Nature, nurture or nutrition? Impact of maternal nutrition on maternal care, offspring development and reproductive function

Abstract

Key points• Maternal high fat nutrition during pregnancy and lactation significantly reduced maternal care during the early neonatal period; but reduced maternal care was not associated with an offspring phenotype.• Maternal high fat nutrition resulted in maternal obesity characterized by increased fat mass, hyperleptinaemia, hyperinsulinaemia.• Maternal high fat nutrition resulted in fatter offspring before puberty and advanced pubertal onset.• Adult female offspring of high fat-fed mothers have altered reproductive function, reflected in an increased likelihood of prolonged or persistent oestrus.• These phenotypic effects were not related to maternal care suggesting that poor maternal nutrition, rather than inadequate maternal care, could be the primary driver of the observed alterations in offspring development and reproductive function. AbstractWe have previously reported that offspring of mothers fed a high fat (HF) diet during pregnancy and lactation enter puberty early and are hyperleptinaemic, hyperinsulinaemic and obese as adults. Poor maternal care and bonding can also impact offspring development and disease risk. We therefore hypothesized that prenatal nutrition would affect maternal care and that an interaction may exist between a maternal HF diet and maternal care, subsequently impacting on offspring phenotype. Wistar rats were mated and randomized to control dams fed a control diet (CON) or dams fed a HF diet from conception until the end of lactation (HF). Maternal care was assessed by observing maternal licking and grooming of pups between postnatal day (P)3 and P8. Postweaning (P22), offspring were fed a control (-con) or HF (-hf) diet. From P27, pubertal onset was assessed. At ∼P105 oestrous cyclicity was investigated. Maternal HF diet reduced maternal care; HF-fed mothers licked and groomed pups less than CON dams. Maternal fat:lean ratio was higher in HF dams at weaning and was associated with higher maternal plasma leptin and insulin concentrations, but there was no effect of maternal care on fat:lean ratio or maternal hormone levels. Both female and male offspring of HF dams were lighter from birth to P11 than offspring of CON dams, but by P19, HF offspring were heavier than controls. Prepubertal retroperitoneal fat mass was greater in pups from HF-fed dams compared to CON and was associated with elevated circulating leptin concentrations in females only, but there was neither an effect of maternal care, nor an interaction between maternal diet and care on prepubertal fat mass. Pups from HF-fed dams went into puberty early and this effect was exacerbated by a postweaning HF diet. HF-fed mothers were more likely to have prolonged or persistent oestrus, whilst female offspring fed a HF diet postweaning were more likely to have irregular oestrous cycles and were more likely to have prolonged or persistent oestrus. These data indicate that maternal HF nutrition during pregnancy and lactation results in a maternal obese phenotype and has significant impact on maternal care during lactation. Mat...

Is in utero exposure to maternal socioeconomic disadvantage related to offspring ovarian reserve in adulthood?

“…This suggests that early life adversity exposures in Bangladeshi neighborhoods, possibly reflecting exposures to nutritional stress, infectious disease, or other yet unidentified stressors, may detrimentally impact adulthood reproductive health outcomes. In animal models, experimental studies have focused on poor maternal nutritional status in particular, showing maternal undernutrition and malnutrition were related to markers of impaired folliculogenesis, lower ovarian reserve, and increased oxidative stress in the adult offspring [63][64][65][66][67]. Consistent with these findings, in a prior study of women, maternal nutritional deprivation during famine was associated with earlier menopausal timing in the offspring [44] as was pre-pregnancy diabetes [43].…”

Gene-Environment Interactions Controlling Energy and Glucose Homeostasis and the Developmental Origins of Obesity

“…Depending on the timing of stress and the sex of the offspring, adverse offspring outcomes of prenatal stress include permanent dysfunction of the neuroendocrine axis (237) and stress responsiveness (160,208), delayed learning (160) and abnormal glucose tolerance, hyperphagia, as well as increased body weight and adiposity (111,363,387,508,546). Importantly, prenatal stress results in less maternal grooming and attention in offspring (81,418), which can have important effects on offspring behavior and metabolic phenotype (80,81,95). In keeping with these fetal/neonatematernal interactions, at least some of the abnormalities in offspring stress responsivity can be reversed by blocking the mother's stress-induced corticosterone response (32), by fostering their offspring to nonstressed dams (32) or by postnatal handling (482).…”

Maternal Overweight Disrupts the Sexual Maturation of the Offspring

“…However, they did not study these offspring at birth or after birth. Connor et al 14 found that the female offspring of high-fat-fed dams were lighter at birth than the offspring of control dams. However, at weaning, these pups were significantly heavier than the offspring of control dams.…”

“…12 In female rats, pubertal timing and subsequent ovarian function are influenced by the nutritional status in utero, with both maternal caloric restriction and maternal high-fat nutrition, resulting in early pubertal onset. 13 Connor et al 14 found that pups from high-fat-fed dams exhibit early puberty and irregular estrous cycles by having a prolonged and persistent estrus. All these data indicate that a poor quality of nutrition, by either excess or restriction, can disrupt the ovarian 1 Universidad de Buenos Aires, Facultad de Medicina, Departamento de Toxicología y Farmacología, Buenos Aires, Argentina 2 Universidad de Buenos Aires, Consejo Nacional de Investigaciones Científi-cas y Técnicas (CONICET), Centro de Estudios Farmacoló gicos y Botánicos (CEFYBO), Facultad de Medicina, Buenos Aires, Argentina function, especially the development and quality of oocytes.…”