Placental adaptation to maternal environment in domestic animals

The developmental origins of health and disease (DOHaD) is based on the observation that environmental conditions during sensitive windows of development shape lifelong physiology and disease susceptibility. While fetal organs are often viewed as direct programming targets, the placenta is a crucial mechanistic hub because it senses maternal conditions and actively constructs the fetal environment through nutrient transport, endocrine signaling, and immune regulation. Placental plasticity spans morphology and how exchanges are favored by tissue topology, vascular development and perfusion, transporter density/localization, mitochondrial metabolism, inflammatory status tone, and endocrine outputs. These adaptive responses can mitigate short-term threats to fetal survival, but also readjust developmental signals (including exposure to nutrients, oxygen, and glucocorticoids) with enduring consequences, particularly when prenatal and postnatal environments are mismatched. This review synthesizes data showing that adverse maternal environments in domestic species induce conserved functional responses-vascular remodeling, altered nutrient transport capacity, endocrine regulation and inflammatory signaling-while species-specific placental architecture constrains adaptative capacity. In ruminants, cotyledonary placentomes exhibit compensatory changes in placentome type, vascularization and transport systems in cases of undernutrition, while heat stress induces placental remodeling associated with changes in placental inflammation, oxygen regulation, and epigenomic/transcriptomic remodeling with measurable neonatal phenotypes. In horses, diffuse microcotyledonary placentation links fetal growth to allantochorion size and microcotyledon density, uterine capacity, parity/age and maternal metabolic status modulate placental vascular structure and gene expression, with postnatal growth and metabolic effects. In pigs, diffuse folded placentation and litter-bearing competition reveal strong within-litter variability. Intrauterine crowding and maternal heat stress lead to fold- and efficiency-related (in terms of transporter expression) remodeling and alter placental nutrient transport and metabolic gene networks. Finally, we highlight the importance of studying placental epigenetic marks as molecular "memory" of in utero exposures and propose future directions for the search for in vivo biomarkers-especially circulating placental extracellular vesicles and microRNAs-associated with in-depth placental phenotyping that could allow for risk assessment during pregnancy and then targeted interventions in veterinary and production settings.