Peer-Reviewed Publications
In Review:
(16) Turcotte C., Raghunath A., Ryan T.M., DeMars L.J.D., Siracusa E.R., Patterson S.K., Cayo Biobank Research Unit, Platt M.L., Brent L.J.N., Snyder-Mackler N., Montague M.J., Martinez M.I., Williams S.A., Antón S.C., Higham J.P., Kuo S. Sources of variation in trabecular bone microarchitecture across rhesus macaque (Macaca mulatta) load-bearing joints. Journal of Bone and Mineral Research, in review.
Abstract: Globally, population structure is quickly trending older, increasing the prevalence and systemic burden of age-related skeletal disorders such as osteoporosis (OP). OP is characterized by the loss of bone mass, including trabecular bone tissue, leading to skeletal fracture. Though clinically important, fundamental questions remain about normal trabecular bone variation as well as the pathogenesis of age-related bone loss. In this study, we use free-ranging rhesus macaques (Macaca mulatta) from the Cayo Santiago Field Station to explore variation in trabecular bone structure as a consequence of weight, demography, sociality and early life adversity. We measured several aspects of trabecular bone structure (e.g., maximum and mean bone volume fraction (BV/TV), degree of anisotropy (DA) and trabecular thickness (Tb.Th)) across epiphyses from the elbow (humerus, ulna, radius), hip (proximal femur), and knee (distal femur, tibia). Descriptive statistics (mean ± SD) were assessed using analyses of variance across morphological (by bone) and functional (by limb, joint) subunits of the skeleton. Analyses of covariance models were then run to assess factors influencing bone structure, including body mass, demography (age, sex, matriline), as well as indices of sociality and early life adversity. Age-related differences in bone structure were then visualized using Bayesian multilevel modeling on canonical point clouds. We observed significant variation in trabecular bone morphology across both bones and joints. Sex influenced Tb.Th, with thicker male trabeculae. Body mass positively correlated with Max and Mean BV/TV and Tb.Th. Age was associated with significantly lower values of Mean BV/TV specifically in the hindlimb. We observed significant bone loss specifically in the femoral head and neck. There were no associations of trabecular bone architecture with either sociality or early life adversity in this sample. This study represents the largest dataset to undergo whole bone microarchitectural quantification to date, a powerful emerging tool in skeletal tissue research.
(15) Pavez Fox M.A., Siracusa E.R., Ellis S., Kimock C., Rivera-Barreto N., Negron-Del Valle J.E., Phillips D., Ruiz-Lambides A., Snyder-Mackler N., Higham J.P., Brent L.J.N., De Moor D. Socioecological drivers of injuries in female and male rhesus macaques (Macaca mulatta). Behavioral Ecology and Sociobiology, in review https://doi.org/10.1101/2023.10.20.563310
Abstract: Competition over access to resources, such as food and mates, is one of the major costs associated with group living. Two socioecological factors believed to drive the intensity of competition are group size and sex ratio. However, empirical evidence linking these factors to injuries with associated survival costs is scarce. Here, we leveraged 10 years of data from a free-ranging rhesus macaque population where injuries are associated with a high mortality risk to test whether group size and adult sex ratio predicted the occurrence of injuries and if these patterns could be explained by the inter- or intrasexual physical aggression. We found that males in larger groups were less likely to be injured while females in larger groups were more likely to be injured. As group size did not predict intragroup aggression risk in males or females, this suggests that group size effects on injury risk might be linked to intergroup aggression. Further, male-biased sex ratios predicted a slight increase in injury risk in females. This, combined with higher male-female aggression risk in male-biased groups, points to male mating coercion as a potential cause of injuries in females. Our results provide insights into the fitness-related costs of competition and empirical evidence for long-standing predictions on the evolution of group living.
Published:
(14) Siracusa E.R., Pavez-Fox M.A., Negron-Del Valle J.E., Phillips D., Platt M.L., Synder-Mackler N., Higham J.P., Brent, L.J.N., Silk, M.J. 2024. Social ageing can protect against infectious disease in a group-living primate. Philosophical Transactions of the Royal Society B, in press https://doi.org/10.1101/2024.03.09.584237
Abstract: The benefits of social living are well established, but sociality also comes with costs, including infectious disease risk. This cost-benefit ratio of sociality is expected to change across individuals’ lifespans, which may drive changes in social behaviour with age. To explore this idea, we combine data from a group-living primate for which social ageing has been described with epidemiological models to show that having lower social connectedness when older can protect against the costs of a hypothetical, directly transmitted endemic pathogen. Assuming no age differences in epidemiological characteristics (susceptibility to, severity, and duration of infection), older individuals suffered lower infection costs, which was explained largely because they were less connected in their social networks than younger individuals. This benefit of ‘social ageing’ depended on epidemiological characteristics and was greatest when infection severity increased with age. When infection duration increased with age, social ageing was beneficial only when pathogen transmissibility was low. Older individuals benefited most from having a lower frequency of interactions (strength) and network embeddedness (closeness) and benefited less from having fewer social partners (degree). Our study provides a first examination of the epidemiology of social ageing, demonstrating the potential for pathogens to influence evolutionary dynamics of social ageing in natural populations.
