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

Tung, Jenny; Lange, Elizabeth C.; Alberts, Susan C.; Archie, Elizabeth A.

doi:10.1016/j.neubiorev.2023.105282

Cited by 13 publications

(3 citation statements)

References 156 publications

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“…Early life adversity in female baboons (Papio sp.) is associated with reduced fecundity and poorer offspring survival (Lange et al, 2023;Lea et al, 2015;Patterson et al, 2021;Tung et al, 2016Tung et al, , 2023Weibel et al, 2020;Zipple et al, 2019). Organisms are hypothesized to adjust their developmental trajectories in response to early life adversity in order to improve immediate survival (Lea et al, 2017;Lea & Rosenbaum, 2020;Patterson, Petersen et al, 2023), but such adjustments may lead to these detrimental outcomes in adulthood.…”

Section: Introductionmentioning

confidence: 99%

Early life adversity has sex-dependent effects on survival across the lifespan in rhesus macaques

Patterson,

Andonov,

Arre

et al. 2023

Preprint

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Exposure to adversity during early life is linked to lasting detrimental effects on evolutionary fitness across many taxa. However, due to the challenges of collecting longitudinal data, especially in species where one sex disperses, direct evidence from long-lived species remains relatively scarce. Here we test the effects of early life adversity on male and female longevity in a free-ranging population of rhesus macaques (Macaca mulatta) at Cayo Santiago, Puerto Rico. We leveraged six decades of data to quantify the relative importance of ten forms of early life adversity for 6,599 macaques (3,230 male, 3,369 female), with a smaller sample size (N=299) for one form of adversity (maternal social isolation) which required high-resolution behavioral data. We found that individuals who experienced more early life adversity died earlier than those who experienced less adversity. Mortality risk was highest during early life, defined as birth to four years old, suggesting acute survival effects of adversity, but heightened mortality risk was also present in macaques who survived to adulthood. Females and males were affected differently by some forms of adversity, and these differences might be driven by varying energetic demands, female philopatry, and male dispersal. By leveraging data on thousands of macaques collected over decades, our results show that the fitness consequences of early life adversity are not uniform across individuals but vary as a function of the type of adversity, timing, and social context, and thus contribute to our limited but growing understanding of the evolution of early life sensitivities in long-lived species.

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Section: Introductionmentioning

confidence: 99%

Early life adversity has sex-dependent effects on survival across the lifespan in rhesus macaques

Patterson,

Andonov,

Arre

et al. 2023

Preprint

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“…Finally, the relative lack of evidence we find for effects of early life adversity on fertility measures suggests that shortened lifespans are the primary mechanism by which early adversity might decrease lifetime fitness. Prior analyses have demonstrated that experiencing more sources of early life adversity, including drought and being born to a low-ranking mother, leads to markedly shorter lifespans in this baboon population [4, 37, 77]. Lifespan is by far the single biggest contributor to females’ lifetime reproductive success, explaining 80-90% of the observed variation in the Amboseli population [57, 77].…”

Section: Discussionmentioning

confidence: 99%

“…Additionally, because this population has been prospectively studied for multiple generations, now spanning more than 50 years, the types of data necessary to investigate the long-term effects of early life are available. Notably, relationships between early life experiences and later life outcomes, including life history traits like fertility and mortality, are also well-established for this study system [e.g., 4,34,35,36,37].…”

Section: Introductionmentioning

confidence: 99%

Testing frameworks for early life effects: the developmental constraints and adaptive response hypotheses do not explain key fertility outcomes in wild female baboons

Rosenbaum,

Malani,

Lea

et al. 2024

Preprint

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In evolutionary ecology, two classes of explanations are frequently invoked to explain "early life effects" on adult outcomes. Developmental constraints (DC) explanations contend that costs of early adversity arise from limitations adversity places on optimal development. Adaptive response (AR) hypotheses propose that later life outcomes will be worse when early and adult environments are poorly "matched." Here, we use recently proposed mathematical definitions for these hypotheses and a quadratic-regression based approach to test the long-term consequences of variation in developmental environments on fertility in wild baboons. We evaluate whether low rainfall and/or dominance rank during development predict three female fertility measures in adulthood, and whether any observed relationships are consistent with DC and/or AR. Neither rainfall during development nor the difference between rainfall in development and adulthood predicted any fertility measures. Females who were low-ranking during development had an elevated risk of losing infants later in life, and greater change in rank between development and adulthood predicted greater risk of infant loss. However, both effects were statistically marginal and consistent with alternative explanations, including adult environmental quality effects. Consequently, our data do not provide compelling support for either of these common explanations for the evolution of early life effects.

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Using non-invasive behavioral and physiological data to measure biological age in wild baboons

Weibel,

Dasari,

Jansen

et al. 2024

GeroScience

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Biological aging is near-ubiquitous in the animal kingdom, but its timing and pace vary between individuals and over lifespans. Prospective, individual-based studies of wild animals—especially non-human primates—help identify the social and environmental drivers of this variation by indicating the conditions and exposure windows that affect aging processes. However, measuring individual biological age in wild primates is challenging because several of the most promising methods require invasive sampling. Here, we leverage observational data on behavior and physiology, collected non-invasively from 319 wild female baboons across 2402 female-years of study, to develop a composite predictor of age: the non-invasive physiology and behavior (NPB) clock. We found that age predictions from the NPB clock explained 51% of the variation in females’ known ages. Further, deviations from the clock’s age predictions predicted female survival: females predicted to be older than their known ages had higher adult mortality. Finally, females who experienced harsh early-life conditions were predicted to be about 6 months older than those who grew up in more benign conditions. While the relationship between early adversity and NPB age is noisy, this estimate translates to a predicted 2–3 year reduction in mean adult lifespan in our model. A constraint of our clock is that it is tailored to data collection approaches implemented in our study population. However, many of the clock’s components have analogs in other populations, suggesting that non-invasive data can provide broadly applicable insight into heterogeneity in biological age in natural populations.

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

Cited by 13 publications

References 156 publications

Early life adversity has sex-dependent effects on survival across the lifespan in rhesus macaques

Early life adversity has sex-dependent effects on survival across the lifespan in rhesus macaques

Testing frameworks for early life effects: the developmental constraints and adaptive response hypotheses do not explain key fertility outcomes in wild female baboons

Using non-invasive behavioral and physiological data to measure biological age in wild baboons

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