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. Abstract We 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. Maternal and postweaning HF diets independently altered oestrous cyclicity in females: female offspring of 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. Maternal and postweaning nutritional signals, independent of maternal care, alter offspring body fat pre‐puberty and female reproductive function in adulthood, which may be associated with advanced ovarian ageing and altered fertility.