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1. Taxonomic, Genomic, and Functional Variation in the Gut Microbiomes of Wild Spotted Hyenas Across 2 Decades of Study

   https://doi.org/10.1128/msystems.00965-22  

   Rojas, Connie A. ; Holekamp, Kay E. ; Viladomat Jasso, Mariette ; Souza, Valeria ; Eisen, Jonathan A. ; Theis, Kevin R. ( January 2022 , mSystems)

   Hird, Sarah M. (Ed.)

   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. 

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2. Risk‐taking in free‐living spotted hyenas is associated with anthropogenic disturbance, predicts survivorship, and is consistent across experimental contexts

   https://doi.org/10.1111/eth.12964  

   Turner, Julie W. ; LaFleur, Rebecca M. ; Richardson, Allie T. ; Holekamp, Kay E. ; Ebensperger, ed., Luis ( October 2019 , Ethology)

   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 clan. The high‐disturbance population lived adjacent to human settlements, and the low‐disturbance population inhabited a relatively undisturbed part of the same national park in Kenya. The mock intruder was presented to individual hyenas to assess their reactions to an alien hyena, and to determine whether their reactions varied with their exposure to anthropogenic activity. We found that human disturbance was indeed associated with hyena risk‐taking behavior in response to the model intruder. Hyenas tested in the low‐disturbance area exhibited more risk‐taking behaviors by approaching the mock intruder more closely, and spending more time near it, than did their counterparts living in high‐disturbance areas. Hyenas that spent less time in close proximity to the model had greater survivorship than those that spent more time in close proximity to it, regardless of disturbance level. Furthermore, the individual differences in risk‐taking measured here were consistent with those obtained previously from the same animals using a different set of experimental manipulations. However, the experimentally induced behaviors were not consistent with naturally occurring risk‐taking behaviors in proximity to lions; this suggests that risk‐taking behaviors are consistent within individuals across experimental contexts, but that exposure to lions elicits different responses. Although our results are consistent with those from earlier tests of anthropogenic disturbance and boldness in spotted hyenas and other predators, they differ from results obtained from birds and small mammals, which are generally found to be bolder in areas characterized by human disturbance.

    

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3. Early-life social experience affects offspring DNA methylation and later life stress phenotype

   https://doi.org/10.1038/s41467-021-24583-x  

   Laubach, Zachary M. ; Greenberg, Julia R. ; Turner, Julie W. ; Montgomery, Tracy M. ; Pioon, Malit O. ; Sawdy, Maggie A. ; Smale, Laura ; Cavalcante, Raymond G. ; Padmanabhan, Karthik R. ; Lalancette, Claudia ; et al ( December 2021 , Nature Communications)

   Abstract 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. 

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4. Pastoralist activities affect the movement patterns of a large African carnivore, the spotted hyena (Crocuta crocuta)

   https://doi.org/10.1093/jmammal/gyz135  

   Green, David S. ; Holekamp, Kay E. ; Goheen, ed., Jacob ( September 2019 , Journal of Mammalogy)

   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 densities, and because changes in their behavior may be subtle or emerge slowly over many years. We studied the effects of livestock presence on the movements of one large carnivore, the spotted hyena (Crocuta crocuta). We fit 22 adult female spotted hyenas with GPS collars to quantify their movements in areas with and without livestock or herders present, in and around a protected area in southwestern Kenya. We investigated anthropogenic, social, and ecological effects on the speed of movement, distances traveled, long-distance movements, and extraterritorial excursions by spotted hyenas. Hyenas living primarily within the protected area, but in the presence of livestock and herders, moved faster, traveled over longer distances, and were more likely to be within their territories than did conspecifics living in areas without livestock and herders. Hyenas of low social rank were more likely than hyenas of high social rank to engage in long-distance travel events, and these were more likely to occur when prey were scarce. The movement patterns of this large African carnivore indicate a flexibility that may allow them to persist in landscapes that are becoming increasingly defined by people.

    

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5. Mother of all bonds: Influences on spatial association across the lifespan in capuchins

   https://doi.org/10.1111/desc.13486  

   Godoy, Irene ; Korsten, Peter ; Perry, Susan E. ( February 2024 , Developmental Science)

   In humans, being more socially integrated is associated with better physical and mental health and/or with lower mortality. This link between sociality and health may have ancient roots: sociality also predicts survival or reproduction in other mammals, such as rats, dolphins, and non‐human primates. A key question, therefore, is which factors influence the degree of sociality over the life course. Longitudinal data can provide valuable insight into how environmental variability drives individual differences in sociality and associated outcomes. The first year of life—when long‐lived mammals are the most reliant on others for nourishment and protection—is likely to play an important role in how individuals learn to integrate into groups. Using behavioral, demographic, and pedigree information on 376 wild capuchin monkeys (Cebus imitator) across 20 years, we address how changes in group composition influence spatial association. We further try to determine the extent to which early maternal social environments have downstream effects on sociality across the juvenile and (sub)adult stages. We find a positive effect of early maternal spatial association, where female infants whose mothers spent more time around others also later spent more time around others as juveniles and subadults. Our results also highlight the importance of kin availability and other aspects of group composition (e.g., group size) in dynamically influencing spatial association across developmental stages. We bring attention to the importance of—and difficulty in—determining the social versus genetic influences that parents have on offspring phenotypes.

   Having more maternal kin (mother and siblings) is associated with spending more time near others across developmental stages in both male and female capuchins.

   Having more offspring as a subadult or adult female is additionally associated with spending more time near others.

   A mother's average sociality (time near others) is predictive of how social her daughters (but not sons) become as juveniles and subadults (a between‐mother effect).

   Additional variation within sibling sets in this same maternal phenotype is not predictive of how social they become later relative to each other (no within‐mother effect).

    

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