hierarchies might emerge and change over time. The 'prior attributes hypothesis' posits that individual differences in fighting ability directly determine dominance ranks. By contrast, the 'social dynamics hypothesis' posits that dominance ranks emerge from social self-organization dynamics such as winner and loser effects. While the prior attributes hypothesis is well supported in the literature, current support for the social dynamics hypothesis is limited to experimental studies that artificially eliminate or minimize individual differences in fighting abilities. Here, we present the first evidence supporting the social dynamics hypothesis in a wild population. Specifically, we test for winner and loser effects on male hierarchy dynamics in wild baboons, using a novel statistical approach based on the Elo rating method for cardinal rank assignment, which enables the detection of winner and loser effects in uncontrolled group settings. Our results demonstrate (i) the presence of winner and loser effects, and (ii) that individual susceptibility to such effects may have a genetic basis. Taken together, our results show that both social self-organization dynamics and prior attributes can combine to influence hierarchy dynamics even when agonistic interactions are strongly influenced by differences in individual attributes. We hypothesize that, despite variation in individual attributes, winner and loser effects exist (i) because these effects could be particularly beneficial when fighting abilities in other group members change over time, and (ii) because the coevolution of prior attributes and winner and loser effects maintains a balance of both effects.
Proceedings of the Royal Society B: Biological Sciences 09/2015; 282(1814). DOI:10.1098/rspb.2015.1512 · 5.05 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: The paradigm of competitive males vying to influence female mate choice has been repeatedly upheld, but, increasingly, studies also report competitive females and choosy males. One female trait that is commonly proposed to influence male mate choice is the exaggerated sexual swelling displayed by females of many Old World primate species. The reliable indicator hypothesis posits that females use the exaggerated swellings to compete for access to mates, and that the swellings advertise variation in female fitness. We tested the two main predictions of this hypothesis in a wild population of baboons (Papio cynocephalus). First, we examined the effect of swelling size on the probability of mate guarding (‘consortship’) by the highest-ranking male and the behaviour of those males that trailed consortships (‘follower males’). Second, we asked whether a female's swelling size predicted several fitness measures. We found that high-ranking males did not prefer females with larger swellings (when controlling for cycle number and conception) and that females with larger swellings did not have higher reproductive success. Our study, the only complete test of the reliable indicator hypothesis in a primate population, rejects the idea that female baboons compete for mates by advertising heritable fitness differences. Furthermore, we found unambiguous evidence that males biased their mating decisions in favour of females who had experienced more sexual cycles since their most recent pregnancy. Thus, rather than tracking the potential differences in fitness between females, male baboons appear to track and target the potential for a given reproductive opportunity to result in fertilization.
[Show abstract][Hide abstract] ABSTRACT: Canines represent an essential component of the dentition for any heterodont mammal. In primates, like many other mammals, canines are frequently used as weapons. Hence, tooth size and wear may have significant implications for fighting ability, and consequently for social dominance rank, reproductive success, and fitness. We evaluated sources of variance in canine growth and length in a well-studied wild primate population because of the potential importance of canines for male reproductive success in many primates. Specifically, we measured maxillary canine length in 80 wild male baboons (aged 5.04–20.45 years) from the Amboseli ecosystem in southern Kenya, and examined its relationship with maturation, age, and social dominance rank. In our analysis of maturation, we compared food-enhanced baboons (those that fed part time at a refuse pit associated with a tourist lodge) with wild-feeding males, and found that food-enhanced males achieved long canines earlier than wild-feeding males. Among adult males, canine length decreased with age because of tooth wear. We found some evidence that, after controlling for age, longer canines were associated with higher adult dominance rank (accounting for 9% of the variance in rank), but only among relatively high-ranking males. This result supports the idea that social rank, and thus reproductive success and fitness, may depend in part on fighting ability mediated by canine size.
PLoS ONE 05/2015; 10(5):e0126415. DOI:10.1371/journal.pone.0126415 · 3.23 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: Early-life experiences can dramatically affect adult traits. However, the evolutionary origins of such early-life effects are debated. The predictive adaptive response hypothesis argues that adverse early environments prompt adaptive phenotypic adjustments that prepare animals for similar challenges in adulthood. In contrast, the developmental constraints hypothesis argues that early adversity is generally costly. To differentiate between these hypotheses, we studied two sets of wild female baboons: those born during low-rainfall, low-quality years and those born during normal-rainfall, high-quality years. For each female, we measured fertility-related fitness components during years in adulthood that matched and mismatched her early conditions. We found support for the developmental constraints hypothesis: females born in low-quality environments showed greater decreases in fertility during drought years than females born in high-quality environments, even though drought years matched the early conditions of females born in low-quality environments. Additionally, we found that females born in low-quality years to high-status mothers did not experience reduced fertility during drought years. These results indicate that early ecological adversity did not prepare individuals to cope with ecological challenges in later life. Instead, individuals that experienced at least one high-quality early environment—either ecological or social—were more resilient to ecological stress in later life. Together, these data suggest that early adversity carries lifelong costs, which is consistent with the developmental constraints hypothesis.
