Edited by Raghavendra Gadagkar, Indian Institute of Science, Bangalore, India, and approved July 10, 2018 (received for review November 27, 2017)
In a colony of naked mole-rats, instead of a single breeding female (the queen) nursing alone, sexually immature members (subordinates) show positive alloparental pup care. Their response to pup vocalizations is not continuous, but rather is enhanced during the queen’s postpartum period through consumption of the pregnant queen’s feces. Furthermore, oral ingestion of the pregnant queen’s feces also induces an increase in the subordinates’ estradiol concentrations. Because subordinates’ responses to pup vocalizations were enhanced through the ingestion of nonpregnant queen’s feces amended with estradiol, we concluded that estradiol is the substance that enhances their responses to pup vocalizations in naked mole-rats. Moreover, these results suggest that naked mole-rats communicate the substance between the queen and subordinates through coprophagy.
Naked mole-rats form eusocial colonies consisting of a single breeding female (the queen), several breeding males, and sexually immature adults (subordinates). Subordinates are cooperative and provide alloparental care by huddling and retrieving pups to the nest. However, the physiological mechanism(s) underlying alloparental behavior of nonbreeders remains undetermined. Here, we examined the response of subordinates to pup voice and the fecal estradiol concentrations of subordinates during the three reproductive periods of the queen, including gestation, postpartum, and nonlactating. Subordinate response to pup voice was observed only during the queen’s postpartum and was preceded by an incremental rise in subordinates’ fecal estradiol concentrations during the queen’s gestation period, which coincided with physiological changes in the queen. We hypothesized that the increased estradiol in the queen’s feces was disseminated to subordinates through coprophagy, which stimulated subordinates’ responses to pup vocalizations. To test this hypothesis, we fed subordinates either fecal pellets from pregnant queens or pellets from nonpregnant queens amended with estradiol for 9 days and examined their response to recorded pup voice. In both treatments, the subordinates exhibited a constant level of response to pup voice during the feeding period but became more responsive 4 days after the feeding period. Thus, we believe that we have identified a previously unknown system of communication in naked mole-rats, in which a hormone released by one individual controls the behavior of another individual and influences the level of responsiveness among subordinate adults to pup vocal signals, thereby contributing to the alloparental pup care by subordinates.
Author contributions: A.W., S.M., K. Miura, K. Mogi, and T.K. designed research; A.W., N.A., and S.M. performed research; H.O. contributed new reagents/analytic tools; A.W., K. Mogi, and T.K. analyzed data; and A.W. and K. Mogi wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1720530115/-/DCSupplemental.
Published under the PNAS license.