(13) Sanchez Rosado M.R, Marzan-Rivera N., Watowich, M.M., Negron-Del Valle A., Pantoja P., Pavez-Fox, M.A., Siracusa E.R., Cooper E.B., Negron-Del Valle J.E., Phillips D., Ruiz-Lambides A., Cayo Biobank Research Unit, Martinez M.I., Montague, M.J., Platt M.L., Higham J.P., Brent L.J.N., Sariol C.A., Snyder-Mackler N. 2023. Immune cell composition varies by age, sex, and exposure to social adversity in free-ranging Rhesus Macaques. GeroScience, 46: 2107-2122 https://doi.org/10.1007/s11357-023-00962-8
Abstract: Increasing age is associated with dysregulated immune function and increased inflammation - patterns that are also observed in individuals exposed to chronic social adversity. Yet we still know little about how social adversity impacts the immune system and how it might promote age-related diseases. Here, we investigated how immune cell diversity varied with age, sex and social adversity (operationalized as low social status) in free-ranging rhesus macaques. We found age-related signatures of immunosenescence, including lower proportions of CD20+ B cells, CD20+/CD3+ ratio, and CD4+/CD8+ T cell ratio – all signs of diminished antibody production. Age was associated with higher proportions of CD3+/CD8+ Cytotoxic T cells, CD16+/CD3- Natural Killer cells, CD3+/CD4+/CD25+ and CD3+/CD8+/CD25+ T cells, and CD14+/CD16+/HLA-DR+ intermediate monocytes, and lower levels of CD14+/CD16-/HLA-DR+ classical monocytes, indicating greater amounts of inflammation and immune dysregulation. We also found a sex-dependent effect of exposure to social adversity (i.e., low social status). High-status males, relative to females, had higher CD20+/CD3+ ratios and CD16+/CD3 Natural Killer cell proportions, and lower proportions of CD8+ Cytotoxic T cells. Further, low-status females had higher proportions of cytotoxic T cells than high-status females, while the opposite was observed in males. High-status males had higher CD20+/CD3+ ratios than low-status males. Together, our study identifies the strong age and sex-dependent effects of social adversity on immune cell proportions in a human-relevant primate model. Thus, these results provide novel insights into the combined effects of demography and social adversity on immunity and their potential contribution to age-related diseases in humans and other animals.
(12) Siracusa E.R., Pereira A.S, Bohr Brask J., Negron-Del Valle J.E., Phillips D., Platt M.L., Higham J.P., Snyder-Mackler N., Brent L.J.N. 2023. Ageing in a collective: The impact of ageing individuals on social network structure. Philosophical Transactions of the Royal Society B, 378: 20220061 https://doi.org/10.1098/rstb.2022.0061
Abstract: 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.
(11) Siracusa E.R., Negron-Del Valle J.E., Phillips D., Platt M.L., Higham J.P., Snyder-Mackler N., Brent L.J.N. 2022. Within-individual changes reveal increasing social selectivity with age in rhesus macaques. PNAS, 119 (49): e2209180119 https://doi.org/10.1073/pnas.2209180119
Abstract: 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.
(10) Pavez-Fox M.A., Kimock, C.M., Rivera-Barreto N., Negron-Del Valle J.E., Phillips D., Ruiz-Lambides A., Synder-Mackler N, Higham J.P., Brent L.J.N.*, Siracusa E.R.*. 2022. Reduced injury risk links sociality to survival in a group-living primate. iScience, 25 (11): 105454
https://doi.org/10.1016/j.isci.2022.105454
*equal contribution
Abstract: 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.
(9) Siracusa E.R. 2022. Social senescence in red deer. Nature Ecology and Evolution, News & Views, 6: 1062-1063 https://doi.org/10.1038/s41559-022-01766-3
Abstract: Longitudinal data spanning 43 years from a wild ungulate population reveal changes in social connectedness as individuals age, and suggest that these changes may in part be driven by changes in spatial behaviour.
(8) Martinig, A.R., Karst H.J, Siracusa E.R., Studd E.K., McAdam A.G., Dantzer B., Delaney D.M., Lane J.E., Pokharel P., Boutin S. 2022. Animal personality: a comparison of standardized assays and focal observations in North American red squirrels. Animal Behaviour, 190: 221-232 https://doi.org/10.1016/j.anbehav.2022.05.012.
