Early-life social experience affects offspring DNA methylation and later life stress phenotype

Laubach, Zachary M.; Greenberg, Julia; Turner, Julie W.; Montgomery, Tracy M.; Pioon, Malit O.; Sawdy, Maggie A.; Smale, Laura; Cavalcante, Raymond G.; Padmanabhan, Karthik Ramaswamy; Lalancette, Claudia; vonHoldt, Bridgett M.; Faulk, Christopher; Dolinoy, Dana C.; Holekamp, Kay E.; Perng, Wei

doi:10.1038/s41467-021-24583-x

Cited by 17 publications

(19 citation statements)

References 110 publications

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“…The prenatal and post-natal context can therefore drive phenotypic adjustments to environmental conditions, and can become an instructive factor during development [10]. Recently, a lot of attention has been paid to the social component of the early-life environment, as the number and type of social interactions that newly born individuals have with their parents, siblings or other conspecifics ('interacting phenotypes' sensu [11]) can have a major impact on a suite of behavioural traits such as exploratory behaviour, aggressive behaviour, sociability, anxiety, learning ability and personality traits [12][13][14][15][16].…”

Section: Introductionmentioning

confidence: 99%

Growing up in a crowd: social environment shapes the offspring's early exploratory phenotype in a colonial breeding species

et al. 2022

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In colonial breeding species, the number of adverse social interactions during early life typically varies with breeding density. Phenotypic plasticity can help deal with this social context, by allowing offspring to adjust their behaviour. Furthermore, offspring may not be unprepared since mothers can allocate resources to their embryos that may pre-adjust them to the post-hatching conditions. Thus, we hypothesize that lesser black-backed gull chicks raised in dense breeding areas, with greater exposure to intra-specific aggression, show higher levels of anxiety and lower levels of exploration compared to chicks in low-density areas, and that this is facilitated by prenatal effects. To test this, we cross-fostered clutches within and across pre-defined high- and low-breeding density areas. We measured chicks' anxiety and exploration activity in an open-field test that included a novel and a familiar object. We found that both pre- and post-natal social environment contributed nearly equally and shaped the offspring's exploratory behaviour, but not its anxiety, in an additive way. Post-natal effects could reflect a learned avoidance of intra-specific aggression, yet identifying the pathways of the prenatal effects will require further study.

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Section: Introductionmentioning

confidence: 99%

Growing up in a crowd: social environment shapes the offspring's early exploratory phenotype in a colonial breeding species

et al. 2022

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“…For example, European starlings ( Sturnus vulgaris ) deprived of food as nestlings exhibit accelerated telomere attrition and feeding behaviours typical of acutely hungry birds despite access to food [110]. In wild spotted hyenas ( Crocuta crocuta ), maternal care and social connectedness during early life predicted later life glucocorticoids and DNA methylation near genes involved in inflammation, immune response, and ageing [111].…”

Section: Discussionmentioning

confidence: 99%

Early life adversity has long-term effects on sociality and interaction style in female baboons

2022

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Social bonds enhance fitness in many group-living animals, generating interest in the processes that create individual variation in sociality. Previous work on female baboons shows that early life adversity and temperament both influence social connectedness in adulthood. Early life adversity might shape sociality by reducing ability to invest in social relationships or through effects on attractiveness as a social partner. We examine how females’ early life adversity predicts sociality and temperament in wild olive baboons, and evaluate whether temperament mediates the relationship between early life adversity and sociality. We use behavioural data on 31 females to quantify sociality. We measure interaction style as the tendency to produce grunts (signals of benign intent) in contexts in which the vocalization does not produce immediate benefits to the actor. Early life adversity was negatively correlated with overall sociality, but was a stronger predictor of social behaviours received than behaviours initiated. Females who experienced less early life adversity had more benign interaction styles and benign interaction styles were associated with receiving more social behaviours. Interaction style may partially mediate the association between early life adversity and sociality. These analyses add to our growing understanding of the processes connecting early life experiences to adult sociality.

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“…Female spotted hyenas invest heavily in the rearing of offspring (East et al, 2009;Watts et al, 2009;Laubach et al, 2021). They usually bear litters of 1 or 2 cubs; when twin cubs are born, neonatal females dominate males in 67-84% of mixedsex twin litters (Smale et al, 1995;Golla et al, 1999;Wahaj and Holekamp, 2006;Benhaiem et al, 2012).…”

Section: Study Speciesmentioning

confidence: 99%

Evaluating drivers of female dominance in the spotted hyena

et al. 2022

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IntroductionDominance relationships in which females dominate males are rare among mammals. Mechanistic hypotheses explaining the occurrence of female dominance suggest that females dominate males because (1) they are intrinsically more aggressive or less submissive than males, and/or (2) they have access to more social support than males.MethodsHere, we examine the determinants of female dominance across ontogenetic development in spotted hyenas (Crocuta crocuta) using 30 years of detailed behavioral observations from the Mara Hyena Project to evaluate these two hypotheses.ResultsAmong adult hyenas, we find that females spontaneously aggress at higher rates than males, whereas males spontaneously submit at higher rates than females. Once an aggressive interaction has been initiated, adult females are more likely than immigrant males to elicit submission from members of the opposite sex, and both adult natal and immigrant males are more likely than adult females to offer submission in response to an aggressive act. We also find that adult male aggressors are more likely to receive social support than are adult female aggressors, and that both adult natal and immigrant males are 2–3 times more likely to receive support when attacking a female than when attacking another male. Across all age classes, females are more likely than males to be targets of aggressive acts that occur with support. Further, receiving social support does slightly help immigrant males elicit submission from adult females compared to immigrant males acting alone, and it also helps females elicit submission from other females. However, adult females can dominate immigrant males with or without support far more often than immigrant males can dominate females, even when the immigrants are supported against females.DiscussionOverall, we find evidence for both mechanisms hypothesized to mediate female dominance in this species: (1) male and female hyenas clearly differ in their aggressive and submissive tendencies, and (2) realized social support plays an important role in shaping dominance relationships within a clan. Nevertheless, our results suggest that social support alone cannot explain sex-biased dominance in spotted hyenas. Although realized social support can certainly influence fight outcomes among females, adult females can easily dominate immigrant males without any support at all.

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Early-life social experience affects offspring DNA methylation and later life stress phenotype

Cited by 17 publications

References 110 publications

Growing up in a crowd: social environment shapes the offspring's early exploratory phenotype in a colonial breeding species

Growing up in a crowd: social environment shapes the offspring's early exploratory phenotype in a colonial breeding species

Early life adversity has long-term effects on sociality and interaction style in female baboons

Evaluating drivers of female dominance in the spotted hyena

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