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.

Paternal social enrichment effects on maternal behavior and offspring growth

“…Interestingly, the effects observed in human epidemiological studies are qualitatively similar to paternal effects observed in species of laboratory rodents that do not engage in postnatal paternal care (4). Although much of the evidence is, at this stage, preliminary, there is emerging support that environmental induction of paternal germline epigenetic changes can have consequences for multiple generations of offspring.…”

“…In these species, paternal care may induce changes in offspring development via similar mechanisms as postnatal maternal care. However, few mammalian species (3-5%) provide paternal care, and paternal effects can occur in the absence of paternal care (4). The underlying mechanisms of these paternal effects are perplexing in nonmonogamous mammalian species because the biological information transmitted during fertilization is thought to be limited to paternal DNA.…”

“…Many of the reported changes occur at genes within molecular pathways that direct and maintain large-scale changes to the epigenome across tissues, with broad implications for development. These molecular changes may play an important role in conferring ancestral epigenetic imprints across generations, although it has been argued that such strict inheritance of acquired epigenetic marks is rare and is limited to a small subset of genes (4).…”

Advanced paternal age and reproductive outcome

“…Interestingly, paternal exposure to toxicant and nutritional state as well as age, have been found to influence not only offspring but sometimes grand-offspring. 106 …”

Health Disparities: A Life Course Health Development Perspective and Future Research Directions

“…Environmental toxicant exposures include a wide range of factors such as smoking and air pollution. Whereas most research has focused on the biological impact of prenatal and postnatal exposures, new studies are beginning to show possible transgenerational effects through epigenetic changes in the germline connected with smoke and toxicant exposure which provides an argument for the importance of the preconception health states of parents (Curley et al 2011;Laubenthal et al 2012). …”