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Queen contact and among-worker interactions dually suppress worker brain dopamine as a potential regulator of reproduction in an ant

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Abstract

How individual organisms whose behavior is potentially driven by selfish interests cooperate to form a society is a central question in evolutionary biology. Worker reproduction and its suppression in eusocial insects provide an illuminating model of such a conflict resolution. Although many theoretical and empirical studies focus on the nature and evolutionary consequences of this reproductive conflict, little is known about its physiological underpinnings. Here, we hypothesized that the dopaminergic system, which has a gonadotropic function in eusocial Hymenoptera, is controlled by social suppression via the queen presence signal and the worker-worker dominance interactions. In Diacamma sp. from Japan, the queen presence signal is transferred to workers by direct contact, and worker-worker dominance interaction occurs commonly in large colonies, even when a queen is present. Using the ant Diacamma sp., we showed that the aggressive interactions among workers suppressed brain dopamine levels of the workers. Moreover, our data suggest that the queen presence signal transmitted by direct contact suppresses the brain dopamine level and the transcription of dopamine synthetic enzyme (ddc) of workers. Our data provide clear empirical evidence that worker brain dopamine is suppressed by both social stimuli directed from dominant workers and the queen.

Significance statement

In eusocial Hymenoptera, worker reproduction is suppressed by social interactions such as queen presence information and dominance interaction. Dopamine, one of the biogenic amines, is a well-known gonadotropic neurohormone in eusocial Hymenoptera. Honeybee studies revealed that the queen presence information regulated dopamine levels in worker brains. In an ant, the dominance interaction also controlled dopamine levels of workers. In a queenless ant Diacamma sp., queen presence information and dominance interaction are known to dually suppress worker reproduction. Given the above examples, dopaminergic signaling is predicted to be a general mechanism that can suppress worker reproduction in multiple ways. We here test whether both the queen- and worker-originated signals (i.e., queen presence information and dominance interaction) affect the worker dopamine level. We show that dopaminergic signaling is affected by dual social factors, suggesting the general role of dopaminergic signaling in mediating social interaction and reproductive suppression.

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Acknowledgements

We are grateful to Devin, O’Brian for editing an early version of this manuscript. We thank Takashi Watanabe for the discussion and Haruki Tatsuta and Chifune Sasa for the ant collection. We also thank Yasuhiro Sugime, Run Minoura, and Kohei Oguchi for the molecular analyses and Masahito Kimura for the experimental setup. We also thank Alison Mercer and two anonymous referees for comments on an earlier draft. This work was supported by Grant-in-Aid for JSPS Fellows (no. 13J04279 to HS), KAKENHI (no. 23300113 to HA; nos. 26249024, 25660266, 25304014, 23405011, 15H04425, 15H02652 to KT; nos. 25251041, 2525104 to MT; no. 26440181 to KS; no.26870121 to YO).

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Authors and Affiliations

  1. Graduate School of Environmental Science, Hokkaido University, Sapporo, Hokkaido, Japan

    Hiroyuki Shimoji & Toru Miura

  2. Faculty of Agriculture, University of the Ryukyus, Nishihara, Okinawa, Japan

    Hiroyuki Shimoji & Kazuki Tsuji

  3. Research Institute for Electronic Science, Hokkaido University, Sapporo, Hokkaido, Japan

    Hitoshi Aonuma

  4. CREST, Japan Science and Technology Agency, Kawaguchi, Saitama, Japan

    Hitoshi Aonuma

  5. Graduate School of Agriculture, Tamagawa University, Machida, Tokyo, Japan

    Ken Sasaki

  6. Graduate School of Arts and Sciences, University of Tokyo, Komaba, Tokyo, Japan

    Yasukazu Okada

Authors
  1. Hiroyuki Shimoji
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  2. Hitoshi Aonuma
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  3. Toru Miura
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  4. Kazuki Tsuji
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  5. Ken Sasaki
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  6. Yasukazu Okada
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Corresponding authors

Correspondence to Hiroyuki Shimoji or Yasukazu Okada.

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Communicated by W. Hughes

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Shimoji, H., Aonuma, H., Miura, T. et al. Queen contact and among-worker interactions dually suppress worker brain dopamine as a potential regulator of reproduction in an ant. Behav Ecol Sociobiol 71, 35 (2017). https://doi.org/10.1007/s00265-016-2263-3

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  • DOI: https://doi.org/10.1007/s00265-016-2263-3

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