Kay E Holekamp

Michigan State University | MSU · Department of Zoology

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 cou...

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 temp...

Fission–fusion dynamics describe the tendency for members of some animal societies to associate in subgroups that change size and structure fluidly over time. These dynamics shape social complexity and social structure, but are difficult to study because they unfold simultaneously over large spatial scales. Here we use simultaneous, fine-scale GPS...

Animal behavior can be decomposed into a continuous sequence of discrete activity bouts over time. Analyzing the statistical structure of such behavioral sequences provides insights into the drivers of behavioral decisions in animals. Laboratory studies, predominantly in invertebrates, have suggested that behavioral sequences are characterized by m...

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...

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 sta...

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 i...

Once considered mere scavengers, it is now widely recognized that hunting is more important than scavenging in the feeding ecology of spotted hyenas (Crocuta crocuta). In this chapter, we outline the extraordinary morphological and behavioral adaptations possessed by these bone-cracking hyenas for efficient hunting and foraging within the context o...

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 often difficult to monitor animals over long periods of time. Here, we developed and validated a machine-learning based behavioural classifier to ide...

Introduction Dominance relationships in which females dominate males are rare among mammals. Mechanistic hypotheses explaining the occurrence of female dominance suggest that females dominate males because (1) they are intrinsically more aggressive or less submissive than males, and/or (2) they have access to more social support than males. Method...

Unlabelled: 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, pr...

The gut microbiome provides vital functions for mammalian hosts, yet research on the variability and function of the microbiome across adult lifespans and multiple generations is limited in large mammalian carnivores. Here we use 16S rRNA gene and metagenomic sequencing to profile the taxonomic composition, genomic diversity, and metabolic function...

In traditional definitions of endurance rivalry, individuals compete to remain reproductively active longer than their rivals, but these time periods are typically brief, such as a single breeding season. Here, we explored endurance rivalry among adult males in a long-lived species that breeds year-round, the spotted hyena (Crocuta crocuta). We fou...

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...

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 t...

Many species engage in risky cooperative behaviors, which pose a challenge to evolutionary theory: participants take on all the costs of cooperation, yet even non-participants benefit from success in these encounters. So, why participate in these risky behaviors? We address this question using data from spotted hyenas fighting with lions. Lions are...

Physical problem-solving paradigms are popular for testing a variety of cognitive abilities linked with intelligence including behavioral flexibility, innovation, and learning. Members of the mammalian order Carnivora are excellent candidates for studying problem-solving because they occupy a diverse array of socio-ecological niches, allowing resea...

Aggressive and submissive behaviours are commonly assumed to represent two extremes of a single personality trait, often labelled ‘aggressiveness’. However, most studies focus exclusively on submissive behaviour elicited by conspecific aggression, and on rates at which aggressive and submissive behaviours are expressed, without considering either u...

As fecal steroid methods increasingly are used by researchers to monitor the physiology of captive and wild populations, we need to expand our validation protocols to test the effects of procedural variation and to identify contamination by exogenous sources of steroid hormones. Mammalian carnivore feces often contain large amounts of hair from the...

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 meth...

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 b...

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...

Environment structure often shapes social interactions. Spatial attractors that draw multiple individuals may play a particularly important role in dispersed groups, where individuals must first encounter one another to interact. We use GPS data recorded simultaneously from five spotted hyenas (Crocuta crocuta) within a single clan to investigate h...

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 beneficia...

Social 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 w...

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 connect...

Mother knows best Inheritance of social status, and its associated costs and benefits, is well demonstrated in humans. Whether such an intergenerational system occurs in other species is harder to demonstrate. Ilany et al. looked at nearly 30 years of social interaction data in spotted hyenas, a female-dominated system with a highly structured soci...

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 be...

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 microbiot...

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 me...

Synopsis 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 holdin...

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‐onl...

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 dietary guild in structuring the gut...

Toxoplasma gondii is widely reported to manipulate the behavior of its non-definitive hosts in ways that promote lethal interactions with the parasite’s definitive feline hosts. Nonetheless, there is a lack of data on the association between T. gondii infection and costly behavioral interactions with felids in nature. Here, we report that three dec...

In a wild population of spotted hyenas, we tested the hypothesis that maternal care during the first year of life and social connectedness during two periods of early development lead to differences in DNA methylation and fecal glucocorticoid metabolites (fGCMs) later in life. We found that although maternal care and social connectedness during the...

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 intraspecif...

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‐live...

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....

There is growing interest in the alteration of host behaviors by parasites, yet crucial gaps remain in our understanding of its ecological and evolutionary significance. Here, we present the first evidence that the enhanced boldness of infected intermediate hosts of Toxoplasma gondii can increase their risk of mortality by the parasite’s definitive...

