Early maternal loss affects diurnal cortisol slopes in immature but not mature wild chimpanzees

AbstractIn mammals, early life adversity negatively affects survival and reproductive success. A key causal mechanism is proposed by the biological embedding model which posits that adversity experienced early in life has deleterious consequences on individual physiology across the lifespan. In particular, early life adversity is expected to be a severe stressor leading to long-term alteration of the hypothalamic pituitary adrenal (HPA) axis activity. Here we tested this idea by assessing whether, as in humans, maternal loss had short and long-term impacts on orphan chimpanzee urinary cortisol levels and diurnal urinary cortisol slopes, as an indicator of the HPA axis functioning. We used 18 years of data on 50 immature and 28 mature male wild chimpanzees belonging to four communities in Taï National Park, Ivory Coast. Immature orphans who experienced early maternal loss had diurnal cortisol slopes characterised by higher early morning and late afternoon cortisol levels indicative of high activation of the HPA axis. Recently orphaned immatures had higher cortisol levels than other immatures, possibly reflecting social and nutritional stress. However, unlike in humans, we did not find significantly different cortisol profiles in orphan and non-orphan adult male chimpanzees. Our study highlights that long-term alteration of stress physiology related to early life adversity may not be viable in some wild animal populations and/or that chimpanzees, as humans, may have access to mechanisms that buffer this physiological stress, such as adoption. Our results suggest that biological embedding of altered HPA axis function is unlikely to be a mechanism contributing to the demonstrated long-term fitness consequences of maternal loss, such as reduced reproductive success, in wild long-lived mammals.

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Early maternal loss leads to short- but not long-term effects on diurnal cortisol slopes in wild chimpanzees

eLife ◽

10.7554/elife.64134 ◽

2021 ◽

Vol 10 ◽

Author(s):

Cédric Girard-Buttoz ◽

Patrick J Tkaczynski ◽

Liran Samuni ◽

Pawel Fedurek ◽

Cristina Gomes ◽

...

Keyword(s):

Hpa Axis ◽

Calibration Model ◽

Wild Chimpanzee ◽

Urinary Cortisol ◽

Short Term ◽

Compensatory Mechanisms ◽

Maternal Loss ◽

Diurnal Cortisol ◽

Adaptive Calibration

The biological embedding model (BEM) suggests that fitness costs of maternal loss arise when early-life experience embeds long-term alterations to hypothalamic-pituitary-adrenal (HPA) axis activity. Alternatively, the adaptive calibration model (ACM) regards physiological changes during ontogeny as short-term adaptations. Both models have been tested in humans but rarely in wild, long-lived animals. We assessed whether, as in humans, maternal loss had short- and long-term impacts on orphan wild chimpanzee urinary cortisol levels and diurnal urinary cortisol slopes, both indicative of HPA axis functioning. Immature chimpanzees recently orphaned and/or orphaned early in life had diurnal cortisol slopes reflecting heightened activation of the HPA axis. However, these effects appeared short-term, with no consistent differences between orphan and non-orphan cortisol profiles in mature males, suggesting stronger support for the ACM than the BEM in wild chimpanzees. Compensatory mechanisms, such as adoption, may buffer against certain physiological effects of maternal loss in this species.

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Early-life adversity programs long-term cytokine and microglia expression within the HPA axis in female Japanese quail

Journal of Experimental Biology ◽

10.1242/jeb.187039 ◽

2019 ◽

Vol 222 (6) ◽

pp. jeb187039 ◽

Cited By ~ 3

Author(s):

David J. Walker ◽

Cédric Zimmer ◽

Maria Larriva ◽

Susan D. Healy ◽

Karen A. Spencer

Keyword(s):

Hpa Axis ◽

Japanese Quail ◽

Early Life ◽

Early Life Adversity

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Effects of Early-Life Adversity on Hippocampal Structures and Associated HPA Axis Functions

Developmental Neuroscience ◽

10.1159/000484238 ◽

2017 ◽

Vol 40 (1) ◽

pp. 13-22 ◽

Cited By ~ 29

Author(s):

Brigitte Dahmen ◽

Vanessa B. Puetz ◽

Wolfgang Scharke ◽

Georg G. von Polier ◽

Beate Herpertz-Dahlmann ◽

...

