Maternal care boosted by paternal imprinting in mammals

Creeth, H. D. J., McNamara, G. I., Tunster, S. J., Boque Sastre, R. ORCID: https://orcid.org/0000-0002-0214-8848, Allen, B., Sumption, L. ORCID: https://orcid.org/0000-0002-2259-9128, Eddy, J. B., Isles, A. R. ORCID: https://orcid.org/0000-0002-7587-5712 and John, R. M. ORCID: https://orcid.org/0000-0002-3827-7617 2018. Maternal care boosted by paternal imprinting in mammals. PLoS Biology 16 (7) , e2006599. 10.1371/journal.pbio.2006599

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Abstract

In mammals, mothers are the primary caregiver, programmed, in part, by hormones produced during pregnancy. High-quality maternal care is essential for the survival and lifelong health of offspring. We previously showed that the paternally silenced imprinted gene pleckstrin homology-like domain family A member 2 (Phlda2) functions to negatively regulate a single lineage in the mouse placenta called the spongiotrophoblast, a major source of hormones in pregnancy. Consequently, the offspring’s Phlda2 gene dosage may influence the quality of care provided by the mother. Here, we show that wild-type (WT) female mice exposed to offspring with three different doses of the maternally expressed Phlda2 gene—two active alleles, one active allele (the extant state), and loss of function—show changes in the maternal hypothalamus and hippocampus during pregnancy, regions important for maternal-care behaviour. After birth, WT dams exposed in utero to offspring with the highest Phlda2 dose exhibit decreased nursing and grooming of pups and increased focus on nest building. Conversely, ‘paternalised’ dams, exposed to the lowest Phlda2 dose, showed increased nurturing of their pups, increased self-directed behaviour, and a decreased focus on nest building, behaviour that was robustly maintained in the absence of genetically modified pups. This work raises the intriguing possibility that imprinting of Phlda2 contributed to increased maternal care during the evolution of mammals.

Item Type:	Article
Date Type:	Publication
Status:	Published
Schools:	Advanced Research Computing @ Cardiff (ARCCA) Biosciences Neuroscience and Mental Health Research Institute (NMHRI) Medicine MRC Centre for Neuropsychiatric Genetics and Genomics (CNGG)
Additional Information:	This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Publisher:	Public Library of Science
ISSN:	1544-9173
Date of First Compliant Deposit:	30 July 2018
Date of Acceptance:	26 June 2018
Last Modified:	12 May 2023 05:09
URI:	https://orca.cardiff.ac.uk/id/eprint/113723

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