Male-mediated early maturation unlikely to evolve via adaptive evolution.

The Vandenbergh effect, or male-mediated maturation, occurs when females reach sexual maturation upon exposure to a novel male. Male-mediated maturation is found across mammals, including in geladas, Theropithecus gelada, where it may be an adaptive counterstrategy to infanticide that follows the immigration of a new male; maturing after male immigration maximizes a female's chances of weaning her first offspring before the next infanticidal male immigrates (the 'optimal timing hypothesis'). Alternatively, the nonadaptive 'Bruce effect by-product hypothesis' posits that male-mediated maturation in geladas (and possibly other mammals) is triggered by the same physiological changes that, in pregnant females, produce spontaneous abortion (the Bruce effect). We test both hypotheses using theory and observational data. We show that neither male-mediated maturation nor its associated hormonal changes occur in baboons (Papio cynocephalus × P. anubis), a primate without the Bruce effect. An individual-based model suggests that male-mediated maturation should not evolve via adaptive evolution in either geladas or baboons. Finally, we derive the selection coefficient for male-mediated maturation and show it is likely to be very small because male-mediated maturation yields only marginal potential benefits unless the system is extremely fine-tuned. We conclude that male-mediated maturation in geladas is a by-product of the Bruce effect and more broadly that the Vandenbergh effect may be nonadaptive.

Using non-invasive behavioral and physiological data to measure biological age in wild baboons.

Biological aging is near-ubiquitous in the animal kingdom, but its timing and pace vary between individuals and over lifespans. Prospective, individual-based studies of wild animals-especially non-human primates-help identify the social and environmental drivers of this variation by indicating the conditions and exposure windows that affect aging processes. However, measuring individual biological age in wild primates is challenging because several of the most promising methods require invasive sampling. Here, we leverage observational data on behavior and physiology, collected non-invasively from 319 wild female baboons across 2402 female-years of study, to develop a composite predictor of age: the non-invasive physiology and behavior (NPB) clock. We found that age predictions from the NPB clock explained 51% of the variation in females' known ages. Further, deviations from the clock's age predictions predicted female survival: females predicted to be older than their known ages had higher adult mortality. Finally, females who experienced harsh early-life conditions were predicted to be about 6 months older than those who grew up in more benign conditions. While the relationship between early adversity and NPB age is noisy, this estimate translates to a predicted 2-3 year reduction in mean adult lifespan in our model. A constraint of our clock is that it is tailored to data collection approaches implemented in our study population. However, many of the clock's components have analogs in other populations, suggesting that non-invasive data can provide broadly applicable insight into heterogeneity in biological age in natural populations.

Thyroid hormone concentrations in female baboons: Metabolic consequences of living in a highly seasonal environment.

How female mammals adapt metabolically in response to environmental variation remains understudied in the wild, because direct measures of metabolic activity are difficult to obtain in wild populations. However, recent advances in the non-invasive measurement of fecal thyroid hormones, triiodothyronine (T3), an important regulator of metabolism, provide an opportunity to understand how female baboons living in the harsh Amboseli ecosystem in southern Kenya adapt to environmental variability and escape strict reproductive seasonality. Specifically, we assessed how a female's activity budget, diet, and concentrations of fecal T3 metabolites (mT3) changed over the course of the year and between years. We then tested which of several environmental variables (season, rainfall, and temperature) and behavioral variables (female activity budget and diet) best predicted mT3 concentrations. Finally, we determined if two important reproductive events - onset of ovarian cycling and conception of an offspring - were preceded by changes in female mT3 concentrations. We found female baboons' mT3 concentrations varied markedly across the year and between years as a function of environmental conditions. Further, changes in a female's behavior and diet only partially mediated the metabolic response to the environment. Finally, mT3 concentrations increased in the weeks prior to menarche and cycling resumption, regardless of the month or season in which cycling started. This pattern indicates that metabolic activation may be an indicator of reproductive readiness in female baboons as their energy balance is restored.

