title: Female-biased dimorphism underlies a female-specific role for post-embryonic Ilp7 neurons in Drosophila fertility.
abstract: In Drosophila melanogaster, much of our understanding of sexually dimorphic neuronal development and function comes from the study of male behavior, leaving female behavior less well understood. Here, we identify a post-embryonic population of Insulin-like peptide 7 (Ilp7)-expressing neurons in the posterior ventral nerve cord that innervate the reproductive tracts and exhibit a female bias in their function. They form two distinct dorsal and ventral subsets in females, but only a single dorsal subset in males, signifying a rare example of a female-specific neuronal subset. Female post-embryonic Ilp7 neurons are glutamatergic motoneurons innervating the oviduct and are required for female fertility. In males, they are serotonergic/glutamatergic neuromodulatory neurons innervating the seminal vesicle but are not required for male fertility. In both sexes, these neurons express the sex-differentially spliced fruitless-P1 transcript but not doublesex. The male fruitless-P1 isoform (fruM) was necessary and sufficient for serotonin expression in the shared dorsal Ilp7 subset, but although it was necessary for eliminating female-specific Ilp7 neurons in males, it was not sufficient for their elimination in females. By contrast, sex-specific RNA-splicing by female-specific transformer is necessary for female-type Ilp7 neurons in females and is sufficient for their induction in males. Thus, the emergence of female-biased post-embryonic Ilp7 neurons is mediated in a subset-specific manner by a tra- and fru-dependent mechanism in the shared dorsal subset, and a tra-dependent, fru-independent mechanism in the female-specific subset. These studies provide an important counterpoint to studies of the development and function of male-biased neuronal dimorphism in Drosophila.
authors: Department of Cellular and Physiological Sciences, 2401 Life Sciences Centre, 2350 Health Sciences Mall, University of British Columbia, Vancouver, BC, V6T 1Z3, Canada.
authors: Monica C
authors: MC
authors: Castellanos
authors: Jonathan C Y
authors: JC
authors: Tang
authors: Douglas W
authors: DW
authors: Allan
mesh_terms: D000375:Aging; D000818:Animals; D029721:Drosophila Proteins / Q000378:metabolism*; D004331:Drosophila melanogaster / Q000166:cytology* / Q000196:embryology* / Q000502:physiology; D004625:Embryo, Nonmammalian / Q000166:cytology* / Q000378:metabolism; D005260:Female; D005298:Fertility; D008297:Male; D009046:Motor Neurons / Q000166:cytology / Q000378:metabolism; D009474:Neurons / Q000166:cytology / Q000378:metabolism*; D009479:Neuropeptides / Q000378:metabolism*; D010641:Phenotype; D012669:Seminal Vesicles / Q000166:cytology / Q000378:metabolism; D059326:Serotonergic Neurons / Q000166:cytology / Q000378:metabolism; D012727:Sex Characteristics; D014566:Urogenital System / Q000166:cytology / Q000294:innervation
chemical_list: D029721:Drosophila Proteins; D009479:Neuropeptides; C527689:insulin-like peptide 7, Drosophila
keywords: Female behavior; Motoneuron; Neuronal identity; Neuronal lineage
references: Nat Neurosci. 2010 Apr;13(4):458-66
references: 20305646
references: BMC Biol. 2006 Jun 12;4:17
references: 16768790
references: Development. 2004 Nov;131(21):5233-42
references: 15456721
references: J Comp Neurol. 2004 Jul 19;475(2):270-87
references: 15211467
references: J Neurosci. 2004 Feb 11;24(6):1406-15
references: 14960613
references: Development. 2013 Apr;140(8):1830-42
references: 23533181
references: Proc Natl Acad Sci U S A. 2012 Mar 27;109(13):E748-56
references: 22393011
references: Curr Biol. 1996 Jun 1;6(6):695-706
references: 8793296
references: Development. 1998 Jul;125(14):2641-51
references: 9636079
references: Development. 2002 Oct;129(20):4661-75
references: 12361959
