Responses to pup vocalizations in subordinate naked mole-rats are induced by estradiol ingested through coprophagy of queen’s feces

Akiyuki Watarai, Natsuki Arai, Shingo Miyawaki, Hideyuki Okano, Kyoko Miura, Kazutaka Mogi, Takefumi Kikusui

Research output: Contribution to journalArticle

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Abstract

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.

Original languageEnglish
Pages (from-to)9264-9269
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume115
Issue number37
DOIs
Publication statusPublished - 2018 Sep 11

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Coprophagia
Mole Rats
Feces
Estradiol
Postpartum Period
Breeding
Pregnancy
Behavior Control
Reproduction
Communication
Hormones

Keywords

  • Alloparental behavior
  • Coprophagy
  • Estradiol
  • Naked mole-rats

ASJC Scopus subject areas

  • General

Cite this

Responses to pup vocalizations in subordinate naked mole-rats are induced by estradiol ingested through coprophagy of queen’s feces. / Watarai, Akiyuki; Arai, Natsuki; Miyawaki, Shingo; Okano, Hideyuki; Miura, Kyoko; Mogi, Kazutaka; Kikusui, Takefumi.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 115, No. 37, 11.09.2018, p. 9264-9269.

Research output: Contribution to journalArticle

Watarai, Akiyuki ; Arai, Natsuki ; Miyawaki, Shingo ; Okano, Hideyuki ; Miura, Kyoko ; Mogi, Kazutaka ; Kikusui, Takefumi. / Responses to pup vocalizations in subordinate naked mole-rats are induced by estradiol ingested through coprophagy of queen’s feces. In: Proceedings of the National Academy of Sciences of the United States of America. 2018 ; Vol. 115, No. 37. pp. 9264-9269.
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