Universal gut microbial relationships in the gut microbiome of wild baboons.

Ecological relationships between bacteria mediate the services that gut microbiomes provide to their hosts. Knowing the overall direction and strength of these relationships is essential to learn how ecology scales up to affect microbiome assembly, dynamics, and host health. However, whether bacterial relationships are generalizable across hosts or personalized to individual hosts is debated. Here, we apply a robust, multinomial logistic-normal modeling framework to extensive time series data (5534 samples from 56 baboon hosts over 13 years) to infer thousands of correlations in bacterial abundance in individual baboons and test the degree to which bacterial abundance correlations are 'universal'. We also compare these patterns to two human data sets. We find that, most bacterial correlations are weak, negative, and universal across hosts, such that shared correlation patterns dominate over host-specific correlations by almost twofold. Further, taxon pairs that had inconsistent correlation signs (either positive or negative) in different hosts always had weak correlations within hosts. From the host perspective, host pairs with the most similar bacterial correlation patterns also had similar microbiome taxonomic compositions and tended to be genetic relatives. Compared to humans, universality in baboons was similar to that in human infants, and stronger than one data set from human adults. Bacterial families that showed universal correlations in human infants were often universal in baboons. Together, our work contributes new tools for analyzing the universality of bacterial associations across hosts, with implications for microbiome personalization, community assembly, and stability, and for designing microbiome interventions to improve host health.

Communities of bacteria living in the guts of humans and other animals perform essential services for their hosts such as digesting food, degrading toxins, or fighting viruses and other bacteria that cause disease. These services emerge from so-called 'ecological' relationships between different species of bacteria. One species, for example, may break down a molecule in human food into another compound that is, in turn, digested by another species into a small molecule that the human gut can absorb and use. The bacteria involved in such a process may become more or less common together in their host. In other situations, some bacteria may have opposing roles to each other, meaning that if one species becomes more abundant it may reduce the level of the other. However, it is not known if relationships between different bacteria are consistent across hosts (i.e., universal) or unique to each host (personalized). In other words, if a pair of bacteria increase and decrease in abundance together in one host, do they do the same in other hosts? Microbes often swap genes with each other to gain new traits; as each host harbors a distinctive set of gut microbes, it may be possible for microbial relationships to change depending on the bacterial species present in a specific environment. To investigate, Roche et al. studied the bacteria in thousands of samples of feces collected from 56 baboons over a 13-year period. These samples came from a long-term research project in Amboseli, Kenya which has been studying a population of wild baboons continuously since 1971. Roche et al. measured the abundance of hundreds of gut bacteria in the feces to understand the relationships between pairs. This revealed that connections between species were largely universal rather than personalized to each baboon. Furthermore, the pairs of bacteria with the strongest positive or negative associations had the most consistent relationships across the baboons. Microbial relationships that have strong effects on the microbiome's composition might therefore be especially universal. Further analyses measuring gut bacteria in human babies also found that relationships between pairs of bacteria were largely universal. Hence, individual species of bacteria may fill similar ecological roles in each host across humans and other primates, and perhaps also in other mammals. These findings suggest that it may be possible to leverage the ecological relationships between bacteria to develop universal therapies for human diseases associated with gut bacteria, such as inflammatory bowel disease or Clostridium difficile infection.

Synchrony and idiosyncrasy in the gut microbiome of wild baboons.

