title: Sex-differential selection and the evolution of X inactivation strategies.
abstract: X inactivation--the transcriptional silencing of one X chromosome copy per female somatic cell--is universal among therian mammals, yet the choice of which X to silence exhibits considerable variation among species. X inactivation strategies can range from strict paternally inherited X inactivation (PXI), which renders females haploid for all maternally inherited alleles, to unbiased random X inactivation (RXI), which equalizes expression of maternally and paternally inherited alleles in each female tissue. However, the underlying evolutionary processes that might account for this observed diversity of X inactivation strategies remain unclear. We present a theoretical population genetic analysis of X inactivation evolution and specifically consider how conditions of dominance, linkage, recombination, and sex-differential selection each influence evolutionary trajectories of X inactivation. The results indicate that a single, critical interaction between allelic dominance and sex-differential selection can select for a broad and continuous range of X inactivation strategies, including unequal rates of inactivation between maternally and paternally inherited X chromosomes. RXI is favored over complete PXI as long as alleles deleterious to female fitness are sufficiently recessive, and the criteria for RXI evolution is considerably more restrictive when fitness variation is sexually antagonistic (i.e., alleles deleterious to females are beneficial to males) relative to variation that is deleterious to both sexes. Evolutionary transitions from PXI to RXI also generally increase mean relative female fitness at the expense of decreased male fitness. These results provide a theoretical framework for predicting and interpreting the evolution of chromosome-wide expression of X-linked genes and lead to several useful predictions that could motivate future studies of allele-specific gene expression variation.
authors: Department of Molecular Biology and Genetics, Cornell University, Ithaca, New York, United States of America. tmc233@cornell.edu
authors: Tim
authors: T
authors: Connallon
authors: Andrew G
authors: AG
authors: Clark
mesh_terms: D000483:Alleles; D000818:Animals; D005075:Biological Evolution; D050172:Genes, X-Linked; D014960:X Chromosome; D049951:X Chromosome Inactivation
references: Evolution. 2010 Mar 1;64(3):663-74
references: 19796145
references: Trends Genet. 2009 May;25(5):226-33
references: 19359064
references: Nature. 1991 May 23;351(6324):273-4
references: 2034271
references: Proc Natl Acad Sci U S A. 2001 Feb 13;98(4):1671-5
references: 11172009
references: J Evol Biol. 2011 Sep;24(9):1918-26
references: 21658188
references: Genome Biol. 2010;11(7):R79
references: 20663224
references: Am Nat. 2010 Oct;176(4):511-21
references: 20795831
references: Evolution. 2008 Aug;62(8):2097-104
references: 18507742
references: Genet Res. 1999 Dec;74(3):329-40
references: 10689809
references: Science. 2010 Aug 6;329(5992):682-5
references: 20616234
references: PLoS One. 2007 Aug 15;2(8):e744
references: 17710144
references: Evolution. 1984 Jul;38(4):735-742
references: 28555827
references: Theor Popul Biol. 1997 Feb;51(1):23-35
references: 9149816
references: Evolution. 2013 Jul;67(7):1915-25
references: 23815649
references: Genetics. 2004 Aug;167(4):1537-46
references: 15342496
references: Science. 2011 Nov 18;334(6058):972-4
references: 22096197
references: Annu Rev Genet. 2008;42:733-72
references: 18729722
references: Aust J Biol Sci. 1976 Jul;29(3):245-50
references: 985224
references: Genetics. 2012 Nov;192(3):1095-107
references: 22887817
references: Genetics. 2012 Dec;192(4):1455-64
references: 23023005
references: Evolution. 2012 Jul;66(7):2127-37
references: 22759290
references: Proc Natl Acad Sci U S A. 1978 Nov;75(11):5618-22
references: 281711
references: Chromosome Res. 2009;17(5):671-85
references: 19802707
references: Am J Hum Genet. 1988 Jan;42(1):8-16
references: 3276178
