Persistent social isolation reflects identity and social context but not maternal effects or early environment

This is the final version of the article. Available from Springer Nature via the DOI in this record.Individuals who are well integrated into society have greater access to resources and tend to live longer. Why some individuals are socially isolated and others are not is therefore puzzling from an evolutionary perspective. Answering this question requires establishing the mix of intrinsic and contextual factors that contribute to social isolation. Using social network data spanning up to half of the median adult lifespan in a gregarious primate, we found that some measures of social isolation were modestly repeatable within individuals, consistent with a trait. By contrast, social isolation was not explained by the identity of an animal’s mother or the group into which it was born. Nevertheless, age, sex and social status each played a role, as did kin dynamics and familiarity. Females with fewer close relatives were more isolated, and the more time males spent in a new group the less isolated they became, independent of their social status. These results show that social isolation results from a combination of intrinsic and environmental factors. From an evolutionary perspective, these findings suggest that social isolation could be adaptive in some contexts and partly maintained by selection.This work was supported by National Institute of Mental Health grants R01-MH089484 and R01-MH096875, and an Incubator Award from the Duke Institute for Brain Sciences. L.J.N.B. was supported by an Early Career Fellowship from the Leverhulme Trust. Data provided by the University of Puerto Rico, and its facilities, are funded by grant number 2 P40 OD012217 from the Office of Research Infrastructure Programs (ORIP) of the National Institutes of Health (NIH)

Social network dynamics precede a mass eviction in group-living rhesus macaques

This is the author accepted manuscript. The final version is available from Elsevier Masson via the DOI in this record.Network dynamics can reveal information about the adaptive function of social behaviour and the extent to which social relationships can flexibly respond to extrinsic pressures. Changes in social networks occur following changes to the social and physical environment. By contrast, we have limited understanding of whether changes in social networks precede major group events. Permanent evictions can be important determinants of gene flow and population structure and are a clear example of an event that might be preceded by social network dynamics. Here we examined the social networks of a group of rhesus macaques, Macaca mulatta, in the 2 years leading up to the eviction of 22% of adult females, which are the philopatric sex. We found that females engaged in the same amount of aggression and grooming in the 2 years leading up to the eviction but that there were clear changes in their choice of social partners. Females that would eventually be evicted received more aggression from lower-ranking females as the eviction approached. Evicted females also became more discriminating in their grooming relationships in the year nearer the split, showing a greater preference for one another and becoming more cliquish. Put simply, the females that would later be evicted continued to travel with the rest of the group as the eviction approached but were less likely to interact with other group members in an affiliative manner. These results have potential implications for understanding group cohesion and the balance between cooperation and competition that mediates social groups.We were supported by National Institute of Mental Health grants R01-MH089484 and R01-MH096875, and an Incubator Award from the Duke Institute for Brain Sciences. L.J.N.B. was supported by a Duke Center for Interdisciplinary Decision Sciences Fellowship and by an Early Career Fellowship from the Leverhulme Trust. The CPRC is funded by grant number 2 P40 OD012217 from the Office of Research Infrastructure Programs (ORIP) of the National Institutes of Health (NIH)

Using Machine Learning to Discover Latent Social Phenotypes in Free-Ranging Macaques

This is the final version of the article. Available from MDPI via the DOI in this record.Investigating the biological bases of social phenotypes is challenging because social behavior is both high-dimensional and richly structured, and biological factors are more likely to influence complex patterns of behavior rather than any single behavior in isolation. The space of all possible patterns of interactions among behaviors is too large to investigate using conventional statistical methods. In order to quantitatively define social phenotypes from natural behavior, we developed a machine learning model to identify and measure patterns of behavior in naturalistic observational data, as well as their relationships to biological, environmental, and demographic sources of variation. We applied this model to extensive observations of natural behavior in free-ranging rhesus macaques, and identified behavioral states that appeared to capture periods of social isolation, competition over food, conflicts among groups, and affiliative coexistence. Phenotypes, represented as the rate of being in each state for a particular animal, were strongly and broadly influenced by dominance rank, sex, and social group membership. We also identified two states for which variation in rates had a substantial genetic component. We discuss how this model can be extended to identify the contributions to social phenotypes of particular genetic pathways.The authors would like to thank John Pearson, Sam Larson, Ashley Walker, Joel Glick, Josue Negron, and the CPRC staff for their feedback and research support. This research supported by NIH grant 5R01-MH096875-02. The CPRC is supported by grant 8-P40 OD012217-25 from the National Center for Research Resources and the Office of Research Infrastructure Programs of the National Institutes of Health

