title: Positive selection at the binding sites of the male-specific lethal complex involved in dosage compensation in Drosophila.
abstract: In many taxa, males and females differ with respect to their sex chromosomes, and dosage compensation mechanisms have evolved to equalize X-linked gene transcription. In Drosophila, the male-specific lethal (MSL) complex binds to hundreds of sites along the male X chromosome and mediates twofold hypertranscription of the single male X. Two recent studies found evidence for lineage-specific adaptive evolution in all five core protein-coding genes of the MSL complex in Drosophila melanogaster. In particular, dramatic positive selection was detected in domains shown to be responsible for their specific targeting to the X chromosome. Here I use population genetics to show that three previously characterized MSL-binding DNA segments on the X themselves underwent adaptive evolution in D. melanogaster, but not in its close relatives D. simulans and D. yakuba. MSL components have been shown to not correctly target the D. melanogaster X chromosome in hybrids between D. melanogaster and D. simulans. My finding supports the idea of selection-driven coevolution among DNA-protein interactions of the dosage compensation machinery and suggests that misregulated dosage compensation could contribute to male hybrid inviability in Drosophila.
authors.affiliation: Department of Integrative Biology, University of California, Berkeley, California 94720, USA. dbachtrog@berkeley.edu
authors.forename: Doris
authors.initials: D
authors.lastname: Bachtrog
mesh_terms: D000818:Animals; D001665:Binding Sites; D004268:DNA-Binding Proteins / Q000235:genetics / Q000378:metabolism; D004303:Dosage Compensation, Genetic; D004330:Drosophila / Q000235:genetics* / Q000378:metabolism; D019143:Evolution, Molecular; D005828:Genetics, Population; D008297:Male; D009687:Nuclear Proteins / Q000235:genetics* / Q000378:metabolism; D012641:Selection, Genetic; D014960:X Chromosome
chemical_list: D004268:DNA-Binding Proteins; D009687:Nuclear Proteins
references.citation: EMBO J. 2001 May 1;20(9):2236-45
references.pmid: 11331589
references.citation: Genes Dev. 2006 Apr 1;20(7):858-70
references.pmid: 16547172
references.citation: Genetics. 2007 Nov;177(3):1959-62
references.pmid: 18039888
references.citation: PLoS Genet. 2006 Feb;2(2):e5
references.pmid: 16462942
references.citation: Genes Dev. 2003 Jun 1;17(11):1334-9
references.pmid: 12782651
references.citation: Genes Dev. 2006 Apr 1;20(7):848-57
references.pmid: 16547173
references.citation: PLoS Biol. 2007 Sep;5(9):e243
references.pmid: 17850182
references.citation: Evolution. 2006 Feb;60(2):292-302
references.pmid: 16610321
references.citation: Science. 1978 Nov 17;202(4369):711-6
references.pmid: 715437
references.citation: Comput Appl Biosci. 1997 Oct;13(5):555-6
references.pmid: 9367129
references.citation: Curr Biol. 1996 Feb 1;6(2):149-62
references.pmid: 8673462
references.citation: Nature. 2002 Feb 28;415(6875):1024-6
references.pmid: 11875569
references.citation: Mol Cell. 2003 Apr;11(4):977-86
references.pmid: 12718883
references.citation: Cell. 1999 Aug 20;98(4):513-22
references.pmid: 10481915
references.citation: Annu Rev Genet. 1994;28:491-521
references.pmid: 7893138
references.citation: Mol Biol Evol. 2007 Jan;24(1):306-14
references.pmid: 17056646
references.citation: Mol Biol Evol. 2008 Sep;25(9):1825-34
references.pmid: 18515263
references.citation: Nature. 1991 Jun 20;351(6328):652-4
references.pmid: 1904993
references.citation: Trends Cell Biol. 2000 Feb;10(2):54-9
references.pmid: 10652515
references.citation: Curr Biol. 2004 Mar 23;14(6):481-7
references.pmid: 15043812
references.citation: Genome Biol. 2005;6(8):R67
references.pmid: 16086849
references.citation: Mol Biol Evol. 2004 Feb;21(2):374-83
references.pmid: 14660692
references.citation: Mol Cell. 2007 Oct 12;28(1):121-33
references.pmid: 17936709
references.citation: Genetics. 2006 Nov;174(3):1151-9
references.pmid: 16951071
references.citation: Genetics. 1987 May;116(1):153-9
references.pmid: 3110004
references.citation: Genome Res. 2006 Jul;16(7):875-84
references.pmid: 16751341
references.citation: Nature. 2005 Oct 20;437(7062):1149-52
references.pmid: 16237443
references.citation: Proc Natl Acad Sci U S A. 2007 Sep 25;104(39):15412-7
references.pmid: 17878295
references.citation: Genetics. 1989 Aug;122(4):891-4
references.pmid: 2503427
references.citation: Genetics. 2004 Oct;168(2):1071-6
references.pmid: 15514076
references.citation: Genetics. 2006 Dec;174(4):2045-59
references.pmid: 17028331
references.citation: Mol Biol Evol. 1995 Nov;12(6):1002-11
references.pmid: 8524036
references.citation: Nature. 2002 Feb 28;415(6875):1022-4
references.pmid: 11875568
references.citation: Mol Phylogenet Evol. 2004 Sep;32(3):998-1009
references.pmid: 15288072
references.citation: Mol Biol Evol. 2004 Jul;21(7):1350-60
references.pmid: 15044594
references.citation: Genetics. 2007 Dec;177(4):2233-41
references.pmid: 17947412
references.citation: Bioessays. 2000 Dec;22(12):1106-14
references.pmid: 11084626