Abstract: As interest in animal personality research grows, methodologies for quantifying consistent among-individual differences in behaviour are expanding. Two of the most common methods for quantifying animal personality are standardized behavioural assays and focal animal sampling. We evaluated whether assays and focals provided similar animal personality measures in a wild population of free-ranging North American red squirrels, Tamiasciurus hudsonicus, by comparing the among-individual correlations of traits between methods. Assays described two behavioural axes—one associated with movement behaviours and another associated with antagonistic behaviours towards conspecifics. Focals described two additional behavioural axes—one associated with movement and territorial behaviours, and another associated with the trade-off between vigilant and feeding behaviours. Although we found evidence of high trait repeatability for behavioural axes measured with assays, both focal behavioural axes had low trait repeatability regardless of whether among-individual differences in the social environment were controlled for (i.e. to account for ‘pseudopersonality’). We also found no among-individual correlations between assay and focal behavioural axes. The lack of correlation between methods may be because the dominant axes of variation differ between methods or because of the low trait repeatability of focals due to high behavioural plasticity. Given this, we conclude that assays will likely remain the mainstay for measuring consistent among-individual differences in behaviour given their ability to standardize for environmental conditions.
(7) Siracusa E.R., Higham J.P., Snyder-Mackler N., Brent L. J. N. 2022. Social ageing: Exploring the drivers of late-life changes in social behaviour in mammals, Biology Letters, 18: 20210643 https://doi.org/10.1098/rsbl.2021.0643.
Abstract: 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 toward 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.
(6) Fisher D.N., Kilgour R.J., Siracusa E.R., Foote J.R., Hobson E.A., Montiglio P.O., Saltz J.B., Wey T., Wice E.W. 2021. Anticipated effects of abiotic environmental change on intraspecific social interactions, Biological Reviews, 96: 2661-2693 https://doi.org/10.1111/brv.12772
Abstract: Social interactions are ubiquitous across the animal kingdom. A variety of ecological and evolutionary processes are dependent on social interactions, such as movement, disease spread, information transmission, and density-dependent reproduction and survival. Social interactions, like any behaviour, are context dependent, varying with environmental conditions. Currently, environments are changing rapidly across multiple dimensions, becoming warmer and more variable, while habitats are increasingly fragmented and contaminated with pollutants. Social interactions are expected to change in response to these stressors and to continue to change into the future. However, a comprehensive understanding of the form and magnitude of the effects of these environmental changes on social interactions is currently lacking. Focusing on four major forms of rapid environmental change currently occurring, we review how these changing environmental gradients are expected to have immediate effects on social interactions such as communication, agonistic behaviours, and group formation, which will thereby induce changes in social organisation including mating systems, dominance hierarchies, and collective behaviour. Our review covers intraspecific variation in social interactions across environments, including studies in both the wild and in laboratory settings, and across a range of taxa. The expected responses of social behaviour to environmental change are diverse, but we identify several general themes. First, very dry, variable, fragmented, or polluted environments are likely to destabilise existing social systems. This occurs as these conditions limit the energy available for complex social interactions and affect dissimilar phenotypes differently. Second, a given environmental change can lead to opposite responses in social behaviour, and the direction of the response often hinges on the natural history of the organism in question. Third, our review highlights the fact that changes in environmental factors are not occurring in isolation: multiple factors are changing simultaneously, which may have antagonistic or synergistic effects, and more work should be done to understand these combined effects. We close by identifying methodological and analytical techniques that might help to study the response of social interactions to changing environments, highlight consistent patterns among taxa, and predict subsequent evolutionary change. We expect that the changes in social interactions that we document here will have consequences for individuals, groups, and for the ecology and evolution of populations, and therefore warrant a central place in the study of animal populations, particularly in an era of rapid environmental change.
(5) Siracusa E.R., Boutin S., Dantzer B., Lane J.E., Coltman D.W., McAdam A.G. 2021. Familiar neighbors, but not relatives, enhance fitness in a territorial mammal, Current Biology 31: 438-445 https://doi.org/10.1016/j.cub.2020.10.072
Abstract: One of the outstanding questions in evolutionary biology is the extent to which mutually beneficial interactions and kin-selection can facilitate the evolution of cooperation by mitigating conflict between interacting organisms. The indirect fitness benefits gained from associating with kin are an important pathway to conflict resolution, but conflict can also be resolved if individuals gain direct benefits from cooperating with one another (e.g. mutualism or reciprocity). Owing to the kin-structured nature of many animal societies, it has been difficult for previous research to assess the relative importance of these mechanisms. However, one area that might allow for the relative roles of kin-selection and mutualistic benefits to be disentangled is in the resolution of conflict over territorial space. While much research has focused on group-living species, the question of how cooperation can first be favored in solitary, territorial species remains a key question. Using 22 years of data from a population of North American red squirrels, we assessed how kinship and familiarity with neighbors affected fitness in a territorial mammal. While living near kin did not enhance fitness, familiarity with neighbors increased survival and annual reproductive success. These fitness benefits were strong enough to compensate for the effects of aging later in life, with potential consequences for the evolution of senescence. We suggest that such substantial fitness benefits provide the opportunity for the evolution of cooperation between adversarial neighbors, offering insight into the role that mutually beneficial behaviors might play in facilitating and stabilizing social systems.
