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Evolutionary Theories of Imprinting— Enough Already!

  • Tom Moore
  • Walter Mills
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 626)

Abstract

In our view, the conflict theory of imprinting explains the evolution of parental allele-specific gene expression patterns in the somatic tissues of mammals and angiosperms. Not surprisingly, given its importance in mammalian development and pathology, the evolution of imprinting continues to attract considerable interest from theoretical and experimental biologists. However, we contend that much of the ensuing debate is of poor quality. We discuss several problems with the manner in which workers in the field engage in this debate and we argue for a more formal approach to the discussion of theories of the evolution of imprinting.

Keywords

Imprint Gene Somatic Tissue Maternal Investment Imprint Locus Monoallelic Expression 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. 1.
    Beatty J. The evolutionary contingency thesis. In: Wolters G, Lennox JG, McLaughlin P, eds. Concepts, Theories and Rationality in the Biological Sciences: the Second Pittsburgh-Konstanz Colloquium in the Philosophy of Science. Pittsburgh: University of Pittsburgh Press, 45–81.Google Scholar
  2. 2.
    Popper KR. The Logic of Scientific Discovery. New York: Harper. 1959.Google Scholar
  3. 3.
    Thornton S. “Karl Popper”, the Stanford Encyclopedia of Philosophy (Summer 2005 Edition) Zalta EN (ed.), URL=<http://;plato.stanford.edu/archives/sum2005/entries/popper/>.Google Scholar
  4. 4.
    Kuhn TS. The Structure of Scientific Revolutions Chicago: University of Chicago Press, 1962.Google Scholar
  5. 5.
    Lakatos I. Falsification and the Methodology of Scientific Research Programmes. In: Lakatos I, Musgrave A, eds. Criticism and the Growth of Knowledge. Cambridge: Cambridge University Press. 1970:91–195.Google Scholar
  6. 6.
    Maynard Smith J. The Evolution of Sex. Cambridge: Cambridge University Press. 1978.Google Scholar
  7. 7.
    Hamilton WD. Sex versus nonsex versus parasite. Oikos 1980: 35:282–290.CrossRefGoogle Scholar
  8. 8.
    Kondrashov AS. Deleterious mutations and the evolution of sexual reproduction. Nature 1988; 336:435–440.PubMedCrossRefGoogle Scholar
  9. 9.
    Peters AD, Otto SP. Liberating genetic variance through sex. Bioessays 2003; 25(6):533–7.PubMedCrossRefGoogle Scholar
  10. 10.
    Miyoshi N, Barton SC, Kaneda M et al. The continued quest to comprehend genomic imprinting. Cytogenet Genome Res 2006; 113(1–4):6–11.PubMedCrossRefGoogle Scholar
  11. 11.
    Solter D. Imprinting today: end of the beginning or beginning of the end? Cytogenet Genome Res 2006; 113(1–4):12–6.PubMedCrossRefGoogle Scholar
  12. 12.
    Cattanach BM, Beechey CV, Peters J. Interactions between imprinting effects: summary and review. Cytogenet Genome Res 2006; 113(1–4):17–23.PubMedCrossRefGoogle Scholar
  13. 13.
    Sasaki H, Ishihara K, Kato R. Mechanisms of Igf2/H19 imprinting: DNA methylation, chromatin and long-distance gene regulation. J Biochem (Tokyo) 2000; 127(5):711–5.Google Scholar
  14. 14.
    Holmes R, Soloway PD. Regulation of imprinted DNA methylation. Cytogenet Genome Res 2006; 113(1–4):122–9.PubMedCrossRefGoogle Scholar
  15. 15.
    Haig D, Westoby M. Parent-specific gene expression and the triploid endosperm. American Naturalist 1989; 134:147–155.CrossRefGoogle Scholar
  16. 16.
    Moore T, Haig D. Genomic imprinting in mammalian development: a parental tug-of-war. Trends in Genetics 1991; 7:45–49.PubMedGoogle Scholar
  17. 17.
    Mochizuki A, Takeda Y, Iwasa Y. The evolution of genomic imprinting. Genetics 1996; 144(3):1283–95.PubMedGoogle Scholar
  18. 18.
    Orr HA. Somatic mutation favors the evolution of diploidy. Genetics 1995; 139(3):1441–7.PubMedGoogle Scholar
  19. 19.
    Spencer HG. Mutation-selection balance under genomic imprinting at an autosomal locus. Genetics 1997; 147(1):281–7.PubMedGoogle Scholar
  20. 20.
    Wray GA. Transcriptional regulation and the evolution of development. Int J Dev Biol 2003; 47(7–8):675–84.PubMedGoogle Scholar
  21. 21.
    Pritchard C, Coil D, Hawley S et al. The contributions of normal variation and genetic background to mammalian gene expression. Genome Biol 2006; 7(3):R26.PubMedCrossRefGoogle Scholar
  22. 22.
    Mills W, Moore T. Polyandry, life-history trade-offs and the evolution of imprinting at Mendelian loci. Genetics. 2004 168(4):2317–27. Erratum in: Genetics 2005; 171(3):1443.PubMedCrossRefGoogle Scholar
  23. 23.
    Vinkenoog R, Bushell C, Spielman M et al. Genomic imprinting and endosperm development in flowering plants. Mol Biotechnol 2003; 25(2):149–84.PubMedCrossRefGoogle Scholar
  24. 24.
    Morison IM, Ramsay JP, Spencer HG. Trends Genet 2005; 21(8):457–65.PubMedCrossRefGoogle Scholar
