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Studies in rodents and captive primates suggest that the early-life social environment affects future phenotype, potentially through alterations to DNA methylation. Little is known of these associations in wild animals. In a wild population of spotted hyenas, we test the hypothesis that maternal care during the first year of life and social connectedness during two periods of early development leads to differences in DNA methylation and fecal glucocorticoid metabolites (fGCMs) later in life. Here we report that although maternal care and social connectedness during the den-dependent life stage are not associated with fGCMs, greater social connectedness during the subadult den-independent life stage is associated with lower adult fGCMs. Additionally, more maternal care and social connectedness after den independence correspond with higher global (%CCGG) DNA methylation. We also note differential DNA methylation near 5 genes involved in inflammation, immune response, and aging that may link maternal care with stress phenotype. Early social experience can alter epigenetic patterns and stress responses later in life. A study on wild spotted hyenas finds that maternal care and social connections after leaving the den influence DNA methylation and contribute to a developmentally plastic stress response.

Host-associated microbial communities, henceforth ‘microbiota’, can affect the physiology and behavior of their hosts. In mammals, host ecological, social and environmental variables are associated with variation in microbial communities. Within individuals in a given mammalian species, the microbiota also partitions by body site. Here, we build on this work and sequence the bacterial 16S rRNA gene to profile the microbiota at six distinct body sites (ear, nasal and oral cavities, prepuce, rectum and anal scent gland) in a population of wild spotted hyenas (Crocuta crocuta), which are highly social, large African carnivores. We inquired whether microbiota at these body sites vary with host sex or social rank among juvenile hyenas, and whether they differ between juvenile females and adult females. We found that the scent gland microbiota differed between juvenile males and juvenile females, whereas the prepuce and rectal microbiota differed between adult females and juvenile females. Social rank, however, was not a significant predictor of microbiota profiles. Additionally, the microbiota varied considerably among the six sampled body sites and exhibited strong specificity among individual hyenas. Thus, our findings suggest that site-specific niche selection is a primary driver of microbiota structure in mammals, but endogenous host factors may also be influential.

All animals harbor beneficial microbes. One way these microbes can benefit their animal hosts is by increasing the diversity and efficacy of communication signals available to the hosts. The fermentation hypothesis for mammalian chemical communication posits that bacteria in the scent glands of mammals generate odorous metabolites used by their hosts for communication and that variation in host chemical signals is a product of underlying variation in the bacterial communities inhabiting the scent glands. An effective test of this hypothesis would require accurate surveys of the bacterial communities in mammals’ scent glands and complementary data on the odorant profiles of scent secretions—both of which have been historically lacking. Here we use next-generation sequencing to survey deeply the bacterial communities in the scent glands of wild spotted and striped hyenas. We show that these communities are dominated by fermentative bacteria and that the structures of these communities covary with the volatile fatty acid profiles of scent secretions in both hyena species. The bacterial and volatile fatty acid profiles of secretions differ between spotted and striped hyenas, and both profiles vary with sex and reproductive state among spotted hyenas within a single social group. Our results strongly support the fermentation hypothesis for chemical communication, suggesting that symbiotic bacteria underlie species-specific odors in both spotted and striped hyenas and further underlie sex and reproductive state-specific odors among spotted hyenas. We anticipate that the fermentation hypothesis for chemical communication will prove broadly applicable among scent-marking mammals as others use the technical and analytical approaches used here.

We suggest that variation in mammalian behavioural flexibility not accounted for by current socioecological models may be explained in part by developmental constraints. From our own work, we provide examples of constraints affecting variation in behavioural flexibility, not only among individuals, but also among species and higher taxonomic units. We first implicate organizational maternal effects of androgens in shaping individual differences in aggressive behaviour emitted by female spotted hyaenas throughout the lifespan. We then compare carnivores and primates with respect to their locomotor and craniofacial adaptations. We inquire whether antagonistic selection pressures on the skull might impose differential functional constraints on evolvability of skulls and brains in these two orders, thus ultimately affecting behavioural flexibility in each group. We suggest that, even when carnivores and primates would theoretically benefit from the same adaptations with respect to behavioural flexibility, carnivores may nevertheless exhibit less behavioural flexibility than primates because of constraints imposed by past adaptations in the morphology of the limbs and skull. Phylogenetic analysis consistent with this idea suggests greater evolutionary lability in relative brain size within families of primates than carnivores. Thus, consideration of developmental constraints may help elucidate variation in mammalian behavioural flexibility.