The American Naturalist 04/2015; 185(6):000-000. DOI:10.1086/681016 · 3.83 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: Social relationships have profound effects on health in humans and other primates, but the mechanisms that explain this relationship are not well understood. Using shotgun metagenomic data from wild baboons, we found that social group membership and social network relationships predicted both the taxonomic structure of the gut microbiome and the structure of genes encoded by gut microbial species. Rates of interaction directly explained variation in the gut microbiome, even after controlling for diet, kinship, and shared environments. They therefore strongly implicate direct physical contact among social partners in the transmission of gut microbial species. We identified 51 socially structured taxa, which were significantly enriched for anaerobic and non-spore-forming lifestyles. Our results argue that social interactions are an important determinant of gut microbiome composition in natural animal populations-a relationship with important ramifications for understanding how social relationships influence health, as well as the evolution of group living.
[Show abstract][Hide abstract] ABSTRACT: Social network structures can crucially impact complex social processes such as collective behaviour or the transmission of information and diseases. However, currently it is poorly understood how social networks change over time. Previous studies on primates suggest that 'knockouts' (due to death or dispersal) of high-ranking individuals might be important drivers for structural changes in animal social networks. Here we test this hypothesis using long-term data on a natural population of baboons, examining the effects of 29 natural knockouts of alpha or beta males on adult female social networks. We investigated whether and how knockouts affected (1) changes in grooming and association rates among adult females, and (2) changes in mean degree and global clustering coefficient in these networks. The only significant effect that we found was a decrease in mean degree in grooming networks in the first month after knockouts, but this decrease was rather small, and grooming networks rebounded to baseline levels by the second month after knockouts. Taken together our results indicate that the removal of high-ranking males has only limited or no lasting effects on social networks of adult female baboons. This finding calls into question the hypothesis that the removal of high-ranking individuals has a destabilizing effect on social network structures in social animals
Current Zoology 02/2015; 61(1):107-113. · 1.59 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: Social integration and support can have profound effects on human survival. The extent of this phenomenon in non-human animals is largely unknown, but such knowledge is important to understanding the evolution of both lifespan and sociality. Here, we report evidence that levels of affiliative social behaviour (i.e. 'social connectedness') with both same-sex and opposite-sex conspecifics predict adult survival in wild female baboons. In the Amboseli ecosystem in Kenya, adult female baboons that were socially connected to either adult males or adult females lived longer than females who were socially isolated from both sexes-females with strong connectedness to individuals of both sexes lived the longest. Female social connectedness to males was predicted by high dominance rank, indicating that males are a limited resource for females, and females compete for access to male social partners. To date, only a handful of animal studies have found that social relationships may affect survival. This study extends those findings by examining relationships to both sexes in by far the largest dataset yet examined for any animal. Our results support the idea that social effects on survival are evolutionarily conserved in social mammals.
Proceedings of the Royal Society B: Biological Sciences 10/2014; 281(1793). DOI:10.1098/rspb.2014.1261 · 5.05 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: The development of non-invasive methods, particularly fecal determination, has made possible the assessment of hormone concentrations in wild animal populations. However, measuring fecal metabolites needs careful validation for each species and for each sex. We investigated whether radioimmunoassays (RIAs) previously used to measure fecal testosterone (fT) in male baboons and fecal estrogens (fE) in female baboons were well suited to measure these hormones in the opposite sex. We compared fE and fT concentrations determined by RIA to those measured by liquid chromatography combined with triple quadropole mass spectrometry (LC/MS/MS), a highly specific method. Additionally, we conducted a biological validation to assure that the measurements of fecal concentrations reflected physiological levels of the hormone of interest. Several tests produced expected results that led us to conclude that our RIAs can reliably measure fT and fE in both sexes, and that within-sex comparisons of these measures are valid: (i) fTRIA were significantly correlated to fTLC/MS/MS for both sexes; (ii) fTRIA were higher in adult than in immature males; (iii) fTRIA were higher in pregnant than non-pregnant females; (iv) fERIA were correlated with 17β-estradiol (fE2) and with estrone (fE1) determined by LC/MS/MS in pregnant females; (v) fERIA were significantly correlated with fE2 in non-pregnant females and nearly significantly correlated in males; (vi) fERIA were higher in adult males than in immature males. fERIA were higher in females than in males, as predicted, but unexpectedly, fTRIA were higher in females than in males, suggesting a difference in steroid metabolism in the two sexes; consequently, we conclude that while within-sex comparisons are valid, fTRIA should not be used for intersexual comparisons. Our results should open the field to important additional studies, as to date the roles of testosterone in females and estrogens in males have been little investigated.
