Genetic Conflict and Imprinting

Abstract

‘Imprinting’ is a mechanism causing differential expression of the parental alleles of certain genes during embryonic and postnatal development in mammals and during seed development in angiosperm plants. Imprinting evolves due to the reduced genetic relatedness of paternal, relative to maternal, alleles at loci influencing maternal investment in the offspring of polygamous females.

Keywords: kin selection; parent–offspring conflict; placenta; endosperm; X‐chromosome inactivation

Figure 1.

Influence of polyandry on parental allele relatedness. Note that relatedness of maternal alleles is ‘neutral’ with respect to number of mates, whereas polyandry (different fathers) abolishes relatedness between paternal allelic components of embryo genotype.

Figure 2.

Schematic of a transcriptional ‘arms race’ between maternal and paternal alleles at a locus that influences parental investment (PI). Incremental increases in expression of one parental allele are tracked by incremental decreases in expression of the other parental allele.

Figure 3.

(a) Active ‘selfish’ Xp. Embryos of genotype XmXp (female) and XmY (male) compete for maternal resources. Thickness of vertical arrows represents relative amount of maternal resources demanded or transferred. In the absence of preferential paternal X‐inactivation, ‘selfish’ Xp‐linked alleles (e.g. X‐linked placental growth factors) will cause dosage imbalances between male and female embryos that may be translated into relatively increased PI in female embryos to the detriment of male sibs. (b) Inactivated Xp. On the assumption that the Y‐chromosome does not contain loci encoding significant effects on PI, imprinted Xp inactivation equalizes gene dosage and PI between male and female embryos.

close

References

Cattanach BM and Beechey CV (1997) Genomic imprinting in the mouse: possible final analysis. In: Reik W and Surani A (eds) Genomic Imprinting, Frontiers in Molecular Biology, pp. 118–145. Oxford, UK: IRL Press.

Colosi DC, Martin D, Moré K and Lalande M (2006) Genomic organisation and allelic expression of UBE3A in chicken. Gene 383: 93–98.

Crouse HV (1960) The controlling element in sex chromosome behavior in Sciara. Genetics 45: 1429–1443.

Davies W, Isles AR, Humby T and Wilkinson LS (2008) What are imprinted genes doing in the brain? In: Wilkins JF (ed.) Genomic Imprinting. Landes Bioscience: Austin, TX. Advances in Experimental Medicine and Biology 626: 62–70.

DeChiara TM, Robertson EJ and Efstratiadis A (1991) Parental imprinting of the mouse insulin‐like growth factor II gene. Cell 64(4): 849–859.

Haig D (1993) Genetic conflicts in human pregnancy. Quarterly Reviews of Biology 68(4): 495–532.

Haig D and Westoby M (1989) Parent‐specific gene expression and the triploid endosperm. American Naturalist 134: 147–155.

Hamilton WD (1964) The genetical evolution of social behavior. Journal of Theoretical Biology 7: 1–52.

Hurst LD (1997) Evolutionary theories of genomic imprinting. In: Reik W and Surani A (eds) Genomic Imprinting, Frontiers in Molecular Biology, pp. 211–237. Oxford, UK: IRL Press.

Kermicle JL and Alleman M (1990) Gametic imprinting in maize in relation to the angiosperm life cycle. Development (suppl.): 9–14.

Lau MM, Stewart CE, Liu Z et al. (1994) Loss of the imprinted IGF2/cation‐independent mannose 6‐phosphate receptor results in fetal overgrowth and perinatal lethality. Genes & Development 8(24): 2953–2963.

Li Y and Behringer RR (1998) Esx1 is an X‐chromosome‐imprinted regulator of placental development and fetal growth. Nature Genetics 20(3): 309–311.

Lyon MF and Rastan S (1984) Parental source of chromosome imprinting and its relevance for X chromosome inactivation. Differentiation 26(1): 63–67.

McGrath J and Solter D (1984) Completion of mouse embryogenesis requires both the maternal and paternal genomes. Cell 37(1): 179–183.

