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Integrated community models-an emerging framework in which multiple data sources for multiple species are analyzed simultaneously-offer opportunities to expand inferences beyond the single-species and single-data-source approaches common in ecology. We developed a novel integrated community model that combines distance sampling and single-visit count data; within the model, information is shared among data sources (via a joint likelihood) and species (via a random-effects structure) to estimate abundance patterns across a community. Parameters relating to abundance are shared between data sources, and the model can specify either shared or separate observation processes for each data source. Simulations demonstrated that the model provided unbiased estimates of abundance and detection parameters even when detection probabilities varied between the data types. The integrated community model also provided more accurate and more precise parameter estimates than alternative single-species and single-data-source models in many instances. We applied the model to a community of 11 herbivore species in the Masai Mara National Reserve, Kenya, and found considerable interspecific variation in response to local wildlife management practices: Five species showed higher abundances in a region with passive conservation enforcement (median across species: 4.5× higher), three species showed higher abundances in a region with active conservation enforcement (median: 3.9× higher), and the remaining three species showed no abundance differences between the two regions. Furthermore, the community average of abundance was slightly higher in the region with active conservation enforcement but not definitively so (posterior mean: higher by 0.20 animals; 95% credible interval: 1.43 fewer animals, 1.86 more animals). Our integrated community modeling framework has the potential to expand the scope of inference over space, time, and levels of biological organization, but practitioners should carefully evaluate whether model assumptions are met in their systems and whether data integration is valuable for their applications., (© 2024 The Author(s). Ecology published by Wiley Periodicals LLC on behalf of The Ecological Society of America.)

Much historic work has focused on establishing geographical and ecological rules that broadly explain patterns in size variation. We examined geographic variation in Spotted Hyena skull size using geometric morphometrics and spatial statistics. We quantified size variation and sexual size dimorphism of the skull, and evaluated the influence of temperature, precipitation, land cover type, and population density on skull size. We found that female spotted hyenas are slightly larger on average than males. Our analysis of regional differences did not indicate geographic variation in sexual size dimorphism. Skull size of Spotted Hyenas varies with geography but does not adhere to Bergmann's Rule. The smallest individuals of both sexes occur between -5.00° and 10.00° latitude and east of 28.50° longitude, with larger individuals being found elsewhere. Although Spotted Hyena skull size co-varies in some views with such variables as habitat type and climate indicators, skull size in this species most strongly co-varies with population density. The highest population densities are associated with the smallest skull size, possibly reflecting a relationship between high population density and access to resources. These results suggest that geographic variation in Spotted Hyena skull size is better explained by the energetic equivalence rule than Bergmann's Rule., Competing Interests: None declared., (© The Author(s) 2024. Published by Oxford University Press on behalf of the American Society of Mammalogists.)

Collective action problems arise when cooperating individuals suffer costs of cooperation, while the benefits of cooperation are received by both cooperators and defectors. We address this problem using data from spotted hyenas fighting with lions. Lions are much larger and kill many hyenas, so these fights require cooperative mobbing by hyenas for them to succeed. We identify factors that predict when hyena groups engage in cooperative fights with lions, which individuals choose to participate and how the benefits of victory are distributed among cooperators and non-cooperators. We find that cooperative mobbing is better predicted by lower costs (no male lions, more hyenas) than higher benefits (need for food). Individual participation is facilitated by social factors, both over the long term (close kin, social bond strength) and the short term (greeting interactions prior to cooperation). Finally, we find some direct benefits of participation: after cooperation, participants were more likely to feed at contested carcasses than non-participants. Overall, these results are consistent with the hypothesis that, when animals face dangerous cooperative dilemmas, selection favours flexible strategies that are sensitive to dynamic factors emerging over multiple time scales.

Animal activity patterns are highly variable and influenced by internal and external factors, including social processes. Quantifying activity patterns in natural settings can be challenging, as it is difficult to monitor animals over long time periods. Here, we developed and validated a machine-learning-based classifier to identify behavioural states from accelerometer data of wild spotted hyenas (Crocuta crocuta) , social carnivores that live in large fission-fusion societies. By combining this classifier with continuous collar-based accelerometer data from five hyenas, we generated a complete record of activity patterns over more than one month. We used these continuous behavioural sequences to investigate how past activity, individual idiosyncrasies, and social synchronization influence hyena activity patterns. We found that hyenas exhibit characteristic crepuscular-nocturnal daily activity patterns. Time spent active was independent of activity level on previous days, suggesting that hyenas do not show activity compensation. We also found limited evidence for an effect of individual identity on activity, and showed that pairs of hyenas who synchronized their activity patterns must have spent more time together. This study sheds light on the patterns and drivers of activity in spotted hyena societies, and also provides a useful tool for quantifying behavioural sequences from accelerometer data., Competing Interests: We declare we have no competing interests., (© 2023 The Authors.)

Wide-ranging carnivores experience tradeoffs between dynamic resource availabilities and heterogeneous risks from humans, with consequences for their ecological function and conservation outcomes. Yet, research investigating these tradeoffs across large carnivore distributions is rare. We assessed how resource availability and anthropogenic risks influence the strength of lion (Panthera leo) responses to disturbance using data from 31 sites across lions' contemporary range. Lions avoided human disturbance at over two-thirds of sites, though their responses varied depending on site-level characteristics. Lions were more likely to exploit human-dominated landscapes where resources were limited, indicating that resource limitation can outweigh anthropogenic risks and might exacerbate human-carnivore conflict. Lions also avoided human impacts by increasing their nocturnal activity more often at sites with higher production of cattle. The combined effects of expanding human impacts and environmental change threaten to simultaneously downgrade the ecological function of carnivores and intensify human-carnivore conflicts, escalating extinction risks for many species., (© 2023. Springer Nature Limited.)

