Behavioural traits propagate across generations via segregated iterative-somatic and gametic epigenetic mechanisms

Mitchell, Emma J.; Klein, Shifra Liba; Argyropoulos, Kimon V.; Sharma, Abhijeet; Chan, Robin B.; Toth, Judit Gal; Barboza, Luendreo; Bavley, Charlotte C.; Bortolozzi, Analı́a; Chen, Qiuying; Liu, Bingfang; Ingenito, Joanne; Mark, Willie; Dudakov, Jarrod A; Gross, Steven S.; Paolo, Gilberto di; Artigas, Francesc; Brink, Marcel van den; Tóth, Miklós

doi:10.1038/ncomms11492

Cited by 33 publications

(29 citation statements)

References 70 publications

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“…It is not uncommon to observe sex‐differences in the effects of intergenerational influences of salient parental environments. Exposing parental rodents to stressors as well as dietary manipulations have been shown to affect one sex and not the other depending not only on the parental perturbation but also the task on which the offspring are tested . Therefore, once again, our data agree with the existing literature that male and female offspring may shoulder the legacy of parental stress differently and attention needs to be paid to the parental environmental experience and the dependent variable being tested in the offspring.…”

Section: Discussionsupporting

confidence: 88%

Proximate causes and consequences of intergenerational influences of salient sensory experience

Aoued¹,

Sannigrahi²,

Hunter³

et al. 2020

Genes Brain and Behavior

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Salient sensory environments experienced by a parental generation can exert intergenerational influences on offspring. While these data provide an exciting new perspective on biological inheritance, questions remain about causes and consequences of intergenerational influences of salient sensory experience. We previously showed that exposing male mice to a salient olfactory experience, like olfactory fear conditioning, resulted in offspring demonstrating a sensitivity to the odor used to condition the paternal generation and possessing enhanced neuroanatomical representation for that odor. In this study, we first injected RNA extracted from sperm of male mice that underwent olfactory fear conditioning into naïve single‐cell zygotes and found that adults that developed from these embryos had increased sensitivity and enhanced neuroanatomical representation for the odor (Odor A) with which the paternal male had been conditioned. Next, we found that female, but not male offspring sired by males conditioned with Odor A show enhanced consolidation of a weak single‐trial Odor A + shock fear conditioning protocol. Our data provide evidence that RNA found in the paternal germline after exposure to salient sensory experiences can contribute to intergenerational influences of such experiences, and that such intergenerational influences confer an element of adaptation to the offspring. In so doing, our study of intergenerational influences of parental sensory experience adds to existing literature on intergenerational influences of parental exposures to stress and dietary manipulations and suggests that some causes (sperm RNA) and consequences (behavioral flexibility) of intergenerational influences of parental experiences may be conserved across a variety of parental experiences.

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Section: Discussionsupporting

confidence: 88%

Proximate causes and consequences of intergenerational influences of salient sensory experience

Aoued¹,

Sannigrahi²,

Hunter³

et al. 2020

Genes Brain and Behavior

View full text Add to dashboard Cite

show abstract

“…It is not uncommon to observe sex-differences in the effects of intergenerational influences of salient parental environments. Exposing parental rodents to stressors as well as dietary manipulations have been shown to affect one sex and not the other depending not only on the parental perturbation but also the task on which the offspring are tested [46][47][48][49][50][51][52][53]. Therefore, once again, our data agree with the existing literature that male and female offspring may shoulder the legacy of parental stress differently and attention needs to be paid to the parental environmental experience and the dependent variable being tested in the offspring.…”

Section: Discussionmentioning

confidence: 99%

Proximate causes and consequences of intergenerational influences of salient sensory experience

Aoued

Sannigrahi

Hunter

et al. 2019

Preprint

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Salient sensory environments experienced by a parental generation can exert intergenerational influences on offspring, including offspring not conceived at the time of the parental experience. While these data provide an exciting new perspective on biological inheritance, questions remain about causes and consequences of intergenerational influences of across parental experiences as diverse as stress exposure, dietary perturbations and sensory experiences. ACKNOWLEDGEMENTS.We thank the Veterinary and Animal Care staff in the Yerkes Neuroscience Vivarium for animal husbandry.

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“…The real transgenerational inheritance, however, is still under debate, especially for humans [32,33,52,75,81,87,88,114]. There is some evidence of transmission of epigenetic changes through the germ line [5,13,25,130,203], as the erasure of methylation marks seems to be incomplete in mammalian cells [114,158]. Moreover, various kinds of RNA has been detected in gametes, that can influence chromatin remodeling and gene expression [78,93,99,101,102,112,132,165,209].…”

Section: Epigenetic Revolutionmentioning

confidence: 99%

Nature or Nurture – Will Epigenomics Solve the Dilemma?

Plonka

2016

Studia Humana

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The concept of "nature and nurture" is used to distinguish between genetic and environmental influences on the formation of individual, mainly behavioral, traits. Different approaches that interpret nature and nurture as completely opposite or complementary aspects of human development have been discussed for decades. The paper addresses the most important points of nature vs nurture debate from the perspective of biological research, especially in the light of the recent findings in the field of epigenetics. The most important biological concepts, such as the trait, phenotype and genotype, as well as the evolution of other crucial notions are presented. Various attempts to find the main source of human variation are discussedmainly the search for structural variants and the genome-wide association studies (GWAS). A new approach resulting from the discovery of "missing heritability", as well as the current knowledge about the possible influence of epigenetic mechanisms on human traits are analyzed. Finally, the impact of epigenetic revolution on the society (public attitude, health policy, human rights etc.) is discussed.

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Behavioural traits propagate across generations via segregated iterative-somatic and gametic epigenetic mechanisms

Cited by 33 publications

References 70 publications

Proximate causes and consequences of intergenerational influences of salient sensory experience

Proximate causes and consequences of intergenerational influences of salient sensory experience

Proximate causes and consequences of intergenerational influences of salient sensory experience

Nature or Nurture – Will Epigenomics Solve the Dilemma?

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