Mills W and Moore T (2004) Polyandry, life‐history trade‐offs and the evolution of imprinting at Mendelian loci. Genetics 168(4): 2317–2327.

Mills W and Moore T (2006) Evolution of mammalian X chromosome‐linked imprinting. Cytogenetic and Genome Research 113(1–4): 336–344.

Mochizuki A, Takeda Y and Iwasa Y (1996) The evolution of genomic imprinting. Genetics 144(3): 1283–1289.

Moore T and Haig D (1991) Genomic imprinting in mammalian development: a parental tug‐of‐war. Trends in Genetics 7(2): 45–49.

Moore T and Mills W (2008) Evolutionary theories of imprinting – enough already! In: Wilkins JF (ed.) Genomic Imprinting. Landes Bioscience: Austin, TX. Advances in Experimental Medicine and Biology 626: 116–122.

Morison IM, Ramsay JP and Spencer HG (2005) A census of mammalian imprinting. Trends in Genetics 21(8): 457–465.

Orr HA (1995) Somatic mutation favors the evolution of diploidy. Genetics 139(3): 1441–1447.

Spencer HG (2000) Population genetics and evolution of genomic imprinting. Annual Reviews of Genetics 34: 457–477.

Surani MA, Barton SC and Norris ML (1984) Development of reconstituted mouse eggs suggests imprinting of the genome during gametogenesis. Nature 308(5959): 548–550.

Takagi N and Sasaki M (1975) Preferential inactivation of the paternally derived X chromosome in the extraembryonic membranes of the mouse. Nature 256(5519): 640–642.

Trivers RL (1974) Parent–offspring conflict. American Zoologist 11: 249–264.

Wilkins JF and Haig D (2003) What good is genomic imprinting: the function of parent‐specific gene expression. Nature Reviews. Genetics 4(5): 359–368.

Zechner U, Reule M, Orth A et al. (1996) An X‐chromosome linked locus contributes to abnormal placental development in mouse interspecific hybrid. Nature Genetics 12(4): 398–403.

Further Reading

Baroux C, Spillane C and Grossniklaus U (2002) Genomic imprinting during seed development. Advances in Genetics 46: 165–214.

Clutton‐Brock TH (1991) The evolution of parental care. In: Krebs JR and Clutton‐Brock T (eds) Monographs in Behaviour and Ecology. Princeton, NJ: Princeton University Press.

Forsyth IA (1994) Comparative aspects of placental lactogens: structure and function. Experimental and Clinical Endocrinology 102(3): 244–251.

Haig D (2000) The kinship theory of genomic imprinting. Annual Reviews of Ecological Systems 31: 9–32.

Haig D (2002) Genomic Imprinting and Kinship. New Brunswick, NJ: Rutgers University Press.

Haig D (2008) Huddling: brown fat, genomic imprinting and the warm inner glow. Current Biology 18(4): R172–R174.

Hall DW (2000) The evolution of haploid, diploid and polymorphic haploid‐diploid life cycles: the role of meiotic mutation. Genetics 156(2): 893–898.

Maynard Smith J (1989) Evolutionary Genetics. Oxford, UK: Oxford University Press.

Moore T (2001) Genetic conflict, genomic imprinting and establishment of the epigenotype in relation to growth. Reproduction 122: 185–193.

Reik W, Davies K, Dean W, Kelsey G and Constancia M (2001) Imprinted genes and the coordination of fetal and postnatal growth in mammals. Novartis Foundation Symposium 237: 19–42.

Trivers RL (1972) Parental investment and sexual selection. In: Campbell B (ed.) Sexual Selection and the Descent of Man, pp. 136–179. Chicago, IL: Aldine.

Web Links

Geneimprint http://www.geneimprint.com

MRC Mammalian Genetics Unit. Genetic and physical imprinting maps of the mouse http://www.mgu.har.mrc.ac.uk/imprinting/imprinting.html

Contact Editor close
Submit a note to the editor about this article by filling in the form below.

* Required Field

How to Cite close
Moore, Tom(Dec 2008) Genetic Conflict and Imprinting. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0005978.pub2]