Display options
Share it on

Curr Biol. 2021 Oct 11;31(19):4231-4245.e4. doi: 10.1016/j.cub.2021.07.029. Epub 2021 Aug 05.

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

Current biology : CB

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

Affiliations

  1. School of Biosciences, University of Birmingham, Birmingham B15 2TT, UK.
  2. Centre for Neural Circuits and Behaviour, University of Oxford, Oxford OX1 3SR, UK.
  3. School of Biosciences, University of Birmingham, Birmingham B15 2TT, UK. Electronic address: [email protected].

PMID: 34358444 PMCID: PMC8538064 DOI: 10.1016/j.cub.2021.07.029

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.

Copyright © 2021 The Authors. Published by Elsevier Inc. All rights reserved.

Keywords: Drosophila; action selection; courtship; decision-making; feeding; mating; motivation; sensory conflict; tyramine

Conflict of interest statement

Declaration of interests The authors declare no competing interests.

References

  1. Neuron. 2013 Aug 21;79(4):754-65 - PubMed
  2. Neuron. 2016 Jul 6;91(1):168-81 - PubMed
  3. Neuron. 2008 Sep 11;59(5):759-69 - PubMed
  4. Neuron. 2018 Jul 25;99(2):376-388.e6 - PubMed
  5. Annu Rev Entomol. 2005;50:447-77 - PubMed
  6. Curr Biol. 2010 Jun 8;20(11):1006-11 - PubMed
  7. Curr Biol. 2018 May 7;28(9):1445-1452.e3 - PubMed
  8. Elife. 2016 Nov 22;5: - PubMed
  9. Curr Opin Neurobiol. 2012 Aug;22(4):592-601 - PubMed
  10. Sci Rep. 2017 Dec;7(1):168 - PubMed
  11. Curr Biol. 2010 Jun 8;20(11):1000-5 - PubMed
  12. Curr Biol. 2016 Apr 4;26(7):972-980 - PubMed
  13. Elife. 2019 Mar 25;8: - PubMed
  14. Mol Brain. 2015 Dec 21;8:87 - PubMed
  15. Nature. 2012 Dec 20;492(7429):433-7 - PubMed
  16. Neuron. 2011 Feb 10;69(3):509-22 - PubMed
  17. Neuron. 2018 Apr 18;98(2):350-365.e5 - PubMed
  18. J Exp Biol. 2014 Aug 1;217(Pt 15):2796-805 - PubMed
  19. Sci Rep. 2015 Aug 10;5:13132 - PubMed
  20. Proc Natl Acad Sci U S A. 2019 Feb 26;116(9):3805-3810 - PubMed
  21. Curr Biol. 2016 Sep 12;26(17):2246-56 - PubMed
  22. Nature. 2008 Jun 26;453(7199):1244-7 - PubMed
  23. Aging (Albany NY). 2010 Aug;2(8):519-22 - PubMed
  24. Brain Res. 1985 Jun 3;335(2):207-12 - PubMed
  25. Neuron. 2011 Feb 10;69(3):498-508 - PubMed
  26. Neuron. 2015 Sep 2;87(5):1036-49 - PubMed
  27. Biomed Eng Online. 2003 May 17;2:13 - PubMed
  28. J Neurosci. 1996 Jun 15;16(12):3900-11 - PubMed
  29. J Insect Physiol. 2001 Dec;47(12):1467-1473 - PubMed
  30. Proc Biol Sci. 1996 Jun 22;263(1371):755-9 - PubMed
  31. Pharmacol Biochem Behav. 1994 Aug;48(4):1011-7 - PubMed
  32. Nat Commun. 2015 Mar 06;6:6457 - PubMed
  33. Nat Methods. 2012 Jun 28;9(7):676-82 - PubMed
  34. J Evol Biol. 2010 Jan;23(1):157-65 - PubMed
  35. Sci Rep. 2016 Jan 18;6:19441 - PubMed
  36. Nature. 2008 Jul 10;454(7201):217-20 - PubMed
  37. Behav Brain Res. 1984 Jun;12(3):275-81 - PubMed
  38. Anim Behav. 1966 Apr-Jul;14(2):226-35 - PubMed
  39. Elife. 2015 Dec 29;4: - PubMed
  40. Nat Commun. 2014 Aug 04;5:4560 - PubMed
  41. Nat Commun. 2017 Jul 28;8(1):154 - PubMed
  42. Physiol Behav. 1985 Aug;35(2):209-14 - PubMed
  43. Elife. 2016 Oct 22;5: - PubMed
  44. J Insect Sci. 2011;11:132 - PubMed
  45. Curr Biol. 2016 Sep 26;26(18):2508-2515 - PubMed
  46. Trends Endocrinol Metab. 2020 Jul;31(7):495-507 - PubMed
  47. Open Biol. 2019 Mar 29;9(3):180259 - PubMed
  48. J Neurophysiol. 1980 Feb;43(2):469-87 - PubMed
  49. Curr Opin Insect Sci. 2017 Dec;24:21-28 - PubMed
  50. Front Neurosci. 2013 Feb 12;7:12 - PubMed
  51. J Comp Neurol. 2009 Apr 20;513(6):643-67 - PubMed
  52. Curr Biol. 2011 May 10;21(9):746-50 - PubMed
  53. PLoS Genet. 2016 Sep 30;12(9):e1006346 - PubMed
  54. Neuron. 1990 Mar;4(3):343-54 - PubMed
  55. Nat Neurosci. 2013 May;16(5):526-8 - PubMed
  56. Curr Biol. 2003 Feb 18;13(4):R140-2 - PubMed
  57. Science. 2003 Dec 5;302(5651):1765-8 - PubMed
  58. Pharmacol Biochem Behav. 1983 Dec;19(6):945-50 - PubMed
  59. Cell. 2018 Aug 9;174(4):982-998.e20 - PubMed
  60. Sci Rep. 2016 Oct 19;6:35359 - PubMed
  61. Development. 1993 Jun;118(2):401-15 - PubMed
  62. Cell. 2014 Jan 16;156(1-2):221-35 - PubMed
  63. Neuron. 1995 Feb;14(2):341-51 - PubMed
  64. Neuron. 2016 Dec 7;92(5):1049-1062 - PubMed
  65. Nat Neurosci. 2014 Jun;17(6):884-9 - PubMed
  66. Curr Biol. 2017 Aug 7;27(15):2227-2238.e3 - PubMed
  67. Nature. 2011 Jun 08;474(7350):204-7 - PubMed
  68. Neuron. 2014 Jul 2;83(1):149-63 - PubMed
  69. PLoS One. 2018 Jun 27;13(6):e0198362 - PubMed
  70. Curr Biol. 2019 Jan 7;29(1):13-22.e3 - PubMed
  71. Nat Neurosci. 2019 Dec;22(12):2029-2039 - PubMed
  72. Curr Biol. 2017 May 8;27(9):1342-1349 - PubMed
  73. Neuron. 2016 Oct 5;92(1):187-201 - PubMed
  74. Elife. 2015 Nov 14;4:e11188 - PubMed
  75. Curr Biol. 2008 Oct 14;18(19):R928-32 - PubMed

Publication Types

Grant support