Pheromones mediating copulation and attraction in Drosophila

Abstract

Intraspecific olfactory signals known as pheromones play important roles in insect mating systems. In the model Drosophila melanogaster, a key part of the pheromone-detecting system has remained enigmatic through many years of research in terms of both its behavioral significance and its activating ligands. Here we show that Or47b-and Or88a-expressing olfactory sensory neurons (OSNs) detect the fly-produced odorants methyl laurate (ML), methyl myristate, and methyl palmitate. Fruitless (fru M )-positive Or47b-expressing OSNs detect ML exclusively, and Or47b-and Or47b-expressing OSNs are required for optimal male copulation behavior. In addition, activation of Or47b-expressing OSNs in the male is sufficient to provide a competitive mating advantage. We further find that the vigorous male courtship displayed toward oenocyte-less flies is attributed to an oenocyte-independent sustained production of the Or47b ligand, ML. In addition, we reveal that Or88a-expressing OSNs respond to all three compounds, and that these neurons are necessary and sufficient for attraction behavior in both males and females. Beyond the OSN level, information regarding the three fly odorants is transferred from the antennal lobe to higher brain centers in two dedicated neural lines. Finally, we find that both Or47b-and Or88a-based systems and their ligands are remarkably conserved over a number of drosophilid species. Taken together, our results close a significant gap in the understanding of the olfactory background to Drosophila mating and attraction behavior; while reproductive isolation barriers between species are created mainly by species-specific signals, the mating enhancing signal in several Drosophila species is conserved. Drosophila | pheromone | mating | olfaction | olfactory circuit I n the vinegar fly Drosophila melanogaster, cuticular hydrocarbons (CHCs) act as pheremones and play important roles in courtship and aggregation behaviors. These pheremones include the female-specific aphrodisiacs (Z,Z)-7,11-heptacosadiene (7,11-HD) and (Z,Z)-7,11-nonacosadiene (7,11-ND) and the male specific antiaphrodisiacs (Z)-7-tricosene (7-T) and 11-cis-vaccenyl acetate (cVA) (1). However, several lines of evidence suggest that other unidentified pheromones likely contribute to courtship and aggregation behaviors. Previous studies have demonstrated that an unidentified volatile sex pheromone produced by female flies stimulates male courtship (2-6). Flies anosmic to cVA exhibit residual attraction to live male flies, suggesting that other attractive cues are produced by flies that are independent of cVA and its neural circuit (7). Furthermore, no specific ligands other than cVA have been identified for the potential pheromone receptors expressed in OSNs of antennal trichoid sensilla (8). Moreover, OSNs expressing olfactory receptors Or47a and Or88a housed in trichoid sensilla respond to unidentified odors in male and female body wash extracts (9).Although the CHC profile of D. melanogaster has been characterized by several analytical techniq...

Cytochrome P450 associated with insecticide resistance catalyzes cuticular hydrocarbon production in Anopheles gambiae

“…gambiae strains examined have a distinct and remarkable abundance of very-long-chain methyl-branched HCs (VLCMHCs) compared with other insects examined to date (29). VLCMHCs have been associated with increased waterproofing properties (30) and may be correlated with a need for greater desiccation resistance in these relatively small insects.…”

Sleep and Development in Genetically Tractable Model Organisms

“…This finding, however, resurrects an older question: How are sleep disturbances in early life linked to later behavioral abnormalities? In the fly, courtship deficits in adult flies that were sleep deprived when young are accompanied by abnormal development of a specific olfactory glomerulus, known as VA1v, that plays a pheromone-related role in social behaviors (Dweck et al 2015;Lone et al 2015). Surprisingly, VA1v grows more rapidly during early posteclosion development compared to its neighboring glomeruli (Kayser et al 2014), likely reflecting a higher rate of synapse addition.…”

The role of cVA and the Odorant binding protein Lush in social and sexual behavior in Drosophila melanogaster

“…Interestingly, mutants for the Or47b receptor, another Or expressed in trichoid sensilla, are not attracted to Oe − flies (Couto et al, 2005;Fishilevich and Vosshall, 2005;Wang et al, 2011). A newly identified pheromone called methyl laurate made outside the Oenocytes by both males and females is detected by the Or47b and Or88a odorant receptors (Dweck et al, 2015). This new pheromone is detected by a trichoid sensillum like cVA.…”