Genetics, Vol 143, 331-344, Copyright © 1996

INVESTIGATIONS

Courtship Anomalies Caused by doublesex Mutations in Drosophila melanogaster

A. Villella and J. C. Hall
Department of Biology, Brandeis University, Waltham, Massachusetts 02254

The role played by the sex-determining gene doublesex (dsx) and its influence on Drosophila courtship were examined. Against a background of subnormal male-like behavior that is reported to be an attribute of haplo-X flies homozygous for the original dsx mutation, and given that a sex-specific muscle is unaffected by genetic variation at this locus, analyses of several reproductive behaviors and control for genetic background effects indicated that XY dsx mutants are impaired in their willingness to court females. When they did court, certain behavioral actions were normal, including components of courtship song. However, these mutants never produced courtship humming sounds. Mature XY dsx flies elicited anomalously high levels of courtship; that this occurs merely because of a delay in imaginal development was experimentally discounted. The current analysis reconciled two ostensibly conflicting reports involving the courtship-stimulating qualities of this mutant type. Such experiments also uncovered a new behavioral anomaly: dsx mutations caused chromosomal males to court other males at abnormally high levels. These results are discussed from the perspective of doublesex's influence on internal tissues of adult Drosophila involved in the triggering and neural control of male- and female-like elements of courtship, reproductive pheromone production, or a combination of such factors.

This article has been cited by other articles:

				B. J. Dickson Wired for Sex: The Neurobiology of Drosophila Mating Decisions Science, November 7, 2008; 322(5903): 904 - 909. [Abstract] [Full Text] [PDF]

				Y. Yang, W. Zhang, J. R. Bayrer, and M. A. Weiss Doublesex and the Regulation of Sexual Dimorphism in Drosophila melanogaster: STRUCTURE, FUNCTION, AND MUTAGENESIS OF A FEMALE-SPECIFIC DOMAIN J. Biol. Chem., March 14, 2008; 283(11): 7280 - 7292. [Abstract] [Full Text] [PDF]

				T. Chertemps, L. Duportets, C. Labeur, R. Ueda, K. Takahashi, K. Saigo, and C. Wicker-Thomas A female-biased expressed elongase involved in long-chain hydrocarbon biosynthesis and courtship behavior in Drosophila melanogaster PNAS, March 13, 2007; 104(11): 4273 - 4278. [Abstract] [Full Text] [PDF]

				M. D. Drapeau, S. A. Cyran, M. M. Viering, P. K. Geyer, and A. D. Long A cis-regulatory Sequence Within the yellow Locus of Drosophila melanogaster Required for Normal Male Mating Success Genetics, February 1, 2006; 172(2): 1009 - 1030. [Abstract] [Full Text] [PDF]

				A. Villella, S. L. Ferri, J. D. Krystal, and J. C. Hall Inaugural Article: Functional analysis of fruitless gene expression by transgenic manipulations of Drosophila courtship PNAS, November 15, 2005; 102(46): 16550 - 16557. [Abstract] [Full Text] [PDF]

				H. Lin, K. J. Mann, E. Starostina, R. D. Kinser, and C. W. Pikielny A Drosophila DEG/ENaC channel subunit is required for male response to female pheromones PNAS, September 6, 2005; 102(36): 12831 - 12836. [Abstract] [Full Text] [PDF]

				T. F. C. Mackay, S. L. Heinsohn, R. F. Lyman, A. J. Moehring, T. J. Morgan, and S. M. Rollmann Genetics and genomics of Drosophila mating behavior PNAS, May 3, 2005; 102(suppl_1): 6622 - 6629. [Abstract] [Full Text] [PDF]

				L. M. Ditch, T. Shirangi, J. L. Pitman, K. L. Latham, K. D. Finley, P. T. Edeen, B. J. Taylor, and M. McKeown Drosophila retained/dead ringer is necessary for neuronal pathfinding, female receptivity and repression of fruitless independent male courtship behaviors Development, January 1, 2005; 132(1): 155 - 164. [Abstract] [Full Text] [PDF]

				J. E. Mehren and L. C. Griffith Calcium-Independent Calcium/Calmodulin-Dependent Protein Kinase II in the Adult Drosophila CNS Enhances the Training of Pheromonal Cues J. Neurosci., November 24, 2004; 24(47): 10584 - 10593. [Abstract] [Full Text] [PDF]

