Gustatory pheromones play an essential role in shaping the behavior of many organisms. However, little is known about the processing of taste pheromones in higher order brain centers. Here, we describe a male-specific gustatory circuit in Drosophila that underlies the detection of the anti-aphrodisiac pheromone (3R,11Z,19Z)-3-acetoxy-11,19-octacosadien-1-ol (CH503). Using behavioral analysis, genetic manipulation, and live calcium imaging, we show that Gr68a-expressing neurons on the forelegs of male flies exhibit a sexually dimorphic physiological response to the pheromone and relay information to the central brain via peptidergic neurons. The release of tachykinin from 8 to 10 cells within the subesophageal zone is required for the pheromone-triggered courtship suppression. Taken together, this work describes a neuropeptide-modulated central brain circuit that underlies the programmed behavioral response to a gustatory sex pheromone. These results will allow further examination of the molecular basis by which innate behaviors are modulated by gustatory cues and physiological state.

Significance: How sexual features and preferences originate and evolve is one of the most important and contentious problems in evolutionary biology. In some species, females choose male traits that indicate genetic quality or confer benefits. Thus, male traits and female preferences are assumed to originate at the same time and to coevolve. In contrast, sensory exploitation occurs when males take advantage of females’ preexisting sensory biases. We show inDrosophilasensory exploitation of males by other males through the use of a pheromone to gain sexual advantage. Notably, sensory exploitation leads to male sensory adaptation. These findings provide a mechanism for the evolutionary origins of a pheromone and are a previously unidentified example of sensory exploitation between males.

Eight analogues of (3R,11Z,19Z)-CH503 (3-acetoxy-11,19-octacosadien-1-ol), the anti-aphrodisiac pheromone of male Drosophila melanogaster, were synthesized for a bioassay. These were the enantiomers of 3-acetoxy-11,19-octacosadiyn-1-ol (1), 3-acetoxyoctacosan-1-ol (2), (Z)-3-acetoxy-11-octacosen-1-ol (3), and (Z)-3-acetoxy-19-octacosen-1-ol (4). None of them were pheromonally active, indicating that the two double bonds at C-11 and C-19 were necessary for bioactivity.

The yellow fever mosquito Aedes aegypti is a prolific vector of arboviral and filarial diseases that largely relies on its sense of smell to find humans. To facilitate in-depth analysis of the neural circuitry underlying Ae. aegypti olfactory-driven behaviors, we generated an updated in vitro atlas for the antennal lobe olfactory brain region of this disease vector using two independent neuronal staining methods. We performed morphological reconstructions with replicate fixed, dissected and stained brain samples from adult male and female Ae. aegypti of the LVPib12 genome reference strain and determined that the antennal lobe in both sexes is comprised of approximately 80 discrete glomeruli. Guided by landmark features in the antennal lobe, we found 63 of these glomeruli are stereotypically located in spatially invariant positions within these in vitro preparations. A posteriorly positioned, mediodorsal glomerulus denoted MD1 was identified as the largest spatially invariant glomerulus in the antennal lobe. Spatial organization of glomeruli in a recently field-derived strain of Ae. aegypti from Puerto Rico was conserved, despite differences in antennal lobe shape relative to the inbred LVPib12 strain. This model in vitro atlas will serve as a useful community resource to improve antennal lobe annotation and anatomically map projection patterns of neurons expressing target genes in this olfactory center. It will also facilitate the development of chemotopic maps of odor representation in the mosquito antennal lobe to decode the molecular and cellular basis of Ae. aegypti attraction to human scent and other chemosensory cues. The olfactory system of the yellow fever mosquito Aedes aegypti is highly tuned for the detection of human odorants, as well as other chemical cues influencing host and food-search behavior, egg-laying and mating. To provide insights into the neuroanatomical organization of the olfactory system of this globally important disease vector, we have generated an updated in vitro atlas for the primary smell processing center of the Ae. aegypti brain, called the antennal lobe. These new guide maps facilitate systematic interrogation of antennal lobe morphology and naming of associated substructures in dissected brain samples of this species labeled with two common neural staining methods. We report that landmark features of the Ae. aegypti antennal lobe morphology and spatial organization appear conserved between mosquito sexes and across geographically divergent strains of this mosquito species. An improved understanding of Ae. aegypti antennal lobe neuroanatomy and how attractive or repellent odorant stimuli are encoded in this brain center has the potential to rapidly accelerate reverse engineering of synthetic chemical blends that effectively lure, confuse or repel this major disease vector.