references: Nature. 1975 Jan 17;253(5488):165-8
references: 1089205
references: Evolution. 2011 Aug;65(8):2133-44
references: 21790564
references: Evolution. 2009 Mar;63(3):569-82
references: 19154364
references: Genetics. 2012 Dec;192(4):1389-409
references: 22982578
references: Genetics. 1995 Mar;139(3):1441-7
references: 7768451
references: Trends Ecol Evol. 1999 May;14(5):197-201
references: 10322534
references: Genetics. 1992 Jul;131(3):741-4
references: 1628814
references: Am Nat. 2009 Oct;174(4):E141-69
references: 19737113
references: J Theor Biol. 1999 Apr 21;197(4):487-95
references: 10196091
references: Genetics. 2011 Feb;187(2):553-66
references: 21098719
references: Trends Genet. 1991 Feb;7(2):45-9
references: 2035190
references: Evolution. 2010 Jun;64(6):1671-82
references: 20050912
references: Trends Genet. 2011 Jul;27(7):251-7
references: 21683468
references: Nat Rev Genet. 2006 Aug;7(8):645-53
references: 16847464
references: Evolution. 2011 Jul;65(7):2085-97
references: 21729062
references: Genetics. 2001 Aug;158(4):1801-9
references: 11514463
references: Genetics. 2007 Jun;176(2):1101-18
references: 17435253
references: Curr Biol. 2008 Dec 23;18(24):R1121-4
references: 19108763
references: Nature. 1961 Apr 22;190:372-3
references: 13764598
references: Genetics. 1969 Oct;63(2):467-78
references: 5366220
references: Evolution. 2013 Apr;67(4):1189-95
references: 23550766
references: Evolution. 2009 Nov;63(11):2888-95
references: 19573084
references: Am J Med Genet A. 2004 Aug 30;129A(2):136-43
references: 15316978
references: Trends Ecol Evol. 2009 May;24(5):280-8
references: 19307043
references: Annu Rev Genet. 2011;45:379-403
references: 21942369
references: Evolution. 1995 Jun;49(3):512-520
references: 28565083
references: J Theor Biol. 2006 Jul 7;241(1):81-93
references: 16387326
references: PLoS Biol. 2010 Mar 16;8(3):e1000335
references: 20305719
references: Evolution. 2006 Mar;60(3):440-7
references: 16637489
references: Am Nat. 1999 Jun;153(6):561-574
references: 29585648
references: Annu Rev Genet. 1977;11:49-78
references: 413473
references: Nature. 1971 Mar 26;230(5291):231-2
references: 4926712
references: Genetics. 2004 Jan;166(1):565-79
references: 15020445
references: Genetica. 1998;102-103(1-6):3-19
references: 9720268
references: Genetics. 2012 Apr;190(4):1477-89
references: 22298707
references: Bioessays. 2011 Dec;33(12):938-45
references: 22006834
references: Genetics. 2011 Mar;187(3):919-37
references: 21220356
references: Genetics. 1977 Jan;85(1):171-83
references: 838269
references: Nature. 1991 May 23;351(6324):314-5
references: 2034273
references: Nature. 2004 May 6;429(6987):65-7
references: 15129280
references: Nature. 1991 May 23;351(6324):315-7
references: 2034274
references: Science. 2010 Apr 2;328(5974):92-4
references: 20203012
references: Evolution. 1985 Jan;39(1):24-40
references: 28563655
references: Am Nat. 2009 Feb;173(2):176-87
references: 19138156
references: Genetics. 2000 Oct;156(2):893-8
references: 11014834
references: Ann N Y Acad Sci. 2009 Jun;1168:52-71
references: 19566703
references: BMC Evol Biol. 2011 Jun 06;11:156
references: 21645375
references: Curr Opin Genet Dev. 2006 Jun;16(3):246-53
references: 16647851
references: Genetics. 2010 Sep;186(1):277-86
references: 20551442
references: Nature. 2007 Jun 28;447(7148):1107-10
references: 17597758
references: Mol Syst Biol. 2011 Aug 02;7:522
references: 21811232
references: Genetics. 1998 Feb;148(2):893-904
references: 9504935
references: Curr Biol. 1996 Feb 1;6(2):149-62
references: 8673462
references: Proc Biol Sci. 2007 Jan 7;274(1606):1-10
references: 17134994
references: Nat Rev Genet. 2003 May;4(5):359-68
references: 12728278
references: Genetics. 1992 Jul;131(3):745-51
references: 1628815
references: Evolution. 2012 Dec;66(12):3743-53
references: 23206133
references: New Phytol. 2011 Oct;192(2):542-52
references: 21726233
references: Nat New Biol. 1971 Mar 31;230(13):155-7
references: 5279474
references: Adv Genet. 2002;46:451-83
references: 11931235