Early life adversity and adult social relationships have independent effects on survival in a wild primate

Lange, Elizabeth C.; Zeng, Shuxi; Campos, Fernando A.; Li, Fan; Tung, Jenny; Archie, Elizabeth A.; Alberts, Susan C.

doi:10.1126/sciadv.ade7172

Cited by 18 publications

(9 citation statements)

References 122 publications

(225 reference statements)

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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, 2016, 2023; Weibel 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%

“…Females who live longer have a longer reproductive span, and are able to produce more offspring. Long-term studies have shown that early life adversity is associated with reduced survival in adult female baboons and hyenas ( Crocuta crocuta ) (Gicquel et al, 2022; Lange et al, 2023; Strauss et al, 2020; Tung et al, 2016). In populations characterized by high mortality rates prior to reproductive maturity, LRS based on the total number of offspring reaching reproductive maturity is the best proxy for fitness (e.g., Alif et al 2022).…”

Section: Introductionmentioning

confidence: 99%

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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%

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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“…Because we are less likely to observe a given grooming interaction in a large group compared to a small group, we included a measure of observer effort in our models of age at first grooming (e.g. [24,54]).…”

Section: Methods (A) Study Population and Study Subjectsmentioning

confidence: 99%

“…The importance of mothers for the development of social behaviour and fitness is also well-established in many species [3][4][5]24,25]. For example, in elephants, chimpanzees, and yellow baboons, early maternal loss, even after weaning, is associated with altered social relationships in adulthood [3][4][5]24,26] and reduced lifespan [8,10,12,24]. However, many gaps remain in our understanding of behavioural development in natural populations.…”

Section: Introductionmentioning

confidence: 99%

“…We focused on grooming because social bonds are often developed and maintained through grooming, a primary affiliative behaviour in many social species, including baboons [49][50][51][52]. Furthermore, stronger grooming relationships and/or more frequent grooming have been linked to longer lifespans in both male and female baboons [24,49,53,54]. Investigating the development of grooming behaviour can therefore shed light on how environmental and genetic sources of variance contribute to the emergence of a social behaviour with clear links to fitness.…”

Section: Introductionmentioning

confidence: 99%

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Environmental, sex-specific and genetic determinants of infant social behaviour in a wild primate

Lange,

Griffin,

Fogel

et al. 2023

Proc. R. Soc. B.

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Affiliative social bonds are linked to fitness components in many social mammals. However, despite their importance, little is known about how the tendency to form social bonds develops in young animals, or if the timing of development is heritable and thus can evolve. Using four decades of longitudinal observational data from a wild baboon population, we assessed the environmental determinants of an important social developmental milestone in baboons—the age at which a young animal first grooms a conspecific—and we assessed how the rates at which offspring groom their mothers develops during the juvenile period. We found that grooming development differs between the sexes: female infants groom at an earlier age and reach equal rates of grooming with their mother earlier than males. We also found that age at first grooming for both sexes is weakly heritable ( h 2 = 0.043, 95% CI: 0.002–0.110). These results show that sex differences in grooming emerge at a young age; that strong, equitable social relationships between mothers and daughters begin very early in life; and that age at first grooming is heritable and therefore can be shaped by natural selection.

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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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Early life adversity and adult social relationships have independent effects on survival in a wild primate

Cited by 18 publications

References 122 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

Environmental, sex-specific and genetic determinants of infant social behaviour in a wild primate

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

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