Decline in parenting behaviors by queen of naked mole-rats, Heterocephalus glaber

Abstract

Naked mole-rats (Heterocephalus glaber) is a eusocial rodent, and their colony consists of a single breeding female (the queen), several breeding males, and sexually immature adults (subordinates). Mother animals in mammals trigger the onset of maternal behaviors by the surge of estrogen level through their gestation. On the other hand, caring of pups in the naked mole-rat colony is not performed by the queen, but non-reproductive subordinates. The paper reviews the mechanisms by which subordinates trigger the onset of maternal behaviors and the queen decreases maternal behavior. Even though female subordinates can not synthesize estrogen from the placenta, their urinary estrogen concentration during the queen's gestation period was higher than during the queen's nonlactating period. Naked mole-rats routinely eat feces (coprophagy) excreted by other individuals, including those from the queen. The feces of queen included more estrogen during her gestation period than her non-lactating period. Furthermore, by oral ingestion of estrogen, subordinates increased the urinary estrogen concentration and enhanced the maternal response to pup vocalizations. These results suggest that subordinates ingest estrogen to trigger the onset of maternal behaviors through the coprophagy of pregnant queen feces. When subordinates became reproductive by separation from the queen and gave birth to pups, they decrease the number of maternal behaviors. Therefore, the queen does not innately unmotivated to care pups in innate and might acquire the neural changes to decrease maternal behaviors. It is reported that there are gene expression ifferences in the brain between the queen and subordinates. The gene expression associated with synthesis and reuptake of dopamine is upregulated in the queen's brain, such as tyrosine hydroxylase gene and dopamine transporter gene. However, the gene expression of dopamine receptor D1 and D2 are decreased in the brain of the queen, compared with subordinates. Dopamine receptor D1 and D2 are expressed in the striatum including nucleus accumbens and regulate the amount of maternal behavior in reproducing females. Taken together, the motherhood in naked mole-rats might be enhanced by the surge of estrogen level through the coprophagy and be restrained by the inhibition of dopamine receptor D1 and D2 gene expressions.