We review matrilineal relationships in the societies of fissiped mammalian carnivores, focusing on how the most complex of these may have evolved from simpler systems. Although competition for food is very intense at the trophic level occupied by most carnivores, and although most species of extant fissiped carnivores therefore lead solitary lives, some species show at least rudimentary clustering of maternal kin and matrilineal resource-sharing or transmission of critical resources between generations. The resources shared or transmitted range from individual food items and territories to entire networks of potential allies. The greatest elaboration of matrilineal relationships has occurred in two large carnivores, lions and spotted hyenas, which occur sympatrically throughout much of Africa. The societies of both these species apparently evolved in response to a shared suite of ecological conditions. The highly matrilineal societies of spotted hyenas are unique among carnivores and closely resemble the societies of many cercopithecine primates. The conditions favouring the evolution of matrilineal societies in carnivores include male-biased dispersal, female philopatry, the need for assistance in protecting or provisioning offspring, reliance on large or abundant prey, particularly in open habitat, high population density and kin-structured cooperative interactions that have strong positive effects on fitness. This article is part of the theme issue ‘The evolution of female-biased kinship in humans and other mammals’.

Intergroup conflict is a major evolutionary force shaping animal and human societies. Males and females should, on average, experience different costs and benefits for participating in collective action. Specifically, among mammals, male fitness is generally limited by access to mates whereas females are limited by access to food and safety. Here we analyse sex biases among 72 species of group-living mammals in two contexts: intergroup conflict and collective movements. Our comparative phylogenetic analyses show that the modal mammalian pattern is male-biased participation in intergroup conflict and female-biased leadership in collective movements. However, the probability of male-biased participation in intergroup conflicts decreased and female-biased participation increased with female-biased leadership in movements. Thus, female-biased participation in intergroup conflict only emerged in species with female-biased leadership in collective movements, such as in spotted hyenas and some lemurs. Sex differences are probably attributable to costs and benefits of participating in collective movements (e.g. towards food, water, safety) and intergroup conflict (e.g. access to mates or resources, risk of injury). Our comparative review offers new insights into the factors shaping sex bias in leadership across social mammals and is consistent with the 'male warrior hypothesis' which posits evolved sex differences in human intergroup psychology. This article is part of the theme issue 'Intergroup conflict across taxa'.

In mammals, two factors likely to affect the diversity and composition of intestinal bacteria (bacterial microbiome) and eukaryotes (eukaryome) are social status and age. In species in which social status determines access to resources, socially dominant animals maintain better immune processes and health status than subordinates. As high species diversity is an index of ecosystem health, the intestinal biome of healthier, socially dominant animals should be more diverse than those of subordinates. Gradual colonization of the juvenile intestine after birth predicts lower intestinal biome diversity in juveniles than adults. We tested these predictions on the effect of: (1) age (juvenile/adult) and (2) social status (low/high) on bacterial microbiome and eukaryome diversity and composition in the spotted hyena ( ), a highly social, female-dominated carnivore in which social status determines access to resources. We comprehensively screened feces from 35 individually known adult females and 7 juveniles in the Serengeti ecosystem for bacteria and eukaryotes, using a set of 48 different amplicons (4 for bacterial 16S, 44 for eukaryote 18S) in a multi-amplicon sequencing approach. We compared sequence abundances to classical coprological egg or oocyst counts. For all parasite taxa detected in more than six samples, the number of sequence reads significantly predicted the number of eggs or oocysts counted, underscoring the value of an amplicon sequencing approach for quantitative measurements of parasite load. In line with our predictions, our results revealed a significantly less diverse microbiome in juveniles than adults and a significantly higher diversity of eukaryotes in high-ranking than low-ranking animals. We propose that free-ranging wildlife can provide an intriguing model system to assess the adaptive value of intestinal biome diversity for both bacteria and eukaryotes.