Keyword(s):

Hpa Axis ◽

Early Life ◽

Brain Structures ◽

Hippocampal Volume ◽

Granule Cell Layer ◽

Control Group ◽

Stress System ◽

Early Life Adversity ◽

Diurnal Cortisol ◽

Hippocampal Subfields

Early-life adversity (ELA) is one of the major risk factors for serious mental and physical health risks later in life. ELA has been associated with dysfunctional neurodevelopment, especially in brain structures such as the hippocampus, and with dysfunction of the stress system, including the hypothalamic-pituitary-adrenal (HPA) axis. Children who have experienced ELA are also more likely to suffer from mental health disorders such as depression later in life. The exact interplay of aberrant neurodevelopment and HPA axis dysfunction as risks for psychopathology is not yet clear. We investigated volume differences in the bilateral hippocampus and in stress-sensitive hippocampal subfields, behavior problems, and diurnal cortisol activity in 24 children who had experienced documented ELA (including out-of-home placement) in a circumscribed duration of adversity only in their first 3 years of life in comparison to data on 25 control children raised by their biological parents. Hippocampal volumes and stress-sensitive hippocampal subfields (Cornu ammonis [CA]1, CA3, and the granule-cell layer of the dentate gyrus [GCL-DG]) were significantly smaller in children who had experienced ELA, taking psychiatric diagnoses and dimensional psychopathological symptoms into account. ELA moderated the relationship between left hippocampal volume and cortisol: in the control group, hippocampal volumes were not related to diurnal cortisol, while in ELA children, a positive linear relationship between left hippocampal volume and diurnal cortisol was present. Our findings show that ELA is associated with altered development of the hippocampus, and an altered relationship between hippocampal volume and HPA axis activity in youth in care, even after they have lived in stable and caring foster family environments for years. Altered hippocampal development after ELA could thus be associated with a risk phenotype for the development of psychiatric disorders later in life.

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Experiences of adversity in childhood and adolescence and cortisol in late adolescence

Development and Psychopathology ◽

10.1017/s0954579421001152 ◽

2021 ◽

pp. 1-16

Author(s):

Courtenay L. Kessler ◽

Suzanne Vrshek-Schallhorn ◽

Susan Mineka ◽

Richard E. Zinbarg ◽

Michelle Craske ◽

...

Keyword(s):

Sexual Abuse ◽

Early Life ◽

Community Sample ◽

Late Adolescence ◽

Developmental Timing ◽

Cortisol Awakening Response ◽

Childhood And Adolescence ◽

Childhood Adversities ◽

Early Life Adversity ◽

Diurnal Cortisol

Abstract Early life adversity influences the diurnal cortisol rhythm, yet the relative influence of different characteristics of adversity remains unknown. In this study, we examine how developmental timing (childhood vs. adolescence), severity (major vs. minor), and domain of early life adversity relate to diurnal cortisol rhythms in late adolescence. We assessed adversity retrospectively in early adulthood in a subsample of 236 participants from a longitudinal study of a diverse community sample of suburban adolescents oversampled for high neuroticism. We used multilevel modeling to assess associations between our adversity measures and the diurnal cortisol rhythm (waking and bedtime cortisol, awakening response, slope, and average cortisol). Major childhood adversities were associated with flatter daily slope, and minor adolescent adversities were associated with greater average daily cortisol. Examining domains of childhood adversities, major neglect and sexual abuse were associated with flatter slope and lower waking cortisol, with sexual abuse also associated with higher cortisol awakening response. Major physical abuse was associated with higher waking cortisol. Among adolescent adversities domains, minor neglect, emotional abuse, and witnessing violence were associated with greater average cortisol. These results suggest severity, developmental timing, and domain of adversity influence the association of early life adversity with stress response system functioning.