(4) Studd E.K., Menzies A.K., Siracusa E.R., Dantzer B., Lane J.E., McAdam A.G., Boutin S., Humphries M.M. 2020. Optimization of energetic and reproductive gains explains behavioural responses to environmental variation across seasons and years, Ecology Letters 23: 841-850. https://doi.org/10.1111/ele.13494
Abstract: Animals switch between inactive and active states, simultaneously impacting their energy intake, energy expenditure and predation risk, and collectively defining how they engage with environmental variation and trophic interactions. We assess daily activity responses to long‐term variation in temperature, resources and mating opportunities to examine whether individuals choose to be active or inactive according to an optimisation of the relative energetic and reproductive gains each state offers. We show that this simplified behavioural decision approach predicts most activity variation (R2 = 0.83) expressed by free‐ranging red squirrels over 4 years, as quantified through accelerometer recordings (489 deployments; 5066 squirrel‐days). Recognising activity as a determinant of energetic status, the predictability of activity variation aggregated at a daily scale, and the clear signal that behaviour is environmentally forced through optimisation of gain, provides an integrated approach to examine behavioural variation as an intermediary between environmental variation and energetic, life‐history and ecological outcomes.
(3) Siracusa E.R., Wilson D.R., Studd E.K., Boutin S., Humphries M.M., Dantzer B., Lane J.E., McAdam A.G. 2019. Red squirrels mitigate costs of territory defence through social plasticity, Animal Behaviour 151: 29-42. https://doi.org/10.1016/j.anbehav.2019.02.014
Abstract: For territorial species, the ability to be behaviourally plastic in response to changes in their social environment may be beneficial by allowing individuals to mitigate conflict with conspecifics and reduce the costs of territoriality. Here we investigated whether North American red squirrels, Tamiasciurus hudsonicus, are able to minimize costs of territory defence by adjusting behaviour in response to the familiarity of neighbouring conspecifics. Since red squirrels living in familiar neighbourhoods face reduced intrusion risk, we predicted that increasing familiarity among territorial neighbours would allow squirrels to spend less time on territorial defence and more time in the nest. Longitudinal behavioural data (1995–2004) collected from the same squirrels across several different social environments indicated that red squirrels reduced rates of territorial vocalizations and increased nest use in response to increasing familiarity with neighbours. In contrast, cross-sectional data (2015–2016), which provided observations from each individual in a single social environment, did not provide evidence of this plasticity. Post hoc analyses revealed that evidence of social plasticity in this system is primarily due to within-individual changes in behaviour, which we were unable to estimate in the cross-sectional data. Our results demonstrate that red squirrels respond to changes in their social environment by adjusting their behaviour in a manner that reduces the costs of territoriality. However, our results also suggest that estimating plasticity by comparing behaviour among individuals (i.e. cross-sectional analyses) may not always be reliable. Our ability to detect these effects may therefore depend on having data with multiple observations from the same individuals across different social environments.
(2) Siracusa E., Morandini M., Boutin S., Humphries M.M., Dantzer B., Lane J.E., & McAdam A.G. 2017. Red squirrel territorial vocalizations deter intrusions by conspecific rivals, Behaviour 154: 1259-1273. 10.1163/1568539X-00003467
Abstract: In many species, territory defense is thought to be one of the primary functions of acoustic communication. Here we used a speaker occupation experiment to test whether North American red squirrel ‘rattle’ vocalizations function to deter conspecific rivals. We studied 29 male squirrels and removed each individual from his territory twice in a paired design. During the experimental treatment we simulated the owner’s presence after its removal by broadcasting the owner’s rattle from a loudspeaker at the center of the territory. During the control treatment the territory was left in silence. We found that the presence of a speaker replacement reduced the probability of intrusion by 34% and increased the latency to first intrusion by 7%, providing support for the hypothesis that rattles reduce intrusion risk. However, intrusions were not completely averted by the speaker replacement, indicating that vocalizations alone are not sufficient without other cues of the territory owner.
(1) Siracusa E., Boutin S., Humphries M.M., Gorrell J.C., Coltman D.W., Dantzer B., Lane J.E., & McAdam A.G. 2017. Familiarity with neighbours affects intrusion risk in territorial red squirrels, Animal Behaviour 133: 11-20. https://doi.org/10.1016/j.anbehav.2017.08.024
Abstract: Interactions with conspecifics are an important aspect of an individual’s environment. Although it is well known that the presence of conspecifics can have important effects on behaviour, in general it is also now acknowledged that the composition of the social environment can vary, and that this variation may have profound effects on individual behaviour and fitness. Using a wild population of North American red squirrels (Tamiasciurus hudsonicus), we investigated the importance of the composition of the social environment in a territorial species by assessing whether the risk of intrusion faced by territory owners varied with the degree of relatedness and familiarity in their social neighbourhoods. To test this, we conducted temporary removals of territory owners and observed the time until intrusion and the identity of intruding individuals. We found that individuals in neighbourhoods with low average familiarity faced a higher risk of intrusion and that unfamiliar neighbours were more likely to intrude. Surprisingly, we found that related neighbours also posed a higher risk of intrusion. The results from our study suggest that familiarity with neighbours may be an ecologically and evolutionarily relevant measure of the social environment, even in a species considered to be ‘asocial’. Future studies should consider the potential importance of the social environment, which has heretofore been mostly overlooked, as a relevant selective pressure in asocial, territorial species.