Social hierarchies are widespread in human and animal societies, and an individual’s position in its hierarchy affects both its access to resources and its fitness. Hierarchies are traditionally thought of in terms of variation in individual ability to win fights, but many are structured around arbitrary conventions like nepotistic inheritance rather than such traits as physical strength or weapon size. These convention-based societies are perplexing because position in the hierarchy appears to be gained irrespective of individual physical ability, yet social status strongly affects access to resources and fitness. It remains unclear why individuals abide by seemingly arbitrary conventions regarding social status when they stand to benefit by ignoring these conventions and competing for top positions or access to resources. Using data from wild spotted hyenas collected over 27 y and five generations, we show that individuals who repeatedly form coalitions with their top allies are likely to improve their position in the hierarchy, suggesting that social alliances facilitate revolutionary social change. Using lifetime reproductive success as a fitness measure, we go on to demonstrate that these status changes can have major fitness consequences. Finally, we show that the consequences of these changes may become even more dramatic over multiple generations, as small differences in social rank become amplified over time. This work represents a first step in reconciling the advantages of high status with the appearance of “arbitrary” conventions that structure inequality in animal and human societies.

Background The aardwolf skulls were analyzed and compared to the spotted hyena, the brown hyena and the striped hyena, using specimens from Polish and South African collections. Addressing gaps in detailed anatomy and morphometrics, this study used extensive analyzes, encompassing 64 morphometric parameters and 7 indices, to examine the morphology and morphometrics of cranial and mandibular structures and quantify interspecific and intraspecific variation. Results The comparative analysis of hyena skulls revealed significant differences between the aardwolf and the other three species. The aardwolf consistently had the smallest and proportionally narrowest skull, characterized by high morphological stability and a wide neurocranium. The brown hyena and spotted hyena had the largest skulls; however, the brown hyena showed greater homogeneity, while the spotted hyena displayed higher absolute variability. Morphologically, the aardwolf’s basilar part was cylindrical, unlike the pyramidal shape in the spotted hyena, and it possessed prominent nuchal tubercles that were reduced in the brown and spotted hyenas. Conclusions This study demonstrates that the morphological and morphometric features of the aardwolf’s skull are highly specialized and fundamentally distinct from the other three hyena species, reflecting its unique dietary niche. The powerful skulls of the spotted and brown hyenas, in contrast, correlate with their roles as apex predators and scavengers.

Background: The striped hyena (Hyaena hyaena) occurs in a wide range from north and east Africa, through southwest Asia to India, but its distribution is increasingly patchy and many of its populations are in decline due to intense human pressure. Its genetic diversity and structure, phylogeography, and evolutionary history, remain poorly understood. Methods: In this study, we investigated mitochondrial DNA variation in Algerian striped hyenas. Moreover, with the aim of contributing to our understanding of the evolutionary history of the species, we also examined samples from other geographic regions and compared our results with those of the only previous study in which individuals from across the range of the species were analyzed. In particular, we performed a wide range of analyses of demographic history and estimation of the age of the extant mitochondrial DNA variation. Results and Conclusions: The Algerian population sample was monomorphic. Overall, the global patterns of genetic diversity and the results of some demographic history analyses support a scenario of population growth in the species, estimated to have occurred in the Late Pleistocene, but many of the analyses did not detect a significant signal of growth, most likely a result of the limited power provided by a small number of segregating sites. The estimates, from three different methods, for the time to the most recent common ancestor (TMRCA) of the mitochondrial DNA variation hovered around 400 ka, coinciding with one of the longest and warmest interglacials of the last 800,000 years, with environmental conditions similar to the Holocene.