Human gut microbial dynamics are highly individualized, making it challenging to link microbiota to health and to design universal microbiome therapies. This individuality is typically attributed to variation in host genetics, diets, environments and medications but it could also emerge from fundamental ecological forces that shape microbiota more generally. Here, we leverage extensive gut microbial time series from wild baboons-hosts who experience little interindividual dietary and environmental heterogeneity-to test whether gut microbial dynamics are synchronized across hosts or largely idiosyncratic. Despite their shared lifestyles, baboon microbiota were only weakly synchronized. The strongest synchrony occurred among baboons living in the same social group, probably because group members range over the same habitat and simultaneously encounter the same sources of food and water. However, this synchrony was modest compared to each host's personalized dynamics. In support, host-specific factors, especially host identity, explained, on average, more than three times the deviance in longitudinal dynamics compared to factors shared with social group members and ten times the deviance of factors shared across the host population. These results contribute to mounting evidence that highly idiosyncratic gut microbiomes are not an artefact of modern human environments and that synchronizing forces in the gut microbiome (for example, shared environments, diets and microbial dispersal) are not strong enough to overwhelm key drivers of microbiome personalization, such as host genetics, priority effects, horizontal gene transfer and functional redundancy.

Gut microbiome heritability is nearly universal but environmentally contingent.

Relatives have more similar gut microbiomes than nonrelatives, but the degree to which this similarity results from shared genotypes versus shared environments has been controversial. Here, we leveraged 16,234 gut microbiome profiles, collected over 14 years from 585 wild baboons, to reveal that host genetic effects on the gut microbiome are nearly universal. Controlling for diet, age, and socioecological variation, 97% of microbiome phenotypes were significantly heritable, including several reported as heritable in humans. Heritability was typically low (mean = 0.068) but was systematically greater in the dry season, with low diet diversity, and in older hosts. We show that longitudinal profiles and large sample sizes are crucial to quantifying microbiome heritability, and indicate scope for selection on microbiome characteristics as a host phenotype.

Glucocorticoid exposure predicts survival in female baboons.

Are differences in hypothalamic-pituitary-adrenal (HPA) axis activation across the adult life span linked to differences in survival? This question has been the subject of considerable debate. We analyze the link between survival and fecal glucocorticoid (GC) measures in a wild primate population, leveraging an unusually extensive longitudinal dataset of 14,173 GC measurements from 242 adult female baboons over 1634 female years. We document a powerful link between GCs and survival: Females with relatively high current GCs or high lifelong cumulative GCs face an elevated risk of death. A hypothetical female who maintained GCs in the top 90% for her age across adulthood would be expected to lose 5.4 years of life relative to a female who maintained GCs in the bottom 10% for her age. Hence, differences among individuals in HPA axis activity provide valuable prognostic information about disparities in life span.

A comparison of dominance rank metrics reveals multiple competitive landscapes in an animal society.

Across group-living animals, linear dominance hierarchies lead to disparities in access to resources, health outcomes and reproductive performance. Studies of how dominance rank predicts these traits typically employ one of several dominance rank metrics without examining the assumptions each metric makes about its underlying competitive processes. Here, we compare the ability of two dominance rank metrics-simple ordinal rank and proportional or 'standardized' rank-to predict 20 traits in a wild baboon population in Amboseli, Kenya. We propose that simple ordinal rank best predicts traits when competition is density-dependent, whereas proportional rank best predicts traits when competition is density-independent. We found that for 75% of traits (15/20), one rank metric performed better than the other. Strikingly, all male traits were best predicted by simple ordinal rank, whereas female traits were evenly split between proportional and simple ordinal rank. Hence, male and female traits are shaped by different competitive processes: males are largely driven by density-dependent resource access (e.g. access to oestrous females), whereas females are shaped by both density-independent (e.g. distributed food resources) and density-dependent resource access. This method of comparing how different rank metrics predict traits can be used to distinguish between different competitive processes operating in animal societies.

Higher dominance rank is associated with lower glucocorticoids in wild female baboons: A rank metric comparison.