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The Ecology of Stress: linking life-history traits with physiological control mechanisms in free-living guanacos

PeerJ ◽

10.7717/peerj.2640 ◽

2016 ◽

Vol 4 ◽

pp. e2640 ◽

Cited By ~ 4

Author(s):

Ramiro J.A. Ovejero Aguilar ◽

Graciela A. Jahn ◽

Mauricio Soto-Gamboa ◽

Andrés J. Novaro ◽

Pablo Carmanchahi

Keyword(s):

Life History ◽

Seasonal Variation ◽

Reproductive Success ◽

Hpa Axis ◽

Life History Traits ◽

Mating Period ◽

Entire Study ◽

Non Invasive ◽

Animal Populations

BackgroundProviding the context for the evolution of life-history traits, habitat features constrain successful ecological and physiological strategies. In vertebrates, a key response to life’s challenges is the activation of the Stress (HPA) and Gonadal (HPG) axes. Much of the interest in stress ecology is motivated by the desire to understand the physiological mechanisms in which the environment affects fitness. As reported in the literature, several intrinsic and extrinsic factors affect variability in hormone levels. In both social and non-social animals, the frequency and type of interaction with conspecifics, as well as the status in social species, can affect HPA axis activity, resulting in changes in the reproductive success of animals. We predicted that a social environment can affect both guanaco axes by increasing the secretion of testosterone (T) and Glucocorticoid (GCs) in response to individual social interactions and the energetic demands of breeding. Assuming that prolonged elevated levels of GCs over time can be harmful to individuals, it is predicted that the HPA axis suppresses the HPG axis and causes T levels to decrease, as GCs increase.MethodsAll of the data for individuals were collected by non-invasive methods (fecal samples) to address hormonal activities. This is a novel approach in physiological ecology because feces are easily obtained through non-invasive sampling in animal populations.ResultsAs expected, there was a marked adrenal (p-value = .3.4e−12) and gonadal (p-value = 0.002656) response due to seasonal variation inLama guanicoe. No significant differences were found in fecal GCs metabolites between males/females*season for the entire study period (p-value = 0.2839). Despite the seasonal activity variation in the hormonal profiles, our results show a positive correlation (p-value = 1.952e−11, COR = 0.50) between the adrenal and gonadal system. The marked endocrine (r2 = 0.806) and gonad (r2 = 0.7231) response due to seasonal variation in male guanaco individuals highlights the individual’s energetic demands according to life-history strategies. This is a remarkable result because no inhibition was found between the axes as theory suggests. Finally, the dataset was used to build a reactive scope model for guanacos.DiscussionGuanacos cope with the trade-off between sociability and reproductive benefits and costs, by regulating their GCs and T levels on a seasonal basis, suggesting an adaptive role of both axes to different habitat pressures. The results presented here highlight the functional role of stress and gonad axes on a critical phase of a male mammal’s life—the mating period—when all of the resources are at the disposal of the male and must be used to maximize the chances for reproductive success.

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The differential calibration of the HPA axis as a function of trauma versus adversity: A systematic review and p-curve meta-analyses

10.31234/osf.io/qnyr8 ◽

2021 ◽

Author(s):

Niki H. Kamkar ◽

Cassandra J Lowe ◽

J. Bruce Morton

Keyword(s):

Hpa Axis ◽

Early Life ◽

Life Experiences ◽

Curve Analysis ◽

Early Life Adversity ◽

Cortisol Reactivity ◽

Evidential Value ◽

Dsm 5 ◽

Meta Analyses ◽

The Relationship

Although there is an abundance of evidence linking the function of the hypothalamic-pituitary-adrenal (HPA) axis to adverse early-life experiences, the precise nature of the association remains unclear. Some evidence suggests early-life adversity leads to cortisol hyper-reactivity, while other evidence suggests adversity leads to cortisol hypo-reactivity. Here, we distinguish between trauma and adversity, and use p-curves to interrogate the conflicting literature. In Study 1, trauma was operationalized according to DSM-5 criteria; the p-curve analysis included 68 articles and revealed that the literature reporting associations between trauma and blunted cortisol reactivity contains evidential value. Study 2 examined the relationship between adversity and cortisol reactivity. Thirty articles were included in the analysis, and p-curve demonstrated that adversity is related to heightened cortisol reactivity. These results support an inverted U-shaped function relating severity of adversity and cortisol reactivity, and underscore the importance of distinguishing between “trauma” and “adversity”.

