Paternal effects on fetal programming

Abstract

Paternal programming is the concept that the environmental signals from the sire’s experiences leading up to mating can alter semen and ultimately affect the phenotype of resulting offspring. Potential mechanisms carrying the paternal effects to offspring can be associated with epigenetic signatures (DNA methylation, histone modification and non-coding RNAs), oxidative stress, cytokines, and the seminal microbiome. Several opportunities exist for sperm/semen to be influenced during development; these opportunities are within the testicle, the epididymis, or accessory sex glands. Epigenetic signatures of sperm can be impacted during the pre-natal and pre-pubertal periods, during sexual maturity and with advancing sire age. Sperm are susceptible to alterations as dictated by their developmental stage at the time of the perturbation, and sperm and seminal plasma likely have both dependent and independent effects on offspring. Research using rodent models has revealed that many factors including over/under nutrition, dietary fat, protein, and ingredient composition (e.g., macro- or micronutrients), stress, exercise, and exposure to drugs, alcohol, and endocrine disruptors all elicit paternal programming responses that are evident in offspring phenotype. Research using livestock species has also revealed that sire age, fertility level, plane of nutrition, and heat stress can induce alterations in the epigenetic, oxidative stress, cytokine, and microbiome profiles of sperm and/or seminal plasma. In addition, recent findings in pigs, sheep, and cattle have indicated programming effects in blastocysts post-fertilization with some continuing into post-natal life of the offspring. Our research group is focused on understanding the effects of common management scenarios of plane of nutrition and growth rates in bulls and rams on mechanisms resulting in paternal programming and subsequent offspring outcomes. Understanding the implication of paternal programming is imperative as short-term feeding and management decisions have the potential to impact productivity and profitability of our herds for generations to come.

Investigating the impact of paternal age, paternal heat stress, and estimation of non-genetic paternal variance on dairy cow phenotype

“…Our results for the two factors analysed, together with the low estimates of non-genetic paternal variance differ from emerging evidence suggesting ejaculate-mediated non-genetic effects on offspring phenotypes, a phenomenon observed in various species, including livestock (reviewed in [ 3 ]). We attribute these discrepancies primarily to differences in experimental design.…”

“…The genetic models used to estimate breeding values or genetic variances in livestock species traditionally consider the sire’s effect as purely genetic. However, this assumption is being challenged by a growing body of evidence suggesting that in mammals, sires transmit more than just genetic material (e.g., small non-coding RNA or DNA methylation marks), and also that environmental contexts surrounding semen collection may play a significant role in shaping offspring phenotype [ 1 – 3 ].…”

Perspective: science and the future of livestock industries

“…This proliferation-apoptosis balance can also be affected during prenatal development, when undernutrition or stress seem to elicit epigenetic changes in developing gonads that affect offspring fertility in adult life. Indeed, the whole field of 'fetal programming' , or developmental origins of health and disease (DoHaD) has exploded since the first CGE paper was published in 2004, with evidence gathering for a lengthening list of productivity measures that are affected by epigenetic effects on sperm, oocytes, embryos and fetuses [eg., (17)(18)(19)(20)]. For postnatal life, it has become clear that puberty can be advanced by accelerating the accumulation of muscle as well as fat, a major advantage for meat production systems.…”