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PLOS Biology  2006 

A Maternal–Offspring Coadaptation Theory for the Evolution of Genomic Imprinting

DOI: 10.1371/journal.pbio.0040380

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Abstract:

Imprinted genes are expressed either from the maternally or paternally inherited copy only, and they play a key role in regulating complex biological processes, including offspring development and mother–offspring interactions. There are several competing theories attempting to explain the evolutionary origin of this monoallelic pattern of gene expression, but a prevailing view has emerged that holds that genomic imprinting is a consequence of conflict between maternal and paternal gene copies over maternal investment. However, many imprinting patterns and the apparent overabundance of maternally expressed genes remain unexplained and may be incompatible with current theory. Here we demonstrate that sole expression of maternal gene copies is favored by natural selection because it increases the adaptive integration of offspring and maternal genomes, leading to higher offspring fitness. This novel coadaptation theory for the evolution of genomic imprinting is consistent with results of recent studies on epigenetic effects, and it provides a testable hypothesis for the origin of previously unexplained major imprinting patterns across different taxa. In conjunction with existing hypotheses, our results suggest that imprinting may have evolved due to different selective pressures at different loci.

References

[1]  Bartolomei MS, Tilghman SM (1997) Genomic imprinting in mammals. Ann Rev Gen 31: 493–525.
[2]  Surani MA, Barton SC, Norris ML (1984) Development of reconstituted mouse eggs suggests imprinting of the genome during gametogenesis. Nature 308: 548–550.
[3]  Moore T, Haig D (1991) Genomic imprinting in mammalian development: A parental tug-of-war. Trends Gen 7: 45–49.
[4]  Spencer HG, Clark AG, Feldman MW (1999) Genetic conflicts and the evolutionary origin of genomic imprinting. Trends Ecol Evol 14: 197–201.
[5]  Iwasa Y, Pomiankowski A (2001) The evolution of X-linked genomic imprinting. Genetics 158: 1801–1809.
[6]  Burt A, Trivers R (2006) Genes in conflict. Cambridge (Massachussets): Harvard University Press. 632 p.
[7]  Kondrashov AS, Crow JF (1991) Haploidy or diploidy: Which is better? Nature 351: 314–315.
[8]  Wilkins JF, Haig D (2003) What good is genomic imprinting: The function of parent-specific gene expression. Nat Gen Rev 4: 1–19.
[9]  Haig D, Graham C (1991) Genomic imprinting and the strange case of the insulin-like growth factor II receptor. Cell 64: 1045–1046.
[10]  Haig D (2004) Genomic imprinting and kinship: How good is the evidence? Ann Rev Gen 38: 553–585.
[11]  Day T, Bonduriansky R (2004) Intralocus sexual conflict can drive the evolution of genomic imprinting. Genetics 167: 1537–1546.
[12]  Li LL, Keverne EB, Aparicio SA, Ishino F, Barton SC, et al. (1999) Regulation of maternal behaviour and offspring growth by paternally expressed Peg3. Science 284: 330–333.
[13]  Haig D (1996) Placental hormones, genomic imprinting, and maternal-fetal communication. J Evol Biol 9: 357–380.
[14]  Haig D (1997) Parental antagonism, relatedness asymmetries, and genomic imprinting. Proc R Soc Lond Ser B Biol Sci 264: 1657–1661.
[15]  Burt A, Trivers R (1998) Genetic conflicts in genomic imprinting. Proc R Soc Lond Ser B Biol Sci 265: 2393–2397.
[16]  Spencer HG, Feldman MW, Clark AG (1998) Genetic conflicts, multiple paternity and the evolution of genomic imprinting. Genetics 148: 893–904.
[17]  Bateson P (1994) The dynamics of parent-offspring relationships in mammals. Trends Ecol Evol 10: 99–403.
[18]  K?lliker M, Brinkhof MW, Heeb P, Fitze PS, Richner H (2000) The quantitative genetic basis of offspring solicitation and parental response in a passerine bird with biparental care. Proc R Soc Lond Ser B Biol Sci 267: 2127–2132.
[19]  Agrawal AF, Brodie ED, Brown J (2001) Parent-offspring coadaptation and the dual genetic control of maternal care. Science 292: 1710–1712.
[20]  Lock JE, Smiseth PT, Moore AJ (2004) Selection, inheritance, and the evolution of parent-offspring interactions. Am Nat 164: 13–24.
[21]  Hager R, Johnstone RA (2003) The genetic basis of family conflict resolution in mice. Nature 421: 533–535.