Under the direction of Erik Goodman, BEACON has been a remarkable success. It has been a fabulous boon to those of us whose research interests are constantly evolving. Here I explain how Erik’s guidance of BEACON facilitated the professional development of many graduate students and post-docs in my lab, and allowed me to reinvent myself as a scient...

Surprising social complexity and variability have recently been documented in several mammalian species once believed to be strictly solitary, and variation in resource abundance may drive this variation in sociality. Wagner et al. (Wagner, A. P., S. Creel, L. G. Frank, and S. T. Kalinowski. 2007. Patterns of relatedness and parentage in an asocial...

Infanticide, or the killing of offspring by a conspecific, occurs in many animal species. Although both males and females can kill infants, sexually selected infanticide by males has been the primary focus in studies of infanticide. In contrast, the prevalence and function of infanticide by females is less well understood. Here we use 30 years of d...

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 on 73,767 social interactions among wild spotted hyenas over 27 years, we show that a process of social inheritance determines...

Grassland monitoring can be challenging because it is time-consuming and expensive to measure grass condition at large spatial scales. Remote sensing offers a time- and cost-effective method for mapping and monitoring grassland condition at both large spatial extents and fine temporal resolutions. Combinations of remotely sensed optical and radar i...

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 conseq...

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 o...

This edited research monograph brings together contributions from computer scientists, biologists, and engineers who are engaged with the study of evolution and how it may be applied to solve real-world problems. It also serves as a Festschrift dedicated to Erik D. Goodman, the founding director of the BEACON Center for the Study of Evolution in Ac...

Inhibitory control is the ability to resist performing a prepotent, but ultimately incorrect, behaviour in situations that demand restraint. Inhibitory control is linked to brain size and intelligence in humans and animals, but it is unclear just how it evolves. Inhibitory control is thought to be particularly important in complex social environmen...

Innovation is a well-studied cognitive phenomenon related to general intelligence and brain size. Innovative ability varies considerably within species and it is widely assumed that this variation must have important fitness consequences. However, direct evidence for a link between innovative ability and fitness has rarely been shown. Previous rese...

Social rank has been identified as 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 social development. Here, we use the highly predictable process of rank acquisition in spotted...

Anthropogenic disturbance can have important influences on the fitness and behaviors of wild animals, including their boldness when exposed to risky conditions. We presented spotted hyenas (Crocuta crocuta) from two populations, each exposed to a different level of human activity, with a life‐size model hyena representing an intruder from another c...

Populations of large carnivores are declining in many parts of the world due to anthropogenic activity. Some species of large carnivores, however, are able to coexist with people by altering their behavior. Altered behaviors may be challenging to identify in large carnivores because these animals are typically cryptic, nocturnal, live at low densit...

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,...

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,...

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 Kenya, grouped...

Protected areas in sub-Saharan Africa are fast becoming islands on which to conserve biodiversity as surrounding human populations grow exponentially, rangelands become urbanized, and natural habitats are fragmented. The Masai Mara National Reserve in the Mara-Serengeti ecosystem in Kenya is renowned for having one of the highest densities and dive...

Significance What forces produce and maintain social inequality, and why do society members tolerate this inequality? The “One Percent” clearly benefit from having high status, but low-status individuals have strong incentive to challenge the established pecking order and try to improve their position. This conundrum is particularly striking in the...

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...

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. p...

Innovation is widely linked to cognitive ability, brain size, and adaptation to novel conditions. However, successful innovation appears to be influenced by both cognitive factors, such as inhibitory control, and non-cognitive behavioral traits. We used a multi-access box (MAB) paradigm to measure repeated innovation, the number of unique innovatio...

Large carnivore populations are declining worldwide due to direct and indirect conflicts with humans. Protected areas are critical for conserving large carnivores, but increasing human-wildlife conflict, tourism, and human population growth near these sanctuaries may have negative effects on the carnivores within sanctuary borders. Our goals were t...

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...

Social development is crucial in the ontogeny of animals living in complex societies and has lasting consequences in adulthood. Spotted hyenas (Crocuta crocuta) live in fission-fusion societies as complex as those of cercopithecine primates. The social positions adult hyenas hold within their groups are complex and varied, but little is known about...

Human activity can dramatically affect personality traits in birds and small mammals. However, we know very little about how anthropogenic disturbance shapes personality in mammalian carnivores, and whether the personality traits that may be affected have fitness consequences in human-dominated landscapes. We adapted standard experiments commonly u...

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 m...

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...

Most carnivorans (members of the mammalian order Carnivora) are elusive and long lived, so long-term studies are required to understand their basic biology and, ultimately, to conserve them. Here, we review examples of the wealth of information about the social systems, ecophysiology, and ecology of gregarious, terrestrial, carnivorous carnivorans...

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 i...

Testosterone and cortisol are steroid hormones that have effects on dominance behavior and are in turn influenced by dominance-related social interactions.