(16) Turcotte C., Raghunath A., Ryan T.M., DeMars L.J.D., Siracusa E.R., Patterson S.K., Cayo Biobank Research Unit, Platt M.L., Brent L.J.N., Snyder-Mackler N., Montague M.J., Martinez M.I., Williams S.A., Antón S.C., Higham J.P., Kuo S. Sources of variation in trabecular bone microarchitecture across rhesus macaque (Macaca mulatta) load-bearing joints. Journal of Bone and Mineral Research, in review.
Abstract: Globally, population structure is quickly trending older, increasing the prevalence and systemic burden of age-related skeletal disorders such as osteoporosis (OP). OP is characterized by the loss of bone mass, including trabecular bone tissue, leading to skeletal fracture. Though clinically important, fundamental questions remain about normal trabecular bone variation as well as the pathogenesis of age-related bone loss. In this study, we use free-ranging rhesus macaques (Macaca mulatta) from the Cayo Santiago Field Station to explore variation in trabecular bone structure as a consequence of weight, demography, sociality and early life adversity. We measured several aspects of trabecular bone structure (e.g., maximum and mean bone volume fraction (BV/TV), degree of anisotropy (DA) and trabecular thickness (Tb.Th)) across epiphyses from the elbow (humerus, ulna, radius), hip (proximal femur), and knee (distal femur, tibia). Descriptive statistics (mean ± SD) were assessed using analyses of variance across morphological (by bone) and functional (by limb, joint) subunits of the skeleton. Analyses of covariance models were then run to assess factors influencing bone structure, including body mass, demography (age, sex, matriline), as well as indices of sociality and early life adversity. Age-related differences in bone structure were then visualized using Bayesian multilevel modeling on canonical point clouds. We observed significant variation in trabecular bone morphology across both bones and joints. Sex influenced Tb.Th, with thicker male trabeculae. Body mass positively correlated with Max and Mean BV/TV and Tb.Th. Age was associated with significantly lower values of Mean BV/TV specifically in the hindlimb. We observed significant bone loss specifically in the femoral head and neck. There were no associations of trabecular bone architecture with either sociality or early life adversity in this sample. This study represents the largest dataset to undergo whole bone microarchitectural quantification to date, a powerful emerging tool in skeletal tissue research.
(15) Pavez Fox M.A., Siracusa E.R., Ellis S., Kimock C., Rivera-Barreto N., Negron-Del Valle J.E., Phillips D., Ruiz-Lambides A., Snyder-Mackler N., Higham J.P., Brent L.J.N., De Moor D. Socioecological drivers of injuries in female and male rhesus macaques (Macaca mulatta). Behavioral Ecology and Sociobiology, in review https://doi.org/10.1101/2023.10.20.563310
Abstract: Competition over access to resources, such as food and mates, is one of the major costs associated with group living. Two socioecological factors believed to drive the intensity of competition are group size and sex ratio. However, empirical evidence linking these factors to injuries with associated survival costs is scarce. Here, we leveraged 10 years of data from a free-ranging rhesus macaque population where injuries are associated with a high mortality risk to test whether group size and adult sex ratio predicted the occurrence of injuries and if these patterns could be explained by the inter- or intrasexual physical aggression. We found that males in larger groups were less likely to be injured while females in larger groups were more likely to be injured. As group size did not predict intragroup aggression risk in males or females, this suggests that group size effects on injury risk might be linked to intergroup aggression. Further, male-biased sex ratios predicted a slight increase in injury risk in females. This, combined with higher male-female aggression risk in male-biased groups, points to male mating coercion as a potential cause of injuries in females. Our results provide insights into the fitness-related costs of competition and empirical evidence for long-standing predictions on the evolution of group living.
Published:
(14) Siracusa E.R., Pavez-Fox M.A., Negron-Del Valle J.E., Phillips D., Platt M.L., Synder-Mackler N., Higham J.P., Brent, L.J.N., Silk, M.J. 2024. Social ageing can protect against infectious disease in a group-living primate. Philosophical Transactions of the Royal Society B, in press https://doi.org/10.1101/2024.03.09.584237
Abstract: The benefits of social living are well established, but sociality also comes with costs, including infectious disease risk. This cost-benefit ratio of sociality is expected to change across individuals’ lifespans, which may drive changes in social behaviour with age. To explore this idea, we combine data from a group-living primate for which social ageing has been described with epidemiological models to show that having lower social connectedness when older can protect against the costs of a hypothetical, directly transmitted endemic pathogen. Assuming no age differences in epidemiological characteristics (susceptibility to, severity, and duration of infection), older individuals suffered lower infection costs, which was explained largely because they were less connected in their social networks than younger individuals. This benefit of ‘social ageing’ depended on epidemiological characteristics and was greatest when infection severity increased with age. When infection duration increased with age, social ageing was beneficial only when pathogen transmissibility was low. Older individuals benefited most from having a lower frequency of interactions (strength) and network embeddedness (closeness) and benefited less from having fewer social partners (degree). Our study provides a first examination of the epidemiology of social ageing, demonstrating the potential for pathogens to influence evolutionary dynamics of social ageing in natural populations.
