Epigenetic signatures of social status in wild female spotted hyenas (Crocuta crocuta).

In mammalian societies, dominance hierarchies translate into inequalities in health, reproductive performance and survival. DNA methylation is thought to mediate the effects of social status on gene expression and phenotypic outcomes, yet a study of social status-specific DNA methylation profiles in different age classes in a wild social mammal is missing. We tested for social status signatures in DNA methylation profiles in wild female spotted hyenas (Crocuta crocuta), cubs and adults, using non-invasively collected gut epithelium samples. In spotted hyena clans, female social status influences access to resources, foraging behavior, health, reproductive performance and survival. We identified 149 differentially methylated regions between 42 high- and low-ranking female spotted hyenas (cubs and adults). Differentially methylated genes were associated with energy conversion, immune function, glutamate receptor signalling and ion transport. Our results provide evidence that socio-environmental inequalities are reflected at the molecular level in cubs and adults in a wild social mammal.

Sex roles and sex ratios in animals.

In species with separate sexes, females and males often differ in their morphology, physiology and behaviour. Such sex-specific traits are functionally linked to variation in reproductive competition, mate choice and parental care, which have all been linked to sex roles. At the 150th anniversary of Darwin's theory on sexual selection, the question of why patterns of sex roles vary within and across species remains a key topic in behavioural and evolutionary ecology. New theoretical, experimental and comparative evidence suggests that variation in the adult sex ratio (ASR) is a key driver of variation in sex roles. Here, we first define and discuss the historical emergence of the sex role concept, including recent criticisms and rebuttals. Second, we review the various sex ratios with a focus on ASR, and explore its theoretical links to sex roles. Third, we explore the causes, and especially the consequences, of biased ASRs, focusing on the results of correlational and experimental studies of the effect of ASR variation on mate choice, sexual conflict, parental care and mating systems, social behaviour, hormone physiology and fitness. We present evidence that animals in diverse societies are sensitive to variation in local ASR, even on short timescales, and propose explanations for conflicting results. We conclude with an overview of open questions in this field integrating demography, life history and behaviour.

Early-life adversity predicts performance and fitness in a wild social carnivore.

Studies on humans indicate that encountering multiple sources of adversity in childhood increases the risk of poor long-term health and premature death. Far less is known about cumulative effects of adversity during early life in wildlife. Focusing on the spotted hyena Crocuta crocuta, a social mammal with small litters, extensive maternal care, slow development and access to resources determined by social rank, we determined the contribution of ecological, maternal, social and demographic factors during early life on performance and fitness, and tested whether the impact of early-life adversity is cumulative. Using longitudinal data from 666 female hyenas in the Serengeti National Park, we determined the early growth rate, survival to adulthood, age at first reproduction (AFR), lifetime reproductive success (LRS) and longevity. We fitted multivariate models in which we tested the effects of environmental factors on these performance measures. We then constructed a cumulative adversity index and fitted models to test the effect of this index on each performance measure. Finally, the value of cumulative adversity models was tested by comparing them to multivariate and single-effect models in which the effect of each environmental factor was considered separately. High maternal rank decreased the AFR of daughters. Singleton and dominant cubs had higher growth rate than subordinate cubs, and singletons also had a higher survival chance to adulthood than subordinates. Daughters of prime age mothers had a higher growth rate, longevity and LRS. Little and heavy rainfall decreased survival to adulthood. Increasing numbers of lactating female clan members decreased growth rate, survival to adulthood and LRS. Cumulative adversity negatively affected short-term performance and LRS. Multivariate models outperformed cumulative adversity and single-effect models for all measures except for AFR and longevity, for which single-effect models performed better. Our results suggest that in some wildlife populations the combination of specific conditions in early life may matter more than the accumulation of adverse conditions as such.

