2.4 Social animal models for the biodemography of aging
 The biological pathways from social adversity to health and longevity, together with the proximate physiological and molecular mechanisms that shape these changes, are now being revealed (Cavigelli and Caruso, 2015; Snyder-Mackler et al., 2020; Shively and Wilson, 2016). Yet, the need for a unified evolutionary framework for the social determinants of health and aging across species remains. Animal models provide several advantages relative to human studies, as they allow us to record the specific nature of social relationships through direct observations without complex processes of human cultural evolution (Mesoudi and Thornton, 2018). Animal models allow us to measure the natural course of health deterioration and recovery with no interventions or significant confounding factors that may impact human outcomes (Challenge 1; Blumstein et al., 2018). Animal models also allow us to quantify nonrandom mortality risks given that each individual’s endpoint is known (Challenge 2). Finally, animal models allow us to evaluate the accuracy of health and aging forecasting models using systematic data collection methods impossible to implement in most human studies, such as survey-based research (Challenge 3; Colman, 2018). Thus, animal models provide comparative approaches that could become our gateway to explore the evolutionary origins of the social determinants of human aging and how this relates to health: whether and how our closest relatives are similarly shaped by social gradients, and why certain aging trajectories across the tree of life are shared by some but not others (Jones et al., 2014). We recognize that our human concept of aging cannot be directly transferred to numerous species, especially within social contexts, but we also emphasize that this represents an opportunity and not an occasion for disengagement (Cohen, 2018).
A call to advance studies on cross-species comparisons of social environments and their effects on health, longevity, and life histories was enthusiastically made almost a decade ago when the National Research Council of the National Academies prompted a discussion about sociality, hierarchy, and health within a comparative biodemographic perspective (Committee on Population National Research Council, 2014). Since then, several advances in our understanding of the social mechanisms of aging have highlighted the complex dynamics between social relationships and life outcomes, as well as the need to study animals with long lifespans if we intend to understand the extraordinary longevity of humans (Colchero et al., 2016; Korb and Heinze, 2021). In this section, we review recent comparative reports on the evolution of aging within social contexts that followed such call.
 While many mechanistic questions on the evolution of increased longevity remain unanswered, both physiological and social mechanisms appear to shape mortality schedules across species (Lucas and Keller, 2020; Noren Hooten et al., 2022; Snyder-Mackler et al., 2020). Evidence that sociality is associated with long lives across the tree of life has been accumulating, partly due to the recent focus of aging researchers on eusocial insects (Johnson and Carey 2014) and the counterintuitive observation that those who reproduce more also have exceptionally long lives (i.e., absence of the fecundity/longevity trade-off; Dixon et al., 2014; Heinze and Giehr, 2021; Korb et al., 2021; Kramer et al., 2021; Negroni et al., 2021; Rau and Korb, 2021; Tasaki et al., 2021). Here, the evolution of a reproductive division of labor confers strong advantage to reproductive individuals through increased survival. Transcriptome analyses revealed that experimental reproductive activation in worker honeybees increased survival through a reduction in risk of disease and increased oxidative stress resistance (Kennedy et al., 2021).  Similar patterns of resilience to oxidative stress were observed in leaf-cutting ant workers (Majoe et al., 2021) and the antTemnothorax rugatulus (Korb et al., 2021) after experimental loss of the nest’s queen. This is especially intriguing because leaf-cutting ant workers, for example, do not produce fertile offspring. Thus, such findings raise important questions regarding the evolution of improved health trajectories in queenless workers (Majoe et al., 2021).