The gut microbiome provides vital functions for mammalian hosts, yet research on its variability and function across adult life spans and multiple generations is limited in large mammalian carnivores. Here, we used 16S rRNA gene and metagenomic high-throughput sequencing to profile the bacterial taxonomic composition, genomic diversity, and metabolic function of fecal samples collected from 12 wild spotted hyenas ( Crocuta crocuta ) residing in the Masai Mara National Reserve, Kenya, over a 23-year period spanning three generations. The metagenomic data came from four of these hyenas and spanned two 2-year periods. With these data, we determined the extent to which host factors predicted variation in the gut microbiome and identified the core microbes present in the guts of hyenas. We also investigated novel genomic diversity in the mammalian gut by reporting the first metagenome-assembled genomes (MAGs) for hyenas. We found that gut microbiome taxonomic composition varied temporally, but despite this, a core set of 14 bacterial genera were identified. The strongest predictors of the microbiome were host identity and age, suggesting that hyenas possess individualized microbiomes and that these may change with age during adulthood. The gut microbiome functional profiles of the four adult hyenas were also individual specific and were associated with prey abundance, indicating that the functions of the gut microbiome vary with host diet. We recovered 149 high-quality MAGs from the hyenas' guts; some MAGs were classified as taxa previously reported for other carnivores, but many were novel and lacked species-level matches to genomes in existing reference databases. IMPORTANCE There is a gap in knowledge regarding the genomic diversity and variation of the gut microbiome across a host's life span and across multiple generations of hosts in wild mammals. Using two types of sequencing approaches, we found that although gut microbiomes were individualized and temporally variable among hyenas, they correlated similarly to large-scale changes in the ecological conditions experienced by their hosts. We also recovered 149 high-quality MAGs from the hyena gut, greatly expanding the microbial genome repertoire known for hyenas, carnivores, and wild mammals in general. Some MAGs came from genera abundant in the gastrointestinal tracts of canid species and other carnivores, but over 80% of MAGs were novel and from species not previously represented in genome databases. Collectively, our novel body of work illustrates the importance of surveying the gut microbiome of nonmodel wild hosts, using multiple sequencing methods and computational approaches and at distinct scales of analysis.

In animal societies, identity signals are common, mediate interactions within groups, and allow individuals to discriminate group-mates from out-group competitors. However, individual recognition becomes increasingly challenging as group size increases and as signals must be transmitted over greater distances. Group vocal signatures may evolve when successful in-group/out-group distinctions are at the crux of fitness-relevant decisions, but group signatures alone are insufficient when differentiated within-group relationships are important for decision-making. Spotted hyenas are social carnivores that live in stable clans of less than 125 individuals composed of multiple unrelated matrilines. Clan members cooperate to defend resources and communal territories from neighbouring clans and other mega carnivores; this collective defence is mediated by long-range (up to 5 km range) recruitment vocalizations, called whoops. Here, we use machine learning to determine that spotted hyena whoops contain individual but not group signatures, and that fundamental frequency features which propagate well are critical for individual discrimination. For effective clan-level cooperation, hyenas face the cognitive challenge of remembering and recognizing individual voices at long range. We show that serial redundancy in whoop bouts increases individual classification accuracy and thus extended call bouts used by hyenas probably evolved to overcome the challenges of communicating individual identity at long distance.

In ecology and evolutionary biology (EEB), the study of developmental plasticity seeks to understand ontogenetic processes underlying the phenotypes upon which natural selection acts. A central challenge to this inquiry is ascertaining a causal effect of the exposure on the manifestation of later-life phenotype due to the time elapsed between the two events. The exposure is a potential cause of the outcome-i.e. an environmental stimulus or experience. The later phenotype might be a behaviour, physiological condition, morphology or life-history trait. The latency period between the exposure and outcome complicates causal inference due to the inevitable occurrence of additional events that may affect the relationship of interest. Here, we describe six distinct but non-mutually exclusive conceptual models from the field of lifecourse epidemiology and discuss their applications to EEB research. The models include Critical Period with No Later Modifiers, Critical Period with Later Modifiers, Accumulation of Risk with Independent Risk Exposures, Accumulation of Risk with Risk Clustering, Accumulation of Risk with Chains of Risk and Accumulation of Risk with Trigger Effect. These models, which have been widely used to test causal hypotheses regarding the early origins of adult-onset disease in humans, are directly relevant to research on developmental plasticity in EEB.

The apparent virilization of the female spotted hyena raises questions about sex differences in behavior and morphology. We review these sex differences to find a mosaic of dimorphic traits, some of which conform to mammalian norms. These include space-use, dispersal behavior, sexual behavior, and parental behavior. By contrast, sex differences are reversed from mammalian norms in the hyena's aggressive behavior, social dominance, and territory defense. Androgen exposure early in development appears to enhance aggressiveness in female hyenas. Weapons, hunting behavior, and neonatal body mass do not differ between males and females, but females are slightly larger than males as adults. Sex differences in the hyena's nervous system are relatively subtle. Overall, it appears that the "masculinized" behavioral traits in female spotted hyenas are those, such as aggression, that are essential to ensuring consistent access to food; food critically limits female reproductive success in this species because female spotted hyenas have the highest energetic investment per litter of any mammalian carnivore. Evidently, natural selection has acted to modify traits related to food access, but has left intact those traits that are unrelated to acquiring food, such that they conform to patterns of sexual dimorphism in other mammals., (Copyright © 2022 Cold Spring Harbor Laboratory Press; all rights reserved.)

Aim: Comprehensive, global information on species' occurrences is an essential biodiversity variable and central to a range of applications in ecology, evolution, biogeography and conservation. Expert range maps often represent a species' only available distributional information and play an increasing role in conservation assessments and macroecology. We provide global range maps for the native ranges of all extant mammal species harmonised to the taxonomy of the Mammal Diversity Database (MDD) mobilised from two sources, the Handbook of the Mammals of the World (HMW) and the Illustrated Checklist of the Mammals of the World (CMW)., Location: Global., Taxon: All extant mammal species., Methods: Range maps were digitally interpreted, georeferenced, error-checked and subsequently taxonomically aligned between the HMW (6253 species), the CMW (6431 species) and the MDD taxonomies (6362 species)., Results: Range maps can be evaluated and visualised in an online map browser at Map of Life (mol.org) and accessed for individual or batch download for non-commercial use., Main Conclusion: Expert maps of species' global distributions are limited in their spatial detail and temporal specificity, but form a useful basis for broad-scale characterizations and model-based integration with other data. We provide georeferenced range maps for the native ranges of all extant mammal species as shapefiles, with species-level metadata and source information packaged together in geodatabase format. Across the three taxonomic sources our maps entail, there are 1784 taxonomic name differences compared to the maps currently available on the IUCN Red List website. The expert maps provided here are harmonised to the MDD taxonomic authority and linked to a community of online tools that will enable transparent future updates and version control., Competing Interests: CONFLICT OF INTEREST The authors declare no competing interests.

