Neuropeptides Modulate Female Chemosensory Processing upon Mating in Drosophila

PLoS Biol. 2016 May 4;14(5):e1002455. doi: 10.1371/journal.pbio.1002455. eCollection 2016 May.

Abstract

A female's reproductive state influences her perception of odors and tastes along with her changed behavioral state and physiological needs. The mechanism that modulates chemosensory processing, however, remains largely elusive. Using Drosophila, we have identified a behavioral, neuronal, and genetic mechanism that adapts the senses of smell and taste, the major modalities for food quality perception, to the physiological needs of a gravid female. Pungent smelling polyamines, such as putrescine and spermidine, are essential for cell proliferation, reproduction, and embryonic development in all animals. A polyamine-rich diet increases reproductive success in many species, including flies. Using a combination of behavioral analysis and in vivo physiology, we show that polyamine attraction is modulated in gravid females through a G-protein coupled receptor, the sex peptide receptor (SPR), and its neuropeptide ligands, MIPs (myoinhibitory peptides), which act directly in the polyamine-detecting olfactory and taste neurons. This modulation is triggered by an increase of SPR expression in chemosensory neurons, which is sufficient to convert virgin to mated female olfactory choice behavior. Together, our data show that neuropeptide-mediated modulation of peripheral chemosensory neurons increases a gravid female's preference for important nutrients, thereby ensuring optimal conditions for her growing progeny.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Animals, Genetically Modified
  • Drosophila Proteins / genetics
  • Drosophila Proteins / metabolism*
  • Drosophila melanogaster / physiology*
  • Female
  • Male
  • Oviposition / physiology
  • Peptides / genetics
  • Peptides / metabolism*
  • Polyamines
  • Receptors, Ionotropic Glutamate / genetics
  • Receptors, Ionotropic Glutamate / metabolism*
  • Receptors, Peptide
  • Sensory Receptor Cells / physiology
  • Sexual Behavior, Animal / physiology*
  • Signal Transduction
  • Sodium Channels / genetics
  • Sodium Channels / metabolism*

Substances

  • Drosophila Proteins
  • IR76b protein, Drosophila
  • Peptides
  • Polyamines
  • Receptors, Ionotropic Glutamate
  • Receptors, Peptide
  • Sodium Channels
  • myoinhibitory peptide, Drosophila
  • sex peptide receptor, Drosophila

Grants and funding

This study was generously supported by a Boehringer Ingelheim Exploration Grant to ICGK (http://www.boehringer-ingelheim-stiftung.de/de/was-wir-foerdern/exploration-grants.html), the Max Planck Society to ICGK (www.mpg.de), an ERC starting grant, Grant number: 637472 to ICGK, (https://erc.europa.eu/funding-and-grants/funding-schemes/starting-grants), and the EMBO Young Investigator award to ICGK (www.embo.org) The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.