Genetic origins of social networks in rhesus macaques

This is the final version of the article. Available from the publisher via the DOI in this record.Sociality is believed to have evolved as a strategy for animals to cope with their environments. Yet the genetic basis of sociality remains unclear. Here we provide evidence that social network tendencies are heritable in a gregarious primate. The tendency for rhesus macaques, Macaca mulatta, to be tied affiliatively to others via connections mediated by their social partners - analogous to friends of friends in people - demonstrated additive genetic variance. Affiliative tendencies were predicted by genetic variation at two loci involved in serotonergic signalling, although this result did not withstand correction for multiple tests. Aggressive tendencies were also heritable and were related to reproductive output, a fitness proxy. Our findings suggest that, like humans, the skills and temperaments that shape the formation of multi-agent relationships have a genetic basis in nonhuman primates, and, as such, begin to fill the gaps in our understanding of the genetic basis of sociality.We thank Bonn Aure, Jacqueline Buhl, Monica Carlson, Matthew McConnell, Elizabeth Maldonado, David Paulsen, Cecilia Penedo & the Caribbean Primate Research Center (CPRC) for assistance, and Roger Mundry for the use of PSAM software. The authors were supported by NIMH grant R01-MH089484, an Incubator Award from the Duke Institute for Brain Sciences, and a Duke Center for Interdisciplinary Decision Sciences Fellowship to LJNB. The CPRC is supported by grant 8-P40 OD012217-25 from the National Center for Research Resources (NCRR) and the Office of Research Infrastructure Programs (ORIP) of the National Institutes of Health

No evidence that grooming is exchanged for coalitionary support in the short- or long-term via direct or generalized reciprocity in unrelated rhesus macaques

This is the final version. Available on open access from Springer via the DOI in this recordData availability: The datasets generated during and/or analyzed during the current study are available in the Dryad repository, (doi:https://doi.org/10.5061/dryad.pvmcvdnks).Reciprocity is a prominent explanation for cooperation between non-kin. Studies designed to demonstrate reciprocity often focus on direct reciprocity in the timescale of minutes to hours, whereas alternative mechanisms like generalized reciprocity and the possibility of reciprocation over longer timescales of months and years are less often explored. Using a playback experiment, we tested for evidence of direct and generalized reciprocity across short and longer timescales. We examined the exchange of grooming for coalitionary support between unrelated female rhesus macaques in a population with a complete genetic pedigree. Females that received grooming were not more responsive to calls for coalitionary support from unrelated female group mates compared to control females that received agonism or no interaction — even when the call belonged to a females’ most recent grooming partner. Similarly, females were not more responsive to calls for support from their most frequent unrelated grooming partner of the last two years, nor if they received large amounts of grooming from all other females in their group. We interpret these results as an absence of evidence for direct or generalized reciprocity on any timescale in the exchange of grooming for coalitionary support in rhesus macaques. If grooming is exchanged for support in this population, it is with an intensity below our ability to detect it or over a longer timescale than we examined. We propose by-product explanations may also be at play and highlight the importance of investigating multiple mechanisms when testing apparently cooperative behaviors.National Institutes of Health (NIH)Leverhulme Trus

Simultaneous transcranial magnetic stimulation and single-neuron recording in alert non-human primates.

Transcranial magnetic stimulation (TMS) is a widely used, noninvasive method for stimulating nervous tissue, yet its mechanisms of effect are poorly understood. Here we report new methods for studying the influence of TMS on single neurons in the brain of alert non-human primates. We designed a TMS coil that focuses its effect near the tip of a recording electrode and recording electronics that enable direct acquisition of neuronal signals at the site of peak stimulus strength minimally perturbed by stimulation artifact in awake monkeys (Macaca mulatta). We recorded action potentials within ∼1 ms after 0.4-ms TMS pulses and observed changes in activity that differed significantly for active stimulation as compared with sham stimulation. This methodology is compatible with standard equipment in primate laboratories, allowing easy implementation. Application of these tools will facilitate the refinement of next generation TMS devices, experiments and treatment protocols

Deconstructing sociality: the types of social connections that predict longevity in a group-living primate

This is the author accepted manuscript. The final version is available from Royal Society via the DOI in this record.Many species use social interactions to cope with challenges in their environment and a growing number of studies show that individuals which are well-connected to their group have higher fitness than socially isolated individuals. However, there are many ways to be 'well-connected' and it is unclear which aspects of sociality drive fitness benefits. Being well-connected can be conceptualized in four main ways: individuals can be socially integrated by engaging in a high rate of social behaviour or having many partners; they can have strong and stable connections to favoured partners; they can indirectly connect to the broader group structure; or directly engage in a high rate of beneficial behaviours, such as grooming. In this study, we use survival models and long-term data in adult female rhesus macaques (Macaca mulatta) to compare the fitness outcomes of multiple measures of social connectedness. Females that maintained strong connections to favoured partners had the highest relative survival probability, as did females well-integrated owing to forming many weak connections. We found no survival benefits to being structurally well-connected or engaging in high rates of grooming. Being well-connected to favoured partners could provide fitness benefits by, for example, increasing the efficacy of coordinated or mutualistic behaviours.Leverhulme TrustNational Institutes of HealthNational Center for Research Resource

