Olfactory Preference for Egg Laying on Citrus Substrates in Drosophila

• Published in: Current biology 2013-12, Vol.23 (24), p.2472-2480
• Main Authors: Dweck, Hany K.M., Ebrahim, Shimaa A.M., Kromann, Sophie, Bown, Deni, Hillbur, Ylva, Sachse, Silke, Hansson, Bill S., Stensmyr, Marcus C.
• Format: Article
• Language: English
• Subjects: Adaptation, Biological; Animals; Behavior, Animal - drug effects; Citrus; Citrus - chemistry; citrus fruits; Cyclohexenes - analysis; Cyclohexenes - pharmacology; Drosophila melanogaster; Drosophila melanogaster - parasitology; Drosophila melanogaster - physiology; Drosophila Proteins - physiology; eggs; endoparasitoids; fruits; functional properties; habitats; Host-Parasite Interactions; Hymenoptera; insect larvae; insects; odor compounds; Oviposition; oviposition sites; parasitism; progeny; Receptors, Odorant - physiology; risk; sensory neurons; Sesquiterpenes - analysis; Sesquiterpenes - pharmacology; smell; Terpenes - analysis; Terpenes - pharmacology; terpenoids; vinegars; Wasps - physiology
• ISSN: 0960-9822; 1879-0445
• DOI: 10.1016/j.cub.2013.10.047

Egg-laying animals, such as insects, ensure the survival of their offspring by depositing their eggs in favorable environments. To identify suitable oviposition sites, insects, such as the vinegar fly Drosophila melanogaster, assess a complex range of features. The fly selectively lays eggs in fermenting fruit. However, the precise cues and conditions that trigger oviposition remain unclear, including whether flies are also selective for the fruit substrate itself. Here, we demonstrate that flies prefer Citrus fruits as oviposition substrate. Flies detect terpenes characteristic of these fruits via a single class of olfactory sensory neurons, expressing odorant receptor Or19a. These neurons are necessary and sufficient for selective oviposition. In addition, we find that the Citrus preference is an ancestral trait, presumably representing an adaptation toward fruits found within the native African habitat. Moreover, we show that endoparasitoid wasps that parasitize fly larvae are strongly repelled by the smell of Citrus, as well as by valencene, the primary ligand of Or19a. Finally, larvae kept in substrates enriched with valencene suffer a reduced risk of parasitism. Our results demonstrate that a single dedicated olfactory pathway determines oviposition fruit substrate choice. Moreover, our work suggests that the fly’s fruit preference—reflected in the functional properties of the identified neuron population—stem from a need to escape parasitism from endoparasitoid wasps. •Flies prefer Citrus as oviposition substrate•This preference is mediated exclusively via Or19a•Or19a is found in intermediate sensillum neurons and is selective for Citrus terpenes•Citrus volatiles confer protection against endoparasitoid wasps