A neuropeptide circuit that coordinates sperm transfer and copulation duration in Drosophila
Innate behaviors are often executed in concert with accompanying physiological programs. How this coordination is achieved is poorly understood. Mating behavior and the transfer of sperm and seminal fluid (SSFT) provide a model for understanding how concerted behavioral and physiological programs are coordinated. Here we identify a male-specific neural pathway that coordinates the timing of SSFT with the duration of copulation behavior in Drosophila. Silencing four abdominal ganglion (AG) interneurons (INs) that contain the neuropeptide corazonin (Crz) both blocked SSFT and substantially lengthened copulation duration. Activating these Crz INs caused rapid ejaculation in isolated males, a phenotype mimicked by injection of Crz peptide. Crz promotes SSFT by activating serotonergic (5-HT) projection neurons (PNs) that innervate the accessory glands. Activation of these PNs in copulo caused premature SSFT and also shortened copulation duration. However, mating terminated normally when these PNs were silenced, indicating that SSFT is not required for appropriate copulation duration. Thus, the lengthened copulation duration phenotype caused by silencing Crz INs is independent of the block to SSFT. We conclude that four Crz INs independently control SSFT and copulation duration, thereby coupling the timing of these two processes.
© 2012 National Academy of Sciences. Freely available online through the PNAS open access option Contributed by David J. Anderson, October 21, 2012 (sent for review September 2, 2012). Published online before print November 28, 2012. We thank Barry Dickson and Jan Veenstra for sharing antibodies, Monica Martinez and Jung-Sook Chang for technical assistance, Shilpa Jeeda for maintaining fly stocks, Gabriele Mosconi and Holly Oates-Barker for laboratory management, and Gina Mancuso for administrative support. Fly strains were provided by the Bloomington Stock Center, the Janelia Farm Research Campus (JFRC) [Howard Hughes Medical Institute (HHMI)]. We thank Loren Looger, Vivek Jayaraman, Julie Simpson, and the Janelia Genetically-Encoded Neuronal Indicator and Effector (GENIE) team (JFRC) for providing UAS-GCaMP5G flies ahead of publication. T.D.T. was supported by a Gosney fellowship (Caltech Biology), National Institutes of Health postdoctoral training Grant NS007251 and National Research Service Award Fellowship 5F32NS058132. A.C.H. was supported by an HHMI Predoctoral Fellowship and National Science Foundation Frontiers in Integrative Biological Research Grant EF-0623527 (M. J. Dickinson, principal investigator). M.M. is funded by the Alfred P. Sloan Foundation, the National Science Foundation, the Human Frontiers Science Program, the Klingenstein Fund, and the McKnight Foundation. D.J.A. is an Investigator of the HHMI. Author contributions: T.D.T. and D.J.A. designed research; T.D.T. and D.A.P. performed research; T.D.T., A.C.H., and M.M. contributed new reagents/analytic tools; T.D.T., M.M., and D.J.A. analyzed data; and T.D.T. and D.J.A. wrote the paper.
Published - PNAS-2012-Tayler-20697-702.pdf
Supplemental Material - pnas.201218246SI.pdf