Salivary hormone analyses provide a useful alternative to fecal and urinary hormone analyses in non-invasive studies of behavioral endocrinology. Here, we use saliva to assess cortisol levels in a wild population of spotted hyenas (Crocuta crocuta), a gregarious carnivore living in complex social groups. We first describe a novel, non-invasive method of collecting saliva from juvenile hyenas and validate a salivary cortisol assay for use in this species. We then analyze over 260 saliva samples collected from nearly 70 juveniles to investigate the relationships between cortisol and temporal and social variables in these animals. We obtain some evidence of a bimodal daily rhythm with salivary cortisol concentrations dropping around dawn and dusk, times at which cub activity levels are changing substantially. We also find that dominant littermates have lower cortisol than singleton juveniles, but that cortisol does not vary with age, sex, or maternal social rank. Finally, we examine how social behaviors such as aggression or play affect salivary cortisol concentrations. We find that inflicting aggression on others was associated with lower cortisol concentrations. We hope that the detailed description of our methods provides wildlife researchers with the tools to measure salivary cortisol in other wild carnivores., (Copyright © 2021 Elsevier Inc. All rights reserved.)

From population estimates to social evolution, much of our understanding of the family Hyaenidae is drawn from studies of known individuals. The extant species in this family (spotted hyenas, Crocuta crocuta , brown hyenas, Parahyaena brunnea , striped hyenas, Hyaena hyaena , and aardwolves, Proteles cristata ) are behaviorally diverse, presenting an equally diverse set of logistical constraints on capturing and marking individuals. All these species are individually identifiable by their coat patterns, providing a useful alternative to man-made markings. Many studies have demonstrated the utility of this method in answering a wide range of research questions across all four species, with some employing a creative fusion of techniques. Despite its pervasiveness in basic research on hyenas and aardwolves, individual identification has rarely been applied to the conservation and management of these species. We argue that individual identification using naturally occurring markings in applied research could prove immensely helpful, as this could further improve accuracy of density estimates, reveal characteristics of suitable habitat, identify threats to population persistence, and help to identify individual problem animals., Supplementary Information: The online version contains supplementary material available at 10.1007/s42991-022-00309-4., Competing Interests: Conflict of interestOn behalf of all authors, the corresponding author states that there is no conflict of interest., (© The Author(s) under exclusive licence to Deutsche Gesellschaft für Säugetierkunde 2022, Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.)

Toxoplasma gondii is a common parasite that infects warm-blooded animals and influences host physiology. T. gondii is known to target the host's central nervous system, affecting circulating levels of steroid hormones, fear-related behaviors, and health, although these effects appear to vary among host taxa. Here, we investigated the relationship between T. gondii infection and levels of plasma testosterone and cortisol within a wild population of spotted hyenas ( Crocuta crocuta , n = 109). In our analyses, we accounted for age and sex via stratified regression analyses. We detected a negative association between circulating plasma testosterone and T. gondii infection among female cubs and subadults as well as adult male hyenas. We found no associations between T. gondii infection and cortisol in any age class or sex group of hyenas. Our work adds to a growing body of literature by characterizing the relationship between T. gondii infection and physiology in a novel host in its natural habitat. In a broader context, our findings indicate that responses to infection vary with characteristics of the host and point to a clear need for additional studies and priorities for future work that include diverse taxa and ecological settings., Competing Interests: The authors have declared that no competing interests exist., (© 2021 The Authors.)

AbstractSocial animals benefit from their groupmates, so why do they sometimes kill each other's offspring? Using 30 years of data from multiple groups of wild spotted hyenas, we address three critical aims for understanding infanticide in any species: (1) quantify the contribution of infanticide to overall mortality, (2) describe the circumstances under which infanticide occurs, and (3) evaluate hypotheses about the evolution of infanticide. We find that infanticide, although observed only rarely, is in fact a leading source of juvenile mortality. Infanticide accounted for 24% of juvenile mortality, and one in 10 hyenas born in our population perished as a result of infanticide. In all observed cases of infanticide, killers were adult females, but victims could be of both sexes. Of four hypotheses regarding the evolution of infanticide, we found the most support for the hypothesis that infanticide in spotted hyenas reflects competition over social status among matrilines.

Urbanization represents a dramatic form of evolutionary novelty in the landscapes inhabited by many extant animals. The Cognitive Buffer Hypothesis suggests that innovation, the process by which animals solve novel problems or use novel behaviors, may be key for many animals when adapting to novel environments. If innovation is especially beneficial in urban environments, then we would expect urban animals to be more innovative than their non-urban counterparts. However, studies comparing innovative problem-solving between urban and rural habitats have produced mixed results. Here, we hypothesized that these findings result from comparing only two levels of urbanization when related research suggests that the stage of invasion of urban habitats likely has a strong effect on demand for innovation, with demand being highest during early establishment in a novel environment. To test this hypothesis, we assessed innovation in three locations where spotted hyenas experienced varying degrees of urbanization. Spotted hyenas are relatively innovative compared to other carnivores and, although many large carnivores in Africa are endangered, spotted hyenas remain abundant both inside and outside protected areas. We measured innovation with a multi-access puzzle box with four different doors through which hyenas could obtain a food reward. We predicted that hyenas in a transitional, rapidly urbanizing habitat would be more innovative, measured by the number of unique doors opened, than those in rural or fully urban habitats. Contrary to our predictions, hyenas in the rural habitat were the most innovative. These results challenge the idea that the evolutionary novelty associated with urbanization favors greater innovativeness., (© 2021. The Author(s), under exclusive licence to Springer-Verlag GmbH, DE part of Springer Nature.)

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., (© 2021. The Author(s).)

The structure of animal social networks influences survival and reproductive success, as well as pathogen and information transmission. However, the general mechanisms determining social structure remain unclear. Using data from 73,767 social interactions among wild spotted hyenas collected over 27 years, we show that the process of social inheritance determines how offspring relationships are formed and maintained. Relationships between offspring and other hyenas bear resemblance to those of their mothers for as long as 6 years, and the degree of similarity increases with maternal social rank. Mother-offspring relationship strength affects social inheritance and is positively correlated with offspring longevity. These results support the hypothesis that social inheritance of relationships can structure animal social networks and be subject to adaptive tradeoffs., (Copyright © 2021 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works.)

