Paternal line effects of early experiences persist across three generations in rhesus macaques

Kinnally, Erin L.; Gonzalez, Mireille; Capitanio, John P.

doi:10.1002/dev.21771

Cited by 11 publications

(11 citation statements)

References 68 publications

(123 reference statements)

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“…23 These studies did not consider lineage (paternal grandparents or maternal grandparents) which have different influence on certain diseases. 24,25 In our study, based on the sufficiently large sample, we were able to distinguish grandparents between paternal and maternal lineage. Our results showed that a family history on either a paternal grandparent or a maternal grandparent with asthma was associated with an increased risk of childhood asthma, independent of parental asthma, although the impact on the asthma risk was less than a family history of a parent.…”

Section: Discussionmentioning

confidence: 87%

Familial Risk of Asthma for Children with Affected Family Members in Multiple Generations

Yu¹,

Guan²,

Hemminki³

et al. 2020

Preprint

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Background: While a parental history of asthma has been widely reported as a risk factor for childhood asthma, less is known about the impact of multigenerational family history of asthma on the occurrence of asthma in children. Methods: From 2012 to 2013, a cross-sectional study was carried out in seven Chinese cities. Participants were randomly selected from 94 middle schools, elementary schools and kindergartens. Questionnaires, from which information on asthma, environmental exposure and family members (parents, paternal grandparents and maternal grandparents) affected by asthma were obtained, were completed by the children's parents or guardians. Two-level logistic regressions were used to assess hereditary patterns of asthma, adjusted for potential confounding factors. Mediation analysis was performed to estimate the potential mediation effect of parents on the association between grandparental asthma and offspring asthma. Results: A paternal grandfather (OR: 2.59, 95%CI: 2.14-3.13), paternal grandmother (OR: 2.40, 95%CI: 1.93-2.99), maternal grandfather (OR: 2.08, 95%CI: 1.71-2.53) and maternal grandmother (OR: 2.08, 95%CI: 1.67-2.59) with asthma were associated with childhood asthma, independent of parental asthma. Of the children who had two family members with asthma, the risk of childhood asthma was highest when both parents had asthma (OR: 15.92, 95%CI: 4.66-54.45) or when both father and paternal grandfather had asthma (OR: 11.11, 95%CI: 5.77-21.38). Parents had a small proportion of mediation effect on the association between grandparental asthma and childhood asthma. Conclusions: A family history of grandparental asthma was associated with childhood asthma and parents only partially mediate the association.

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Section: Discussionmentioning

confidence: 87%

Familial Risk of Asthma for Children with Affected Family Members in Multiple Generations

Yu¹,

Guan²,

Hemminki³

et al. 2020

Preprint

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“…However, prior studies using this model did not consider the possible non-genetic transmission of maltreatment-related phenotypes across generations and their relevance for disease risk. Importantly, models of ELS or early rearing experiences in NHP support the hypothesis that effects of nursery rearing, variable foraging demand stress, and variations in normal nurturing behavior, among others, may be transmitted across generations 61–64 . Thus, we sought to use our ELS model with cross-fostering to examine the possibility of transmission of epigenetic risk in a well-controlled design.…”

Section: Introductionmentioning

confidence: 83%

Molecular and Behavioral Effects of Infant Maltreatment across Generations in Rhesus Monkeys

Klengel

Morin

Howell

et al. 2019

Preprint

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36Childhood maltreatment is among the most robust risk factors for subsequent psychiatric and 37 medical disorders, and data in humans and rodents suggest that effects of adverse childhood 38 experiences may be transmitted across generations. Recent indications for biological processes 39 underlying this transfer of experiential effects are intriguing; yet, their relevance in primates is 40 inconclusive due to limitations of current studies. In this study, we bridge research in rodent 41 models and humans with a natural non-human primate model on intergenerational effects of 42 childhood maltreatment. Using a unique, well-controlled, randomized cross-fostering design in 43 rhesus monkeys, we test the influence of ancestral maltreatment on molecular, neuroendocrine 44 and behavioral outcomes in offspring, and show that childhood maltreatment results in 45 transmission of information to the subsequent generation independent of behavioral 46 transmission. We further demonstrate differences in the offspring longitudinal DNA methylation 47 profile of the FKBP5 gene, an important regulator of the hypothalamus-pituitary-adrenal axis in 48 offspring of the maltreatment lineage compared to the control lineage. Finally, we show that 49 differences in FKBP5 methylation have functional effects on molecular, neuroendocrine and 50 behavioral outcomes in offspring of the maltreatment ancestral line, even if the infants were 51 never exposed to maltreatment nor interacted with their exposed ancestors. Although the 52 molecular mechanism underlying our observations remains unknown, our data point to a 53 potential germline-dependent effect. In summary, our data suggest that history of maltreatment 54 in primates can induce molecular and behavioral changes in a subsequent generation 55 independent of behavioral transmission that may influence risk for mental and physical diseases 56 across generations. 57 58 59 60 61 62 63 64 65 66 67 68 69 70 71 72 Exposure to childhood maltreatment is one the most important risk factors for a variety of 73 psychiatric disorders 1,2 . However, both human studies and animal models suggest that effects 74 of environmental experiences such as maltreatment extend beyond the affected individual, 75 influencing phenotypes in subsequent generations. This sparked a controversial discussion on 76 the prevalence of these phenomena, the underlying mechanisms and their biomedical relevance77 3-5 . Strong evidence exists for effects of environmental cues on offspring phenotypes when 78 exposed during in utero development 6-8 , or for the consequences of parental experience on 79 offspring phenotypes mediated by parental behavior 9 . More recently, experiments in rodents 80 suggested that pre-conceptional exposure to chemicals 10 , drugs 11 , nutritional abnormalities 12 81 and stress 13-15 can prompt intergenerational effects or even lead to transgenerational 82 inheritance of specific phenotypes 16 . These events seem independent of in utero perturbations 83 or behavioral transmission and point to p...

