Review: Epigenetics, developmental programming and nutrition in herbivores

Abstract

Epidemiological studies in humans and animal models (including ruminants and horses) have highlighted the critical role of nutrition on developmental programming. Indeed, it has been demonstrated that the nutritional environment during the periconceptional period and foetal development can altered the postnatal performance of the resultant offspring. This nutritional programming can be exerted by maternal and paternal lineages and can affect offspring beyond the F1 generation. Alterations in epigenetic mechanisms have been proposed as the causative link behind the programming trajectories observed in the offspring. Although a clear cause-effect relationship between epigenetic modifications during early development and later offspring phenotype has not been demonstrated in livestock species, strong associations have been reported for some epigenetic marks (e.g. messenger RNA) that are worth exploring as possible predictors of future offspring phenotype. In this review, we shortly describe the main epigenetic mechanisms studied so far in mammals (i.e. mainly in the mouse) thought to be associated with developmental programming, and discuss the few studies available in mammalian herbivores (e.g. cattle) showing the effect of nutrition on epigenetic marks and the associated phenotype. Clearly, there is a need to develop research on nutritional strategies capable of modulating the epigenetic machinery with positive influence on the phenotype of livestock herbivores. This type of research is needed to alleviate the challenges currently faced by the livestock industry (e.g. impaired fertility of high-yielding dairy cows). This in turn will have a positive influence on animal welfare and productivity of livestock enterprises.

Associations between maternal characteristics and health, survival, and performance of dairy heifers from birth through first lactation

“…Although not evaluated in our study, it is important to mention that epigenetic changes are often associated with developmental programming. Environmental factors such as nutrition and stressors have already been shown to have effects on epigenetic marks in multiple tissues and were associated with distinct phenotypes of the offspring (Chavatte-Palmer et al, 2018;Skibiel et al, 2018). Differences in epigenetics result in changes of gene expression and biology of tissues, which ultimately can affect the observed phenotypes.…”

“…In addition to its importance in biomedical sciences, the main concepts of DOHaD seem to be also relevant for livestock, not only to animal health but also to production performance. For instance, there is growing evi-dence that environmental and maternal characteristics during gestation can influence health, reproduction, and production traits in ruminants (Berry et al, 2008;Opsomer et al, 2016;Chavatte-Palmer et al, 2018;Vonnahme et al, 2018). Nonetheless, multiple research models used to study DOHaD in livestock animals were developed as proof of concept, and not necessarily reflect conditions commonly observed in commercial herds.…”

Physiological development of the equine fetus during late gestation

“…Changes in fetal growth and development induced by alterations in placental development and maternal dietary intake may have consequences for the foal long after birth . In other species, both epidemiological and experimental studies have shown that environmental conditions during early life have an important role in determining the adult physiological phenotype that develops from the genotype inherited at conception, even when there is little if any change in birth weight .…”

“…To date, the pre‐ and post‐natal studies suggest that developmental programming of equine physiological phenotype by environmental conditions in utero tracks from intra‐ to extra‐uterine life and is related to alterations in resource allocation to the fetus, mediated, in part, by the accompanying changes in placental development (Table ). This potential role of the placenta in developmental programming also has implications for the phenotype of foals produced by assisted reproductive technologies because use of in vitro culture and a recipient uterus unprimed by a natural embryo produces an abnormal environment for development that can alter embryonic cell fate decisions and trophoblast differentiation epigenetically .…”

Effects of maternal protein supplementation and inclusion of rumen‐protected fat in the finishing diet on nutrient digestibility and expression of intestinal genes in Nellore steers

“…Few studies evaluated the consequences of fetal programming on the gastrointestinal tract (GIT) of adult ruminants, even though it plays an essential role in the whole organism (Guilloteau, Zabielski, Hammon, & Metges, ), affecting nutrient utilization of the offspring from suckling to finishing phases (Peñagaricano, Wang, Rosa, Radunz, & Khatib, ). According to Chavatte‐Palmer, Velazquez, Jammes, and Duranthon (), alterations in epigenetic marks are the link between maternal nutrition and offspring phenotype in mammalian. Therefore, genes responsible to encode proteins involved in intestine development, as well as membrane transporters, could be down‐ or up‐regulated by epigenetic changes, which could affect nutrient absorption as carbohydrates or fatty acids later in life.…”