Toxoplasma gondii is hypothesized to manipulate the behavior of warm-blooded hosts to promote trophic transmission into the parasite's definitive feline hosts. A key prediction of this hypothesis is that T. gondii infections of non-feline hosts are associated with costly behavior toward T. gondii's definitive hosts; however, this effect has not been documented in any of the parasite's diverse wild hosts during naturally occurring interactions with felines. Here, three decades of field observations reveal that T. gondii-infected hyena cubs approach lions more closely than uninfected peers and have higher rates of lion mortality. We discuss these results in light of 1) the possibility that hyena boldness represents an extended phenotype of the parasite, and 2) alternative scenarios in which T. gondii has not undergone selection to manipulate behavior in host hyenas. Both cases remain plausible and have important ramifications for T. gondii's impacts on host behavior and fitness in the wild.

The gut microbiota is critical for host function. Among mammals, host phylogenetic relatedness and diet are strong drivers of gut microbiota structure, but one factor may be more influential than the other. Here, we used 16S rRNA gene sequencing to determine the relative contributions of host phylogeny and host diet in structuring the gut microbiotas of 11 herbivore species from 5 families living sympatrically in southwest Kenya. Herbivore species were classified as grazers, browsers, or mixed-feeders and dietary data (% C4 grasses in diet) were compiled from previously published sources. We found that herbivore gut microbiotas were highly species-specific, and that host taxonomy accounted for more variation in the gut microbiota (30%) than did host dietary guild (10%) or sample month (8%). Overall, similarity in the gut microbiota increased with host phylogenetic relatedness (r = 0.74) across the 11 species of herbivores, but among 7 closely related Bovid species, dietary %C4 grass values more strongly predicted gut microbiota structure (r = 0.64). Additionally, within bovids, host dietary guild explained more of the variation in the gut microbiota (17%) than did host species (12%). Lastly, while we found that the gut microbiotas of herbivores residing in southwest Kenya converge with those of distinct populations of conspecifics from central Kenya, fine-scale differences in the abundances of bacterial amplicon sequence variants (ASVs) between individuals from the two regions were also observed. Overall, our findings suggest that host phylogeny and taxonomy strongly structure the gut microbiota across broad host taxonomic scales, but these gut microbiotas can be further modified by host ecology (i.e., diet, geography), especially among closely related host species.

How social development in early-life affects fitness remains poorly understood. Though there is growing evidence that early-life relationships can affect fitness, little research has investigated how social positions develop or whether there are particularly important periods for social position development in an animal's life history. In long-lived species in particular, understanding the lasting consequences of early-life social environments requires detailed, long-term datasets. Here we used a 25-year dataset to test whether social positions held during early development predicted adult fitness. Specifically, we quantified social position using three social network metrics: degree, strength and betweenness. We determined the social position of each individual in three types of networks during each of three stages of ontogeny to test whether they predict annual reproductive success (ARS) or longevity among adult female spotted hyenas Crocuta crocuta. The social positions occupied by juvenile hyenas did predict their fitness, but the effects of social position on fitness measures differed between stages of early development. Network metrics when individuals were young adults better predicted ARS, but network metrics for younger animals, particularly when youngsters were confined to the communal den, better predicted longevity than did metrics assessed during other stages of development. Our study shows how multiple types of social bonds formed during multiple stages of social development predict lifetime fitness outcomes. We suggest that social bonds formed during specific phases of development may be more important than others when considering fitness outcomes., (© 2020 British Ecological Society.)

Integrated models combine multiple data types within a unified analysis to estimate species abundance and covariate effects. By sharing biological parameters, integrated models improve the accuracy and precision of estimates compared to separate analyses of individual data sets. We developed an integrated point process model to combine presence-only and distance sampling data for estimation of spatially explicit abundance patterns. Simulations across a range of parameter values demonstrate that our model can recover estimates of biological covariates, but parameter accuracy and precision varied with the quantity of each data type. We applied our model to a case study of black-backed jackals in the Masai Mara National Reserve, Kenya, to examine effects of spatially varying covariates on jackal abundance patterns. The model revealed that jackals were positively affected by anthropogenic disturbance on the landscape, with highest abundance estimated along the Reserve border near human activity. We found minimal effects of landscape cover, lion density, and distance to water source, suggesting that human use of the Reserve may be the biggest driver of jackal abundance patterns. Our integrated model expands the scope of ecological inference by taking advantage of widely available presence-only data, while simultaneously leveraging richer, but typically limited, distance sampling data., (© 2020 by the Ecological Society of America.)

Like many scientific disciplines, the field of reproductive biology is subject to biases in terminology and research foci. For example, females are often described as coy and passive players in reproductive behaviors and are termed "promiscuous" if they engage in extra-pair copulations. Males on the other hand are viewed as actively holding territories and fighting with other males. Males are termed "multiply mating" if they mate with multiple females. Similarly, textbooks often illustrate meiosis as it occurs in males but not females. This edition of Integrative and Comparative Biology (ICB) includes a series of papers that focus on reproduction from the female perspective. These papers represent a subset of the work presented in our symposium and complementary sessions on female reproductive biology. In this round table discussion, we use a question and answer format to leverage the diverse perspectives and voices involved with the symposium in an exploration of theoretical, cultural, pedagogical, and scientific issues related to the study of female biology. We hope this dialog will provide a stepping-stone toward moving reproductive science and teaching to a more inclusive and objective framework., (© The Author(s) 2020. Published by Oxford University Press on behalf of the Society for Integrative and Comparative Biology. All rights reserved. For permissions please email: journals.permissions@oup.com.)

The reproductive biology of many female mammals is affected by their social environment and their interactions with conspecifics. In mammalian societies structured by linear dominance hierarchies, such as that of the spotted hyena (Crocuta crocuta), a female's social rank can have profound effects on both her reproductive success and her longevity. In this species, social rank determines priority of access to food, which is the resource limiting reproduction. Due largely to rank-related variation in access to food, reproduction from the perspective of a female spotted hyena can only be understood in the context of her position in the social hierarchy. In this review, we examine the effects of rank on the various phases of reproduction, from mating to weaning. Summed over many individual reproductive lifespans, the effect of rank at these different reproductive phases leads to dramatic rank-related variation in fitness among females and their lineages. Finally, we ask why females reproduce socially despite these apparent costs of group living to low-ranking females. Gregariousness enhances the fitness of females regardless of their positions in the social hierarchy, and females attempting to survive and reproduce without clanmates lose all their offspring. The positive effects of gregariousness appear to result from having female allies, both kin and non-kin, who cooperate to advertise and defend a shared territory, acquire, and defend food resources, maintain the status quo, and occasionally also to rise in social rank., (© The Author(s) 2020. Published by Oxford University Press on behalf of the Society for Integrative and Comparative Biology. All rights reserved. For permissions please email: journals.permissions@oup.com.)