In vertebrates, glucocorticoid secretion occurs in response to energetic and psychosocial stressors that trigger the hypothalamic-pituitary-adrenal (HPA) axis. Measuring glucocorticoid concentrations can therefore shed light on the stressors associated with different social and environmental variables, including dominance rank. Using 14,172 fecal samples from 237 wild female baboons, we test the hypothesis that high-ranking females experience fewer psychosocial and/or energetic stressors than lower-ranking females. We predicted that high-ranking females would have lower fecal glucocorticoid (fGC) concentrations than low-ranking females. Because dominance rank can be measured in multiple ways, we employ an information theoretic approach to compare 5 different measures of rank as predictors of fGC concentrations: ordinal rank; proportional rank; Elo rating; and two approaches to categorical ranking (alpha vs non-alpha and high-middle-low). Our hypothesis was supported, but it was also too simplistic. We found that alpha females exhibited substantially lower fGCs than other females (typical reduction = 8.2%). If we used proportional rank instead of alpha versus non-alpha status in the model, we observed a weak effect of rank such that fGCs rose 4.2% from the highest- to lowest-ranking female in the hierarchy. Models using ordinal rank, Elo rating, or high-middle-low categories alone failed to explain variation in female fGCs. Our findings shed new light on the association between dominance rank and the stress response, the competitive landscape of female baboons as compared to males, and the assumptions inherent in a researcher's choice of rank metric.

Social bonds do not mediate the relationship between early adversity and adult glucocorticoids in wild baboons.

In humans and other animals, harsh conditions in early life can have profound effects on adult physiology, including the stress response. This relationship may be mediated by a lack of supportive relationships in adulthood. That is, early life adversity may inhibit the formation of supportive social ties, and weak social support is itself often linked to dysregulated stress responses. Here, we use prospective, longitudinal data from wild baboons in Kenya to test the links between early adversity, adult social bonds, and adult fecal glucocorticoid hormone concentrations (a measure of hypothalamic-pituitary-adrenal [HPA] axis activation and the stress response). Using a causal inference framework, we found that experiencing one or more sources of early adversity led to a 9 to 14% increase in females' glucocorticoid concentrations across adulthood. However, these effects were not mediated by weak social bonds: The direct effects of early adversity on adult glucocorticoid concentrations were 11 times stronger than the effects mediated by social bonds. This pattern occurred, in part, because the effect of social bonds on glucocorticoids was weak compared to the powerful effects of early adversity on glucocorticoid levels in adulthood. Hence, in female baboons, weak social bonds in adulthood are not enough to explain the effects of early adversity on glucocorticoid concentrations. Together, our results support the well-established notions that early adversity and weak social bonds both predict poor adult health. However, the magnitudes of these two effects differ considerably, and they may act independently of one another.

Noninvasive measurement of mucosal immunity in a free-ranging baboon population.

Ecoimmunological patterns and processes remain understudied in wild primates, in part because of the lack of noninvasive methods to measure immunity. Secretory immunoglobulin A (sIgA) is the most abundant antibody present at mammalian mucosal surfaces and provides an important first line of defense against pathogens. Recent studies show that sIgA can be measured noninvasively in feces and is a good marker of mucosal immunity. Here we validated a commercial ELISA kit to measure fecal IgA in baboons, tested the robustness of its results to variation in collection and storage conditions, and developed a cost-effective in-house ELISA for baboon fecal IgA. Using data from the custom ELISA, we assessed the relationship between fecal IgA concentrations and gastrointestinal parasite burden, and tested how sex, age, and reproductive effort predict fecal IgA in wild baboons. We find that IgA concentrations can be measured in baboon feces using an in-house ELISA and are highly correlated to the values obtained with a commercial kit. Fecal IgA concentrations are stable when extracts are stored for up to 22 months at -20°C. Fecal IgA concentrations were negatively correlated with parasite egg counts (Trichuris trichiura), but not parasite richness. Fecal IgA did not vary between the sexes, but for males, concentrations were higher in adults versus adolescents. Lactating females had significantly lower fecal IgA than pregnant females, but neither pregnant nor lactating female concentrations differed significantly from cycling females. Males who engaged in more mate-guarding exhibited similar IgA concentrations to those who engaged in little mate-guarding. These patterns may reflect the low energetic costs of mucosal immunity, or the complex dependence of IgA excretion on individual condition. Adding a noninvasive measure of mucosal immunity will promote a better understanding of how ecology modulates possible tradeoffs between the immune system and other energetically costly processes in the wild.

