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. 2004 Aug;167(4):1537–1546. doi: 10.1534/genetics.103.026211

Intralocus sexual conflict can drive the evolution of genomic imprinting.

Troy Day 1, Russell Bonduriansky 1
PMCID: PMC1470977  PMID: 15342496

Abstract

Genomic imprinting is a phenomenon whereby the expression of an allele differs depending upon its parent of origin. There is an increasing number of examples of this form of epigenetic inheritance across a wide range of taxa, and imprinting errors have also been implicated in several human diseases. Various hypotheses have been put forward to explain the evolution of genomic imprinting, but there is not yet a widely accepted general hypothesis for the variety of imprinting patterns observed. Here a new evolutionary hypothesis, based on intralocus sexual conflict, is proposed. This hypothesis provides a potential explanation for much of the currently available empirical data, and it also makes new predictions about patterns of genomic imprinting that are expected to evolve but that have not, as of yet, been looked for in nature. This theory also provides a potential mechanism for the resolution of intralocus sexual conflict in sexually selected traits and a novel pathway for the evolution of sexual dimorphism.

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Selected References

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  1. Anderson R. J., Spencer H. G. Population models of genomic imprinting. I. Differential viability in the sexes and the analogy with genetic dominance. Genetics. 1999 Dec;153(4):1949–1958. doi: 10.1093/genetics/153.4.1949. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Barlow D. P. Gametic imprinting in mammals. Science. 1995 Dec 8;270(5242):1610–1613. doi: 10.1126/science.270.5242.1610. [DOI] [PubMed] [Google Scholar]
  3. Beukeboom L. W., van den Assem J. Courtship and mating behaviour of interspecific Nasonia hybrids (Hymenoptera, Pteromalidae): a grandfather effect. Behav Genet. 2001 Mar;31(2):167–177. doi: 10.1023/a:1010201427204. [DOI] [PubMed] [Google Scholar]
  4. Bunzel R., Blümcke I., Cichon S., Normann S., Schramm J., Propping P., Nöthen M. M. Polymorphic imprinting of the serotonin-2A (5-HT2A) receptor gene in human adult brain. Brain Res Mol Brain Res. 1998 Aug 15;59(1):90–92. doi: 10.1016/s0169-328x(98)00146-6. [DOI] [PubMed] [Google Scholar]
  5. Burt A., Trivers R. Genetic conflicts in genomic imprinting. Proc Biol Sci. 1998 Dec 22;265(1413):2393–2397. doi: 10.1098/rspb.1998.0589. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Butler Merlin G. Imprinting disorders: non-Mendelian mechanisms affecting growth. J Pediatr Endocrinol Metab. 2002 Dec;15 (Suppl 5):1279–1288. [PMC free article] [PubMed] [Google Scholar]
  7. Chippindale A. K., Gibson J. R., Rice W. R. Negative genetic correlation for adult fitness between sexes reveals ontogenetic conflict in Drosophila. Proc Natl Acad Sci U S A. 2001 Jan 30;98(4):1671–1675. doi: 10.1073/pnas.041378098. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Croteau S., Polychronakos C., Naumova A. K. Imprinting defects in mouse embryos: stochastic errors or polymorphic phenotype? Genesis. 2001 Sep;31(1):11–16. doi: 10.1002/gene.1077. [DOI] [PubMed] [Google Scholar]
  9. Ferguson-Smith A. C., Surani M. A. Imprinting and the epigenetic asymmetry between parental genomes. Science. 2001 Aug 10;293(5532):1086–1089. doi: 10.1126/science.1064020. [DOI] [PubMed] [Google Scholar]
  10. Giannoukakis N., Deal C., Paquette J., Kukuvitis A., Polychronakos C. Polymorphic functional imprinting of the human IGF2 gene among individuals, in blood cells, is associated with H19 expression. Biochem Biophys Res Commun. 1996 Mar 27;220(3):1014–1019. doi: 10.1006/bbrc.1996.0524. [DOI] [PubMed] [Google Scholar]
  11. Gibson Jonathan R., Chippindale Adam K., Rice William R. The X chromosome is a hot spot for sexually antagonistic fitness variation. Proc Biol Sci. 2002 Mar 7;269(1490):499–505. doi: 10.1098/rspb.2001.1863. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Gorlova Olga Y., Amos Christopher I., Wang Nancy W., Shete Sanjay, Turner Stephen T., Boerwinkle Eric. Genetic linkage and imprinting effects on body mass index in children and young adults. Eur J Hum Genet. 2003 Jun;11(6):425–432. doi: 10.1038/sj.ejhg.5200979. [DOI] [PubMed] [Google Scholar]
