Nociceptive neurons protect Drosophila larvae from parasitoid wasps.
BACKGROUND
Natural selection has resulted in a complex and fascinating repertoire of innate behaviors that are produced by insects. One puzzling example occurs in fruit fly larvae that have been subjected to a noxious mechanical or thermal sensory input. In response, the larvae "roll" with a motor pattern that is completely distinct from the style of locomotion that is used for foraging.


RESULTS
We have precisely mapped the sensory neurons that are used by the Drosophila larvae to detect nociceptive stimuli. By using complementary optogenetic activation and targeted silencing of sensory neurons, we have demonstrated that a single class of neuron (class IV multidendritic neuron) is sufficient and necessary for triggering the unusual rolling behavior. In addition, we find that larvae have an innately encoded preference in the directionality of rolling. Surprisingly, the initial direction of rolling locomotion is toward the side of the body that has been stimulated. We propose that directional rolling might provide a selective advantage in escape from parasitoid wasps that are ubiquitously present in the natural environment of Drosophila. Consistent with this hypothesis, we have documented that larvae can escape the attack of Leptopilina boulardi parasitoid wasps by rolling, occasionally flipping the attacker onto its back.


CONCLUSIONS
The class IV multidendritic neurons of Drosophila larvae are nociceptive. The nociception behavior of Drosophila melanagaster larvae includes an innately encoded directional preference. Nociception behavior is elicited by the ecologically relevant sensory stimulus of parasitoid wasp attack.
Hwang
Richard Y
RY
Department of Neurobiology, Duke University Medical Center, Durham, North Carolina 27710.
Zhong
Lixian
L
Department of Pharmacology, Duke University Medical Center, Durham, North Carolina 27710.
Xu
Yifan
Y
Department of Anesthesiology, Duke University Medical Center, Durham, North Carolina 27710.
Johnson
Trevor
T
Department of Neurobiology, Duke University Medical Center, Durham, North Carolina 27710.
Zhang
Feng
F
Department of Bioengineering, Duke University Medical Center, Durham, NC; 27710.|Department of Psychiatry, Stanford University, Stanford, California 94305.
Deisseroth
Karl
K
Department of Bioengineering, Duke University Medical Center, Durham, NC; 27710.|Department of Psychiatry, Stanford University, Stanford, California 94305.
Tracey
W Daniel
WD
Department of Anesthesiology, Duke University Medical Center, Durham, North Carolina 27710.|Department of Neurobiology, Duke University Medical Center, Durham, North Carolina 27710.|Department of Cell Biology, Duke University Medical Center, Durham, North Carolina 27710.
D000818:Animals; D030801:Animals, Genetically Modified / Q000502:physiology; D004330:Drosophila / Q000235:genetics / Q000502:physiology*; D004924:Escape Reaction / Q000502:physiology*; D005260:Female; D006790:Host-Parasite Interactions / Q000502:physiology*; D006358:Hot Temperature; D007814:Larva / Q000502:physiology; D008297:Male; D009474:Neurons / Q000502:physiology; D009619:Nociceptors / Q000502:physiology; D014863:Wasps / Q000502:physiology*