Early experience affects the intergenerational transmission of infant abuse in rhesus monkeys

Maestripieri, Dario

doi:10.1073/pnas.0504122102

Cited by 166 publications

(156 citation statements)

References 26 publications

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“…Females reared without mothers abandoned their juveniles for longer and provisioned them with less food than females reared with tending mothers. To the best of our knowledge, the long-term, negative effects of maternal loss on the expression of maternal care have only been reported in altricial vertebrates [8][9][10]13]. In these species, the effects of maternal loss typically result from a disrupted learning process [30] and/or from induced hormonal/neurobiological changes during juvenile development.…”

Section: Discussionmentioning

confidence: 99%

“…Somewhat surprisingly, the long-term and transgenerational effects of parental loss have only been studied in altricial vertebrates, in which juveniles exhibit limited foraging capabilities and thus heavily rely on parental resources [11][12][13]. However, investigating the occurrence of these effects in precocial invertebrates, in which juveniles exhibit early foraging capabilities and consequently only facultatively rely on parental resources [14,15], could provide crucial information on the early evolution of parental care.…”

Section: Introductionmentioning

confidence: 99%

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Short-term benefits, but transgenerational costs of maternal loss in an insect with facultative maternal care

et al. 2015

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A lack of parental care is generally assumed to entail substantial fitness costs for offspring that ultimately select for the maintenance of family life across generations. However, it is unknown whether these costs arise when parental care is facultative, thus questioning their fundamental importance in the early evolution of family life. Here, we investigated the short-term, long-term and transgenerational effects of maternal loss in the European earwig Forficula auricularia, an insect with facultative post-hatching maternal care. We showed that maternal loss did not influence the developmental time and survival rate of juveniles, but surprisingly yielded adults of larger body and forceps size, two traits associated with fitness benefits. In a cross-breeding/ cross-fostering experiment, we then demonstrated that maternal loss impaired the expression of maternal care in adult offspring. Interestingly, the resulting transgenerational costs were not only mediated by the early-life experience of tending mothers, but also by inherited, parent-of-origin-specific effects expressed in juveniles. Orphaned females abandoned their juveniles for longer and fed them less than maternally-tended females, while foster mothers defended juveniles of orphaned females less well than juveniles of maternally-tended females. Overall, these findings reveal the key importance of transgenerational effects in the early evolution of family life.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Short-term benefits, but transgenerational costs of maternal loss in an insect with facultative maternal care

et al. 2015

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“…Crossfostered infants were reared in groups different from those in which their biological mothers resided. The control and the abusive mothers did not differ significantly in their age and dominance rank (Maestripieri, 2005a).…”

Section: Methods Subjectsmentioning

confidence: 98%

“…Study subjects were 13 females that were successfully crossfostered between abusive and nonabusive mothers within 24-48 hr after birth (see Maestripieri, 2005a, for definitions of infant abuse, relevant information on it, and details of the crossfostering procedure). Crossfostered infants were reared in groups different from those in which their biological mothers resided.…”

Section: Methods Subjectsmentioning

confidence: 99%

Intergenerational transmission of maternal behavior in rhesus macaques and its underlying mechanisms

Maestripieri

Lindell

Higley

2007

Developmental Psychobiology

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Thirteen group-living rhesus macaque females that were crossfostered shortly after birth were followed longitudinally until they gave birth for the first time. Their maternal behavior was compared to the behavior of both their foster and their biological mothers, and analyzed in relation to the cerebrospinal fluid (CSF) concentrations of serotonin, dopamine, and norepinephrine metabolites (5-HIAA, HVA, and MHPG) measured in their second year of life. Crossfostered females were similar to their foster mothers in their rates of maternal rejection and grooming, whereas their contact-making behavior was more similar to that of their biological mothers. Crossfostered females with lower CSF concentrations of 5-HIAA exhibited higher rates of maternal rejection than females with higher CSF 5-HIAA. In a related article (Maestripieri et al., 2006), we reported that rhesus infants reared by highly rejecting mothers had lower CSF 5-HIAA in their first 3 years of life. Taken together, these findings suggest that early social experience and experience-related long-term changes in serotonergic function may play a role in the intergenerational transmission of maternal rejection from mothers to daughters. ß 2007 Wiley Periodicals, Inc. Dev Psychobiol 49: 165-171, 2007.

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“…Infants cross-fostered from an abusive female to a non-abusive female were not found to abuse their own offspring suggesting the role of the postnatal environment in mediating these effects [20]. Such a transmission of abuse has long been suspected from observational studies of rhesus and pigtail macaques social groups where infant abuse is highly concentrated within certain matrilines and among closely related females [19;21].…”

Section: Matrilineal Transmission Of Maternal Carementioning

confidence: 99%

Epigenetic mechanisms and the transgenerational effects of maternal care

Champagne

2008

Frontiers in Neuroendocrinology

686

447

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The transmission of traits across generations has typically been attributed to the inheritance by offspring of genomic information from parental generations. However, recent evidence suggests that epigenetic mechanisms are capable of mediating this type of transmission. In the case of maternal care, there is evidence for the behavioral transmission of postpartum behavior from mothers to female offspring. The neuroendocrine and molecular mediators of this transmission have been explored in rats and implicate estrogen-oxytocin interactions and the differential methylation of hypothalamic estrogen receptors. These maternal effects can influence multiple aspects of neurobiology and behavior of offspring and this particular mode of inheritance is dynamic in response to environmental variation. In this review, evidence for the generational transmission of maternal care and the mechanisms underlying this transmission will be discussed as will the implications of this inheritance system for offspring development and for the transmission of environmental information from parents to offspring. Keywords maternal; epigenetic; DNA methylation; estrogen receptor α; oxytocin; environment; cross-fostering Maternal effects have been demonstrated across many species and serve as an important cue to offspring development. In mammals, the lengthy period of prenatal and postnatal motherinfant interaction provides an opportunity for mothers to influence offspring through a variety of mechanisms. During gestation, interactions between mother and fetus are critical for growth and development and variations in these interactions can have long-term consequences for offspring physiological and psychological health. These effects have best been demonstrated through study of prenatal stress [1] and maternal malnutrition [2;3] in which changes to the mother's neuroendocrine system and physiology produces a shift in fetal neurodevelopment. Likewise, the care received by an infant early in life can produce changes in the development of neural systems regulating response to novelty and social behavior [4]. Thus, the maternal environment experienced by a developing organism can play a critical role in shaping adult patterns of behavior. Moreover, there can be transmission of these effects to subsequent generations through alterations in the reproductive behavior of offspring. Thus maternal care can be transmitted from mothers to daughters and grand-daughters. The mechanisms mediating Correspondence should be addressed to: Dr. Frances A. Champagne, Department of Psychology, Columbia University, Room 406 Schermerhorn Hall, 1190 Amsterdam Avenue, New York, NY 10017, Phone: (212) 854-2589, Fax: (212) 854-3609, Email: E-mail: fac2105@columbia.edu. Publisher's Disclaimer: This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is ...

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Early experience affects the intergenerational transmission of infant abuse in rhesus monkeys

Cited by 166 publications

References 26 publications

Short-term benefits, but transgenerational costs of maternal loss in an insect with facultative maternal care

Short-term benefits, but transgenerational costs of maternal loss in an insect with facultative maternal care

Intergenerational transmission of maternal behavior in rhesus macaques and its underlying mechanisms

Epigenetic mechanisms and the transgenerational effects of maternal care

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