Individual differences in behavior are the raw material upon which natural selection acts, but despite increasing recognition of the value of considering individual differences in the behavior of wild animals to test evolutionary hypotheses, this approach has only recently become popular for testing cognitive abilities. In order for the intraspecific approach with wild animals to be useful for testing evolutionary hypotheses about cognition, researchers must provide evidence that measures of cognitive ability obtained from wild subjects reflect stable, general traits. Here, we used a multi-access box paradigm to investigate the intra-individual reliability of innovative problem-solving ability across time and contexts in wild spotted hyenas (Crocuta crocuta). We also asked whether estimates of reliability were affected by factors such as age-sex class, the length of the interval between tests, or the number of times subjects were tested. We found significant contextual and temporal reliability for problem-solving. However, problem-solving was not reliable for adult subjects, when trials were separated by more than 17 days, or when fewer than seven trials were conducted per subject. In general, the estimates of reliability for problem-solving were comparable to estimates from the literature for other animal behaviors, which suggests that problem-solving is a stable, general trait in wild spotted hyenas.

Social rank is a significant determinant of fitness in a variety of species. The importance of social rank suggests that the process by which juveniles come to establish their position in the social hierarchy is a critical component of development. Here, we use the highly predictable process of rank acquisition in spotted hyenas to study the consequences of variation in rank acquisition in early life. In spotted hyenas, rank is 'inherited' through a learning process called 'maternal rank inheritance.' This pattern is very consistent: approximately 80% of juveniles acquire the exact rank expected under the rules of maternal rank inheritance. The predictable nature of rank acquisition in these societies allows the process of rank acquisition to be studied independently from the ultimate rank that each juvenile attains. In this study, we use Elo-deviance scores, a novel application of the Elo-rating method, to calculate each juvenile's deviation from the expected pattern of maternal rank inheritance during development. Despite variability in rank acquisition among juveniles, most of these juveniles come to attain the exact rank expected of them according to the rules of maternal rank inheritance. Nevertheless, we find that transient variation in rank acquisition in early life is associated with long-term fitness consequences for these individuals: juveniles 'underperforming' their expected ranks show reduced survival and lower lifetime reproductive success than better-performing peers, and this relationship is independent of both maternal rank and rank achieved in adulthood. We also find that multiple sources of early life adversity have cumulative, but not compounding, effects on fitness. Future work is needed to determine if variation in rank acquisition directly affects fitness, or if some other variable, such as maternal investment or juvenile condition, causes variation in both of these outcomes.

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., (© FEMS 2020.)

Mammalian carnivores are declining worldwide owing to human activities. Behavioural indicators have the potential to help identify population trends and inform conservation actions, although this area of research is understudied. We investigate whether behaviour is linked to abundance in a community of carnivores in the Masai Mara National Reserve, Kenya. Anthropogenic disturbance increased exponentially in parts of the Reserve between 1988 and 2017, mainly owing to daily incursions by large numbers of livestock and tourists. Previous research showed that hyena behaviour changed markedly during this period. Through a series of vignettes, we inquire whether hyena behaviours correlate with changes in abundance of hyenas themselves, or those of other carnivore species in the region. We find that changes in spotted hyena behaviour in disturbed areas, but not in undisturbed areas, can be linked to changes in their demography (vignette 1). We also find that declines in observed lion-hyena interactions, as well as increases in spotted hyena abundance, are probably caused by competitive release of hyenas from declining lion abundance (vignette 2). Finally, we demonstrate that in some cases, hyena behaviour and demography is linked to the density and distribution of sympatric carnivores, and that behavioural changes in hyenas can provide information on shifts within the carnivore community (vignettes 3 and 4). Our vignettes reveal intriguing relationships between behaviour and demography that should be explored in future research. Pairing behavioural studies with more traditional monitoring efforts can yield useful insights regarding population and community trends, and aid wildlife conservation and management. This article is part of the theme issue 'Linking behaviour to dynamics of populations and communities: application of novel approaches in behavioural ecology to conservation'.

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'.

Environmental factors early in life can have lasting influence on the development and phenotypes of animals, but the underlying molecular modifications remain poorly understood. We examined cross-sectional associations among early life socioecological factors and global DNA methylation in 293 wild spotted hyenas (Crocuta crocuta) in the Masai Mara National Reserve, Kenya, grouped according to three age classes (cub, subadult and adult). Explanatory variables of interest included annual maternal rank based on outcomes of dyadic agonistic interactions, litter size, wild ungulate prey density and anthropogenic disturbance in the year each hyena was born based on counts of illegal livestock in the Reserve. The dependent variable of interest was global DNA methylation, assessed via the LUminometric Methylation Assay, which provides a percentage methylation value calculated at CCGG sites across the genome. Among cubs, we observed approximately 2.75% higher CCGG methylation in offspring born to high- than low-ranking mothers. Among cubs and subadults, higher anthropogenic disturbance corresponded with greater %CCGG methylation. In both cubs and adults, we found an inverse association between prey density measured before a hyena was 3 months old and %CCGG methylation. Our results suggest that maternal rank, anthropogenic disturbance and prey availability early in life are associated with later life global DNA methylation. Future studies are required to understand the extent to which these DNA methylation patterns relate to adult phenotypes and fitness outcomes., (© 2019 John Wiley & Sons Ltd.)

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., Competing Interests: The authors declare no conflict of interest.