By expanding comparative studies beyond eusocial insects, we gain further insights into whether and how multiple social dimensions including status, integration, and early life environments shape health and aging trajectories across a physiological and cognitive complexity gradient (Marmot and Sapolsky 2014). For example, social status in a cooperative breeder population of Seychelles warblers is associated to the pace of aging through a reduction in telomere attrition (a marker of cellular senescence) among dominant females, likely due to reduced costs of parental care trading-off against increased senescence (Hammers et al., 2019). The observation that breeders receiving help in raising the young age more slowly than the helpers has been observed across several taxa (Berger et al., 2018; Downing et al., 2021), although causality or associations to health remain unknown. In primates, evidence from genome-wide and multi-region transcriptomic studies show that social status affects immune regulation and aging producing evidence of antiviral phenotypes (Snyder-Mackler et al., 2016; 2018) and younger relative transcriptional ages (Chiou et al., 2022) in high-status females. However, associations among social status, health, and aging are often sex-specific and context-dependent. High-status male baboons exhibit up-regulation in inflammation and immune defense-related genes, but such traits may have been present in these males before moving up in the hierarchy (Lea et al., 2018). This complex causal relationship between socioenvironmental factors and aging trajectories was further highlighted by Anderson et al. (2021), who found that high-status males were predicted to be older than their chronological ages with respect to a DNA methylation-based age predictor (‘epigenetic clock’). High-status meerkats similarly show higher rates of both telomere attrition and survival (Cram et al., 2018). While such accelerated aging may be indicative of costs associated to higher reproductive effort in high social status individuals, this raises questions regarding the role, if any, of other social dimensions on epigenetic age across populations.
Social networks metrics, such as how integrated and connected an individual is to others in the network, have recently emerged as an important domain for understanding aging and mortality processes (Silk 2014). Social network statistics have open the opportunity to deconstruct sociality into the types of social connections that predict longevity (Ellis et al., 2019). Individuals with strong connections and central roles in the network, or those that are highly integrated, exhibit lower risks of mortality. This is potentially mediated through social security (Montero et al., 2020), mutualistic behaviors (Archie et al., 2014; Cheney et al., 2016; Ellis et al., 2019; Lehmann et al., 2015), stronger social support (Nuñez et al., 2015), and better access to social information (Ellis et al., 2017). Whether these associations between an individual’s social integration and connectedness and their life trajectory are equally conserved at old ages requires more attention. Using physiological and anatomical markers of immunity in an adult population of rhesus macaques which included aging individuals, Pavez-Fox et al. (2021) found associations between social integration and low white blood cell counts suggesting links between social integration and inflammation markers. On the other hand, increased social support through higher pack size in cooperative grey wolves was found to offset individual costs of disease (Almberg et al., 2015). The absence of an association between group size and increased senescence was also described for a socially foraging bat (Gager et al., 2016). These findings contradict long-standing hypothesized costs of group living (i.e., disease transmission, increased infection rates) and further highlights the need to revisit classical hypotheses on life history trade-offs in social animals.
Finally, several comparative studies echoing the potential role that the early life social environment has on compromising health and shaping the fate of individuals have emerged. An accumulation of adverse events early in life predicted longevity in baboons (Tung et al., 2016) and such adverse environment had intergenerational effects (Zipple et al., 2019). Early adversity was also found to elevate glucocorticoid levels in adult female baboons, a measure of stress response associated to health (Patterson et al., 2021; Rosenbaum et al., 2020). The mechanisms behind the relationship between early life adversity and health across the lifespan may involve physiological changes such as inflammation and disease risk (Kinnally et al. 2019)
These relationships between sociality, health and aging also involve complex interactions among them. Multiple species show shifts in patterns of social behavior and underlying psychological processes as individuals age (Kroeger et al., 2021; Machanda and Rosati, 2020; Siracusa et al., 2022) indicating that sociality trajectories are as varied as health and aging trajectories and likely modulated by social status, social organization, and sex. For example, while many primates show reductions in sociality during aging, in very long-lived chimpanzees older males have higher-quality relationships and are more gregarious by many metrics than are younger males, despite their lower social status (Rosati et al 2020). Thus, there are likely reciprocal causalities whereby longevity changes an individual’s social patterns, which in turn impacts senescence (Carey and Judge, 2001; Lucas and Keller, 2020). Other, contrasting patterns have also been reported. Several mammal species have shown increased mortality risk in highly connected individuals (Blumstein et al., 2018; Thompson and Cords, 2018), in cooperatively breeding species versus non-cooperative ones (Vágási et al., 2021) and in individuals lacking social support (Begall et al., 2021), suggesting that benefits from social relations may not be universal across species (Blumstein et al., 2018). Together, these patterns highlight further the need for a foundational eco-evolutionary methodological framework to study health and aging within social contexts (Lange et al., 2022).