Costs and drivers of helminth parasite infection in wild female baboons.

Helminth parasites can have wide-ranging, detrimental effects on host reproduction and survival. These effects are best documented in humans and domestic animals, while only a few studies in wild mammals have identified both the forces that drive helminth infection risk and their costs to individual fitness. Working in a well-studied population of wild baboons (Papio cynocephalus) in the Amboseli ecosystem in Kenya, we pursued two goals, to (a) examine the costs of helminth infections in terms of female fertility and glucocorticoid hormone levels and (b) test how processes operating at multiple scales-from individual hosts to social groups and the population at large-work together to predict variation in female infection risk. To accomplish these goals, we measured helminth parasite burdens in 745 faecal samples collected over 5 years from 122 female baboons. We combine these data with detailed observations of host environments, social behaviours, hormone levels and interbirth intervals (IBIs). We found that helminths are costly to female fertility: females infected with more diverse parasite communities (i.e., higher parasite richness) exhibited longer IBIs than females infected by fewer parasite taxa. We also found that females exhibiting high Trichuris trichiura egg counts also had high glucocorticoid levels. Female infection risk was best predicted by factors at the host, social group and population level: females facing the highest risk were old, socially isolated, living in dry conditions and infected with other helminths. Our results provide an unusually holistic understanding of the factors that contribute to inter-individual differences in parasite infection, and they contribute to just a handful of studies linking helminths to host fitness in wild mammals.

Estimation of energetic condition in wild baboons using fecal thyroid hormone determination.

Understanding how environmental and social factors affect reproduction through variation in energetic condition remains understudied in wild animals, in large part because accurately and repeatedly measuring energetic condition in the wild is a challenge. Thyroid hormones (THs), such as triiodothyronine (T3) and thyroxine (T4), have a key role in mitigating metabolic responses to energy intake and expenditure, and therefore are considered important biomarkers of an animal's energetic condition. Recent method development has shown that T3 and T4 metabolites can be measured in feces, but studies measuring THs in wild populations remain rare. Here we measured fecal T3 metabolites (mT3) in baboons, and tested whether the conditions of collection and storage used for steroid hormones could also be used for mT3; we focused on mT3 as it is the biologically active form of TH and because fecal T4 metabolites (mT4) were below detection levels in our samples. We also tested if mT3 could be determined in freeze-dried samples stored for long periods of time, and if these concentrations reflected expected biological variations across seasons and reproductive states. Our results show that mT3 can be measured with accuracy and precision in baboon feces. The conditions of collection and storage we use for steroid hormones are appropriate for mT3 determination. In addition, mT3 concentrations can be determined in samples stored at -20 °C for up to 9 years, and are not predicted by the amount of time in storage. As expected, wild female baboons have lower mT3 concentrations during the dry season. Interestingly, mT3 concentrations are lower in pregnant and lactating females, possibly reflecting an energy sparing mechanism. Retroactive determination of mT3 concentration in stored, freeze-dried feces opens the door to novel studies on the role of energetic condition on fitness in wild animals.

Interbirth intervals in wild baboons: Environmental predictors and hormonal correlates.

