Early-life social adversity and developmental processes in nonhuman primates

French, Jeffrey A.; Carp, Sarah B.

doi:10.1016/j.cobeha.2015.11.004

Cited by 32 publications

(33 citation statements)

References 47 publications

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“…Given the centrality, complexity, and life-time continuity of social relationships in primates (Platt, Seyfarth, & Cheney, 2016; Silk, Cheney, & Seyfarth, 2013), it should come as no surprise that separation from significant social partners produces a host of neurobiological and behavioral perturbations during the period of separation (French & Carp, 2016; Meyer & Hamel, 2014). Affiliative and prosocial interactions with social partners following separation are critical for the reestablishment of normative relationship dynamics (Fernandez-Duque, Mason, & Mendoza, 1997; Sheperd & French, 1999; Taylor, Mustoe, Hochfelder, & French, 2015).…”

Section: | Introductionmentioning

confidence: 99%

Oxytocin regulates reunion affiliation with a pairmate following social separation in marmosets

Cavanaugh

Mustoe

French

2018

American J Primatol

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While separation from significant social partners produces a host of neurobiological and behavioral perturbations, including behavioral distress and increased glucocorticoid production, positive social interactions upon reunion are critical for the reestablishment of normative relationship dynamics and the attenuation of the biobehavioral stress response. The hormone oxytocin has critical and pervasive roles in reproductive and behavioral processes across the lifespan, and plays a particularly prominent role in social bonding. In this study, we examined the extent that oxytocin modulates interactions with a pairmate following separation challenges that varied in both social context (isolation; separation) and duration (long; short), in marmosets. We demonstrated that the impact of pharmacological manipulations of the oxytocin system on the expression of affiliation upon reunion depended on both the context and duration of the separation challenge. Specifically, marmosets treated with an oxytocin antagonist spent less time in proximity with their pairmate upon reunion following a long-separation challenge. During the short-separation challenge, marmosets engaged in more social gaze when separated with an opposite-sex stranger, but not when separated with their mate. Furthermore, marmosets that received the most social gaze from opposite-sex strangers spent the most time in proximity with their long-term mate upon reunion. We also showed that marmosets treated with an OT agonist received increased levels of gaze from opposite-sex strangers, but not from their mate. Overall, these results suggest that marmosets are sensitive to the nature of the social interactions during separation, and subsequently alter their expression of affiliation upon reunion with their long-term mate. These findings further implicate oxytocin as a bond-enhancing molecule that regulates the reestablishment of normative levels of affiliation with a mate following separation, and add to the emerging literature that suggests the OT system underlies critical behavioral processes that contribute to the preservation of long-lasting social bonds.

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Section: | Introductionmentioning

confidence: 99%

Oxytocin regulates reunion affiliation with a pairmate following social separation in marmosets

Cavanaugh

Mustoe

French

2018

American J Primatol

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“…In line with the majority of the theoretical literature, we assume that helping is assumed to increase the fecundity of the reproductives in the local group [27]. The helping tendency expressed by a newborn can then evolve to become dependent on the number of helpers in the local patch present at the time of birth, reflecting the results of empirical studies in which developmental plasticity is based on the current social structure of the local group (e.g., [4,28,29]). We then study whether social behaviours are indeed likely to become sensitive to social experience in early life, and if so, what form such developmental plasticity takes.…”

Section: Introductionmentioning

confidence: 95%

“…In many taxa, the social environment experienced during early life gives rise to predictable between-individual differences in adult social behaviour [1][2][3][4][5]. For example, in many rodents, individuals who have received limited parental care also provide less parental care themselves to their own offspring [6,7].…”

Section: Introductionmentioning

confidence: 99%

The Evolution of Early-Life Effects on Social Behaviour – Why Should Social Adversity Carry Over to the Future?

Kuijper

Johnstone

2018

Preprint

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Numerous studies have shown that social adversity in early life can have long-lasting negative consequences for social behaviour in adulthood, consequences that may in turn be propagated to future generations. Given these intergenerational effects, it is puzzling why natural selection might favour such sensitivity to an individual's early social environment. To address this question, we model the evolution of social sensitivity in the development of in helping behaviours, showing that natural selection indeed favours individuals whose tendency to help others is dependent on early-life social experience. We find that natural selection typically favours positive social feedbacks, in which individuals who received more help in early life are also more likely to help others in adulthood, while individuals who received no early-life help develop low tendencies to helping others later in life. This positive social sensitivity is favoured because of an intergenerational relatedness feedback: patches with many helpers tend to be more productive, leading to higher relatedness within the local group, which in turn favours higher levels of help in the next generation.Keywords: predictive adaptive response, developmental plasticity, inclusive fitness, maternal effect, parental effect, intergenerational effect Running title: Early life effects on social behaviour

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“…Human biologists, epidemiologists, and primatologists have long been aware that adversity during early life can profoundly impact development and the resulting adult phenotype. Famine during prenatal life has been repeatedly linked to diseases such as hypertension, diabetes, and depression, and exposure to nutritional (e.g., drought) and social stressors (e.g., isolation, abusive parenting) during early life have been associated with altered social development, dysregulation of the hypothalamic–pituitary–adrenal (HPA) axis, and reduced longevity and birth rate…”

Section: Introductionmentioning

confidence: 99%

Developmental responses to early‐life adversity: Evolutionary and mechanistic perspectives

Petrullo

Carrera

et al. 2019

Evolutionary Anthropology

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Adverse ecological and social conditions during early life are known to influence development, with rippling effects that may explain variation in adult health and fitness. The adaptive function of such developmental plasticity, however, remains relatively untested in long‐lived animals, resulting in much debate over which evolutionary models are most applicable. Furthermore, despite the promise of clinical interventions that might alleviate the health consequences of early‐life adversity, research on the proximate mechanisms governing phenotypic responses to adversity have been largely limited to studies on glucocorticoids. Here, we synthesize the current state of research on developmental plasticity, discussing both ultimate and proximate mechanisms. First, we evaluate the utility of adaptive models proposed to explain developmental responses to early‐life adversity, particularly for long‐lived mammals such as humans. In doing so, we highlight how parent‐offspring conflict complicates our understanding of whether mothers or offspring benefit from these responses. Second, we discuss the role of glucocorticoids and a second physiological system—the gut microbiome—that has emerged as an additional, clinically relevant mechanism by which early‐life adversity can influence development. Finally, we suggest ways in which nonhuman primates can serve as models to study the effects of early‐life adversity, both from evolutionary and clinical perspectives.

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Early-life social adversity and developmental processes in nonhuman primates

Cited by 32 publications

References 47 publications

Oxytocin regulates reunion affiliation with a pairmate following social separation in marmosets

Oxytocin regulates reunion affiliation with a pairmate following social separation in marmosets

The Evolution of Early-Life Effects on Social Behaviour – Why Should Social Adversity Carry Over to the Future?

Developmental responses to early‐life adversity: Evolutionary and mechanistic perspectives

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