Des études menées chez l'homme indiquent que le fait de rencontrer de multiples sources d'adversité pendant l'enfance augmente le risque de troubles de la santé à long terme et de décès prématuré. On en sait beaucoup moins sur les effets cumulatifs de l'adversité en début de vie chez les animaux sauvages. En nous concentrant sur la hyène tachetée Crocuta crocuta, un mammifère social avec des portées de petite taille, des soins maternels intensifs, un développement lent et un accès aux ressources déterminé par le rang social, nous avons déterminé la contribution des facteurs écologiques, maternels, sociaux et démographiques en début de vie sur la performance et le succès reproducteur, et nous avons testé si l'adversité précoce a un effet cumulatif. En utilisant les données longitudinales de 666 hyènes femelles dans le parc national du Serengeti, nous avons calculé le taux de croissance précoce, la survie à l'âge adulte, l'âge à la première reproduction, le succès reproducteur et la longévité. Nous avons utilisé des modèles multivariés dans lesquels nous avons testé les effets des facteurs environnementaux sur ces mesures de performance. Nous avons ensuite construit un indice de risque cumulatif et utilisé des modèles pour tester l'effet de cet indice sur chaque mesure de performance. Enfin, nous avons testé la valeur de ces modèles en les comparant aux modèles multivariés et simples dans lesquels l'effet de chaque facteur environnemental était considéré séparément. Un rang maternel élevé diminue l'âge à la première reproduction des filles. Les femelles sans frère ou sœur ou dominantes dans une portée de jumeaux ont un taux de croissance plus élevé que les femelles subordonnées, et les femelles sans frère ou sœur ont également une plus grande chance de survie à l'âge adulte que les subordonnées. Les filles de mères dans la fleur de l'âge montrent de meilleurs taux de croissance, longévité et succès reproducteur. Des précipitations faibles ou fortes réduisent la survie à l'âge adulte. L'augmentation du nombre de femelles allaitantes dans le clan réduit le taux de croissance, la survie à l'âge adulte et le succès reproducteur. L'adversité précoce cumulée a un effet négatif sur la performance à court terme et le succès reproducteur. Les modèles multivariés sont toutefois plus performants que les modèles avec l'indice de risque cumulatif et plus performants que les modèles simples pour toutes les mesures, à l'exception de l'âge à la première reproduction et de la longévité, pour lesquelles les modèles simples sont plus performants. Nos résultats suggèrent que chez certaines populations sauvages, la combinaison de conditions spécifiques rencontrées en début de vie peut avoir plus d'importance que l'accumulation de conditions défavorables en tant que telles.

'Keeping the kids at home' can limit the persistence of contagious pathogens in social animals.

Social networks are considered to be 'highly modular' when individuals within one module are more connected to each other than they are to individuals in other modules. It is currently unclear how highly modular social networks influence the persistence of contagious pathogens that generate lifelong immunity in their hosts when between-group interactions are age dependent. This trait occurs in social species with communal nurseries, where juveniles are reared together for a substantial period in burrows or similar forms of containment and are thus in isolation from contact with individuals in other social groups. Our main objective was to determine whether, and to what extent, such age-dependent patterns of between-group interactions consistently increased the fade-out probability of contagious pathogens that generate lifelong immunity in their hosts. We hypothesised that in populations of species where juveniles are raised in communal nurseries, a high proportion of recovered adults in a group would form a 'protective barrier' around susceptible juveniles against pathogen transmission, thereby increasing the probability of epidemic fade-out in the population. To test this idea, we implemented a spatially implicit individual-based susceptible-infected-recovered (SIR) model for a large range of generic host and pathogen traits. Our results indicated that (a) the probability of epidemic fade-out was consistently higher in populations with communal nurseries, especially for highly contagious pathogens (high basic reproduction number, R0 ) and (b) communal nurseries can counteract the cost of group living in terms of infection risk to a greater extent than variation in other traits. We discuss our findings in relation to herd immunity and outline the importance of considering the network structure of a given host population before implementing management measures such as vaccinations, since interventions focused on individuals with high between-group contact should be particularly effective for controlling pathogen spread in hosts with communal nurseries.

Epigenomics and gene regulation in mammalian social systems.

Social epigenomics is a new field of research that studies how the social environment shapes the epigenome and how in turn the epigenome modulates behavior. We focus on describing known gene-environment interactions (GEIs) and epigenetic mechanisms in different mammalian social systems. To illustrate how epigenetic mechanisms integrate GEIs, we highlight examples where epigenetic mechanisms are associated with social behaviors and with their maintenance through neuroendocrine, locomotor, and metabolic responses. We discuss future research trajectories and open questions for the emerging field of social epigenomics in nonmodel and naturally occurring social systems. Finally, we outline the technological advances that aid the study of epigenetic mechanisms in the establishment of GEIs and vice versa.

Slow recovery from a disease epidemic in the spotted hyena, a keystone social carnivore.

Predicting the impact of disease epidemics on wildlife populations is one of the twenty-first century's main conservation challenges. The long-term demographic responses of wildlife populations to epidemics and the life history and social traits modulating these responses are generally unknown, particularly for K-selected social species. Here we develop a stage-structured matrix population model to provide a long-term projection of demographic responses by a keystone social predator, the spotted hyena, to a virulent epidemic of canine distemper virus (CDV) in the Serengeti ecosystem in 1993/1994 and predict the recovery time for the population following the epidemic. Using two decades of longitudinal data from 625 known hyenas, we demonstrate that although the reduction in population size was moderate, i.e., the population showed high ecological 'resistance' to the novel CDV genotype present, recovery was slow. Interestingly, high-ranking females accelerated the population's recovery, thereby lessening the impact of the epidemic on the population.

