title: Genetic control of courtship behavior in the housefly: evidence for a conserved bifurcation of the sex-determining pathway.
abstract: In Drosophila melanogaster, genes of the sex-determination hierarchy orchestrate the development and differentiation of sex-specific tissues, establishing sex-specific physiology and neural circuitry. One of these sex-determination genes, fruitless (fru), plays a key role in the formation of neural circuits underlying Drosophila male courtship behavior. Conservation of fru gene structure and sex-specific expression has been found in several insect orders, though it is still to be determined whether a male courtship role for the gene is employed in these species due to the lack of mutants and homologous experimental evidence. We have isolated the fru ortholog (Md-fru) from the common housefly, Musca domestica, and show the gene's conserved genomic structure. We demonstrate that male-specific Md-fru transcripts arise by conserved mechanisms of sex-specific splicing. Here we show that Md-fru, is similarly involved in controlling male courtship behavior. A male courtship behavioral function for Md-fru was revealed by the behavioral and neuroanatomical analyses of a hypomorphic allele, Md-tra(man) , which specifically disrupted the expression of Md-fru in males, leading to severely impaired male courtship behavior. In line with a role in nervous system development, we found that expression of Md-fru was confined to neural tissues in the brain, most prominently in optic neuropil and in peripheral sensory organs. We propose that, like in Drosophila, overt sexual differentiation of the housefly depends on a sex-determining pathway that bifurcates downstream of the Md-tra gene to coordinate dimorphic development of non-neuronal tissues mediated by Md-dsx with that of neuronal tissues largely mediated by Md-fru.
authors: Institute of Molecular Life Sciences, University of Zürich, Zürich, Switzerland.
authors: Nicole
authors: N
authors: Meier
authors: Simone Catherine
authors: SC
authors: Käppeli
authors: Monika
authors: M
authors: Hediger Niessen
authors: Jean-Christophe
authors: JC
authors: Billeter
authors: Stephen F
authors: SF
authors: Goodwin
authors: Daniel
authors: D
authors: Bopp
mesh_terms: D000483:Alleles; D017398:Alternative Splicing; D000818:Animals; D002490:Central Nervous System / Q000378:metabolism; D005260:Female; D005725:Ganglia, Autonomic / Q000166:cytology / Q000378:metabolism; D015870:Gene Expression; D055785:Gene Knockdown Techniques; D006793:Houseflies / Q000235:genetics* / Q000378:metabolism; D019476:Insect Proteins / Q000235:genetics* / Q000378:metabolism; D008297:Male; D009419:Nerve Tissue Proteins / Q000235:genetics / Q000378:metabolism; D009928:Organ Specificity; D020033:Protein Isoforms; D034622:RNA Interference; D011984:Sensory Receptor Cells / Q000378:metabolism; D012727:Sex Characteristics; D019849:Sex Determination Processes; D012726:Sexual Behavior, Animal; D014157:Transcription Factors / Q000235:genetics / Q000378:metabolism
chemical_list: D019476:Insect Proteins; D009419:Nerve Tissue Proteins; D020033:Protein Isoforms; D014157:Transcription Factors
references: Int J Dev Biol. 2009;53(1):109-20
references: 19123132
references: Curr Biol. 2007 Sep 4;17(17):1473-8
references: 17716899
references: Curr Opin Neurobiol. 2010 Dec;20(6):764-9
references: 20934322
references: Trends Neurosci. 2006 Aug;29(8):444-51
references: 16806511
references: Cell. 2008 Apr 18;133(2):354-63