  25. 25.
    O’Neill MJ, Ingram RS, Vrana PB et al. Allelic expression of IGF2 in marsupials and birds. Dev Genes Evol 2000; 210(1):18–20.PubMedCrossRefGoogle Scholar
  26. 26.
    Nolan CM, Killian JK, Petitte JN et al. Imprint status of M6P/IGF2R and IGF2 in chickens. Dev Genes Evol 2001;211(4):179–83.PubMedCrossRefGoogle Scholar
  27. 27.
    Lawton BR, Sevigny L, Obergfell C et al. Allelic expression of IGF2 in live-bearing, matrotrophic fishes. Dev Genes Evol 2005; 215(4):207–12.PubMedCrossRefGoogle Scholar
  28. 28.
    Wittkopp PJ, Haerum BK, Clark AG. Parent-of-Origin Effects on mRNA Expression in Drosophila melanogaster Not Caused by Genomic Imprinting. Genetics 2006;173(3):1817–21.PubMedCrossRefGoogle Scholar
  29. 29.
    Haack H, Hodgkin J. Tests for parental imprinting in the nematode Caenorhabditis elegans. Mol Gen Genet 1991; 228(3):482–5.PubMedCrossRefGoogle Scholar
  30. 30.
    Goday C, Esteban MR. Chromosome elimination in sciarid flies. Bioessays 2001; 23(3):242–50.PubMedCrossRefGoogle Scholar
  31. 31.
    Queller DC. Theory of genomic imprinting conflict in social insects. BMC Evol Biol 2003; 3:15.PubMedCrossRefGoogle Scholar
  32. 32.
    Khosla S, Mendiratta G, Brahmachari V. Genomic imprinting in the mealybugs. Cytogenet Genome Res 2006; 113(1–4):41–52.PubMedCrossRefGoogle Scholar
  33. 33.
    Moore T. Genetic conflict, genomic imprinting and establishment of the epigenotype in relation to growth. Reproduction 2001;122(2):185–93.PubMedCrossRefGoogle Scholar
  34. 34.
    Fowden AL, Sibley C, Reik W et al. Imprinted genes, placental development and fetal growth. Horm Res 2006; 65 Suppl 3:50–8.PubMedCrossRefGoogle Scholar
  35. 35.
    Lin B-Y. Association of endosperm reduction with parental imprinting in maize. Genetics 1982; 100:475–486.PubMedGoogle Scholar
  36. 36.
    Moore T, Hurst LD, Reik W. Genetic conflict and evolution of mammalian X chromosome inactivation. Dev Genet 1995; 17(3):206–11.PubMedCrossRefGoogle Scholar
  37. 37.
    Mills W and Moore T. Evolution of mammalian X chromosome-linked imprinting. Cytogenet Genome Res 2006; 113(1–4):336–44.PubMedCrossRefGoogle Scholar
  38. 38.
    Okamura K, Ito T. Lessons from comparative analysis of species-specific imprinted genes. Cytogenet Genome Res 2006; 113(1–4):159–64.PubMedCrossRefGoogle Scholar
  39. 39.
    Kaneko-Ishino T, Kohda T, Ono R et al. Complementation hypothesis: the necessity of a monoallelic gene expression mechanism in mammalian development. Cytogenet Genome Res 2006; 113(1–4):24–30.PubMedCrossRefGoogle Scholar
  40. 40.
    Normark BB. Perspective: maternal kin groups and the origins of asymmetric genetic systems-genomic imprinting, haplodiploidy and parthenogenesis. Evolution Int J Org Evolution 2006;60(4):631–42.Google Scholar
  41. 41.
    Skuse DH. Genomic imprinting of the X chromosome: a novel mechanism for the evolution of sexual dimorphism. J Lab Clin Med 1999; 133(1):23–32.PubMedCrossRefGoogle Scholar
  42. 42.
    Iwasa Y, Pomiankowski A. The evolution of X-linked genomic imprinting. Genetics 2001; 158(4):1801–9.PubMedGoogle Scholar
  43. 43.
    Guillemot F, Caspary T, Tilghman SM et al. Genomic imprinting of Mash2, a mouse gene required for trophoblast development. Nat Genet 1995; 9(3):235–42.PubMedCrossRefGoogle Scholar
  44. 44.
    Iwasa Y. The conflict theory of genomic imprinting: how much can be explained? Curr Top Dev Biol 1998; 40:255–93.PubMedCrossRefGoogle Scholar
  45. 45.
    Ferguson-Smith AC, Moore T, Detmar J et al. Epigenetics and imprinting of the trophoblast—a workshop report. Placenta 2006;27(Suppl A): S122–6.CrossRefGoogle Scholar
  46. 46.
    Hurst, LD. Evolutionary theories of genomic imprinting. In: Reik W, Surani A, eds. Genomic Imprinting. Oxford: IRL Press, 1997; 211–37.Google Scholar
  47. 47.
    Wilkins JF, Haig D. What good is genomic imprinting: the function of parent-specific gene expression. Nature Reviews Genetics 2003; 4:359–368.PubMedCrossRefGoogle Scholar
  48. 48.
    Weisstein A, Spencer HG. Evolutionary Genetic Models of the Ovarian Time Bomb Hypothesis of Genomic Imprinting. Genetics 2002;162:425–439.PubMedGoogle Scholar
  49. 49.
    Weisstein A, Spencer HG. The Evolution of Genomic Imprinting via Variance Minimization: An Evolutionary Genetic Model. Genetics 2003; 165:205–222.PubMedGoogle Scholar
  50. 50.
    Day T, Bonduriansky R. Intralocus sexual conflict can drive the evolution of genomic imprinting. Genetics 2004; 167(4):1537–46.PubMedCrossRefGoogle Scholar

Copyright information

© Landes Bioscience and Springer Science+Business Media 2008

Authors and Affiliations

  1. 1.Department of Biochemistry, Biosciences InstituteUniversity College CorkCorkIreland

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