(13) Sanchez Rosado M.R, Marzan-Rivera N., Watowich, M.M., Negron-Del Valle A., Pantoja P., Pavez-Fox, M.A., Siracusa E.R., Cooper E.B., Negron-Del Valle J.E., Phillips D., Ruiz-Lambides A., Cayo Biobank Research Unit, Martinez M.I., Montague, M.J., Platt M.L., Higham J.P., Brent L.J.N., Sariol C.A., Snyder-Mackler N. 2023. Immune cell composition varies by age, sex, and exposure to social adversity in free-ranging Rhesus Macaques. GeroScience, 46: 2107-2122 https://doi.org/10.1007/s11357-023-00962-8
Abstract: Increasing age is associated with dysregulated immune function and increased inflammation - patterns that are also observed in individuals exposed to chronic social adversity. Yet we still know little about how social adversity impacts the immune system and how it might promote age-related diseases. Here, we investigated how immune cell diversity varied with age, sex and social adversity (operationalized as low social status) in free-ranging rhesus macaques. We found age-related signatures of immunosenescence, including lower proportions of CD20+ B cells, CD20+/CD3+ ratio, and CD4+/CD8+ T cell ratio – all signs of diminished antibody production. Age was associated with higher proportions of CD3+/CD8+ Cytotoxic T cells, CD16+/CD3- Natural Killer cells, CD3+/CD4+/CD25+ and CD3+/CD8+/CD25+ T cells, and CD14+/CD16+/HLA-DR+ intermediate monocytes, and lower levels of CD14+/CD16-/HLA-DR+ classical monocytes, indicating greater amounts of inflammation and immune dysregulation. We also found a sex-dependent effect of exposure to social adversity (i.e., low social status). High-status males, relative to females, had higher CD20+/CD3+ ratios and CD16+/CD3 Natural Killer cell proportions, and lower proportions of CD8+ Cytotoxic T cells. Further, low-status females had higher proportions of cytotoxic T cells than high-status females, while the opposite was observed in males. High-status males had higher CD20+/CD3+ ratios than low-status males. Together, our study identifies the strong age and sex-dependent effects of social adversity on immune cell proportions in a human-relevant primate model. Thus, these results provide novel insights into the combined effects of demography and social adversity on immunity and their potential contribution to age-related diseases in humans and other animals.
(12) Siracusa E.R., Pereira A.S, Bohr Brask J., Negron-Del Valle J.E., Phillips D., Platt M.L., Higham J.P., Snyder-Mackler N., Brent L.J.N. 2023. Ageing in a collective: The impact of ageing individuals on social network structure. Philosophical Transactions of the Royal Society B, 378: 20220061 https://doi.org/10.1098/rstb.2022.0061
Abstract: 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.
(11) Siracusa E.R., Negron-Del Valle J.E., Phillips D., Platt M.L., Higham J.P., Snyder-Mackler N., Brent L.J.N. 2022. Within-individual changes reveal increasing social selectivity with age in rhesus macaques. PNAS, 119 (49): e2209180119 https://doi.org/10.1073/pnas.2209180119
Abstract: 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.
(10) Pavez-Fox M.A., Kimock, C.M., Rivera-Barreto N., Negron-Del Valle J.E., Phillips D., Ruiz-Lambides A., Synder-Mackler N, Higham J.P., Brent L.J.N.*, Siracusa E.R.*. 2022. Reduced injury risk links sociality to survival in a group-living primate. iScience, 25 (11): 105454
https://doi.org/10.1016/j.isci.2022.105454
*equal contribution
Abstract: 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.
(9) Siracusa E.R. 2022. Social senescence in red deer. Nature Ecology and Evolution, News & Views, 6: 1062-1063 https://doi.org/10.1038/s41559-022-01766-3
Abstract: Longitudinal data spanning 43 years from a wild ungulate population reveal changes in social connectedness as individuals age, and suggest that these changes may in part be driven by changes in spatial behaviour.
(8) Martinig, A.R., Karst H.J, Siracusa E.R., Studd E.K., McAdam A.G., Dantzer B., Delaney D.M., Lane J.E., Pokharel P., Boutin S. 2022. Animal personality: a comparison of standardized assays and focal observations in North American red squirrels. Animal Behaviour, 190: 221-232 https://doi.org/10.1016/j.anbehav.2022.05.012.
Abstract: As interest in animal personality research grows, methodologies for quantifying consistent among-individual differences in behaviour are expanding. Two of the most common methods for quantifying animal personality are standardized behavioural assays and focal animal sampling. We evaluated whether assays and focals provided similar animal personality measures in a wild population of free-ranging North American red squirrels, Tamiasciurus hudsonicus, by comparing the among-individual correlations of traits between methods. Assays described two behavioural axes—one associated with movement behaviours and another associated with antagonistic behaviours towards conspecifics. Focals described two additional behavioural axes—one associated with movement and territorial behaviours, and another associated with the trade-off between vigilant and feeding behaviours. Although we found evidence of high trait repeatability for behavioural axes measured with assays, both focal behavioural axes had low trait repeatability regardless of whether among-individual differences in the social environment were controlled for (i.e. to account for ‘pseudopersonality’). We also found no among-individual correlations between assay and focal behavioural axes. The lack of correlation between methods may be because the dominant axes of variation differ between methods or because of the low trait repeatability of focals due to high behavioural plasticity. Given this, we conclude that assays will likely remain the mainstay for measuring consistent among-individual differences in behaviour given their ability to standardize for environmental conditions.
