Maternal modulation of paternal effects on offspring development

Author:

Mashoodh Rahia12ORCID,Habrylo Ireneusz B.1,Gudsnuk Kathryn M.1,Pelle Geralyn3,Champagne Frances A.14

Affiliation:

1. Department of Psychology, Columbia University, 1190 Amsterdam Avenue, Room 406 Schermerhorn Hall, New York, NY 10027, USA

2. Department of Zoology, University of Cambridge, Downing St, Cambridge, CB2 3EJ, UK

3. Columbia University Medical Center, 650 W 168 St, New York, NY 10032, USA

4. Department of Psychology, University of Texas at Austin, 108 E Dean Keeton St, Austin, TX 78712, USA

Abstract

The paternal transmission of environmentally induced phenotypes across generations has been reported to occur following a number of qualitatively different exposures and appear to be driven, at least in part, by epigenetic factors that are inherited via the sperm. However, previous studies of paternal germline transmission have not addressed the role of mothers in the propagation of paternal effects to offspring. We hypothesized that paternal exposure to nutritional restriction would impact male mate quality and subsequent maternal reproductive investment with consequences for the transmission of paternal germline effects. In the current report, using embryo transfer in mice, we demonstrate that sperm factors in adult food restricted males can influence growth rate, hypothalamic gene expression and behaviour in female offspring. However, under natural mating conditions females mated with food restricted males show increased pre- and postnatal care, and phenotypic outcomes observed during embryo transfer conditions are absent or reversed. We demonstrate that these compensatory changes in maternal investment are associated with a reduced mate preference for food restricted males and elevated gene expression within the maternal hypothalamus. Therefore, paternal experience can influence offspring development via germline inheritance, but mothers can serve as a modulating factor in determining the impact of paternal influences on offspring development.

Funder

NIH Office of the Director

Publisher

The Royal Society

Subject

General Agricultural and Biological Sciences,General Environmental Science,General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine

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