Abstract
We develop a quantitative genetic model to investigate the evolution of X-imprinting. The model compares two forces that select for X-imprinting: genomic conflict caused by polygamy and sex-specific selection. Genomic conflict can only explain small reductions in maternal X gene expression and cannot explain silencing of the maternal X. In contrast, sex-specific selection can cause extreme differences in gene expression, in either direction (lowered maternal or paternal gene expression), even to the point of gene silencing of either the maternal or paternal copy. These conclusions assume that the Y chromosome lacks genetic activity. The presence of an active Y homologue makes imprinting resemble the autosomal pattern, with active paternal alleles (X- and Y-linked) and silenced maternal alleles. This outcome is likely to be restricted as Y-linked alleles are subject to the accumulation of deleterious mutations. Experimental evidence concerning X-imprinting in mouse and human is interpreted in the light of these predictions and is shown to be far more easily explained by sex-specific selection.
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Selected References
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- Bishop D. V., Canning E., Elgar K., Morris E., Jacobs P. A., Skuse D. H. Distinctive patterns of memory function in subgroups of females with Turner syndrome: evidence for imprinted loci on the X-chromosome affecting neurodevelopment. Neuropsychologia. 2000;38(5):712–721. doi: 10.1016/s0028-3932(99)00118-9. [DOI] [PubMed] [Google Scholar]
- Burgoyne P. S., Thornhill A. R., Boudrean S. K., Darling S. M., Bishop C. E., Evans E. P. The genetic basis of XX-XY differences present before gonadal sex differentiation in the mouse. Philos Trans R Soc Lond B Biol Sci. 1995 Nov 29;350(1333):253–261. doi: 10.1098/rstb.1995.0159. [DOI] [PubMed] [Google Scholar]
- Charlesworth B. The evolution of chromosomal sex determination and dosage compensation. Curr Biol. 1996 Feb 1;6(2):149–162. doi: 10.1016/s0960-9822(02)00448-7. [DOI] [PubMed] [Google Scholar]
- Disteche C. M. Escape from X inactivation in human and mouse. Trends Genet. 1995 Jan;11(1):17–22. doi: 10.1016/s0168-9525(00)88981-7. [DOI] [PubMed] [Google Scholar]
- Graves J. A., Schmidt M. M. Mammalian sex chromosomes: design or accident? Curr Opin Genet Dev. 1992 Dec;2(6):890–901. doi: 10.1016/s0959-437x(05)80112-1. [DOI] [PubMed] [Google Scholar]
- Haig D., Graham C. Genomic imprinting and the strange case of the insulin-like growth factor II receptor. Cell. 1991 Mar 22;64(6):1045–1046. doi: 10.1016/0092-8674(91)90256-x. [DOI] [PubMed] [Google Scholar]
- Iwasa Y., Pomiankowski A. Sex specific X chromosome expression caused by genomic imprinting. J Theor Biol. 1999 Apr 21;197(4):487–495. doi: 10.1006/jtbi.1998.0888. [DOI] [PubMed] [Google Scholar]
- Jegalian K., Page D. C. A proposed path by which genes common to mammalian X and Y chromosomes evolve to become X inactivated. Nature. 1998 Aug 20;394(6695):776–780. doi: 10.1038/29522. [DOI] [PubMed] [Google Scholar]
- Mochizuki A., Takeda Y., Iwasa Y. The evolution of genomic imprinting. Genetics. 1996 Nov;144(3):1283–1295. doi: 10.1093/genetics/144.3.1283. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Moore T., Haig D. Genomic imprinting in mammalian development: a parental tug-of-war. Trends Genet. 1991 Feb;7(2):45–49. doi: 10.1016/0168-9525(91)90230-N. [DOI] [PubMed] [Google Scholar]
- Skuse D. H., James R. S., Bishop D. V., Coppin B., Dalton P., Aamodt-Leeper G., Bacarese-Hamilton M., Creswell C., McGurk R., Jacobs P. A. Evidence from Turner's syndrome of an imprinted X-linked locus affecting cognitive function. Nature. 1997 Jun 12;387(6634):705–708. doi: 10.1038/42706. [DOI] [PubMed] [Google Scholar]
- Thornhill A. R., Burgoyne P. S. A paternally imprinted X chromosome retards the development of the early mouse embryo. Development. 1993 May;118(1):171–174. doi: 10.1242/dev.118.1.171. [DOI] [PubMed] [Google Scholar]