Paternal impact on the developmental programming of sexual dimorphism

Front Cell Dev Biol. 2024 Dec 6:12:1520783. doi: 10.3389/fcell.2024.1520783. eCollection 2024.

Abstract

Sexual dimorphism involves distinct anatomical, physiological, behavioral, and developmental differences between males and females of the same species, influenced by factors prior to conception and during early development. These sex-specific traits contribute to varied phenotypes and individual disease risks within and across generations and understanding them is essential in mammalian studies. Hormones, sex chromosomes, and imprinted genes drive this dimorphism, with over half of quantitative traits in wildtype mice showing sex-based variation. This review focuses on the impact of paternal non-genetic factors on sexual dimorphism. We synthesize current research on how paternal health before conception affects offspring phenotypes in a sex-specific manner, examining mechanisms such as DNA methylation, paternally imprinted genes, sperm RNA, and seminal plasma. Additionally, we explore how paternal influences indirectly shape offspring through maternal behavior, uterine environment, and placental changes, affecting males and females differently. We propose mechanisms modulating sexual dimorphism during development, underscoring the need for sex-specific documentation in animal studies.

Keywords: developmental programing; epigenetics; imprinting; paternal inheritance; seminal plasma; sexual dimoprhism; sperm RNAs.

Publication types

  • Review

Grants and funding

The author(s) declare that financial support was received for the research, authorship, and/or publication of this article. The authors thank the Helmholtz Munich and the German Center for Diabetes Research for funding the Environmental Epigenetics Group, the DAAD (German Academic Exchange Service) and the EpiCrossBorders for funding the position of SA(funding program Nr. 57597951) and SP, respectively. The authors also thank the Fritz-Thyssen Foundation for funding RT’s work on epigenetic inheritance (Grant Nr. 10.19.2.027 MN - Epigenetic inheritance of diabetes in mammals).