A neuronal mechanism controlling the choice between feeding and sexual behaviors in Drosophila

Sherry J Cheriyamkunnel, Saloni Rose, Pedro F Jacob, Lauren A Blackburn, Shaleen Glasgow, Jacob Moorse, Mike Winstanley, Patrick J Moynihan, Scott Waddell, Carolina Rezaval

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Abstract

Animals must express the appropriate behavior that meets their most pressing physiological needs and their environmental context. However, it is currently unclear how alternative behavioral options are evaluated and appropriate actions are prioritized. Here, we describe how fruit flies choose between feeding and courtship; two behaviors necessary for survival and reproduction. We show that sex- and food-deprived male flies prioritize feeding over courtship initiation, and manipulation of food quality or the animal's internal state fine-tunes this decision. We identify the tyramine signaling pathway as an essential mediator of this decision. Tyramine biosynthesis is regulated by the fly's nutritional state and acts as a satiety signal, favoring courtship over feeding. Tyramine inhibits a subset of feeding-promoting tyramine receptor (TyrR)-expressing neurons and activates P1 neurons, a known command center for courtship. Conversely, the perception of a nutritious food source activates TyrR neurons and inhibits P1 neurons. Therefore, TyrR and P1 neurons are oppositely modulated by starvation, via tyramine levels, and food availability. We propose that antagonistic co-regulation of neurons controlling alternative actions is key to prioritizing competing drives in a context- dependent manner.

Original languageEnglish
Pages (from-to)4231-4245.e4
JournalCurrent Biology
Volume31
Issue number19
Early online date5 Aug 2021
DOIs
Publication statusPublished - 11 Oct 2021

Bibliographical note

Funding Information:
We thank Andrew Lin, Nuria Romero, and Anissa Kempf for insightful comments and critical assessment of the manuscript. We are grateful to Jan A. Veenstra, Edward Blumenthal, Sarah Certel, Henrike Scholz, Carsten Duch, Thomas Preat, Pierre-Yves Pla?ais, David Anderson, Kim Young-Joon, and Yi Rao for sharing fly stocks or antibodies with us. We thank Alessandro di Maio and the Birmingham Advanced Light Microscopy (BALM) facility for support with confocal microscopy. We would also like to thank Raksha Gohel for help with fly collection and immunohistochemistry, Anand Singh and Saverio Brogna for help with qRT-PCR experiments, Budhaditya Choudhary for help with tracing the trajectories of behaving flies, and Laurie Cazale-Debat for the schematics. Finally, we thank members of the Rezaval lab for useful comments on the manuscript. This work was supported by BBSRC (BB/S009299/1), Wellcome Trust (214062/Z/18/Z), and Royal Society Research (RGS\R2\180272) to C.R.; a Darwin studentship to S.R.; and a BBSRC David Phillips fellowship to P.J.M. Conceptualization, S.J.C. S.R. and C.R.; Methodology, S.J.C. S.R. P.F.J. L.A.B. S.G. J.M. M.W. P.J.M. S.W. and C.R.; Investigation, J.C. S.R. P.F.J. L.A.B. S.G. J.M. M.W. P.J.M. and C.R.; Resources, C.R.; Writing, S.J.C. S.R. P.F.J. S.W. and C.R.; Supervision, C.R.; Funding Acquisition, C.R. The authors declare no competing interests.

Keywords

  • Drosophila
  • action selection
  • courtship
  • decision-making
  • feeding
  • mating
  • motivation
  • sensory conflict
  • tyramine

ASJC Scopus subject areas

  • Neuroscience(all)
  • Biochemistry, Genetics and Molecular Biology(all)
  • Agricultural and Biological Sciences(all)

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