Genetics, Vol 147, 1107-1130, Copyright © 1997

INVESTIGATIONS

Extended Reproductive Roles of the fruitless Gene in Drosophila melanogaster Revealed by Behavioral Analysis of New fru Mutants

A. Villella, D. A. Gailey, B. Berwald, S. Ohshima, P. T. Barnes and J. C. Hall
Department of Biology, Brandeis University, Waltham, Massachusetts 02254

The fruitless mutants fru(3) and fru(4) were assessed for sex-specific reproductive-behavioral phenotypes and compared to the previously reported fru mutants. Among the several behavioral anomalies exhibited by males expressing these relatively new mutations, some are unique. fru(3) and fru(4) males are less stimulated to court females than fru(1) and fru(2). No courtship pulse song is generated by either fru(3) or fru(4) males, even though they perform brief wing extensions. fru(3) and fru(4) males display significantly less chaining behavior than do fru(1) males. The hierarchy of courtship responses by fru males directed toward females vs. males, when presented with both sexes simultaneously, is that fru(1) males perform vigorous and indiscriminant courtship directed at either sex; fru(4) males are similarly indiscriminant, but courtship levels were lower than fru(1); fru(2) males prefer females; fru(3) males show a courtship bias toward males. fru(3) and fru(4) males essentially lack the Muscle of Lawrence (MOL). On several reproductive criteria, there was no difference between fru-variant females and fru(+). The increases in phenotypic severity measured for the new mutants are discussed in the context of the emerging molecular genetics of fru and with regard to the gene's position within the sex-determination pathway.

This article has been cited by other articles:

				T. Liu, L. Dartevelle, C. Yuan, H. Wei, Y. Wang, J.-F. Ferveur, and A. Guo Increased Dopamine Level Enhances Male-Male Courtship in Drosophila J. Neurosci., May 21, 2008; 28(21): 5539 - 5546. [Abstract] [Full Text] [PDF]

				S. J. Certel, M. G. Savella, D. C. F. Schlegel, and E. A. Kravitz Modulation of Drosophila male behavioral choice PNAS, March 13, 2007; 104(11): 4706 - 4711. [Abstract] [Full Text] [PDF]

				S. Kadener, A. Villella, E. Kula, K. Palm, E. Pyza, J. Botas, J. C. Hall, and M. Rosbash Neurotoxic protein expression reveals connections between the circadian clock and mating behavior in Drosophila PNAS, September 5, 2006; 103(36): 13537 - 13542. [Abstract] [Full Text] [PDF]

				D. A. Gailey, J.-C. Billeter, J. H. Liu, F. Bauzon, J. B. Allendorfer, and S. F. Goodwin Functional Conservation of the fruitless Male Sex-Determination Gene Across 250 Myr of Insect Evolution Mol. Biol. Evol., March 1, 2006; 23(3): 633 - 643. [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]

				A. Pane, A. De Simone, G. Saccone, and C. Polito Evolutionary Conservation of Ceratitis capitata transformer Gene Function Genetics, October 1, 2005; 171(2): 615 - 624. [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]

				H.-J. Song, J.-C. Billeter, E. Reynaud, T. Carlo, E. P. Spana, N. Perrimon, S. F. Goodwin, B. S. Baker, and B. J. Taylor The fruitless Gene Is Required for the Proper Formation of Axonal Tracts in the Embryonic Central Nervous System of Drosophila Genetics, December 1, 2002; 162(4): 1703 - 1724. [Abstract] [Full Text] [PDF]

				H. Kuniyoshi, K. Baba, R. Ueda, S. Kondo, W. Awano, N. Juni, and D. Yamamoto lingerer, a Drosophila Gene Involved in Initiation and Termination of Copulation, Encodes a Set of Novel Cytoplasmic Proteins Genetics, December 1, 2002; 162(4): 1775 - 1789. [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]

				T. Kitamoto Conditional disruption of synaptic transmission induces male-male courtship behavior in Drosophila PNAS, October 1, 2002; 99(20): 13232 - 13237. [Abstract] [Full Text] [PDF]

				B. Chan, A. Villella, P. Funes, and J. C. Hall Courtship and Other Behaviors Affected by a Heat-Sensitive, Molecularly Novel Mutation in the cacophony Calcium-Channel Gene of Drosophila Genetics, September 1, 2002; 162(1): 135 - 153. [Abstract] [Full Text] [PDF]

				A. Anand, A. Villella, L. C. Ryner, T. Carlo, S. F. Goodwin, H.-J. Song, D. A. Gailey, A. Morales, J. C. Hall, B. S. Baker, et al. Molecular Genetic Dissection of the Sex-Specific and Vital Functions of the Drosophila melanogaster Sex Determination Gene fruitless Genetics, August 1, 2001; 158(4): 1569 - 1595. [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]

				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]

				J. Flint The genetic basis of cognition Brain, November 1, 1999; 122(11): 2015 - 2032. [Abstract] [Full Text] [PDF]

				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]