Yearly variation coupled with social interactions shape the skin microbiome in free-ranging rhesus macaques

This is the final version. Available on open access from the American Society for Microbiology via the DOI in this recordAll data analysis scripts can be found here: https://github.com/CayoBiobankResearchUnit/macaque-skin-microbiome.gitWhile skin microbes are known to mediate human health and disease, there has been minimal research on the interactions between skin microbiota, social behavior, and year-to-year effects in non-human primates—important animal models for translational biomedical research. To examine these relationships, we analyzed skin microbes from 78 rhesus macaques living on Cayo Santiago Island, Puerto Rico. We considered age, sex, and social group membership, and characterized social behavior by assessing dominance rank and patterns of grooming as compared to nonsocial behaviors. To measure the effects of a shifting environment, we sampled skin microbiota (based on sequence analysis of the 16S rRNA V4 region) and assessed weather across sampling periods between 2013 and 2015. We hypothesized that, first, monkeys with similar social behavior and/or in the same social group would possess similar skin microbial composition due, in part, to physical contact, and, second, microbial diversity would differ across sampling periods. We found significant phylum-level differences between social groups in the core microbiome as well as an association between total grooming rates and alpha diversity in the complete microbiome, but no association between microbial diversity and measures of rank or other nonsocial behaviors. We also identified alpha and beta diversity differences in microbiota and differential taxa abundance across two sampling periods. Our findings indicate that social dynamics interact with yearly environmental changes to shape the skin microbiota in rhesus macaques, with potential implications for understanding the factors affecting the microbiome in humans, which share many biological and social characteristics with these animals.National Institutes of Healt

Within-individual changes reveal increasing social selectivity with age in rhesus macaques

This is the final version. Available from National Academy of Sciences via the DOI in this record. Data, Materials, and Software Availability. Data are available from the Figshare Repository (https://doi.org/10.6084/m9.figshare.21551295).Accumulating evidence in humans and other mammals suggests older individuals tend to have smaller social networks. Uncovering the cause of these declines can inform how changes in social relationships with age affect health and fitness in later life. While age-based declines in social networks have been thought to be detrimental, physical and physiological limitations associated with age may lead older individuals to adjust their social behavior and be more selective in partner choice. Greater selectivity with age has been shown in humans, but the extent to which this phenomenon occurs across the animal kingdom remains an open question. Using longitudinal data from a population of rhesus macaques on Cayo Santiago, we provide compelling evidence in a nonhuman animal for within-individual increases in social selectivity with age. Our analyses revealed that adult female macaques actively reduced the size of their networks as they aged and focused on partners previously linked to fitness benefits, including kin and partners to whom they were strongly and consistently connected earlier in life. Females spent similar amounts of time socializing as they aged, suggesting that network shrinkage does not result from lack of motivation or ability to engage, nor was this narrowing driven by the deaths of social partners. Furthermore, females remained attractive companions and were not isolated by withdrawal of social partners. Taken together, our results provide rare empirical evidence for social selectivity in nonhumans, suggesting that patterns of increasing selectivity with age may be deeply rooted in primate evolution.National Institute of HealthNational Institute of HealthNational Institute of HealthNational Institute of HealthNational Institute of HealthNational Institute of HealthNational Institute of HealthNational Institute of HealthKaufman Foundatio

International Veterinary Epilepsy Task Force consensus report on epilepsy definition, classification and terminology in companion animals

Dogs with epilepsy are among the commonest neurological patients in veterinary practice and therefore have historically attracted much attention with regard to definitions, clinical approach and management. A number of classification proposals for canine epilepsy have been published during the years reflecting always in parts the current proposals coming from the human epilepsy organisation the International League Against Epilepsy (ILAE). It has however not been possible to gain agreed consensus, “a common language”, for the classification and terminology used between veterinary and human neurologists and neuroscientists, practitioners, neuropharmacologists and neuropathologists. This has led to an unfortunate situation where different veterinary publications and textbook chapters on epilepsy merely reflect individual author preferences with respect to terminology, which can be confusing to the readers and influence the definition and diagnosis of epilepsy in first line practice and research studies. In this document the International Veterinary Epilepsy Task Force (IVETF) discusses current understanding of canine epilepsy and presents our 2015 proposal for terminology and classification of epilepsy and epileptic seizures. We propose a classification system which reflects new thoughts from the human ILAE but also roots in former well accepted terminology. We think that this classification system can be used by all stakeholders