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).