  13. Haig D. Do imprinted genes have few and small introns? Bioessays. 1996 May;18(5):351–353. doi: 10.1002/bies.950180504. [DOI] [PubMed] [Google Scholar]
  14. Houle D. Comparing evolvability and variability of quantitative traits. Genetics. 1992 Jan;130(1):195–204. doi: 10.1093/genetics/130.1.195. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. 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]
  16. Iwasa Y., Pomiankowski A. The evolution of X-linked genomic imprinting. Genetics. 2001 Aug;158(4):1801–1809. doi: 10.1093/genetics/158.4.1801. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Iyengar Vikram K., Reeve H. Kern, Eisner Thomas. Paternal inheritance of a female moth's mating preference. Nature. 2002 Oct 24;419(6909):830–832. doi: 10.1038/nature01027. [DOI] [PubMed] [Google Scholar]
  18. Kidwell J. F., Clegg M. T., Stewart F. M., Prout T. Regions of stable equilibria for models of differential selection in the two sexes under random mating. Genetics. 1977 Jan;85(1):171–183. doi: 10.1093/genetics/85.1.171. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Lindholm Anna, Breden Felix. Sex chromosomes and sexual selection in poeciliid fishes. Am Nat. 2002 Dec;160 (Suppl 6):S214–S224. doi: 10.1086/342898. [DOI] [PubMed] [Google Scholar]
  20. McGrath J., Solter D. Completion of mouse embryogenesis requires both the maternal and paternal genomes. Cell. 1984 May;37(1):179–183. doi: 10.1016/0092-8674(84)90313-1. [DOI] [PubMed] [Google Scholar]
  21. Moore T. Genetic conflict, genomic imprinting and establishment of the epigenotype in relation to growth. Reproduction. 2001 Aug;122(2):185–193. doi: 10.1530/rep.0.1220185. [DOI] [PubMed] [Google Scholar]
  22. 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]
  23. Rand D. M., Clark A. G., Kann L. M. Sexually antagonistic cytonuclear fitness interactions in Drosophila melanogaster. Genetics. 2001 Sep;159(1):173–187. doi: 10.1093/genetics/159.1.173. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Rhen T. Sex-limited mutations and the evolution of sexual dimorphism. Evolution. 2000 Feb;54(1):37–43. doi: 10.1111/j.0014-3820.2000.tb00005.x. [DOI] [PubMed] [Google Scholar]
  25. Spencer H. G. Mutation-selection balance under genomic imprinting at an autosomal locus. Genetics. 1997 Sep;147(1):281–287. doi: 10.1093/genetics/147.1.281. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Spencer Hamish G., Feldman Marcus W., Clark Andrew G., Weisstein Anton E. The effect of genetic conflict on genomic imprinting and modification of expression at a sex-linked locus. Genetics. 2004 Jan;166(1):565–579. doi: 10.1534/genetics.166.1.565. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Tycko Benjamin, Morison Ian M. Physiological functions of imprinted genes. J Cell Physiol. 2002 Sep;192(3):245–258. doi: 10.1002/jcp.10129. [DOI] [PubMed] [Google Scholar]
  28. Wilcockson R. W., Crean C. S., Day T. H. Heritability of a sexually selected character expressed in both sexes. Nature. 1995 Mar 9;374(6518):158–159. doi: 10.1038/374158a0. [DOI] [PubMed] [Google Scholar]
  29. Wilkins Jon F., Haig David. What good is genomic imprinting: the function of parent-specific gene expression. Nat Rev Genet. 2003 May;4(5):359–368. doi: 10.1038/nrg1062. [DOI] [PubMed] [Google Scholar]
  30. Xu Y., Goodyer C. G., Deal C., Polychronakos C. Functional polymorphism in the parental imprinting of the human IGF2R gene. Biochem Biophys Res Commun. 1993 Dec 15;197(2):747–754. doi: 10.1006/bbrc.1993.2542. [DOI] [PubMed] [Google Scholar]
  31. Yang Howard H., Hu Ying, Edmonson Michael, Buetow Kenneth, Lee Maxwell P. Computation method to identify differential allelic gene expression and novel imprinted genes. Bioinformatics. 2003 May 22;19(8):952–955. doi: 10.1093/bioinformatics/btg127. [DOI] [PubMed] [Google Scholar]

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