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Early and late life events and salivary cortisol in older persons

Psychological Medicine ◽

10.1017/s0033291709991863 ◽

2009 ◽

Vol 40 (9) ◽

pp. 1569-1578 ◽

Cited By ~ 32

Author(s):

L. Gerritsen ◽

M. I. Geerlings ◽

A. T. F. Beekman ◽

D. J. H. Deeg ◽

B. W. J. H. Penninx ◽

...

Keyword(s):

Life Events ◽

Hpa Axis ◽

Early Life ◽

Older Persons ◽

Late Life ◽

Analysis Of Covariance ◽

Diurnal Variability ◽

Morning Cortisol ◽

Cortisol Levels ◽

Early Life Events

BackgroundIt has been hypothesized that stressful life events are associated with changes in hypothalamic–pituitary–adrenal (HPA) axis regulation, which increases susceptibility to psychiatric disorders. We investigated the association of early and late life events with HPA axis regulation in older persons.MethodWithin the Longitudinal Aging Study Amsterdam (LASA) 1055 participants (47% male), aged 63–93 years, collected saliva within 30 min after waking and late in the evening. Early and late life events were assessed during a home interview. The associations between life events and cortisol levels were examined using linear regression and analysis of covariance with adjustments for demographics, cardiovascular risk factors and depressive symptoms.ResultsWithin our sample, the median morning and evening cortisol levels were 15.0 nmol/l [interdecile range (10–90%): 7.4–27.0 nmol/l] and 2.8 nmol/l (10–90%: 1.5–6.3 nmol/l), respectively. Persons who reported early life events showed lower levels of natural log-transformed morning cortisol [B=−0.10, 95% confidence interval (CI) −0.17 to −0.04] and flattened diurnal variability of cortisol (B=−1.06, 95% CI −2.05 to −0.08). Those reporting two or more late life events showed higher levels of natural log-transformed morning cortisol (B=0.10, 95% CI 0.02–0.18) and higher diurnal variability (B=1.19, 95% CI 0.05–2.33). No associations were found with evening cortisol.ConclusionsThe results of this large population-based study of older persons suggest a differential association of early and late life events with HPA axis regulation; early life events were associated with a relative hypo-secretion of morning cortisol and flattened diurnal variability, while late life events were associated with elevated secretion of morning cortisol and high diurnal variability of cortisol.

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Early-Life Adversity and Dysregulation of Adult Diurnal Cortisol Rhythm

The Journals of Gerontology Series B ◽

10.1093/geronb/gby097 ◽

2018 ◽

Vol 74 (1) ◽

pp. 160-169 ◽

Cited By ~ 6

Author(s):

Arun S Karlamangla ◽

Sharon Stein Merkin ◽

David M Almeida ◽

Esther M Friedman ◽

Jacqueline A Mogle ◽

...

Keyword(s):

Early Life ◽

Parental Education ◽

Dynamic Range ◽

Family Welfare ◽

Cortisol Secretion ◽

Early Life Adversity ◽

Diurnal Cortisol ◽

Welfare Dependence ◽

The Impact ◽

Diurnal Dynamic

Abstract Objectives Exposure to life stresses can lead to diminution in the capacity of stress response systems to mount a robust response to new challenges, with blunting of dynamic range—the spread between maximal attainable and minimal resting levels. We investigate the association between early-life adversity and the dynamic range of adult diurnal cortisol secretion. Method In 35- to 86-year-old adults, cortisol assayed from 16 saliva samples over 4 consecutive days was used to compute diurnal dynamic range and area under the curve (AUC). Economic adversity in childhood was indexed by recalled parental education, family welfare dependence, and perceived financial status; and childhood social adversity by parental separation, death, and abuse. Results Adjusted for age, gender, and race/ethnicity, both childhood adversities were strongly associated with smaller adult cortisol diurnal dynamic range, but not with AUC. The association with cortisol dynamic range was explained by adult social and economic variables. Discussion Early-life adversity appears to leave a long-term imprint on cortisol secretion dynamics, reducing diurnal dynamic range without increasing total secretion. This points to the importance of examining the adaptation capacity of physiological systems when studying the impact of early-life and chronic stresses on adult health.

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