references: 18423205
references: Genetics. 1997 Jan;145(1):173-83
references: 9017399
references: Mol Biol Evol. 2006 Mar;23(3):633-43
references: 16319090
references: Genetics. 1995 Jan;139(1):365-74
references: 7705637
references: Cell. 2005 Jun 3;121(5):795-807
references: 15935765
references: J Comp Physiol A Neuroethol Sens Neural Behav Physiol. 2006 Dec;192(12):1253-69
references: 16896687
references: Cell. 1996 Dec 13;87(6):1079-89
references: 8978612
references: BMC Evol Biol. 2011 Feb 10;11:41
references: 21310052
references: Insect Biochem Mol Biol. 2011 May;41(5):340-7
references: 21296153
references: Nature. 2005 Jul 21;436(7049):395-400
references: 15959468
references: PLoS Biol. 2009 Aug;7(8):e1000168
references: 19652700
references: J Genet. 2010 Sep;89(3):287-99
references: 20876995
references: Genetics. 1985 Sep;111(1):89-96
references: 3928434
references: Genetics. 2010 Jan;184(1):155-70
references: 19841093
references: Nat Neurosci. 2010 Apr;13(4):458-66
references: 20305646
references: Cell. 1988 Apr 22;53(2):229-36
references: 3129196
references: Dev Genes Evol. 2004 Jan;214(1):29-42
references: 14673649
references: Curr Top Dev Biol. 2005;66:189-213
references: 15797454
references: J Genet. 2010 Sep;89(3):357-63
references: 20877002
references: Genetics. 2001 Aug;158(4):1569-95
references: 11514448
references: Science. 1994 Jun 17;264(5166):1702-14
references: 8209251
references: Dev Genes Evol. 2011 May;221(1):43-8
references: 21340608
references: Curr Opin Genet Dev. 2010 Aug;20(4):376-83
references: 20570131
references: J Neurobiol. 2000 Jun 15;43(4):404-26
references: 10861565
references: J Insect Physiol. 2012 Feb;58(2):265-9
references: 22138053
references: Mol Biol Evol. 2009 Jul;26(7):1557-69
references: 19349644
references: Mol Cell Biol. 1998 Jan;18(1):450-8
references: 9418892
references: Insect Mol Biol. 2009 Jun;18(3):315-24
references: 19523063
references: J Neurobiol. 2001 May;47(2):121-49
references: 11291102
references: J Neurosci. 2001 Jan 15;21(2):513-26
references: 11160431
references: Genetics. 1989 Apr;121(4):773-85
references: 2542123
references: Proc Natl Acad Sci U S A. 1994 Oct 25;91(22):10717-21
references: 7938017
references: Dev Genes Evol. 2005 Apr;215(4):165-76
references: 15662529
references: J Comp Neurol. 2004 Jul 19;475(2):270-87
references: 15211467
references: Int J Dev Biol. 2008;52(8):1051-7
references: 18956338
references: Int Rev Neurobiol. 2011;99:87-105
references: 21906537
references: Science. 1995 Feb 10;267(5199):902-5
references: 7846534
references: Int J Dev Biol. 2002 Jan;46(1):75-9
references: 11902690
references: Adv Genet. 2008;62:67-184
references: 19010254
references: Cell. 2005 Jun 3;121(5):785-94
references: 15935764
references: Genetics. 1997 Nov;147(3):1107-30
references: 9383056
references: Chromosoma. 1989 Aug;98(2):81-5
references: 2476281
references: Curr Biol. 1998 Oct 22;8(21):1187-90
references: 9799737
references: Dev Biol. 2008 Aug 15;320(2):378-90
references: 18599032
references: Curr Biol. 2006 Jun 6;16(11):1063-76
references: 16753560
references: Proc Natl Acad Sci U S A. 1996 Sep 3;93(18):9687-92
references: 8790392
references: PLoS One. 2013;8(2):e48554
references: 23418412
references: Parasitol Res. 2008 Jun;103(1):123-31
references: 18343951
references: Nat Neurosci. 2006 Dec;9(12):1469-71
references: 17115036
references: Genetics. 1980 Feb;94(2):383-423
references: 6771185
references: J Neurogenet. 2005 Apr-Jun;19(2):109-21
references: 16024442