Social inequality is a consistent feature of animal societies, often manifesting as dominance hierarchies, in which each individual is characterized by a dominance rank denoting its place in the network of competitive relationships among group members. Most studies treat dominance hierarchies as static entities despite their true longitudinal, and sometimes highly dynamic, nature. To guide study of the dynamics of dominance, we propose the concept of a longitudinal hierarchy: the characterization of a single, latent hierarchy and its dynamics over time. Longitudinal hierarchies describe the hierarchy position (r) and dynamics (∆) associated with each individual as a property of its interaction data, the periods into which these data are divided based on a period delineation rule (p) and the method chosen to infer the hierarchy. Hierarchy dynamics result from both active (∆a) and passive (∆p) processes. Methods that infer longitudinal hierarchies should optimize accuracy of rank dynamics as well as of the rank orders themselves, but no studies have yet evaluated the accuracy with which different methods infer hierarchy dynamics. We modify three popular ranking approaches to make them better suited for inferring longitudinal hierarchies. Our three "informed" methods assign ranks that are informed by data from the prior period rather than calculating ranks de novo in each observation period and use prior knowledge of dominance correlates to inform placement of new individuals in the hierarchy. These methods are provided in an R package. Using both a simulated dataset and a long-term empirical dataset from a species with two distinct sex-based dominance structures, we compare the performance of these methods and their unmodified counterparts. We show that choice of method has dramatic impacts on inference of hierarchy dynamics via differences in estimates of ∆a. Methods that calculate ranks de novo in each period overestimate hierarchy dynamics, but incorporation of prior information leads to more accurately inferred ∆a. Of the modified methods, Informed MatReorder infers the most conservative estimates of hierarchy dynamics and Informed Elo infers the most dynamic hierarchies. This work provides crucially needed conceptual framing and methodological validation for studying social dominance and its dynamics., (© 2019 The Authors. Journal of Animal Ecology © 2019 British Ecological Society.)

Carnivore communities face unprecedented threats from humans. Yet, management regimes have variable effects on carnivores, where species may persist or decline in response to direct or indirect changes to the ecosystem. Using a hierarchical multispecies modeling approach, we examined the effects of alternative management regimes (i.e., active vs. passive enforcement of regulations) on carnivore abundances and group sizes at both species and community levels in the Masai Mara National Reserve, Kenya. Alternative management regimes have created a dichotomy in ecosystem conditions within the Reserve, where active enforcement of regulations maintains low levels of human disturbance in the Mara Triangle and passive enforcement of regulations in the Talek region permits multiple forms of human disturbance. Our results demonstrate that these alternative management regimes have variable effects on 11 observed carnivore species. As predicted, some species, such as African lions and bat-eared foxes, have higher population densities in the Mara Triangle, where regulations are actively enforced. Yet, other species, including black-backed jackals and spotted hyenas, have higher population densities in the Talek region where enforcement is passive. Multiple underlying mechanisms, including behavioral plasticity and competitive release, are likely causing higher black-backed jackals and spotted hyena densities in the disturbed Talek region. Our multispecies modeling framework reveals that carnivores do not react to management regimes uniformly, shaping carnivore communities by differentially producing winning and losing species. Some carnivore species require active enforcement of regulations for effective conservation, while others more readily adapt (and in some instances thrive in response) to lax management enforcement and resulting anthropogenic disturbance. Yet, high levels of human disturbance appear to be negatively affecting the majority of carnivores, with potential consequences that may permeate throughout the rest of the ecosystem. Community approaches to monitoring carnivores should be adopted as single species monitoring may overlook important intra-community variability., (© 2019 by the Ecological Society of America.)

Developmental plasticity, a phenomenon of importance in both evolutionary biology and human studies of the developmental origins of health and disease (DOHaD), enables organisms to respond to their environment based on previous experience without changes to the underlying nucleotide sequence. Although such phenotypic responses should theoretically improve an organism's fitness and performance in its future environment, this is not always the case. Herein, we first discuss epigenetics as an adaptive mechanism of developmental plasticity and use signaling theory to provide an evolutionary context for DOHaD phenomena within a generation. Next, we utilize signalling theory to identify determinants of adaptive developmental plasticity, detect sources of random variability - also known as process errors that affect maintenance of an epigenetic signal (DNA methylation) over time, and discuss implications of these errors for an organism's health and fitness. Finally, we apply life-course epidemiology conceptual models to inform study design and analytical strategies that are capable of parsing out the potential effects of process errors in the relationships among an organism's early environment, DNA methylation, and phenotype in a future environment. Ultimately, we hope to foster cross-talk and interdisciplinary collaboration between evolutionary biology and DOHaD epidemiology, which have historically remained separate despite a shared interest in developmental plasticity., (© 2018 Cambridge Philosophical Society.)

Although intelligence should theoretically evolve to help animals solve specific types of problems posed by the environment, it is unclear which environmental challenges favour enhanced cognition, or how general intelligence evolves along with domain-specific cognitive abilities. The social intelligence hypothesis posits that big brains and great intelligence have evolved to cope with the labile behaviour of group mates. We have exploited the remarkable convergence in social complexity between cercopithecine primates and spotted hyaenas to test predictions of the social intelligence hypothesis in regard to both cognition and brain size. Behavioural data indicate that there has been considerable convergence between primates and hyaenas with respect to their social cognitive abilities. Moreover, compared with other hyaena species, spotted hyaenas have larger brains and expanded frontal cortex, as predicted by the social intelligence hypothesis. However, broader comparative study suggests that domain-general intelligence in carnivores probably did not evolve in response to selection pressures imposed specifically in the social domain. The cognitive buffer hypothesis, which suggests that general intelligence evolves to help animals cope with novel or changing environments, appears to offer a more robust explanation for general intelligence in carnivores than any hypothesis invoking selection pressures imposed strictly by sociality or foraging demands., Competing Interests: We declare we have no competing interests.

Understanding the factors that facilitate the emergence of cooperation among organisms is central to the study of social evolution. Spotted hyenas Crocuta crocuta frequently cooperate to mob lions Panthera leo , approaching the lions as a tightknit group while vocalizing loudly in an attempt to overwhelm them and drive them away. Whereas cooperative mobbing behavior has been well documented in birds and some mammals, to our knowledge it has never been described during interactions between 2 apex predators. Using a 27-year dataset, we characterize lion-hyena encounters, assess rates of mobbing behavior observed during these interactions, and inquire whether mobbing results in successful acquisition of food. Lions and hyenas interacted most often at fresh kills, especially as prey size and the number of hyenas present increased. Possession of food at the beginning of an interaction positively affected retention of that food by each predator species. The presence of male lions increased the probability of an interspecific interaction but decreased the likelihood of hyenas obtaining or retaining possession of the food. Hyena mobbing rates were highest at fresh kills, but lower when adult male lions were present. The occurrence of mobbing was predicted by an increase in the number of hyenas present. Whether or not mobbing resulted in acquisition of food from lions was predicted by an increase in the number of mobs formed by the hyenas present, suggesting that cooperation among hyenas enhances their fitness.

We strongly agree that general intelligence occurs in many animals but find the cultural intelligence hypothesis of limited usefulness. Any viable hypothesis explaining the evolution of general intelligence should be able to account for it in all species where it is known to occur, and should also predict the conditions under which we can develop machines with general intelligence as well.