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“…Effects have been demonstrated in three generations, with paternal grandoffspring still showing these effects, and paternal great-grandoffspring showing only increased nervousness (Kinnally et al, 2018).…”

Section: Discussionmentioning

confidence: 99%

“…In addition, research with several species (including humans, rodents, and nonhuman primates) have shown that adverse early life experiences have transgenerational effects (e.g., Babb, Carini, Spears, & Nephew, ; Kundakovic & Champagne, ; Maestripieri, ). For example, offspring of nursery‐reared rhesus macaque males had elevated cortisol, lower immune cell counts, and increased emotionality compared to offspring of control males (Kinnally & Capitanio, ; Kinnally, Gonzalez, & Capitanio, ). Effects have been demonstrated in three generations, with paternal grandoffspring still showing these effects, and paternal great‐grandoffspring showing only increased nervousness (Kinnally et al, ).…”

Section: Discussionmentioning

confidence: 99%

“…For example, offspring of nursery‐reared rhesus macaque males had elevated cortisol, lower immune cell counts, and increased emotionality compared to offspring of control males (Kinnally & Capitanio, ; Kinnally, Gonzalez, & Capitanio, ). Effects have been demonstrated in three generations, with paternal grandoffspring still showing these effects, and paternal great‐grandoffspring showing only increased nervousness (Kinnally et al, ). Follow‐up studies of the offspring of nursery‐reared parents and their subsequent generations would tell us if nursery rearing has similar intergenerational effects in squirrel monkeys.…”

Section: Discussionmentioning

confidence: 99%

See 1 more Smart Citation

Rearing condition may alter neonatal development of captive Bolivian squirrel monkeys (Saimiri boliviensis boliviensis)

Mulholland

Williams

Abee

2020

Developmental Psychobiology

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Nursery rearing has well-known consequences for primate species. Relative to some other primate species, research has indicated a reduced impact of nursery rearing on squirrel monkeys, particularly in terms of rates, severity, and persistence of abnormal behavior. We administered the Primate Neonatal Neurobehavioral Assessment to 29 dam-reared and 13 nursery-reared squirrel monkeys (Saimiri boliviensis boliviensis) at 2 and 6 weeks of age. Mixed-model ANOVAs comparing composite scores and individual assessment items across age, rearing status, and sex revealed a number of developmental differences. Dam-reared infants scored higher on all four composite measures compared to nursery-reared infants (p < .05) indicating that nursery-reared animals had slower motor development, were less active and attentive, and were more passive than their dam-reared counterparts. Consistent with infant rhesus macaques, nursery-reared squirrel monkeys showed an increased sensitivity to tactile stimulation (p < .05). Altogether, these results suggest a disruption of species-typical development when squirrel monkey infants are reared in a nursery setting, with activity, orientation, and state control areas most affected, though experimental research is needed to determine if this is a causal relationship. Contrary to previous behavioral research, there are likely developmental differences between dam-reared infant squirrel monkeys and those reared in a nursery setting.

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Paternal line effects of early experiences persist across three generations in rhesus macaques

Cited by 11 publications

References 68 publications

Familial Risk of Asthma for Children with Affected Family Members in Multiple Generations

Familial Risk of Asthma for Children with Affected Family Members in Multiple Generations

Molecular and Behavioral Effects of Infant Maltreatment across Generations in Rhesus Monkeys

Rearing condition may alter neonatal development of captive Bolivian squirrel monkeys (Saimiri boliviensis boliviensis)

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