[22]  Via S (1986) Genetic covariance between oviposition preference and larval performance in an insect herbivore. Evolution 40: 778–785.
[23]  Ulizzi L, Gravina MF, Terrento L (1981) Natural selection associated with birth weight. II. Stabilizing and directional components. Ann Hum Gen 45: 207–212.
[24]  Wolf JB, Brodie ED (1998) The coadaptation of parental and offspring characters. Evolution 52: 299–308.
[25]  Geordiades P, Watkins M, Burton GJ, Ferguson-Smith AC (2001) Roles for genomic imprinting and the zygotic genome in placental development. Proc Natl Acad Sci U S A 98: 4522–4527.
[26]  Reik W, Lewis A (2005) Co-evolution of X-chromosome inactivation and imprinting in mammals. Nat Rev Gen 6: 633–642.
[27]  Ferguson-Smith AC, Moore T, Detmar J, Lewis A, Hemberger A, et al. (2006) Epigenetics and imprinting of the trophoblast: A workshop report. Placenta 27(Suppl A): S122–S126.
[28]  Wagschal A, Feil R (2006) Genomic imprinting in the placenta. Cytogen Genome Res 113: 90–98.
[29]  Cowley D, Pomp D, Atchley W, Eisen E, Hawkins-Brown D (1989) The impact of maternal uterine genotype on postnatal growth and adult body size in mice. Genetics 122: 193–203.
[30]  Wolf JB (2000) Gene interactions from maternal effects. Evolution 54: 1882–1898.
[31]  Luedi PP, Hartemink AJ, Jirtle RL (2005) Genome-wide prediction of imprinted murine genes. Genome Res 15: 875–884.
[32]  K?lliker M, Brodie ED, Moore AJ (2005) The coadaptation of parental supply and offspring demand. Am Nat 166: 506–516.
[33]  Spencer HG (2002) The correlation between relatives on the supposition of genomic imprinting. Genetics 161: 411–417.
[34]  Tycko B, Morison IM (2002) Physiological functions of imprinted genes. J Cell Physiol 192: 245–258.
[35]  Gavrilets S (1998) One-locus two-allele models with maternal (parental) selection. Genetics 149: 1147–1152.
[36]  Wade MJ (1998) The evolutionary genetics of maternal effects. In: Mousseau TA, Fox CW, editors. Maternal effects as adaptations. Oxford: Oxford University Press. pp. 5–21.
[37]  Hager R, Johnstone RA (2005) Differential growth of own and alien young in mixed litters of mice: A role for genomic imprinting. Ethology 111: 705–711.
[38]  Hager R, Johnstone RA (2006) The influence of phenotypic and genetic effects on maternal provisioning and offspring weight gain in mice. Biol Lett 2: 81–84.
[39]  Jarvis JP, Kenney-Hunt J, Ehrich TH, Pletscher LS, Semenkovich CF, et al. (2005) Maternal genotype affects adult offspring lipid, obesity and diabetes phenotypes in LG X SM recombinant inbred strains. J Lipid Res 46: 1692–1702.
[40]  Cheverud JM, Moore AJ (1994) Quantitative genetics and the role of the environment provided by relatives in behavioral evolution. In: Boake CRB, editor. Quantitative genetic studies of behavioral evolution. Chicago: Chicago University Press. pp. 67–100.
[41]  Bernardo J (1996) Maternal effects in animal ecology. Am Zool 36: 83–105.
[42]  Mousseau TA, Fox CW (1998) Maternal effects as adaptations. New York: Oxford University Press. 375 p.
[43]  Reinhold K (2002) Maternal effects and the evolution of behavioral and morphological characters: a literature review indicates the importance of extended maternal care. J Hered 93: 400–405.
[44]  Mousseau TA, Roff D (1987) Natural selection and the heritability of fitness components. Heredity 59: 181–197.
[45]  Baroux C, Spillane C, Grossniklaus U (2002) Genomic imprinting during seed development. Adv Gen 46: 165–214.
[46]  Thompson JN (1988) Evolutionary ecology of the relationship between oviposition preference and performance of offspring in phytophagous insects. Entomol Exp Appl 47: 3–14.
[47]  Clutton-Brock TJ (1991) The evolution of parental care. Princeton: Princeton University Press. 352 p.
[48]  Tallamy DW (2001) Evolution of exclusive paternal care in arthorpods. Ann Rev Entomol 46: 139–165.
[49]  Hurst LD, McVean GT (1998) Do we understand the evolution of genomic imprinting? Cur Opin Gen Dev 8: 701–708.
[50]  Vrana PB, Guan XJ, Ingram RS, Tilghman SM (1998) Genomic imprinting is disrupted in interspecific Peromyscus hybrids. Nat Genet 20: 362–365.
[51]  Hartl DL (2000) A primer of population genetics, 3rd ed. Sunderland (Massachussets): Sinauer. 221 p.
[52]  Crow JF, Kimura M (1970) An introduction to population genetics theory. New York: Harper & Row. 591 p.

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