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

doi:10.1016/j.cub.2021.07.029

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

Biosciences

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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 language	English
Pages (from-to)	4231-4245.e4
Journal	Current Biology
Volume	31
Issue number	19
Early online date	5 Aug 2021
DOIs	https://doi.org/10.1016/j.cub.2021.07.029
Publication status	Published - 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)

Access to Document

10.1016/j.cub.2021.07.029Licence: Creative Commons: Attribution (CC BY)

CheriyamkunnelSJ2021neuronalFinal published version, 3.56 MBLicence: Creative Commons: Attribution (CC BY)

2 Finished
2 Active

To mate or to flee: neural mechanisms underlying action-selection
Rezaval, C.
Biotechnology & Biological Sciences Research Council
1/11/19 → 30/07/24
Project: Research Councils
Peptidoglycan release and recycling in pathogenic mycobacteria
Moynihan, P.
Biotechnology & Biological Sciences Research Council
1/04/19 → 31/03/25
Project: Research
Neuropeptidergic regulation of behavioural action-selection
Rezaval, C.
THE WELLCOME TRUST
1/03/19 → 1/03/22
Project: Research
Neural Basis of Action-Selection
Rezaval, C.
The Royal Society
5/10/18 → 4/10/19
Project: Research Councils

How Brains Work: Neurology, Fruit Flies and Human Understanding- Carolina Rezaval is interviewed in Scientific Podcast
Carolina Rezaval
29/09/21
1 Media contribution
Press/Media: Press / Media
Sex or food? When deprived of both, dinner wins out — at least for fruit flies
Carolina Rezaval
23/08/21
1 item of Media coverage
Press/Media: Press / Media
How does the brain make key decisions when eating or mating?Drosophila also understands "satisfying lust"!
Carolina Rezaval
23/08/21
1 item of Media coverage
Press/Media: Press / Media
To court or to eat? That is the question- Scientific Blog covering our story
Carolina Rezaval
19/08/21
1 Media contribution
Press/Media: Press / Media
Meals or intercourse? Fruit flies give perception into decision-making –
Carolina Rezaval
19/08/21
1 item of Media coverage
Press/Media: Press / Media
Fruit Flies Choose Food Over Sex When Deprived of Both- News Coverage
Carolina Rezaval
18/08/21
1 item of Media coverage
Press/Media: Press / Media
El cerebro masculino prefiere la comida al sexo
Carolina Rezaval
18/08/21
1 item of Media coverage
Press/Media: Press / Media

Cite this

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title = "A neuronal mechanism controlling the choice between feeding and sexual behaviors in Drosophila",

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.",

keywords = "Drosophila, action selection, courtship, decision-making, feeding, mating, motivation, sensory conflict, tyramine",

author = "Cheriyamkunnel, {Sherry J} and Saloni Rose and Jacob, {Pedro F} and Blackburn, {Lauren A} and Shaleen Glasgow and Jacob Moorse and Mike Winstanley and Moynihan, {Patrick J} and Scott Waddell and Carolina Rezaval",

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.",

year = "2021",

month = oct,

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doi = "10.1016/j.cub.2021.07.029",

language = "English",

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T1 - A neuronal mechanism controlling the choice between feeding and sexual behaviors in Drosophila

AU - Cheriyamkunnel, Sherry J

AU - Rose, Saloni

AU - Jacob, Pedro F

AU - Blackburn, Lauren A

AU - Glasgow, Shaleen

AU - Moorse, Jacob

AU - Winstanley, Mike

AU - Moynihan, Patrick J

AU - Waddell, Scott

AU - Rezaval, Carolina

N1 - 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.

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N2 - 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.

AB - 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.

KW - Drosophila

KW - action selection

KW - courtship

KW - decision-making

KW - feeding

KW - mating

KW - motivation

KW - sensory conflict

KW - tyramine

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DO - 10.1016/j.cub.2021.07.029

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SP - 4231-4245.e4

JO - Current Biology

JF - Current Biology

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ER -

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

Abstract

Bibliographical note

Keywords

ASJC Scopus subject areas

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