Drosophila Avoids Parasitoids by Sensing Their Semiochemicals via a Dedicated Olfactory Circuit

PLoS Biol. 2015 Dec 16;13(12):e1002318. doi: 10.1371/journal.pbio.1002318. eCollection 2015 Dec.

Abstract

Detecting danger is one of the foremost tasks for a neural system. Larval parasitoids constitute clear danger to Drosophila, as up to 80% of fly larvae become parasitized in nature. We show that Drosophila melanogaster larvae and adults avoid sites smelling of the main parasitoid enemies, Leptopilina wasps. This avoidance is mediated via a highly specific olfactory sensory neuron (OSN) type. While the larval OSN expresses the olfactory receptor Or49a and is tuned to the Leptopilina odor iridomyrmecin, the adult expresses both Or49a and Or85f and in addition detects the wasp odors actinidine and nepetalactol. The information is transferred via projection neurons to a specific part of the lateral horn known to be involved in mediating avoidance. Drosophila has thus developed a dedicated circuit to detect a life-threatening enemy based on the smell of its semiochemicals. Such an enemy-detecting olfactory circuit has earlier only been characterized in mice and nematodes.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Alkaloids / pharmacology
  • Animals
  • Animals, Genetically Modified
  • Behavior, Animal / drug effects
  • Bridged Bicyclo Compounds, Heterocyclic / pharmacology
  • Drosophila Proteins / agonists*
  • Drosophila Proteins / genetics
  • Drosophila Proteins / metabolism
  • Drosophila melanogaster / drug effects*
  • Drosophila melanogaster / genetics
  • Drosophila melanogaster / parasitology
  • Drosophila melanogaster / physiology
  • Female
  • Iridoids / pharmacology
  • Larva / drug effects
  • Larva / genetics
  • Larva / parasitology
  • Larva / physiology
  • Mutant Proteins / agonists
  • Mutant Proteins / metabolism
  • Nerve Tissue Proteins / agonists*
  • Nerve Tissue Proteins / genetics
  • Nerve Tissue Proteins / metabolism
  • Odorants
  • Olfactory Bulb / drug effects*
  • Olfactory Bulb / metabolism
  • Oviposition
  • Protein Isoforms / agonists
  • Protein Isoforms / metabolism
  • Pyridines / pharmacology
  • Receptors, Odorant / agonists*
  • Receptors, Odorant / genetics
  • Receptors, Odorant / metabolism
  • Sensory Receptor Cells / drug effects*
  • Sensory Receptor Cells / metabolism
  • Signal Transduction
  • Terpenes / pharmacology
  • Wasps / metabolism*

Substances

  • Alkaloids
  • Bridged Bicyclo Compounds, Heterocyclic
  • Drosophila Proteins
  • Iridoids
  • Mutant Proteins
  • Nerve Tissue Proteins
  • Protein Isoforms
  • Pyridines
  • Receptors, Odorant
  • Terpenes
  • nepetalactol
  • actinidine
  • iridomyrmecin

Grant support

The study was funded by the Max Planck Society (DE 129517720 to BSH), the DFG (STP 966/1-1 to JS), and the German Federal Ministry of Education and REseachr (BMBF1 to SS). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.