Early life adversities and lifelong health outcomes: A review of the literature on large, social, long-lived nonhuman mammals

Dettmer, Amanda M.; Chusyd, Daniella E.

doi:10.1016/j.neubiorev.2023.105297

Cited by 16 publications

(9 citation statements)

References 186 publications

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“…This is further supported by studies in dogs from poorly run large‐scale breeding operations or hoarding situations that have less desirable behaviors as adults and worse mental and physical health scores than dogs from other sources (McMillan et al., 2011, 2016; McMillian et al., 2017; Stella et al., 2019; Wauthier & Williams, 2018). This study supports the ill effects of ELS into adulthood in domestic dogs as demonstrated in other social species (for review, see Dettmer & Chusdy, 2023). Animals and humans that have experienced ELS or adversity often display behavioral and physiological differences well into adulthood.…”

Section: Discussionsupporting

confidence: 87%

A dog's life: Early life histories influence methylation of glucocorticoid (NR3C1) and oxytocin (OXTR) receptor genes, cortisol levels, and attachment styles

Awalt,

Boghean,

Klinkebiel

et al. 2024

Developmental Psychobiology

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Early life deprivation and stress can contribute to life‐long, problematic consequences, including epigenetic variations related to behavior and health. Domestic dogs share human environments and social–cognitive traits, making them a promising comparative model to examine developmental plasticity. We examined 47 owner–dog dyads, including dogs rescued from abusive or neglectful environments, and matched control dogs for changes in DNA methylation of glucocorticoid (NR3C1) and oxytocin (OXTR) receptor genes previously shown to be affected by early life stress in other species including humans. We used an attachment paradigm, which included a separation event to examine cortisol levels and owner–dog attachment styles. Overall, dogs with adverse histories had different NR3C1 methylation patterns as a function of age and less OXTR methylation than comparison dogs. Dogs with adverse histories did not differ in their cortisol change from baseline to poststressor from comparison dogs, but the change in cortisol was associated with NR3C1 methylation. In addition, dogs with a history of early life stress had more insecure attachment styles; for every unit increase of OXTR methylation, the odds increased for insecure attachment style. This study demonstrates that adverse life histories lead to methylation differences, resulting in the hypothalamic–pituitary–adrenal (HPA) axis's dysregulation and differences in behavioral phenotypes.

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Section: Discussionsupporting

confidence: 87%

A dog's life: Early life histories influence methylation of glucocorticoid (NR3C1) and oxytocin (OXTR) receptor genes, cortisol levels, and attachment styles

Awalt,

Boghean,

Klinkebiel

et al. 2024

Developmental Psychobiology

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“…However, this research faces challenges such as the prevalence of confounding variables like smoking and job insecurity, the difficulty of disentangling effects of different adverse experiences which tend to co-occur, and a reliance on retrospective surveys, which are prone to recall and reporting bias. Animal studies can help overcome these challenges because non-human species are characterized by simpler systems with fewer confounding variables and less clustering of different types of adversity, and non-human animals tend to have shorter lifespans, which allows researchers to observe individuals from birth to death (Dettmer & Chusyd, 2023; Patterson et al, 2023; Snyder-Mackler et al, 2020). Research on early life adversity in other species, especially natural populations, can shed light on the evolutionary pressures shaping early life sensitivities and provide the opportunity to disentangle confounding and correlated environmental factors.…”

Section: Discussionmentioning

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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“…Indeed, across taxa, shortened lifespans appear to be a common consequence of early life adversity, accounting for a significant proportion of the studies that provide evidence for DC (e.g. red squirrels: [73]; chimpanzees: [78]; Asian elephants: [79]; hyenas: [80]; reviewed in [26, 39]). Consequently, for long-lived species like primates, lifespan analyses will likely be crucial to understanding the extent to which early life adversity compromises fitness.…”

Section: Discussionmentioning

confidence: 99%

“…In animals with slow life histories, there is more empirical support for developmental constraints than for adaptive response hypotheses [reviewed in 14,16,25]. Many studies have found that organisms do worse on a variety of fitness-relevant outcomes when they experience poor-quality developmental environments [6,26], something we examine in more detail in the discussion (Section 4). However, it is difficult to know which hypothesis (or hypotheses) best explain this relationship.…”

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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Early life adversities and lifelong health outcomes: A review of the literature on large, social, long-lived nonhuman mammals

Cited by 16 publications

References 186 publications

A dog's life: Early life histories influence methylation of glucocorticoid (NR3C1) and oxytocin (OXTR) receptor genes, cortisol levels, and attachment styles

A dog's life: Early life histories influence methylation of glucocorticoid (NR3C1) and oxytocin (OXTR) receptor genes, cortisol levels, and attachment styles

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

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