Understanding age and society using natural populations

Age-related declines in phenotypic traits are widely documented in natural populations, but less is known about how social behaviour changes across the lifespan. Given that social relationships are central to the biological fitness of many group-living animals, understanding why ‘social ageing’ occurs and what the associated consequences are is important for integrating sociality into our broader understanding of the ageing process. Here, Dr Siracusa explores within-individual age-based changes in sociality using eight years of behavioural data from a population of free ranging rhesus macaques (Macaca mulatta) on the island of Cayo Santiago. In this talk she will discuss how social interactions and social relationships change with age in female macaques and will provide evidence that age-based reductions in sociality may not simply be the consequence of senescent declines but might be a proactive response to the physiological and energetic constraints that come with age. She will then discuss how these age-based changes in social behaviour can feed up to influence an individual’s indirect connectedness in their network and overall patterns of network structure. Overall, Dr Siracusa will show that age has the potential to play an important and underappreciated role in the structure and function of animal societies, which warrants further research. 

That social environments can influence ageing is perhaps intuitive in animals with complex societies such as group living mammals, birds or eusocial insects. For example, we might easily predict that an obligate colony-living ant might find social isolation highly stressful, resulting in shortened lifespan. However, it is becoming increasingly apparent that social effects on ageing patterns are seen in animals not classically considered “social”. Drosophila melanogaster fruit flies, a major model in understanding the genetic drivers of ageing, are one such animal. There is growing evidence that fruit flies are highly sensitive to their social environments, including in terms of ageing. In D. melanogaster, patterns of both lifespan and senescence of various traits respond to different types of social contact. In common with other animals including humans, fruit flies show sex differences in response to the same type of social contact. Moreover, being such a tractable model enables us to take a mechanistic approach, to begin to understand how social information is integrated at a molecular level. In this way, work in fruit flies complements evidence from animals more easily studied in the wild, and might lead us to reassess what we regard as a “social animal”.

Changes in social behaviour with age are almost ubiquitous; consequently, variation in population age-structure will determine the overall social organisation of groups, and how social processes operate within them. Here, the authors first assess previous research into age-related effects on social processes with the aim to better understand how a population’s age-structure might influence its social functioning. They propose the potential of using data from natural populations in concert with a social network approach to uncover the causes and consequences of this relationship. Secondly, the authors present ongoing work in a model system of investigating age-structure and sociality: a long-term study of wild great tits (Parus major). They demonstrate how population-level breeding behaviour is mediated by fluctuations in age-structure, as variation in age-assortative pairing is driven by the proportion of juveniles in the population. The authors also present initial findings evaluating spatio-temporal variation in age-structure and how this relates to the formation of territories and emerging neighbourhoods that are assorted by age. Understanding the consequences of age-structure is important as anthropogenic-driven changes may lead to demographic shifts in natural populations. Thus, advancing our knowledge of age-structure will deepen our understanding of how societies age and the potential social implications across systems.

Longitudinal studies of various vertebrate populations increasingly provide evidence for age-specificity of phenotypic traits, with initial improvements in early life usually being followed by senescent declines late in life. Studies of social influences on phenotypic traits are similarly abundant and for example provide evidence for effects of partners, helpers, neighbour familiarity or density on a multitude of phenotypic traits. Interactions between effects of ageing and the social environment, however, have received less empirical attention. In this talk, the authors therefore ask whether individuals show changes in plasticity in response to density as they grow older, and test whether the answer to this question depends on the level at which density is assessed. Hereto, the authors use data obtained from a long-term longitudinal study on a long-lived seabird, the common tern Sterna hirundo, and use laying date, an important determinant of fitness, as our phenotypic trait of interest.

Maria Moiron and Sandra Bouwhuis

Institute of Avian Research, Wilhelmshaven, Germany

In group living animals, social integration is crucial for health and wellbeing. Age-based differences in sociality have been documented in several mammalian systems; however, the potential drivers of social ageing are still poorly understood. Age-related declines in energy regulation may limit individuals’ movement and therefore their ability to socially interact or the likelihood of others coming into social contact, leading to reductions in the quality and quantity of social relationships. Empirical tests of these predictions are lacking, due to methodological limitations. Dr Fürtbauer will present ongoing work on wild chacma baboons (Papio ursinus) combining non-invasive endocrine proxies of energy balance and metabolic rate with measures of physical activity, movement, and sociality derived from high-resolution GPS and tri-axial acceleration data.

Social interactions are a behavioural trait that is subject to natural selection, and thus the nature of these interactions can be understood as an adaptive response to the problems animals face. Attempts to ground social interactions from theoretical foundations have focused on the fitness consequences for individuals applying different interaction rules, while typically taking group membership as a given. This ignores how the decisions individuals make shape which groups they subsequently find themselves in, and thus the role that group maintenance may play in those decisions. In this talk the author will describe a theory of social decision making in which agents rationally seek to maximise their long-term payoffs, by balancing immediate rewards and the long-term benefits of remaining in a cohesive group. By varying the effective time horizon of the agents, we can generate different solutions to this trade-off, explore the social consequences of an increasing long-lived population and likely changes in social behaviour as individuals age.

Ageing is a near-ubiquitous process across the animal kingdom that presents a mounting problem for human health. As animals age (ie “senesce”), they generally experience substantial age-related declines in a variety of immune traits (“immunosenescence”). Because one of the immune system’s main roles is to defend against pathogens, these age-related changes in immunity may have important ramifications for infection status. However, despite these well-appreciated impacts of age on immunity, we have a much shallower appreciation of age-related changes in behaviour, their effects on exposure to pathogens, and the implications for infection. As such, we have a relatively weak understanding of behaviour’s role in influencing the burden of infection in the elderly, both in humans and in wild animals.

Building on a recent surge of interest in behavioural declines over the lifespan (“social ageing”), Gregory Albery will outline how within-individual changes in behaviour and immunity can interact with and counteract one another, and their emergent impacts for population-level social network structure, infection dynamics, and (therefore) host-pathogen coevolution. Using wild systems of long-lived mammals as case studies, the author will outline empirical examples of interactions between ageing, behaviour, immunity, and infection, as well as providing evidence for time-staggered interactions between early life infections with certain parasites, late life infections with different parasites, and their emergent impacts on fitness. Finally, he will describe a framework for using individual-level ageing trajectories and emergent generative social network models to interrogate and decipher these trends. Ultimately, the combined evidence may allow us to examine how age structuring and adaptive changes in behaviour and immunity can contribute to populations’ resilience to epidemics of novel pathogens, particularly with regards to respiratory pathogens exhibiting highly age-skewed morbidity and mortality.