(7) Siracusa E.R., Higham J.P., Snyder-Mackler N., Brent L. J. N. 2022. Social ageing: Exploring the drivers of late-life changes in social behaviour in mammals, Biology Letters, 18: 20210643 https://doi.org/10.1098/rsbl.2021.0643.
Abstract: 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 toward 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.
(6) Fisher D.N., Kilgour R.J., Siracusa E.R., Foote J.R., Hobson E.A., Montiglio P.O., Saltz J.B., Wey T., Wice E.W. 2021. Anticipated effects of abiotic environmental change on intraspecific social interactions, Biological Reviews, 96: 2661-2693 https://doi.org/10.1111/brv.12772
Abstract: Social interactions are ubiquitous across the animal kingdom. A variety of ecological and evolutionary processes are dependent on social interactions, such as movement, disease spread, information transmission, and density-dependent reproduction and survival. Social interactions, like any behaviour, are context dependent, varying with environmental conditions. Currently, environments are changing rapidly across multiple dimensions, becoming warmer and more variable, while habitats are increasingly fragmented and contaminated with pollutants. Social interactions are expected to change in response to these stressors and to continue to change into the future. However, a comprehensive understanding of the form and magnitude of the effects of these environmental changes on social interactions is currently lacking. Focusing on four major forms of rapid environmental change currently occurring, we review how these changing environmental gradients are expected to have immediate effects on social interactions such as communication, agonistic behaviours, and group formation, which will thereby induce changes in social organisation including mating systems, dominance hierarchies, and collective behaviour. Our review covers intraspecific variation in social interactions across environments, including studies in both the wild and in laboratory settings, and across a range of taxa. The expected responses of social behaviour to environmental change are diverse, but we identify several general themes. First, very dry, variable, fragmented, or polluted environments are likely to destabilise existing social systems. This occurs as these conditions limit the energy available for complex social interactions and affect dissimilar phenotypes differently. Second, a given environmental change can lead to opposite responses in social behaviour, and the direction of the response often hinges on the natural history of the organism in question. Third, our review highlights the fact that changes in environmental factors are not occurring in isolation: multiple factors are changing simultaneously, which may have antagonistic or synergistic effects, and more work should be done to understand these combined effects. We close by identifying methodological and analytical techniques that might help to study the response of social interactions to changing environments, highlight consistent patterns among taxa, and predict subsequent evolutionary change. We expect that the changes in social interactions that we document here will have consequences for individuals, groups, and for the ecology and evolution of populations, and therefore warrant a central place in the study of animal populations, particularly in an era of rapid environmental change.
(5) Siracusa E.R., Boutin S., Dantzer B., Lane J.E., Coltman D.W., McAdam A.G. 2021. Familiar neighbors, but not relatives, enhance fitness in a territorial mammal, Current Biology 31: 438-445 https://doi.org/10.1016/j.cub.2020.10.072
Abstract: One of the outstanding questions in evolutionary biology is the extent to which mutually beneficial interactions and kin-selection can facilitate the evolution of cooperation by mitigating conflict between interacting organisms. The indirect fitness benefits gained from associating with kin are an important pathway to conflict resolution, but conflict can also be resolved if individuals gain direct benefits from cooperating with one another (e.g. mutualism or reciprocity). Owing to the kin-structured nature of many animal societies, it has been difficult for previous research to assess the relative importance of these mechanisms. However, one area that might allow for the relative roles of kin-selection and mutualistic benefits to be disentangled is in the resolution of conflict over territorial space. While much research has focused on group-living species, the question of how cooperation can first be favored in solitary, territorial species remains a key question. Using 22 years of data from a population of North American red squirrels, we assessed how kinship and familiarity with neighbors affected fitness in a territorial mammal. While living near kin did not enhance fitness, familiarity with neighbors increased survival and annual reproductive success. These fitness benefits were strong enough to compensate for the effects of aging later in life, with potential consequences for the evolution of senescence. We suggest that such substantial fitness benefits provide the opportunity for the evolution of cooperation between adversarial neighbors, offering insight into the role that mutually beneficial behaviors might play in facilitating and stabilizing social systems.
