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Beehner, J. C.

Publications and source records attributed to Beehner, J. C..

9 recordsLinked to original sources

Social and reproductive benefits of group fission in wild geladas

Living in large, crowded groups can result in fitness costs due to increased competition and conflict. When dispersing from large groups isn't possible, fissioning into two or more smaller 'daughter' groups may provide an important mechanism for mitigating these costs. Here, we leveraged 15 years of behavioral and demographic data to identify both (i) the social factors that predict group membership decisions and (ii) the adaptive consequences of group fission in the gelada (Theropithecus gelada), a grass-eating primate in which the risk of male infanticide -- the largest fitness cost to females -- is highest in larger groups. After fissioning, females tended to join the same daughter groups as their close kin, closely ranked females, and other strong grooming partners, both female and male. However, females did not join the likely fathers of their dependent infants, even though doing so is expected to prevent infanticide. Group fissions were not preceded by increases in female-female aggression or salient changes in activity budgets but were preceded by increases in infant mortality. In particular, infanticide was elevated prior to fission and plummeted after groups split. Taken together, these data illustrate how animals navigate competing social priorities and highlight the role of fission in ameliorating the costs of group-living.

animal behavior and cognition↗

Disparate social structures are underpinned by distinct social rules across a primate radiation

Over six decades of research on wild baboons and their close relatives (collectively, the African papionins) have uncovered substantial variation in their behavior and social systems. While most papionins form discrete social groups (single-level societies), a few others form small social units that are nested within larger supergroups (multi-level societies). These two systems are generally thought to be qualitatively distinct, but data from wild populations increasingly suggest that there may be areas of overlap. To quantify this potential gradient in social structure, a more systematic, comparative analysis is needed. Here, we constructed a database of behavioral and demographic records spanning 135 group-years, 28 social groups, 13 long-term field studies, and 11 species to quantify variation in grooming network structure, and identify the individual and dyadic properties (e.g., kinship and social status effects) that underlie this variation. Consistent with accumulating observations in the field, the single-level species could be divided into two categories: cohesive and cliquish. Cohesive single-level networks were dense, kin-biased, and moderately rank-structured, while cliquish single-level networks were more differentiated, slightly more kin-biased, and strongly rank-structured. As expected, multi-level networks were very modular and shaped by females ties to specific dominant males but varied in their kin biases. Taken together, these data suggest that (i) kin and rank biases are widespread but vary in their strength; (ii) male-centered subgroups are exclusive to multi-level systems; and (iii) increases in network modularity can emerge in response to heightened nepotism and male-centered clustering. SIGNIFICANCE STATEMENTWhat forces explain variation in primate societies? While kinship and dominance shape the social lives of many of our close relatives, it is unclear how their effects differ across species. Using a new database comprising decades of field research, we found that baboons and their close relatives fell into three general patterns: one in which groups were cohesive, kin-biased, and moderately rank-biased, another in which groups were more cliquish and nepotistic, and a third in which groups were divided into clusters centered on dominant males. Distinct primate societies may thus reflect differences in the strength of females nepotistic biases and the degree of males social influence.

animal behavior and cognition↗

Determinants of hyena participation in risky collective action

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 much larger, and kill many hyenas, so these fights require cooperative mobbing by hyenas for them to succeed. We identify factors that predict: (1) when hyena groups engage in cooperative fights with lions, (2) which individuals choose to participate, and (3) how the benefits of victory are distributed among cooperators and non-cooperators. We find that cooperative mobbing is more strongly influenced 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 suggest that, when animals play dangerous cooperative games, selection favors flexible strategies that are sensitive to dynamic factors emerging over multiple time-scales.

animal behavior and cognition↗

Maternal effects on early-life gut microbiome maturation in a wild nonhuman primate

Early-life gut microbial colonization is an important process shaping host physiology, immunity and long-term health outcomes in humans and other animals. However, our understanding of this dynamic process remains poorly investigated in wild animals, where developmental mechanisms can be better understood within ecological and evolutionary relevant contexts. Using 16s rRNA amplicon sequencing on 525 fecal samples from a large cohort of infant and juvenile geladas (Theropithecus gelada), we characterized gut microbiome maturation during the first three years of life and assessed the role of maternal effects in shaping offspring microbiome assembly. Microbial diversity increased rapidly in the first months of life, followed by more gradual changes until weaning. As expected, changes in gut microbiome composition and function with increasing age reflected progressive dietary transitions: in early infancy when infants rely heavily on their mothers milk, microbes that facilitate milk glycans and lactose utilization dominated, while later in development as graminoids are progressively introduced into the diet, microbes that metabolize plant complex polysaccharides became dominant. Furthermore, the microbial community of nursing infants born to first-time (primiparous) mothers was more "milk-oriented" compared to similarly-aged infants born to experienced (multiparous) mothers. Comparisons of matched mother-offspring fecal samples to random dyads did not support vertical transmission as a conduit for these maternal effects, which instead could be explained by slower phenotypic development (and associated slower gut microbiome maturation) in infants born to first-time mothers. Together, our findings highlight the dynamic nature of gut colonization in early life and the role of maternal effects in modulating this trajectory in a wild primate.