references: Nat Cell Biol. 2000 Aug;2(8):500-6
references: 10934470
references: Development. 2004 Dec;131(24):6093-105
references: 15537690
references: J Neurosci. 2009 Mar 25;29(12):3852-64
references: 19321782
references: Neuron. 1998 Dec;21(6):1363-74
references: 9883729
references: Nature. 2005 Jul 28;436(7050):510-7
references: 16049479
references: Dev Biol. 2003 Dec 1;264(1):38-49
references: 14623230
references: PLoS Genet. 2010 Feb 26;6(2):e1000857
references: 20195512
references: Prog Brain Res. 2010;186:13-28
references: 21094883
references: Curr Opin Neurobiol. 2010 Dec;20(6):764-9
references: 20934322
references: Neuron. 2009 Feb 12;61(3):373-84
references: 19217375
references: Development. 1992 Mar;114(3):625-42
references: 1618132
references: Proc Natl Acad Sci U S A. 1997 May 13;94(10):5131-6
references: 9144202
references: Neuron. 2006 Mar 16;49(6):833-44
references: 16543132
references: Development. 2001 Apr;128(7):1033-43
references: 11245569
references: BMC Dev Biol. 2008 Dec 08;8:114
references: 19063748
references: Curr Biol. 2010 Sep 28;20(18):1589-601
references: 20832311
references: Neuron. 2008 Sep 11;59(5):759-69
references: 18786359
references: Ann N Y Acad Sci. 2004 Jun;1016:540-59
references: 15313794
references: Dev Growth Differ. 2011 Feb;53(2):236-44
references: 21338349
references: PLoS Biol. 2010 May 04;8(5):e1000365
references: 20454565
references: Gene Expr Patterns. 2006 Mar;6(3):299-309
references: 16378756
references: Int Rev Neurobiol. 2006;75:165-79
references: 17137928
references: J Neurobiol. 2001 May;47(2):121-49
references: 11291102
references: J Neurosci. 2001 Jan 15;21(2):513-26
references: 11160431
references: Int Rev Neurobiol. 2011;99:87-105
references: 21906537
references: PLoS Genet. 2007 Nov;3(11):e216
references: 18039034
references: Adv Genet. 2008;62:67-184
references: 19010254
references: Dev Biol. 2008 Feb 15;314(2):329-40
references: 18199432
references: Cell. 2005 Jun 3;121(5):785-94
references: 15935764
references: Neuron. 1997 Nov;19(5):1007-16
references: 9390515
references: J Neurobiol. 1990 Oct;21(7):1072-84
references: 1979610
references: Front Neuroendocrinol. 1998 Oct;19(4):323-62
references: 9799588
references: Dev Genes Evol. 2005 Jan;215(1):1-12
references: 15645316
references: Fly (Austin). 2010 Jan-Mar;4(1):60-70
references: 20160499
references: Z Zellforsch Mikrosk Anat. 1967;76(1):56-99
references: 5340226
references: Cell Metab. 2011 Jan 5;13(1):92-104
references: 21195352
references: Neuron. 2009 Feb 26;61(4):511-8
references: 19249272
references: Cell. 2005 Jun 3;121(5):795-807
references: 15935765
references: J Neurobiol. 1993 Aug;24(8):1025-44
references: 8409967
references: Neuron. 2001 Nov 8;32(3):415-24
references: 11709153
references: Dev Biol. 2012 Oct 1;370(1):86-97
references: 22841645
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: Genes Dev. 1998 Apr 15;12(8):1155-65
references: 9553045
references: Genes Dev. 2001 Mar 15;15(6):672-86
references: 11274053
references: Adv Genet. 2007;59:39-66
references: 17888794
references: Nature. 2008 Jan 3;451(7174):33-7
references: 18066048
references: J Cell Physiol. 2006 Oct;209(1):183-98
references: 16826564
references: Proc Natl Acad Sci U S A. 1997 Feb 4;94(3):913-8
references: 9023356
references: Sci STKE. 2004 Feb 12;2004(220):pl6
references: 14970377
references: PLoS Biol. 2008 Mar 11;6(3):e58
references: 18336071
references: J Biol Chem. 2005 Apr 15;280(15):14948-55
references: 15691831
references: Curr Biol. 2012 Jul 10;22(13):1155-65
references: 22658598
references: Science. 2008 Mar 21;319(5870):1679-83
references: 18356529
references: Curr Biol. 2010 Sep 28;20(18):1602-14
references: 20832315
references: Neuron. 2009 Feb 26;61(4):519-26
references: 19249273
references: Int Rev Neurobiol. 2006;75:71-90
references: 17137924
references: Cell. 1993 Feb 26;72(4):527-40
references: 8440019