OBJECTIVES: Interbirth intervals (IBIs) are a key metric of female reproductive success; understanding how they are regulated by environmental, social, and demographic factors can provide insight into sources of variance in female fitness. MATERIALS AND METHODS: Using 36 years of reproductive data on 490 IBIs for 160 wild female baboons, we identified sources of variance in the duration of IBIs and of their component phases: postpartum amenorrhea (PPA), sexual cycling, and pregnancy. We also examined how body fat and fecal hormone concentrations varied during female IBIs. RESULTS: We found that IBIs tended to be shorter (reproduction was accelerated) when female traits and environmental variables promoted energy acquisition, but with different specific effects for different component phases of the IBI. We also found that females lost a substantial amount of body fat during PPA, indicating that PPA imposes accumulating energetic costs as it progresses. Prior to cycle resumption females began to regain body fat; body fat was stable across the cycling phase and increased throughout most of pregnancy. However, body fat scores per se were not associated with the duration of any of the component phases. Finally, we found that fecal glucocorticoid concentrations decreased as PPA progressed, suggesting a decline in energetic stress over this phase. Fecal progestogen and estrogen concentrations changed over time during sexual cycling; the direction of these changes depended on the phase of the sexual cycle (luteal versus early or late follicular phases). DISCUSSION: Our study lends insight into the energetic constraints on female primate reproduction, revealing how female environments, changes in body fat, and steroid hormone concentrations relate to IBI duration and to reproductive readiness.

Validation of salivary oxytocin and vasopressin as biomarkers in domestic dogs.

BACKGROUND: Oxytocin (OT) and Vasopressin (AVP) are phylogenetically conserved neuropeptides with effects on social behavior, cognition and stress responses. Although OT and AVP are most commonly measured in blood, urine and cerebrospinal fluid (CSF), these approaches present an array of challenges including concerns related to the invasiveness of sample collection, the potential for matrix interference in immunoassays, and whether samples can be collected at precise time points to assess event-linked endocrine responses. NEW METHOD: We validated enzyme-linked immunosorbent assays (ELISAs) for the measurement of salivary OT and AVP in domestic dogs. RESULTS: Both OT and AVP were present in dog saliva and detectable by ELISA and high performance liquid chromatography - mass spectrometry (HPLC-MS). OT concentrations in dog saliva were much higher than those typically detected in humans. OT concentrations in the same samples analyzed with and without sample extraction were highly correlated, but this was not true for AVP. ELISA validation studies revealed good accuracy and parallelism, both with and without solid phase extraction. Collection of salivary samples with different synthetic swabs, or following salivary stimulation or the consumption of food led to variance in results. However, samples collected from the same dogs using different techniques tended to be positively correlated. We detected concurrent elevations in salivary and plasma OT during nursing. COMPARISON WITH EXISTING METHODS: There are currently no other validated methods for measuring OT/AVP in dog saliva. CONCLUSIONS: OT and AVP are present in dog saliva, and ELISAs for their detection are methodologically valid.

Effects of Affiliative Human-Animal Interaction on Dog Salivary and Plasma Oxytocin and Vasopressin.

Oxytocin (OT) and vasopressin (AVP) are neuropeptides with diverse effects on social behavior, cognition and stress responses. Recent studies suggest that OT facilitates and responds to affiliative forms of human-animal interaction (HAI). However, previous studies measuring OT and AVP in dogs have been limited to measures from blood or urine, which present concerns related to the invasiveness of sample collection, the potential for matrix interference in immunoassays, and whether samples can be collected at precise time points to assess event-linked endocrine responses. Previous studies from our laboratory validated salivary measures of OT and AVP in dogs, however, it is currently unknown whether these measures respond dynamically to aspects of HAI. Here, we investigated the effects of affiliative forms of HAI on both plasma and salivary OT and AVP in dogs. We employed a within- and between-subjects design with a group of Labrador retrievers and Labrador retriever × golden retriever crosses (23 females, 15 males). Half of the dogs engaged in 10 min of free-form friendly interaction with a human experimenter (HAI condition), and the other half rested quietly in the same environment, without human interaction (control condition). We collected blood and saliva samples before, and immediately following both experimental conditions, and all samples were analyzed using enzyme-linked immunosorbent assays (ELISAs) following previously validated protocols. Dogs participating in HAI exhibited a significant increase in both salivary OT (+39%) and plasma OT (+5.7%) whereas dogs in the control group did not. Salivary AVP showed no change in the HAI group but increased significantly (+33%) in the control group. Plasma AVP decreased significantly following HAI (-13%) but did not change across time in the control condition. Within the dogs exposed to HAI, increases in salivary OT, and decreases in plasma AVP, were predicted by the extent of affiliative behavior between the dog and human (indexed by scores from a principal components analysis of social behaviors between the dog and human). Collectively our results suggest that measures of salivary OT and AVP provide useful biomarkers in studies of HAI, and afford a flexible and non-invasive toolkit than can be employed in diverse research contexts.

