Transgenerational inheritance of ethanol preference is caused by maternal NPF repression

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Abstract

Rapid or even anticipatory adaptation to environmental conditions can provide a decisive fitness advantage to an organism. The memory of recurring conditions could also benefit future generations; however, neuronally-encoded behavior isn’t thought to be inherited across generations. We tested the possibility that environmentally triggered modifications could allow ‘memory’ of parental experiences to be inherited. In Drosophila melanogaster, exposure to predatory wasps leads to inheritance of a predisposition for ethanol-rich food for five generations. Inhibition of Neuropeptide-F (NPF) activates germline caspases required for transgenerational ethanol preference. Further, inheritance of low NPF expression in specific regions of F ₁ brains is required for the transmission of this food preference: a maternally derived NPF locus is necessary for this phenomenon, implicating a maternal epigenetic mechanism of NPF-repression. Given the conserved signaling functions of NPF and its mammalian NPY homolog in drug and alcohol disorders, these observations raise the intriguing possibility of NPY-related transgenerational effects in humans.

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Most cited references 23

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Sperm tsRNAs contribute to intergenerational inheritance of an acquired metabolic disorder.

Q. Chen, M. Yan, Z. Cao … (2016)

Increasing evidence indicates that metabolic disorders in offspring can result from the father's diet, but the mechanism remains unclear. In a paternal mouse model given a high-fat diet (HFD), we showed that a subset of sperm transfer RNA-derived small RNAs (tsRNAs), mainly from 5' transfer RNA halves and ranging in size from 30 to 34 nucleotides, exhibited changes in expression profiles and RNA modifications. Injection of sperm tsRNA fractions from HFD males into normal zygotes generated metabolic disorders in the F1 offspring and altered gene expression of metabolic pathways in early embryos and islets of F1 offspring, which was unrelated to DNA methylation at CpG-enriched regions. Hence, sperm tsRNAs represent a paternal epigenetic factor that may mediate intergenerational inheritance of diet-induced metabolic disorders.

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Transgenerational plasticity is adaptive in the wild.

Laura Galloway, Julie R Etterson (2007)

Plants exhibit adaptive responses to light, but it is not known whether parental plants transmit environmental cues that elicit adaptive responses in offspring. We show that offspring life history (annual versus biennial) is influenced by the maternal light environment (understory versus light gap). This transgenerational plasticity is adaptive when offspring are grown in their maternal light environment, where seeds typically disperse. Projections of population growth show that plants that are appropriately cued for their light environment through maternal effects have 3.4 times greater fitness than otherwise. Transgenerational plasticity has evolved in response to natural variation in light and provides a flexible mechanism by which sedentary organisms cope with heterogeneous environments.

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A neural circuit mechanism integrating motivational state with memory expression in Drosophila.

Michael Krashes, Shamik DasGupta, Andrew P. Vreede … (2009)

Behavioral expression of food-associated memory in fruit flies is constrained by satiety and promoted by hunger, suggesting an influence of motivational state. Here, we identify a neural mechanism that integrates the internal state of hunger and appetitive memory. We show that stimulation of neurons that express neuropeptide F (dNPF), an ortholog of mammalian NPY, mimics food deprivation and promotes memory performance in satiated flies. Robust appetitive memory performance requires the dNPF receptor in six dopaminergic neurons that innervate a distinct region of the mushroom bodies. Blocking these dopaminergic neurons releases memory performance in satiated flies, whereas stimulation suppresses memory performance in hungry flies. Therefore, dNPF and dopamine provide a motivational switch in the mushroom body that controls the output of appetitive memory.

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Author and article information

Contributors

Giovanni Bosco:

ORCID: https://orcid.org/0000-0002-8889-9895

Leslie C Griffith: Role: Reviewing Editor

Maarten van Lohuizen: Role: Senior Editor

Journal

Journal ID (nlm-ta): eLife

Journal ID (iso-abbrev): Elife

Journal ID (publisher-id): eLife

Title: eLife

Publisher: eLife Sciences Publications, Ltd

ISSN (Electronic): 2050-084X

Publication date (Electronic, pub): 09 July 2019

Publication date Collection: 2019

Volume: 8

Electronic Location Identifier: e45391

Affiliations

[1]deptDepartment of Molecular and Systems Biology Geisel School of Medicine at Dartmouth HanoverUnited States

Brandeis University United States

The Netherlands Cancer Institute Netherlands

Brandeis University United States

Author information

Julianna Bozler https://orcid.org/0000-0002-6275-3409

Balint Z Kacsoh https://orcid.org/0000-0001-9171-0611

Giovanni Bosco https://orcid.org/0000-0002-8889-9895

Article

Publisher ID: 45391

DOI: 10.7554/eLife.45391

PMC ID: 6615861

PubMed ID: 31287057

SO-VID: d8fb3f34-ad91-4c6e-8381-feb12fa0ece2

License:

This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.

History

Date received : 21 January 2019

Date accepted : 22 May 2019

Funding

Funded by: FundRef http://dx.doi.org/10.13039/100000002, National Institutes of Health;

Award ID: 1DP1MH110234

Award Recipient : Giovanni Bosco

Funded by: FundRef http://dx.doi.org/10.13039/100000185, Defense Advanced Research Projects Agency;

Award ID: HR0011-15-1-0002

Award Recipient : Giovanni Bosco

Funded by: FundRef http://dx.doi.org/10.13039/100000002, National Institutes of Health;

Award ID: T32-GM009704

Award Recipient : Julianna Bozler

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

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Author impact statement Maternally experienced environmental stress leads to multigenerational inheritance of ethanol preference and an altered rewards pathway in Drosophila melanogaster.

ScienceOpen disciplines: Life sciences

Keywords: epigenetic,transgenerational behavior,ethanol,npf,parasitoid wasp,d. melanogaster

Data availability:

ScienceOpen disciplines: Life sciences

Keywords: epigenetic, transgenerational behavior, ethanol, npf, parasitoid wasp, d. melanogaster

Transgenerational inheritance of ethanol preference is caused by maternal NPF repression

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Abstract

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Applied use of fungi

Most cited references 23

Sperm tsRNAs contribute to intergenerational inheritance of an acquired metabolic disorder.

Transgenerational plasticity is adaptive in the wild.

A neural circuit mechanism integrating motivational state with memory expression in Drosophila.

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