General and Comparative Endocrinology 08/2014; 204. DOI:10.1016/j.ygcen.2014.04.021 · 2.47 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: Many mammalian societies are structured by dominance hierarchies, and an individual's position within this hierarchy can influence reproduction, behaviour, physiology and health. In nepotistic hierarchies, which are common in cercopithecine primates and also seen in spotted hyaenas, Crocuta crocuta, adult daughters are expected to rank immediately below their mother, and in reverse age order (a phenomenon known as ‘youngest ascendancy’). This pattern is well described, but few studies have systematically examined the frequency or causes of departures from the expected pattern. Using a longitudinal data set from a natural population of yellow baboons, Papio cynocephalus, we measured the influence of maternal kin, paternal kin and group size on female rank positions at two life history milestones, menarche and first live birth. At menarche, most females (73%) ranked adjacent to their family members (i.e. the female held an ordinal rank in consecutive order with other members of her maternal family); however, only 33% of females showed youngest ascendancy within their matriline at menarche. By the time they experienced their first live birth, many females had improved their dominance rank: 78% ranked adjacent to their family members and 49% showed youngest ascendancy within their matriline. The presence of mothers and maternal sisters exerted a powerful influence on rank outcomes. However, the presence of fathers, brothers and paternal siblings did not produce a clear effect on female dominance rank in our analyses, perhaps because females in our data set co-resided with variable numbers and types of paternal and male relatives. Our results also raise the possibility that female body size or competitive ability may influence dominance rank, even in this classically nepotistic species. In total, our analyses reveal that the predictors of dominance rank in nepotistic rank systems are much more complex than previously thought.
[Show abstract][Hide abstract] ABSTRACT: Signals of fertility in female animals are of increasing interest to evolutionary biologists, a development that coincides with increasing interest in male mate choice and the potential for female traits to evolve under sexual selection. We characterized variation in size of an exaggerated female fertility signal in baboons and investigated the sources of that variance. The number of sexual cycles that a female had experienced after her most recent pregnancy ("cycles since resumption") was the strongest predictor of swelling size. Furthermore, the relationship between cycles since resumption and swelling size was most evident during rainy periods and was not evident during times of drought. Finally, we found significant differences in swelling size between individual females; these differences endured across cycles (i.e., were not explained by variation within individuals) and persisted in spite of ecological effects. This study is the first to provide conclusive evidence of significant variation in swelling size between female primates (controlling for cycles since resumption) and to demonstrate that ecological constraints influence variation in this signal of fertility.
[Show abstract][Hide abstract] ABSTRACT: Reproduction is a notoriously costly phase of life, exposing individuals to injury, infectious disease, and energetic trade-offs. The strength of these costs should be influenced by life history strategies, and in long-lived species, females may be selected to mitigate costs of reproduction because life span is such an important component of their reproductive success. Here, we report evidence for two costs of reproduction that may influence survival in wild female baboons—injury risk and delayed wound healing. Based on 29 years of observations in the Amboseli ecosystem, Kenya, we found that wild female baboons experienced the highest risk of injury on days when they were most likely to be ovulating. In addition, lactating females healed from wounds more slowly than pregnant or cycling females, indicating a possible trade-off between lactation and immune function. We also found variation in injury risk and wound healing with dominance rank and age: Older and low-status females were more likely to be injured than younger or high-status females, and older females exhibited slower healing than younger females. Our results support the idea that wild nonhuman primates experience energetic and immune costs of reproduction and they help illuminate life history trade-offs in long-lived species.
[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; 110(33). DOI:10.1073/pnas.1311857110 · 9.67 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. DOI:10.1016/j.yhbeh.2013.02.014 · 4.63 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.
[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 04/2013; 368(1618):20120345. DOI:10.1098/rstb.2012.0345 · 7.06 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: Nonhuman primate species spend a conspicuous amount of time grooming during social interactions, a behaviour that probably serves both social and health-related functions. While the social implications of grooming have been relatively well studied, less attention has been paid to the health benefits, especially the removal of ectoparasites, which may act as vectors in disease transmission. In this study, we examined whether grooming behaviour reduced tick load (number of ticks) and haemoprotozoan infection status in a population of wild adult baboons (Papio cynocephalus). We found that younger and higher-ranking adults were groomed more often than older, low-ranking adults, and females were groomed more often than males. Animals that received more grooming, in turn, had lower tick loads. Baboons with lower tick loads had higher packed red cell volume (PCV or haematocrit), one general measure of health status. We detected a tick-borne haemoprotozoan, Babesia microti, but its low prevalence in the population precluded identifying sources of variance in infection.
[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; 63(3). DOI:10.1016/j.yhbeh.2012.11.014 · 4.63 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.