Robustness of Eco-Epidemiological Capture-Recapture Parameter Estimates to Variation in Infection State Uncertainty.

Estimating eco-epidemiological parameters in free-ranging populations can be challenging. As known individuals may be undetected during a field session, or their health status uncertain, the collected data are typically "imperfect". Multi-event capture-mark-recapture (MECMR) models constitute a substantial methodological advance by accounting for such imperfect data. In these models, animals can be "undetected" or "detected" at each time step. Detected animals can be assigned an infection state, such as "susceptible" (S), "infected" (I), or "recovered" (R), or an "unknown" (U) state, when for instance no biological sample could be collected. There may be heterogeneity in the assignment of infection states, depending on the manifestation of the disease in the host or the diagnostic method. For example, if obtaining the samples needed to prove viral infection in a detected animal is difficult, this can result in a low chance of assigning the I state. Currently, it is unknown how much uncertainty MECMR models can tolerate to provide reliable estimates of eco-epidemiological parameters and whether these parameters are sensitive to heterogeneity in the assignment of infection states. We used simulations to assess how estimates of the survival probability of individuals in different infection states and the probabilities of infection and recovery responded to (1) increasing infection state uncertainty (i.e., the proportion of U) from 20 to 90%, and (2) heterogeneity in the probability of assigning infection states. We simulated data, mimicking a highly virulent disease, and used SIR-MECMR models to quantify bias and precision. For most parameter estimates, bias increased and precision decreased gradually with state uncertainty. The probabilities of survival of I and R individuals and of detection of R individuals were very robust to increasing state uncertainty. In contrast, the probabilities of survival and detection of S individuals, and the infection and recovery probabilities showed high biases and low precisions when state uncertainty was >50%, particularly when the assignment of the S state was reduced. Considering this specific disease scenario, SIR-MECMR models are globally robust to state uncertainty and heterogeneity in state assignment, but the previously mentioned parameter estimates should be carefully interpreted if the proportion of U is high.

Social status mediates the fitness costs of infection with canine distemper virus in Serengeti spotted hyenas.

The extent to which the fitness costs of infection are mediated by key life-history traits such as age or social status is still unclear. Within populations, individual heterogeneity in the outcome of infection is the result of two successive processes; the degree of contact with the pathogen (exposure) and the immune response to infection. In social mammals, because individuals holding high social status typically interact more frequently with group members, they should be more often in contact with infected individuals than those of low social status. However, when access to resources is determined by social status, individuals with a high social status are often better nourished, have a greater opportunity to allocate resources to immune processes and therefore should have a smaller chance of succumbing to infection than individuals with low social status.We investigated the risk and fitness costs of infection during a virulent epidemic of canine distemper virus (CDV) in a social carnivore, the spotted hyena, in the Serengeti National Park. We analysed two decades of detailed life-history data from 625 females and 816 males using a multi-event capture-mark-recapture model that accounts for uncertainty in the assignment of individual infection states.Cubs of mothers with a high social status had a lower probability of CDV infection and were more likely to survive infection than those with low social status. Subadult and adult females with high social status had a higher infection probability than those with low social status. Subadult females and pre-breeder males that had recovered from CDV infection had a lower survival than susceptible ones.Our study disentangles the relative importance of individual exposure and resource allocation to immune processes, demonstrates fitness costs of infection for juveniles, particularly for those with low social status, shows that patterns of infection can be driven by different mechanisms among juveniles and adults and establishes a negative relationship between infection and fitness in a free-ranging mammal. A http://onlinelibrary.wiley.com/doi/10.1111/1365-2435.13059/suppinfo is available for this article.

Sibling competition and hunger increase allostatic load in spotted hyaenas.

Allostatis is the process of maintaining homeostatis through behavioural or physiological responses to challenges, and its cumulative energetic cost is termed allostatic load. The allostatic load hypothesis predicts that hunger and the mechanisms that establish and maintain social dominance should have a strong impact on allostatic load. In spotted hyaenas, dominance between twin siblings emerges during intense early competition for maternal milk and involves trained winner/loser effects. Conflict over access to teats declines with age as behavioural dominance conventions are established. In young litters, the allostatic load of subordinates measured in terms of faecal glucocorticoid metabolite concentrations (fGMCs) should be higher than that of dominants. When low milk provisioning threatens survival, hungry subordinates are more assertive, particularly when competing against a dominant sister. Dominants challenged by assertive subordinates should have allostatic loads and fGMCs above those of dominants with subordinates that adhere to dominance conventions. We show that in young litters, subordinates had significantly higher fGMCs than dominants, and dominant sisters had significantly higher fGMCs than dominant brothers. When hungry, both dominants and subordinates had significantly higher fGMCs than when fed. Our results provide evidence that hunger and sibling competition affect allostatic load in spotted hyaenas.