Social rank can profoundly affect many aspects of mammalian reproduction and stress physiology, but little is known about how immune function is affected by rank and other socio-ecological factors in free-living animals.In this study we examine the effects of sex, social rank, and reproductive status on immune function in long-lived carnivores that are routinely exposed to a plethora of pathogens, yet rarely show signs of disease.Here we show that two types of immune defenses, complement-mediated bacterial killing capacity (BKC) and total IgM, are positively correlated with social rank in wild hyenas, but that a third type, total IgG, does not vary with rank.Female spotted hyenas, which are socially dominant to males in this species, have higher BKC, and higher IgG and IgM concentrations, than do males.Immune defenses are lower in lactating than pregnant females, suggesting the immune defenses may be energetically costly.Serum cortisol and testosterone concentrations are not reliable predictors of basic immune defenses in wild female spotted hyenas.These results suggest that immune defenses are costly and multiple socioecological variables are important determinants of basic immune defenses among wild hyenas. Effects of these variables should be accounted for when attempting to understand disease ecology and immune function.

Despite considerable interest in the forces shaping the relationship between brain size and cognitive abilities, it remains controversial whether larger-brained animals are, indeed, better problem-solvers. Recently, several comparative studies have revealed correlations between brain size and traits thought to require advanced cognitive abilities, such as innovation, behavioral flexibility, invasion success, and self-control. However, the general assumption that animals with larger brains have superior cognitive abilities has been heavily criticized, primarily because of the lack of experimental support for it. Here, we designed an experiment to inquire whether specific neuroanatomical or socioecological measures predict success at solving a novel technical problem among species in the mammalian order Carnivora. We presented puzzle boxes, baited with food and scaled to accommodate body size, to members of 39 carnivore species from nine families housed in multiple North American zoos. We found that species with larger brains relative to their body mass were more successful at opening the boxes. In a subset of species, we also used virtual brain endocasts to measure volumes of four gross brain regions and show that some of these regions improve model prediction of success at opening the boxes when included with total brain size and body mass. Socioecological variables, including measures of social complexity and manual dexterity, failed to predict success at opening the boxes. Our results, thus, fail to support the social brain hypothesis but provide important empirical support for the relationship between relative brain size and the ability to solve this novel technical problem.

Evolutionary processes have shaped the vertebrate immune system over time, but proximal mechanisms control the onset, duration, and intensity of immune responses. Based on testing of the hygiene hypothesis, it is now well known that microbial exposure is important for proper development and regulation of the immune system. However, few studies have examined the differences between wild animals in their natural environments, in which they are typically exposed to a wide array of potential pathogens, and their conspecifics living in captivity. Wild spotted hyenas (Crocuta crocuta) are regularly exposed to myriad pathogens, but there is little evidence of disease-induced mortality in wild hyena populations, suggesting that immune defenses are robust in this species. Here we assessed differences in immune defenses between wild spotted hyenas that inhabit their natural savanna environment and captive hyenas that inhabit a captive environment where pathogen control programs are implemented. Importantly, the captive population of spotted hyenas was derived directly from the wild population and has been in captivity for less than four generations. Our results show that wild hyenas have significantly higher serum antibody concentrations, including total IgG and IgM, natural antibodies, and autoantibodies than do captive hyenas; there was no difference in the bacterial killing capacity of sera collected from captive and wild hyenas. The striking differences in serum antibody concentrations observed here suggest that complementing traditional immunology studies, with comparative studies of wild animals in their natural environment may help to uncover links between environment and immune function, and facilitate progress towards answering immunological questions associated with the hygiene hypothesis.

Social structure influences ecological processes such as dispersal and invasion, and affects survival and reproductive success. Recent studies have used static snapshots of social networks, thus neglecting their temporal dynamics, and focused primarily on a limited number of variables that might be affecting social structure. Here, instead we modelled effects of multiple predictors of social network dynamics in the spotted hyena, using observational data collected during 20 years of continuous field research in Kenya. We tested the hypothesis that the current state of the social network affects its long-term dynamics. We employed stochastic agent-based models that allowed us to estimate the contribution of multiple factors to network changes. After controlling for environmental and individual effects, we found that network density and individual centrality affected network dynamics, but that social bond transitivity consistently had the strongest effects. Our results emphasise the significance of structural properties of networks in shaping social dynamics., (© 2015 John Wiley & Sons Ltd/CNRS.)

Calls that catalyse group defence, as in the mobbing of predators, appear to facilitate cooperation by recruiting receivers to act collectively. However, even when such signals reliably precede cooperative behaviour, the extent to which the calls function as recruitment signals is unclear. Calls might simply arouse listeners' attention, setting off a cascade of independent responses to the threat. By contrast, they might convey information, for example, about signaller identity and the nature of a threat that affects receivers' decisions to participate. We explored this distinction by investigating a possible long-distance recruitment call used by spotted hyaenas. These social carnivores live in fission-fusion clans and individuals disperse widely within their territories. Putative recruitment calls must therefore attract receivers that are distant from the inciting threat and free to opt out of risky collective aggression. Hyaenas compete with lions over food, and neighbouring clans sometimes engage in violent border clashes. These high-stakes contests are decided based on numerical asymmetries, so hyaenas can only protect critical resources if the dispersed clan can converge quickly at conflict sites. We recorded and analysed whoop bouts produced in multiple contexts and found that bouts produced in response to signs of lion-hyaena conflict had shorter inter-whoop intervals than spontaneous 'display' bouts. In subsequent field playback experiments, resting hyaenas were significantly more likely to move in response to 'recruitment' bouts with shortened intervals than to otherwise identical 'display' bouts. Whereas only stimulus type predicted movement, lower-ranked subjects responded most quickly, perhaps because their feeding opportunities depend on arriving early at any kill site. Results demonstrate that hyaenas possess a signal that can reliably recruit allies across long distances, despite moderating effects of individual circumstances on the strength of receivers' responses.

