Courtship Initiation Is Stimulated by Acoustic Signals in Drosophila melanogaster

Abstract

Finding a mating partner is a critical task for many organisms. It is in the interest of males to employ multiple sensory modalities to search for females. In Drosophila melanogaster, vision is thought to be the most important courtship stimulating cue at long distance, while chemosensory cues are used at relatively short distance. In this report, we show that when visual cues are not available, sounds produced by the female allow the male to detect her presence in a large arena. When the target female was artificially immobilized, the male spent a prolonged time searching before starting courtship. This delay in courtship initiation was completely rescued by playing either white noise or recorded fly movement sounds to the male, indicating that the acoustic and/or seismic stimulus produced by movement stimulates courtship initiation, most likely by increasing the general arousal state of the male. Mutant males expressing tetanus toxin (TNT) under the control of Gr68a-GAL4 had a defect in finding active females and a delay in courtship initiation in a large arena, but not in a small arena. Gr68a-GAL4 was found to be expressed pleiotropically not only in putative gustatory pheromone receptor neurons but also in mechanosensory neurons, suggesting that Gr68a-positive mechanosensory neurons, not gustatory neurons, provide motion detection necessary for courtship initiation. TNT/Gr68a males were capable of discriminating the copulation status and age of target females in courtship conditioning, indicating that female discrimination and formation of olfactory courtship memory are independent of the Gr68a-expressing neurons that subserve gustation and mechanosensation. This study suggests for the first time that mechanical signals generated by a female fly have a prominent effect on males' courtship in the dark and leads the way to studying how multimodal sensory information and arousal are integrated in behavioral decision making.

Central Regulation of Locomotor Behavior of Drosophila melanogaster Depends on a CASK Isoform Containing CaMK-Like and L27 Domains

“…Since all courtship experiments were performed in the dark, this phenotype cannot stem from differences in visual acuity. Under such conditions, initiation is driven by a combination of olfaction and mechanosensation (Ejima and Griffith 2008). Our data indicate that CASK P18 flies may have either reduced olfactory sensitivity to immature male pheromones or defective mechanosensation.…”

Auditory circuit in the Drosophila brain

“…In Drosophila melanogaster, acoustic communication is essential for making decisions related to mate selection (1)(2)(3)(4). During courtship, male flies flap one wing to produce a complex pattern of airborne vibrations comprising sine song and pulse song (5,6). The pulse song enables the female to determine whether her suitor is of the same species (7).…”

Courtship, aggression and avoidance: Pheromones, receptors and neurons for social behaviors in Drosophila

“…21 However, a recent study showed that males in which Gr68a neurons were inactivated displayed normal courtship behavior towards decapitated, and therefore immobilized, females, but a significantly greater courtship latency when paired with intact, mobile females. 22 Wildtype males showed a similar increase in latency when paired with "silent" decapitated females in the dark, which was "rescued" by playing white noise through a speaker. 22 These results imply that the courtship defects in flies lacking functional Gr68a neurons could also be due to the loss of mechanosensory/auditory neurons that are labeled by the driver.…”

“…22 Wildtype males showed a similar increase in latency when paired with "silent" decapitated females in the dark, which was "rescued" by playing white noise through a speaker. 22 These results imply that the courtship defects in flies lacking functional Gr68a neurons could also be due to the loss of mechanosensory/auditory neurons that are labeled by the driver. Thus a lot remains to be understood about the role of Gr68a in detection of a chemical signal.…”

“…[17][18][19][20] Gr68a is expressed in a sexually dimorphic manner in gustatory neurons in the male forelegs, 21 as well as in a non-dimorphic fashion in a number of mechanosensory neurons in the legs and auditory neurons in the Johnston's organ. 22 Initial studies suggested a role for Gr68a in detection of a courtshipstimulatory pheromone; male flies in which Gr68a neurons are ©2 0 1 1 L a n d e s B i o s c i e n c e .…”