				J. M. Gleason and M. G. Ritchie Do Quantitative Trait Loci (QTL) for a Courtship Song Difference Between Drosophila simulans and D. sechellia Coincide With Candidate Genes and Intraspecific QTL? Genetics, March 1, 2004; 166(3): 1303 - 1311. [Abstract] [Full Text] [PDF]

				G. E. Carney and B. J. Taylor logjam Encodes a Predicted EMP24/GP25 Protein That Is Required for Drosophila Oviposition Behavior Genetics, May 1, 2003; 164(1): 173 - 186. [Abstract] [Full Text] [PDF]

				C. M. Garrett-Engele, M. L. Siegal, D. S. Manoli, B. C. Williams, H. Li, and B. S. Baker intersex, a gene required for female sexual development in Drosophila, is expressed in both sexes and functions together with doublesex to regulate terminal differentiation Development, March 12, 2003; 129(20): 4661 - 4675. [Abstract] [Full Text] [PDF]

				B. Dauwalder, S. Tsujimoto, J. Moss, and W. Mattox The Drosophila takeout gene is regulated by the somatic sex-determination pathway and affects male courtship behavior Genes & Dev., November 15, 2002; 16(22): 2879 - 2892. [Abstract] [Full Text] [PDF]

				G. Lee and J. C. Hall Abnormalities of Male-Specific FRU Protein and Serotonin Expression in the CNS of fruitless Mutants in Drosophila J. Neurosci., January 15, 2001; 21(2): 513 - 526. [Abstract] [Full Text] [PDF]

				C. S. Raymond, M. W. Murphy, M. G. O'Sullivan, V. J. Bardwell, and D. Zarkower Dmrt1, a gene related to worm and fly sexual regulators, is required for mammalian testis differentiation Genes & Dev., October 15, 2000; 14(20): 2587 - 2595. [Abstract] [Full Text]

				L. Zhu, J. Wilken, N. B. Phillips, U. Narendra, G. Chan, S. M. Stratton, S. B. Kent, and M. A. Weiss Sexual dimorphism in diverse metazoans is regulated by a novel class of intertwined zinc fingers Genes & Dev., July 15, 2000; 14(14): 1750 - 1764. [Abstract] [Full Text]

				S. F. Goodwin, B. J. Taylor, A. Villella, M. Foss, L. C. Ryner, B. S. Baker, and J. C. Hall Aberrant Splicing and Altered Spatial Expression Patterns in fruitless Mutants of Drosophila melanogaster Genetics, February 1, 2000; 154(2): 725 - 745. [Abstract] [Full Text]

				W Yi, J. Ross, and D Zarkower Mab-3 is a direct tra-1 target gene regulating diverse aspects of C. elegans male sexual development and behavior Development, January 10, 2000; 127(20): 4469 - 4480. [Abstract] [PDF]

				J. A. Waterbury, L. L. Jackson, and P. Schedl Analysis of the Doublesex Female Protein in Drosophila melanogaster: Role in Sexual Differentiation and Behavior and Dependence on Intersex Genetics, August 1, 1999; 152(4): 1653 - 1667. [Abstract] [Full Text]

				M. Balakireva, R. F. Stocker, N. Gendre, and J.-F. Ferveur Voila, a New Drosophila Courtship Variant that Affects the Nervous System: Behavioral, Neural, and Genetic Characterization J. Neurosci., June 1, 1998; 18(11): 4335 - 4343. [Abstract] [Full Text] [PDF]

				A. A. Peixoto and J. C. Hall Analysis of Temperature-Sensitive Mutants Reveals New Genes Involved in the Courtship Song of Drosophila Genetics, February 1, 1998; 148(2): 827 - 838. [Abstract] [Full Text] [PDF]

				H Li and B. Baker hermaphrodite and doublesex function both dependently and independently to control various aspects of sexual differentiation in Drosophila Development, January 7, 1998; 125(14): 2641 - 2651. [Abstract] [PDF]

				H Li and B. Baker Her, a gene required for sexual differentiation in Drosophila, encodes a zinc finger protein with characteristics of ZFY-like proteins and is expressed independently of the sex determination hierarchy Development, January 1, 1998; 125(2): 225 - 235. [Abstract] [PDF]

				M.-l. A. Joiner and L. C. Griffith CaM Kinase II and Visual Input Modulate Memory Formation in the Neuronal Circuit Controlling Courtship Conditioning J. Neurosci., December 1, 1997; 17(23): 9384 - 9391. [Abstract] [Full Text] [PDF]