(4) Studd E.K., Menzies A.K., Siracusa E.R., Dantzer B., Lane J.E., McAdam A.G., Boutin S., Humphries M.M. 2020. Optimization of energetic and reproductive gains explains behavioural responses to environmental variation across seasons and years, Ecology Letters 23: 841-850. https://doi.org/10.1111/ele.13494
Abstract: Animals switch between inactive and active states, simultaneously impacting their energy intake, energy expenditure and predation risk, and collectively defining how they engage with environmental variation and trophic interactions. We assess daily activity responses to long‐term variation in temperature, resources and mating opportunities to examine whether individuals choose to be active or inactive according to an optimisation of the relative energetic and reproductive gains each state offers. We show that this simplified behavioural decision approach predicts most activity variation (R2 = 0.83) expressed by free‐ranging red squirrels over 4 years, as quantified through accelerometer recordings (489 deployments; 5066 squirrel‐days). Recognising activity as a determinant of energetic status, the predictability of activity variation aggregated at a daily scale, and the clear signal that behaviour is environmentally forced through optimisation of gain, provides an integrated approach to examine behavioural variation as an intermediary between environmental variation and energetic, life‐history and ecological outcomes.
(3) Siracusa E.R., Wilson D.R., Studd E.K., Boutin S., Humphries M.M., Dantzer B., Lane J.E., McAdam A.G. 2019. Red squirrels mitigate costs of territory defence through social plasticity, Animal Behaviour 151: 29-42. https://doi.org/10.1016/j.anbehav.2019.02.014
Abstract: For territorial species, the ability to be behaviourally plastic in response to changes in their social environment may be beneficial by allowing individuals to mitigate conflict with conspecifics and reduce the costs of territoriality. Here we investigated whether North American red squirrels, Tamiasciurus hudsonicus, are able to minimize costs of territory defence by adjusting behaviour in response to the familiarity of neighbouring conspecifics. Since red squirrels living in familiar neighbourhoods face reduced intrusion risk, we predicted that increasing familiarity among territorial neighbours would allow squirrels to spend less time on territorial defence and more time in the nest. Longitudinal behavioural data (1995–2004) collected from the same squirrels across several different social environments indicated that red squirrels reduced rates of territorial vocalizations and increased nest use in response to increasing familiarity with neighbours. In contrast, cross-sectional data (2015–2016), which provided observations from each individual in a single social environment, did not provide evidence of this plasticity. Post hoc analyses revealed that evidence of social plasticity in this system is primarily due to within-individual changes in behaviour, which we were unable to estimate in the cross-sectional data. Our results demonstrate that red squirrels respond to changes in their social environment by adjusting their behaviour in a manner that reduces the costs of territoriality. However, our results also suggest that estimating plasticity by comparing behaviour among individuals (i.e. cross-sectional analyses) may not always be reliable. Our ability to detect these effects may therefore depend on having data with multiple observations from the same individuals across different social environments.
(2) Siracusa E., Morandini M., Boutin S., Humphries M.M., Dantzer B., Lane J.E., & McAdam A.G. 2017. Red squirrel territorial vocalizations deter intrusions by conspecific rivals, Behaviour 154: 1259-1273. 10.1163/1568539X-00003467
Abstract: In many species, territory defense is thought to be one of the primary functions of acoustic communication. Here we used a speaker occupation experiment to test whether North American red squirrel ‘rattle’ vocalizations function to deter conspecific rivals. We studied 29 male squirrels and removed each individual from his territory twice in a paired design. During the experimental treatment we simulated the owner’s presence after its removal by broadcasting the owner’s rattle from a loudspeaker at the center of the territory. During the control treatment the territory was left in silence. We found that the presence of a speaker replacement reduced the probability of intrusion by 34% and increased the latency to first intrusion by 7%, providing support for the hypothesis that rattles reduce intrusion risk. However, intrusions were not completely averted by the speaker replacement, indicating that vocalizations alone are not sufficient without other cues of the territory owner.
(1) Siracusa E., Boutin S., Humphries M.M., Gorrell J.C., Coltman D.W., Dantzer B., Lane J.E., & McAdam A.G. 2017. Familiarity with neighbours affects intrusion risk in territorial red squirrels, Animal Behaviour 133: 11-20. https://doi.org/10.1016/j.anbehav.2017.08.024
Abstract: Interactions with conspecifics are an important aspect of an individual’s environment. Although it is well known that the presence of conspecifics can have important effects on behaviour, in general it is also now acknowledged that the composition of the social environment can vary, and that this variation may have profound effects on individual behaviour and fitness. Using a wild population of North American red squirrels (Tamiasciurus hudsonicus), we investigated the importance of the composition of the social environment in a territorial species by assessing whether the risk of intrusion faced by territory owners varied with the degree of relatedness and familiarity in their social neighbourhoods. To test this, we conducted temporary removals of territory owners and observed the time until intrusion and the identity of intruding individuals. We found that individuals in neighbourhoods with low average familiarity faced a higher risk of intrusion and that unfamiliar neighbours were more likely to intrude. Surprisingly, we found that related neighbours also posed a higher risk of intrusion. The results from our study suggest that familiarity with neighbours may be an ecologically and evolutionarily relevant measure of the social environment, even in a species considered to be ‘asocial’. Future studies should consider the potential importance of the social environment, which has heretofore been mostly overlooked, as a relevant selective pressure in asocial, territorial species.
