Social ageing: exploring the drivers of late-life changes in social behaviour in mammals

This is the final version. Available from The Royal Society via the DOI in this record. No datasets were generated or analysed during the current study.Social interactions help group-living organisms cope with socio-environmental challenges and are central to survival and reproductive success. Recent research has shown that social behaviour and relationships can change across the lifespan, a phenomenon referred to as 'social ageing'. Given the importance of social integration for health and well-being, age-dependent changes in social behaviour can modulate how fitness changes with age and may be an important source of unexplained variation in individual patterns of senescence. However, integrating social behaviour into ageing research requires a deeper understanding of the causes and consequences of age-based changes in social behaviour. Here, we provide an overview of the drivers of late-life changes in sociality. We suggest that explanations for social ageing can be categorized into three groups: changes in sociality that (a) occur as a result of senescence; (b) result from adaptations to ameliorate the negative effects of senescence; and/or (c) result from positive effects of age and demographic changes. Quantifying the relative contribution of these processes to late-life changes in sociality will allow us to move towards a more holistic understanding of how and why these patterns emerge and will provide important insights into the potential for social ageing to delay or accelerate other patterns of senescence.National Institute of HealthNational Institute of Healt

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

Concentrations of urinary neopterin, but not suPAR, positively correlate with age in rhesus macaques

This is the final version. Available on open access from Frontiers Media via the DOI in this recordData availability statement: The datasets presented in this study can be found in online repositories. The names of the repository/repositories and accession number(s) can be found below: BioProject, PRJNA715739.Identifying biomarkers of age-related changes in immune system functioning that can be measured non-invasively is a significant step in progressing research on immunosenescence and inflammaging in free-ranging and wild animal populations. In the present study, we aimed to investigate the suitability of two urinary compounds, neopterin and suPAR, as biomarkers of age-related changes in immune activation and inflammation in a free-ranging rhesus macaque (Macaca mulatta) population. We also investigated age-associated variation in gene transcription from blood samples to understand the underlying proximate mechanisms that drive age-related changes in urinary neopterin or suPAR. Neopterin was significantly positively correlated with age, and had a moderate within-individual repeatability, indicating it is applicable as a biomarker of age-related changes. The age-related changes in urinary neopterin are not apparently driven by an age-related increase in the primary signaler of neopterin, IFN-y, but may be driven instead by an age-related increase in both CD14+ and CD14− monocytes. suPAR was not correlated with age, and had low repeatability within-individuals, indicating that it is likely better suited to measure acute inflammation rather than chronic age-related increases in inflammation (i.e., “inflammaging”). Neopterin and suPAR had a correlation of 25%, indicating that they likely often signal different processes, which if disentangled could provide a nuanced picture of immune-system function and inflammation when measured in tandem.National Institutes of Healt

Specificity of muscle action after anterior cruciate ligament injury

Abstract Neuromuscular control is believed to be a critical factor in dynamic knee stability. The purpose of this study was to evaluate voluntary muscle control in anterior cruciate ligament deficient (ACL-D) and uninjured people. Twenty athletes of similar age participated in this study. Subjects performed a target-matching protocol that required them to produce isometric moments about the knee with fine control in flexion, extension, varus, and valgus (i.e., loads were generated in the plane perpendicular to the long axis of the shank). Electromyographic data were collected from 10 muscles that span the knee. A specificity index was calculated for each muscle to describe how fine-tuned (specific) its muscle activity pattern was with respect to its principal direction of action in the load plane. Diminished specificity of muscle action was observed in 8 of 10 muscles in the ACL-D subjectsÕ involved knees when compared with the activity patterns from their uninvolved knees and those from the uninjured subjectsÕ knees. The vastus lateralis muscle was especially affected. Increased and more global co-contraction was also observed in the ACL-D limbs. The alterations in muscle firing patterns observed in this study are consistent with diminished neuromuscular control

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

The rhesus macaque as a success story of the Anthropocene

This is the final version. Available on open access from eLife Sciences Publications via the DOI in this recordData availability: No new data was generated for this articleOf all the non-human primate species studied by researchers, the rhesus macaque (Macaca mulatta) is likely the most widely used across biological disciplines. Rhesus macaques have thrived during the Anthropocene and now have the largest natural range of any non-human primate. They are highly social, exhibit marked genetic diversity, and display remarkable niche flexibility (which allows them to live in a range of habitats and survive on a variety of diets). These characteristics mean that rhesus macaques are well-suited for understanding the links between sociality, health and fitness, and also for investigating intra-specific variation, adaptation and other topics in evolutionary ecology.National Institutes of Healt