microbiology↗

High-altitude adaptation and incipient speciation in geladas

Survival at high altitude requires adapting to extreme conditions such as environmental hypoxia. To understand high-altitude adaptations in a primate, we assembled the genome of the gelada (Theropithecus gelada), an endemic Ethiopian monkey, and complemented it with population resequencing, hematological, and morphometric data. Unexpectedly, we identified a novel karyotype that may contribute to reproductive isolation between gelada populations. We also identified genomic elements including protein-coding sequences and gene families that exhibit accelerated changes in geladas and may contribute to high-altitude adaptation. Our findings lend insight into mechanisms of speciation and adaptation while providing promising avenues for functional hypoxia research.

genomics↗

Measuring salivary cortisol in wild carnivores

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 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 either subordinate littermates or singletons, 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. HIGHLIGHTSO_LIWe validated methods for collecting and analyzing saliva from wild carnivores. C_LIO_LIWe documented a bimodal daily rhythm in juvenile spotted hyena salivary cortisol. C_LIO_LICortisol varied among juvenile hyenas based on litter size and intra-litter rank. C_LIO_LIInflicting aggression on others was associated with lower cortisol concentrations. C_LI

zoology↗

Male-mediated maturation in a wild primate

In humans, a controversial hypothesis suggests that father absence promotes early puberty in daughters. Data from rodents confirm females accelerate maturation with exposure to novel males (“Vandenbergh effect”) and delay it with exposure to male relatives. Here, we report the first case of male-mediated maturation in a wild primate, geladas (Theropithecus gelada). Females were more likely to mature after a change in the reproductive male: some matured earlier than expected (Vandenbergh effect) and some later (due to father presence). Novel males stimulated a surge in estrogens for all immature females - even females too young to mature. Although male-mediated puberty accelerated first births, the effect was modest, suggesting that alternative scenarios, such as co-evolution with the Bruce effect (male-mediated fetal loss) may explain this phenomenon.One Sentence Summary Novel males induce an estrogen surge, male-mediated puberty, and a head-start on reproduction for immature female geladas.Competing Interest StatementThe authors have declared no competing interest.View Full Text

zoology↗

High density of white-faced capuchins (Cebus capucinus) and habitat quality in the Taboga Forest of Costa Rica

Across the globe, primate species and habitats are threatened by human activity. This is especially true for species found in tropical dry forests, which are widely distributed and comprise diverse habitats that remain largely unprotected. Evidence suggests that some primate species endemic to tropical dry forests may be more sensitive to anthropogenic disturbance than others, but our ability to predict primate abundance in the face of disturbance also depends on the specific variables for each site. Here, we consider the factors that explain the high density of white-faced capuchins (Cebus capucinus) found in the Taboga Forest, Costa Rica, a relatively small fragment of tropical dry forest surrounded by agricultural fields. Our analyses suggest that, for capuchins (and potentially for mantled howler monkeys, Alouatta palliata), the size and disturbance of a forest fragment may matter less than the composition and availability of key resources, like above-ground water. Group sightings for both species were higher near permanent water sources, but group sightings did not vary between edge and interior forest. These findings help explain why some primate species can flourish even alongside anthropogenic disturbance and thus carry important implications for conservation efforts. Smaller forest fragments, like Taboga, may be able to support high densities of some species because they provide a mosaic of habitats and key resources that buffer adverse ecological conditions. Future studies will assess the extent to which primates in the Taboga Forest rely on the canals versus the river and will consider how the high density of capuchins in Taboga influences ranging patterns, home range overlap, and the frequency and intensity of intergroup encounters.\n\nRESEARCH HIGHLIGHTSO_LIHere we introduce a new white-faced capuchin study site in the Taboga Forest, Costa Rica, a fragmented tropical dry forest.\nC_LIO_LIForest fragments like Taboga may support high primate densities because they provide a mosaic of habitats and key resources.\nC_LI

animal behavior and cognition↗

The Goldilocks Effect: Female geladas in mid-sized groups have higher fitness

The cost-benefit ratio of group-living is thought to vary with group size: individuals in "optimally-sized" groups should have higher fitness than individuals in groups that are either too large or too small. However, the relationship between group size and individual fitness has been difficult to establish for long-lived species where the number of groups studied is typically quite low. Here we present evidence for optimal group size that maximizes female fitness in a population of geladas (Theropithecus gelada). Drawing on 14 years of demographic data, we found that females in small groups experienced the highest death rates, while females in mid-sized units exhibited the highest reproductive performance. This group-size effect on female reproductive performance was largely explained by variation in infant mortality (and, in particular, by infanticide from immigrant males) but not by variation in reproductive rates. Taken together, females in mid-sized units are projected to attain optimal fitness due to conspecific infanticide and, potentially, predation. Our findings provide insight into how and why group size shapes fitness in long-lived species.

evolutionary biology↗