Theoretically intelligence should evolve to help animals solve specific types of problems posed by the environment, but it remains unclear how environmental complexity or novelty facilitates the evolutionary enhancement of cognitive abilities, or whether domain-general intelligence can evolve in response to domain-specific selection pressures. The social complexity hypothesis, which posits that intelligence evolved to cope with the labile behaviour of conspecific group-mates, has been strongly supported by work on the sociocognitive abilities of primates and other animals. Here we review the remarkable convergence in social complexity between cercopithecine primates and spotted hyaenas, and describe our tests of predictions of the social complexity hypothesis in regard to both cognition and brain size in hyaenas. Behavioural data indicate that there has been remarkable convergence between primates and hyaenas with respect to their abilities in the domain of social cognition. Furthermore, within the family Hyaenidae, our data suggest that social complexity might have contributed to enlargement of the frontal cortex. However, social complexity failed to predict either brain volume or frontal cortex volume in a larger array of mammalian carnivores. To address the question of whether or not social complexity might be able to explain the evolution of domain-general intelligence as well as social cognition in particular, we presented simple puzzle boxes, baited with food and scaled to accommodate body size, to members of 39 carnivore species housed in zoos and found that species with larger brains relative to their body mass were more innovative and more successful at opening the boxes. However, social complexity failed to predict success in solving this problem. Overall our work suggests that, although social complexity enhances social cognition, there are no unambiguous causal links between social complexity and either brain size or performance in problem-solving tasks outside the social domain in mammalian carnivores.

Telomeres are regarded as important biomarkers of ageing and serve as useful tools in revealing how stress acts at the cellular level. However, the effects of social and ecological factors on telomere length remain poorly understood, particularly in free-ranging mammals. Here, we investigated the influences of within-group dominance rank and group membership on telomere length in wild adult spotted hyenas (Crocuta crocuta). We found large effects of both factors; high-ranking hyenas exhibited significantly greater mean telomere length than did subordinate animals, and group membership significantly predicted mean telomere length within high-ranking females. We further inquired whether prey availability mediates the observed effect of group membership on telomere length, but this hypothesis was not supported. Interestingly, adult telomere length was not predicted by age. Our work shows for the first time, to the best of our knowledge, the effects of social rank on telomere length in a wild mammal and enhances our understanding of how social and ecological variables may contribute to organismal senescence., (© 2015 The Author(s) Published by the Royal Society. All rights reserved.)

Social learning can have profound evolutionary consequences because it drives the diffusion of novel behaviours among individuals and promotes the maintenance of traditions within populations. We inquired whether spotted hyenas (Crocuta crocuta), generalist carnivores living in complex, primate-like societies, acquire information from conspecifics about a novel problem-solving task. Previously, we presented wild hyenas with a food-access puzzle and found that social learning opportunities did not affect problem-solving success among observers, but did reduce observers' neophobia. However, we had little control over which individuals observed conspecifics solve the problem, and few wild hyenas were successful. Therefore, we conducted an experiment in captivity where we controlled observer access to two demonstration styles. Again, social learning opportunities did not affect problem-solving success, but tended to reduce neophobia among captive observers. Social learning opportunities also influenced problem-solving style. Captive hyenas showed limited evidence for directed social learning; low-ranking individuals paid closer attention to demonstrators than high-ranking individuals, although this greater attention did not result in greater success. We conclude that wild and captive hyenas exploit social learning opportunities similarly, and that the limited social learning shown by hyenas on this task is likely based on localized stimulus enhancement., (Copyright © 2014 Elsevier B.V. All rights reserved.)

Previous research has shown that spotted hyenas (Crocuta crocuta) regularly survive exposure to deadly pathogens such as rabies, canine distemper virus, and anthrax, suggesting that they have robust immune defenses. Toll-like receptors (TLRs) recognize conserved molecular patterns and initiate a wide range of innate and adaptive immune responses. TLR genes are evolutionarily conserved, and assessing TLR expression in various tissues can provide insight into overall immunological organization and function. Studies of the hyena immune system have been minimal thus far due to the logistical and ethical challenges of sampling and preserving the immunological tissues of this and other long-lived, wild species. Tissue samples were opportunistically collected from captive hyenas humanely euthanized for a separate study. We developed primers to amplify partial sequences for TLRs 1-10, sequenced the amplicons, compared sequence identity to those in other mammals, and quantified TLR expression in lymph nodes, spleens, lungs, and pancreases. Results show that hyena TLR DNA and protein sequences are similar to TLRs in other mammals, and that TLRs 1-10 were expressed in all tissues tested. This information will be useful in the development of new assays to understand the interactions among the hyena immune system, pathogens, and the microbial communities that inhabit hyenas.

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.

Beginning in 1997 Michigan State University Mara Hyena Project investigators observed waxing and waning progression of oral and genital masses during long-term behavioral observations of a population of wild spotted hyenas (Crocuta crocuta) from the Masai Mara Game Reserve, Kenya. From 1999-2000, we darted adult spotted hyenas to obtain routine physiologic and hematologic data and collected small, raised, lobulated, pigmented masses from the oral or genital areas of eight animals. Microscopically, masses consisted of variably thickened epidermis with thick elongate rete pegs, prominent stratum spinosum, and few koilocytes, consistent with papillomavirus-induced lesions. Immunohistochemistry on formalin-fixed, paraffin-embedded papilloma tissue revealed positive intranuclear labeling for papillomavirus antigen in the superficial stratum granulosum and in sloughing keratin layers of multiple samples. Polymerase chain reaction on DNA extracts from tumor tissue amplified a papillomavirus-specific 418 base pair amplicon in the E1 ORF. Basic Local Alignment Search Tool analysis of the sequenced amplicon suggests a novel hyaenid papillomavirus. Confirmatory complete genomic sequencing was performed later by the Rega Institute in Belgium. To our knowledge, this is the first report of a papillomavirus in a Hyaenidae species. Spotted hyena social behavior might facilitate oral-genital transmission of papillomavirus in this population.

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.

Innovative animals are those able to solve novel problems or invent novel solutions to existing problems. Despite the important ecological and evolutionary consequences of innovation, we still know very little about the traits that vary among individuals within a species to make them more or less innovative. Here we examine innovative problem solving by spotted hyenas (Crocuta crocuta) in their natural habitat, and demonstrate for the first time in a non-human animal that those individuals exhibiting a greater diversity of initial exploratory behaviours are more successful problem solvers. Additionally, as in earlier work, we found that neophobia was a critical inhibitor of problem-solving success. Interestingly, although juveniles and adults were equally successful in solving the problem, juveniles were significantly more diverse in their initial exploratory behaviours, more persistent and less neophobic than were adults. We found no significant effects of social rank or sex on success, the diversity of initial exploratory behaviours, behavioural persistence or neophobia. Our results suggest that the diversity of initial exploratory behaviours, akin to some measures of human creativity, is an important, but largely overlooked, determinant of problem-solving success in non-human animals.