Reduced injury risk links sociality to survival in a group-living primate

This is the final version. Available on open access from Cell Press via the DOI in this recordData and code availability: Data have been deposited at Mendeley Data and are publicly available as of the date of publication. DOI is listed in the key resources table. All original code has been deposited on GitHub and is publicly available as of the date of publication. The link is listed in the key resources table. Any additional information required to reanalyze the data reported in this paper is available from the lead contact upon request.Sociality has been linked to a longer lifespan in many mammals, including humans. Yet, how sociality results in survival benefits remains unclear. Using 10 years of data and over 1,000 recorded injuries in rhesus macaques (Macaca mulatta), we tested two injury-related mechanisms by which social status and affiliative partners might influence survival. Injuries increased individual risk of death by 3-fold in this dataset. We found that sociality can affect individuals’ survival by reducing their risk of injury but had no effect on the probability of injured individuals dying. Both males and females of high social status (measured as female matrilineal rank and male group tenure) and females with more affiliative partners (estimated using the number of female relatives) experienced fewer injuries and thus were less likely to die. Collectively, our results offer rare insights into one mechanism that can mediate the well-known benefits of sociality on an individual’s fitness.ANID-Chilean scholarshipNational Institutes of Health (NIH)European Research Council (ERC)MacCracken FellowshipNational Science Foundation (NSF

Ageing in a collective: the impact of ageing individuals on social network structure

This is the final version. Available on open access from the Royal Society via the DOI in this recordData accessibility: All data are available from the Figshare Repository: https://doi.org/10.6084/m9.figshare.21936426 [97]. The data are provided in the electronic supplementary material [98].Ageing affects many phenotypic traits, but its consequences for social behaviour have only recently become apparent. Social networks emerge from associations between individuals. The changes in sociality that occur as individuals get older are thus likely to impact network structure, yet this remains unstudied. Here we use empirical data from free-ranging rhesus macaques and an agent-based model to test how age-based changes in social behaviour feed up to influence: (i) an individual's level of indirect connectedness in their network and (ii) overall patterns of network structure. Our empirical analyses revealed that female macaques became less indirectly connected as they aged for some, but not for all network measures examined. This suggests that indirect connectivity is affected by ageing, and that ageing animals can remain well integrated in some social contexts. Surprisingly, we did not find evidence for a relationship between age distribution and the structure of female macaque networks. We used an agent-based model to gain further understanding of the link between age-based differences in sociality and global network structure, and under which circumstances global effects may be detectable. Overall, our results suggest a potentially important and underappreciated role of age in the structure and function of animal collectives, which warrants further investigation. This article is part of a discussion meeting issue ‘Collective behaviour through time’.National Institutes of HealthKaufman Foundatio

Reduced injury risk links sociality to survival in a group-living primate

Sociality has been linked to a longer lifespan in many mammals, including humans. Yet, how sociality results in survival benefits remains unclear. Using 10 years of data and over 1,000 recorded injuries in rhesus macaques (Macaca mulatta), we tested two injury-related mechanisms by which social status and affiliative partners might influence survival. Injuries increased individual risk of death by 3-fold in this dataset. We found that sociality can affect individuals’ survival by reducing their risk of injury but had no effect on the probability of injured individuals dying. Both males and females of high social status (measured as female matrilineal rank and male group tenure) and females with more affiliative partners (estimated using the number of female relatives) experienced fewer injuries and thus were less likely to die. Collectively, our results offer rare insights into one mechanism that can mediate the well-known benefits of sociality on an individual’s fitness

Age-Related Differences in Ocular Features of a Naturalistic Free-Ranging Population of Rhesus Macaques

This is the final version. Available on open access from the Association for Research in Vision and Ophthalmology via the DOI in this recordPURPOSE: Rhesus macaques (Macaca mulatta) are the premier nonhuman primate model for studying human health and disease. We investigated if age was associated with clinically relevant ocular features in a large cohort of free-ranging rhesus macaques from Cayo Santiago, Puerto Rico. METHODS: We evaluated 120 rhesus macaques (73 males, 47 females) from 0 to 29 years old (mean ± SD: 12.6 ± 6.4) from September to December 2021. The ophthalmic evaluation included intraocular pressure (IOP) assessment, corneal pachymetry, biomicroscopy, A-scan biometry, automated refraction, and fundus photography after pupil dilation. The associations of age with the outcomes were investigated through multilevel mixed-effects models adjusted for sex and weight. RESULTS: On average, IOP, pachymetry, axial length, and automated refraction spherical equivalent were 18.37 ± 4.68 mmHg, 474.43 ± 32.21 µm, 19.49 ± 1.24 mm, and 0.30 ± 1.70 diopters (D), respectively. Age was significantly associated with pachymetry (β coefficient = -1.20; 95% confidence interval [CI], -2.27 to -0.14; P = 0.026), axial length (β coefficient = 0.03; 95% CI, 0.01 to 0.05; P = 0.002), and spherical equivalent (β coefficient = -0.12; 95% CI, -0.22 to -0.02; P = 0.015). No association was detected between age and IOP. The prevalence of cataracts in either eye was 10.83% (95% CI, 6.34-17.89) and was significantly associated with age (odds ratio [OR] = 1.20; 95% CI, 1.06-1.36; P = 0.004). Retinal drusen in either eye was observed in 15.00% (95% CI, 9.60-22.68) of animals, which was also significantly associated with age (OR = 1.14; 95% CI, 1.02-1.27; P = 0.020). CONCLUSIONS: Rhesus macaques exhibit age-related ocular associations similar to those observed in human aging, including decreased corneal thickness, increased axial length, myopic shift, and higher prevalence of cataract and retinal drusen.New Frontiers in Research FoundationNatural Sciences and Engineering Research CouncilCanada Research Chairs ProgramNational Aging InstituteBrightFocus FoundationNational Institutes of Health (NIH)University of Calgar