Factors influencing Dipylidium sp. infection in a free-ranging social carnivore, the spotted hyaena (Crocuta crocuta).

We provide the first genetic sequence data for a Dipylidium species from a wild carnivore plus an analysis of the effects of ecological, demographic, physiological and behavioural factors on Dipylidium sp. infection prevalence in a social carnivore, the spotted hyaena (Crocuta crocuta), in the Serengeti National Park, Tanzania. Our sequence data from a mitochondrial gene fragment (1176 base pair long) had a similarity of between 99% and 89% to Dipylidium caninum. We determined infection prevalence in 146 faecal samples from 124 known animals in three social groups (termed clans) using molecular screening and Dipylidium proglottid presence. Our analysis revealed significantly higher infection prevalence in juveniles (55%) than adults (15.8%), indicating that predominantly juveniles maintained infection in clans. The likelihood of infection in juveniles significantly: (1) increased as the number of adults and older juveniles (>6 months) at communal dens increased, implying a positive relationship between this factor and the size of the intermediate host (probably a flea species) population at communal dens; (2) decreased as the number of younger juveniles (<6 months) increased, suggesting that the chance of susceptible juveniles ingesting infected fleas during self-grooming declined as the number of infected fleas per younger juvenile declined; and (3) decreased during periods of low prey abundance in clan territories when an increased reliance on long-distances foraging excursions reduces the number of clan members visiting communal dens, possibly resulting in a decline in flea populations at dens. Long-distance foraging also increases the intervals (in days) between nursing visits by lactating females to their offspring. Lengthy intervals between milk intake by infected juveniles may reduce adult Dipylidium fecundity and hence decrease infection prevalence in the den flea population. Our study provides useful insights into Dipylidium epidemiology in a social carnivore population subject to large fluctuations in prey abundance.

Sibling rivalry: training effects, emergence of dominance and incomplete control.

Within-brood or -litter dominance provides fitness-related benefits if dominant siblings selfishly skew access to food provided by parents in their favour. Models of facultative siblicide assume that dominants exert complete control over their subordinate sibling's access to food and that control is maintained, irrespective of the subordinate's hunger level. By contrast, a recent functional hypothesis suggests that subordinates should contest access to food when the cost of not doing so is high. Here, we show that within spotted hyena (Crocuta crocuta) twin litters, dominants most effectively skew access to maternal milk in their favour when their aggression prompts a highly submissive response. When hungry, subordinates were less submissive in response to aggression, thereby decreasing lost suckling time and increasing suckling time lost by dominants. In a species where adult females socially dominate adult males, juvenile females were more often dominant than males in mixed-sex litters, and subordinate sisters used more effective counter-tactics against dominant brothers than subordinate brothers against dominant sisters. Our results provide, to our knowledge, the first evidence in a mammal that dominant offspring in twin litters do not exert complete control over their sibling's access to resources (milk), and that sibling dominance relationships are influenced by sibling sex and training effects.

Validation of an enzyme immunoassay for the measurement of faecal glucocorticoid metabolites in spotted hyenas (Crocuta crocuta).

The use of enzyme immunoassays (EIAs) to measure faecal glucocorticoid metabolites (fGCM) is a useful non-invasive technique to monitor adrenocortical activity in vertebrates. The first objective of this study was to validate an 'in-house' EIA (cortisol-3-CMO) for the measurement of fGCM concentrations in spotted hyenas. High-performance liquid chromatography (HPLC) was used to characterise fGCM in samples from a captive hyena that received an i.v. injection of [(3)H] cortisol. All HPLC fractions were analysed with the EIA for the presence and quantities of radiolabelled fGCM. Radiolabelled fGCM consisted of substances with a higher polarity than cortisol and substances of lower polarity that eluted between cortisol and corticosterone. Authentic radiolabelled cortisol was not detected. The EIA measured substantial amounts of immunoreactivity corresponding to the radioactive peaks. It also detected a significant increase in fGCMs after an adrenocorticotropic hormone (ACTH) challenge in two other captive animals and a significant increase in fGCMs in a fourth captive animal after anaesthesia. The second objective was to investigate an age effect on fGCM: we conducted pairwise comparisons of fGCM concentrations in individual free-ranging juvenile spotted hyenas when less than 6 months of age and when between 6 and 24 months of age. We expected juveniles to experience a more unpredictable and therefore more stressful environment when younger than when older. When younger, juveniles had significantly higher fGCM concentrations than when they were older. Our results demonstrate that our assay can be used to assess adrenocortical activity in spotted hyenas.