Antennae sense heat stress to inhibit mating and promote escaping in Drosophila females

Abstract

Environmental stress is a major factor that affects courtship behavior and evolutionary fitness. Although mature virgin females of Drosophila melanogaster usually accept a courting male to mate, they may not mate under stressful conditions. Above the temperature optimal for mating (20–25 °C), copulation success of D. melanogaster declines with increasing temperature although we observed vigorous courtship attempts by males, and no copulation takes place at temperatures over 36 °C. We attempted to identify the sensory pathway for detecting heat threat that drives a female to escape rather than to engage in mating that detects hot temperature and suppresses courtship behavior. We found that the artificial activation of warmth-sensitive neurons (‘hot cells’) in the antennal arista of females completely abrogates female copulation success even at permissive temperatures below 32 °C. Moreover, mutational loss of the GR28b.d thermoreceptor protein caused females to copulate even at 36 °C. These results indicate that antennal hot cells provide the input channel for detecting the high ambient temperature in the control of virgin female mating under stressful conditions.

Keywords:

• Copulation
• temperature
• Gr28b.d
• hot cells
• arista
• antennal lobe glomerulus

Acknowledgments

We thank H. Amrein, K. Asahina, R. Benton, B. Dickson, M. Gallio, Y. Ishikawa, G. Miesenböck, C. O’Kane, V. Thoma, the Bloomington Drosophila Stock Center, KYOTO Stock Center (DGRC) at Kyoto Institute of Technology, and the Vienna Drosophila Resource Center for fly stocks, and A. Utsumi for secretarial assistance.

Disclosure statement

No potential conflict of interest was reported by the authors.

Additional information

Funding

This work was supported, in part, by Grants-in-Aid for Scientific Research from MEXT to D.Y. (Nos. 17K19371, 17H05935 and 16H06371) and M.K. (Nos. 17H05544, 15H01412 and 15H04397).