Endogenous Oxytocin, Vasopressin, and Aggression in Domestic Dogs.

Aggressive behavior in dogs poses public health and animal welfare concerns, however the biological mechanisms regulating dog aggression are not well understood. We investigated the relationships between endogenous plasma oxytocin (OT) and vasopressin (AVP)-neuropeptides that have been linked to affiliative and aggressive behavior in other mammalian species-and aggression in domestic dogs. We first validated enzyme-linked immunosorbent assays (ELISAs) for the measurement of free (unbound) and total (free + bound) OT and AVP in dog plasma. In Experiment 1 we evaluated behavioral and neuroendocrine differences between a population of pet dogs with a history of chronic aggression toward conspecifics and a matched control group. Dogs with a history of aggression exhibited more aggressive behavior during simulated encounters with conspecifics, and had lower free, but higher total plasma AVP than matched controls, but there were no group differences for OT. In Experiment 2 we compared OT and AVP concentrations between pet dogs and a population of assistance dogs that have been bred for affiliative and non-aggressive temperaments, and investigated neuroendocrine predictors of individual differences in social behavior within the assistance dog population. Compared to pet dogs, assistance dogs had higher free and total OT, but there were no differences in either measure for AVP. Within the assistance dog population, dogs who behaved more aggressively toward a threatening stranger had higher total AVP than dogs who did not. Collectively these data suggest that endogenous OT and AVP may play critical roles in shaping dog social behavior, including aspects of both affiliation and aggression.

Costs and benefits of group living in primates: an energetic perspective.

Group size is a fundamental component of sociality, and has important consequences for an individual's fitness as well as the collective and cooperative behaviours of the group as a whole. This review focuses on how the costs and benefits of group living vary in female primates as a function of group size, with a particular emphasis on how competition within and between groups affects an individual's energetic balance. Because the repercussions of chronic energetic stress can lower an animal's fitness, identifying the predictors of energetic stress has important implications for understanding variation in survivorship and reproductive success within and between populations. Notably, we extend previous literature on this topic by discussing three physiological measures of energetic balance-glucocorticoids, c-peptides and thyroid hormones. Because these hormones can provide clear signals of metabolic states and processes, they present an important complement to field studies of spatial and temporal changes in food availability. We anticipate that their further application will play a crucial role in elucidating the adaptive significance of group size in different social and ecological contexts.This article is part of the themed issue 'Physiological determinants of social behaviour in animals'.

Hormonal correlates of natal dispersal and rank attainment in wild male baboons.

In many mammals, maturational milestones such as dispersal and the attainment of adult dominance rank mark stages in the onset of reproductive activity and depend on a coordinated set of hormonal and socio-behavioral changes. Studies that focus on the link between hormones and maturational milestones are uncommon in wild mammals because of the challenges of obtaining adequate sample sizes of maturing animals and of tracking the movements of dispersing animals. We examined two maturational milestones in wild male baboons-adult dominance rank attainment and natal dispersal-and measured their association with variation in glucocorticoids (fGC) and fecal testosterone (fT). We found that rank attainment is associated with an increase in fGC levels but not fT levels: males that have achieved any adult rank have higher fGC than males that have not yet attained an adult rank. This indicates that once males have attained an adult rank they experience greater energetic and/or psychosocial demands than they did prior to attaining this milestone, most likely because of the resulting participation in both agonistic and sexual behaviors that accompany rank attainment. In contrast, natal dispersal does not produce sustained increases in either fGC or fT levels, suggesting that individuals are either well adapted to face the challenges associated with dispersal or that the effects of dispersal on hormone levels are ephemeral for male baboons.