Courtship in Drosophila

The vinegar fly, drosophila melanogaster Successful species—worldwide, in lab…reproductive rituals must be adaptive and robust.

Courtship is a stereotyped dance Plus video http://www.youtube.com/watch?v=zXXqQ2zJVMA

Sensory input informs progression of the ritual Sensory input informs progression of the ritual. On the right, common metrics to measure courtship success.

Decisions Whom to court? Female vs Male seems innate Visual, olfactory cues Receptive vs. Non-Receptive is learned Olfactory cues Males can save considerable energy by limiting courtship to receptive females

Pheromones aid male decision making Cis-vaccenyl acetate cVA Volatile compound Sensed by males and females Produced by males only Inhibits male courtship, including song

Pheromone receptors OrX=Or67d for cVA

sNMP is required for optimal cVA action sNMP is required for optimal cVA action. LUSH may be the true ligand for Or67d, but requires cVA binding to alter its conformation. Experimentally altering its conformation by making a genetic substitution that mimics what happens when cVA binds results in constitutive activation of Or67d receptor complex.

Organization of the cVA sensing circuit DA1 is sexually dimorphic—larger in males than females. Also the PN that synapse in DA1 have larger and distinct arborizations in the PC than female PN do. Or47b is a receptor for an unknown pheromone, which may provide a species specific mating cue (rather than sex specific). Convergence of pheromone signals in the PC occurs completely distinctly from fruit odors in the sexually dimorphic lateral horn.

Generating sexual dimorphism Fruitless (Fru) and Doublesex (Dsx) Fru acts in the NS Males lacking Fru do not sing Females expressing Fru do sing No effect of Dsx 2000 Fru neurons in both sexes GFP fused to Fru promoter, magenta labels synapses

1996 original report of Fru

Neurons required for singing FruP1 neurons in the dorsal PC (~20) In sexual mosaics, if these cells are masculinized (express male isoform of Fru) females will generate song Female thorax is capable of singing, but this action is never selected Direct stimulation of thoracic ganglion generates song in headless flies of either sex Female FlyPod song improves if her Fru+ neurons express FruM (also DsxM is required for perfect song in both sexes) What does this remind you of? How can we interpret this headless result?

Return to the learning process Virgin females of same species are the best mate Males will be rejected by mated females Experience determines the likelihood of subsequent mating attempts with females of a different species or the same species that has already mated

Candidate mechanisms Dopamine neurons Reinforce pheromone circuits that were active during successful courtship Or67d circuit may be a target for learning that cVA is a pheromone associated with female rejection A set of g neurons in the PC that express FruM are necessary for the learning Require the plasticity protein CPEB during or shortly after training

A gustatory receptor aids in mate selection Gr32a expressing gustatory chemosensory neurons project directly into the ventrolateral PC. May be a site of integration with other signals—auditory, olfactory, visual. There are Fru expressing neurons in this vicinity but have not been studied on cellular level. No sex difference in Gr32a projections. Tetsuya Miyamoto & Hubert Amrein Nature Neuroscience 11, 874 - 876 (2008)

Female Decision Accept or Reject Courtship? Male Quality cVA signal SONG-presence and quality Interpulse interval: provides species cue

Vibrations of the female antenna-left- correspond to the highest frequency of the male wing song. Matching vibration frequencies is one way for the female to pay attention to the conspecific song and block out other suitors.

Female Decision Mate more than once? Female stores sperm, uses it for a while Unless she encounters a much better quality male, she has no need to mate again Common interest to make her unreceptive Transfer of Sex Peptide (SP)

A chemical battle SP and ovulin stimulates egg production, which helps improve the males reproductive success rate, but only SP makes the female less receptive. If a male mates with a female that already mated, he has no need to stimulate egg production, but still wants to keep her unreceptive, so he lowers the amount of ovulin released in his semen. Mechanism unknown.

SP suppresses mating Females that mate with male lacking SP readily mate again Virgins injected with SP are unreceptive SP binds to the SPR, a GPCR that activates cAMP 2nd messenger pathway SPR is expressed in the Fru neurons (and elsewhere)

Summary Adriana Villella*, Jeffrey C. Hall2008.