Epigenetics and the origins of paternal effects

Abstract

Though there are multiple routes through which parents can influence their offspring, recent studies of environmentally induced epigenetic variation have highlighted the role of non-genomic pathways. In addition to the experience-dependent modification of DNA methylation that can be achieved via mother-infant interactions, there has been increasing interest in the epigenetic mechanisms through which paternal influences on offspring development can be achieved. Epidemiological and laboratory studies suggest that paternal nutritional and toxicological exposures as well as paternal age and phenotypic variation can lead to variations in offspring and, in some cases, grand-offspring development. These findings suggest a potential epigenetic germline inheritance of paternal effects. However, it may be important to consider the interplay between maternal and paternal influences as well as the experimental dissociation between experience-dependent and germline transmission when exploring the role of epigenetic variation within the germline as a mediator of these effects. In this review, we will explore these issues, with a particular focus on the potential role of paternally induced maternal investment, highlight the literature illustrating the transgenerational impact of paternal experiences, and discuss the evidence supporting the role of epigenetic mechanisms in maintaining paternal effects both within and across generations.

Fig. 1

Illustration of the non-genomic pathways through which paternal effects on offspring development can be achieved. Experiences of males (drugs, nutrition, toxin, age), particularly those experienced during early development, may lead to epigenetic alterations in the male germline (red circle) which are then transmitted to offspring with consequences for phenotypic variation. Alternatively, or likely in combination with these direct paternal effects, the experiences of a male prior to mating may lead to changes in mate quality or preference as assessed by the female at the time of mating. This assessment may then lead to differential prenatal and/or postnatal maternal investment in the growth and development of offspring generated from this mating with consequences for offspring phenotypic variation. Maternal investment may also vary as a function of paternally mediated variations in offspring phenotype during both the prenatal and/or postnatal periods. Differential maternal investment as a function of paternal experiences or offspring traits may serve either to enhance the transmission of paternal exposures or compensate for deficits in functioning that are induced by these environmental experiences.