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

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

doi:10.1038/s41467-021-24583-x

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

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

Animal Science

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17 Scopus citations

Abstract

Studies in rodents and captive primates suggest that the early-life social environment affects future phenotype, potentially through alterations to DNA methylation. Little is known of these associations in wild animals. In a wild population of spotted hyenas, we test the hypothesis that maternal care during the first year of life and social connectedness during two periods of early development leads to differences in DNA methylation and fecal glucocorticoid metabolites (fGCMs) later in life. Here we report that although maternal care and social connectedness during the den-dependent life stage are not associated with fGCMs, greater social connectedness during the subadult den-independent life stage is associated with lower adult fGCMs. Additionally, more maternal care and social connectedness after den independence correspond with higher global (%CCGG) DNA methylation. We also note differential DNA methylation near 5 genes involved in inflammation, immune response, and aging that may link maternal care with stress phenotype.

Original language	English (US)
Article number	4398
Journal	Nature communications
Volume	12
Issue number	1
DOIs	https://doi.org/10.1038/s41467-021-24583-x
State	Published - Dec 1 2021

Bibliographical note

Funding Information:
We thank the Kenyan National Commission for Science, Technology, and Innovation, the Naboisho Conservancy, the Narok County Government, the Kenya Wildlife Service (KWS) and Brian Heath for permission to conduct research in the Mara ecosystem. We also thank the Mara Hyena Project field crew and the residents of the Mara ecosystem for their direct and indirect support of long-term field research in their backyard. We are indebted to all those who have contributed to long-term data and sample collection on the Mara Hyena Project, including undergraduate researchers, Karee Lesko, Shannon Carvey, and Kaycee Morra. We are also grateful to Dr. Elise Zipkin for suggestions and feedback regarding the statistical modeling, as well as Dr. Lu Tang and Patrick Bills for help processing the behavioral data. This work was supported by National Science Foundation Grants DEB1353110, OISE1556407, and IOS1755089 to KEH, and Doctoral Dissertation Improvement Grant from NSF (DDIG 1701384) to ZML. This work was also supported in part by funds from NSF Grant OIA 0939454 to the BEACON Center for the Study of Evolution in Action as well as Michigan Lifestage Environmental Exposures and Disease (M-LEEaD), NIEHS Core Center (P30 ES017885), as well as the UM NIEHS Institutional Training Grant T32 ES007062 to DCD. Dr. Perng is supported by the Center for Clinical and Translational Sciences Institute via KL2-TR002534.

Publisher Copyright:
© 2021, The Author(s).

PubMed: MeSH publication types

Journal Article
Research Support, N.I.H., Extramural
Research Support, U.S. Gov't, Non-P.H.S.

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Laubach, Z. M., Greenberg, J. R., Turner, J. W., Montgomery, T. M., Pioon, M. O., Sawdy, M. A., Smale, L., Cavalcante, R. G., Padmanabhan, K. R., Lalancette, C., vonHoldt, B., Faulk, C. D., Dolinoy, D. C., Holekamp, K. E., & Perng, W. (2021). Early-life social experience affects offspring DNA methylation and later life stress phenotype. Nature communications, 12(1), Article 4398. https://doi.org/10.1038/s41467-021-24583-x

Laubach, ZM, Greenberg, JR, Turner, JW, Montgomery, TM, Pioon, MO, Sawdy, MA, Smale, L, Cavalcante, RG, Padmanabhan, KR, Lalancette, C, vonHoldt, B, Faulk, CD, Dolinoy, DC, Holekamp, KE & Perng, W 2021, 'Early-life social experience affects offspring DNA methylation and later life stress phenotype', Nature communications, vol. 12, no. 1, 4398. https://doi.org/10.1038/s41467-021-24583-x

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title = "Early-life social experience affects offspring DNA methylation and later life stress phenotype",

abstract = "Studies in rodents and captive primates suggest that the early-life social environment affects future phenotype, potentially through alterations to DNA methylation. Little is known of these associations in wild animals. In a wild population of spotted hyenas, we test the hypothesis that maternal care during the first year of life and social connectedness during two periods of early development leads to differences in DNA methylation and fecal glucocorticoid metabolites (fGCMs) later in life. Here we report that although maternal care and social connectedness during the den-dependent life stage are not associated with fGCMs, greater social connectedness during the subadult den-independent life stage is associated with lower adult fGCMs. Additionally, more maternal care and social connectedness after den independence correspond with higher global (%CCGG) DNA methylation. We also note differential DNA methylation near 5 genes involved in inflammation, immune response, and aging that may link maternal care with stress phenotype.",

author = "Laubach, {Zachary M.} and Greenberg, {Julia R.} and Turner, {Julie W.} and Montgomery, {Tracy M.} and Pioon, {Malit O.} and Sawdy, {Maggie A.} and Laura Smale and Cavalcante, {Raymond G.} and Padmanabhan, {Karthik R.} and Claudia Lalancette and Bridgett vonHoldt and Faulk, {Christopher D.} and Dolinoy, {Dana C.} and Holekamp, {Kay E.} and Wei Perng",

note = "Funding Information: We thank the Kenyan National Commission for Science, Technology, and Innovation, the Naboisho Conservancy, the Narok County Government, the Kenya Wildlife Service (KWS) and Brian Heath for permission to conduct research in the Mara ecosystem. We also thank the Mara Hyena Project field crew and the residents of the Mara ecosystem for their direct and indirect support of long-term field research in their backyard. We are indebted to all those who have contributed to long-term data and sample collection on the Mara Hyena Project, including undergraduate researchers, Karee Lesko, Shannon Carvey, and Kaycee Morra. We are also grateful to Dr. Elise Zipkin for suggestions and feedback regarding the statistical modeling, as well as Dr. Lu Tang and Patrick Bills for help processing the behavioral data. This work was supported by National Science Foundation Grants DEB1353110, OISE1556407, and IOS1755089 to KEH, and Doctoral Dissertation Improvement Grant from NSF (DDIG 1701384) to ZML. This work was also supported in part by funds from NSF Grant OIA 0939454 to the BEACON Center for the Study of Evolution in Action as well as Michigan Lifestage Environmental Exposures and Disease (M-LEEaD), NIEHS Core Center (P30 ES017885), as well as the UM NIEHS Institutional Training Grant T32 ES007062 to DCD. Dr. Perng is supported by the Center for Clinical and Translational Sciences Institute via KL2-TR002534. Publisher Copyright: {\textcopyright} 2021, The Author(s).",

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AU - Sawdy, Maggie A.

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AU - Cavalcante, Raymond G.

AU - Padmanabhan, Karthik R.

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AU - Faulk, Christopher D.

AU - Dolinoy, Dana C.

AU - Holekamp, Kay E.

AU - Perng, Wei

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

Abstract

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