Social and early life determinants of survival from cradle to grave: A case study in wild baboons

Abstract

Field studies of natural mammal populations present powerful opportunities to investigate the determinants of health and aging using fine-grained observations of known individuals across the life course. Here, we synthesize five decades of findings from one such study: the wild baboons of the Amboseli ecosystem in Kenya. First, we discuss the profound associations between early life adversity, adult social conditions, and key aging outcomes in this population, especially survival. Second, we review potential mediators of the relationship between early life adversity and survival in our population. Notably, our tests of two leading candidate mediators-social isolation and glucocorticoid levels-fail to identify a single, strong mediator of early life effects on adult survival. Instead, early adversity, social isolation, and glucocorticoids are independently linked to adult lifespans, suggesting considerable scope for mitigating the negative consequences of early life adversity. Third, we review our work on the evolutionary rationale for early life effects on mortality, which currently argues against clear predictive adaptive responses. Finally, we end by highlighting major themes emerging from the study of sociality, development, and aging in the Amboseli baboons, as well as important open questions for future work.

Keywords: Baboon; Early life adversity; Life course studies; Social determinants of health; Social relationships.

Figure 1.. Conceptual model illustrating how early life environments affect adult social conditions and biodemographic outcomes.

Conditions in early life, including environments linked to resource deprivation, threat, or both, have lifelong consequences for adult physiology, social status, and social connectedness. In turn, the physical and social consequences of early life adversity can have profound effects on outcomes relevant to human health and evolution, including reproductive timing and pace, disease risk, lifespan, and Darwinian fitness. Finally, intergenerational effects can propagate early life adversity across generations to shape offspring outcomes across the lifespan.

Figure 2.. Motivating discoveries on social and early life determinants of health and survival in the Amboseli baboon population.

(A) Female baboons who maintain stronger social connections (measured in terms of overall affiliative sociality) with their female groupmates experience greater longevity (Archie et al., 2014). Not shown is the parallel observation that females who maintain stronger social connections to adult males also experience greater longevity (Archie et al., 2014; Campos et al., 2020). The solid red survival curve indicates females at the lower 25th percentile for social connectedness, while the blue dashed curve are females at the upper 75th percentile for social connectedness. (B) Cumulative adversity in early life (prior to age 4 years) has profound effects on adult female longevity (Tung et al., 2016). Survival curves represent individuals experiencing zero, one, two, or three or more sources of adversity. Median age at death for females who reached age five years after experiencing three or more sources of adversity was 8.85 years, compared to >18.6 years for females who experienced 0 or 1 sources of adversity. (C) The experience of early life adversity is also linked to social isolation from female group mates in adulthood (Tung et al., 2016). The y-axis reflects the strength of female social connectedness relative to all other females alive in the population in the same year, with low values indicating relative social isolation. Colors are the same as in panel B. Heavy lines in the middle of each box mark the median, the top and bottom edges mark the 25th and 75th percentiles, and whiskers are the largest or smallest values at 1.5 times the interquartile range.

Figure 3.. Network of observed correlations between individual early life environments, adult social conditions, and adult physiological and demographic outcomes.

Panel A shows observed correlations in females, and panel B shows correlations in males. The primary variables of interest in this manuscript—early life conditions, social conditions, and demographic outcomes—are in black-outlined boxes, while other phenotypes correlated with these primary variables are in white boxes without outlines (e.g., hormones, gene expression, growth). Unless otherwise noted, early life adversity refers to an individual’s cumulative adversity score (Box 2). The ‘gene regulation’ box here includes patterns of DNA methylation and gene expression levels, including in response to ex vivo immune stimulation. Arrows are colored to denote the qualitative strength and sign of the correlation between the two variables. Dashed white lines are correlative relationships that have not yet been tested. In these analyses, we control for age-related differences in predictors (e.g., social relationships, which can weaken with age: Archie et al., 2014) or outcome variables (e.g., glucocorticoid levels, which increase with age: Campos et al., 2021) by either including it as a covariate, examining the outcome as a function of age itself, or using time-varying survival analyses. Numbers on arrows reflect the references that report evidence for the correlation: 1=Silk et al., 2003; 2=Alberts et al., 2006; 3=Gesquiere et al., 2011; 4=Archie et al., 2014; 5=Lea et al., 2014; 6=Lea et al., 2015; 7=Tung et al., 2016; 8=Onyango et al., 2008; 9=Zipple et al., 2019; 10=Campos et al., 2020; 11=Levy et al., 2020; 12=Rosenbaum et al., 2020; 13=Weibel et al., 2020; 14=Campos et al., 2021; 15=Zeng et al., 2021; 16=Lange et al., 2023; 17=Zeng et al., 2022; 18=Anderson et al., 2022; 19=Anderson et al., 2023; 20=Creighton et al., in prep; 21=Lea et al., 2018; 22=Anderson et al., 2021; 23=Levy et al., 2023 3* – Gesquiere et al. 2011 – alpha males have higher fecal GC concentrations compared to all other adult males 8* – Onyango et al. 2008 found that sons of low-ranking mothers had elevated fGC concentrations as sub-adults. This paper did not test other sources of early life adversity. 18, 21* and 18,19,21* - The effects of dominance rank on gene expression are stronger in males and directionally opposite in males versus females; genes that are more highly expressed in high-ranking females tended to be more lowly expressed in high-ranking males and vice-versa. 23* – Levy et al. (2023) found that the experience of early life drought is linked to shorter long bones, but there were no detectable effects of other sources of early life adversity