Skip to main content
NCBI home page
Proceedings of the Royal Society B: Biological Sciences logoLink to Proceedings of the Royal Society B: Biological Sciences
. 1997 May 22;264(1382):739–746. doi: 10.1098/rspb.1997.0105

Molecular evolution of imprinted genes: no evidence for antagonistic coevolution.

G T McVean 1, L D Hurst 1
PMCID: PMC1688426  PMID: 9178545

Abstract

Genomically imprinted genes are those for which expression is dependent on the sex of the parent from which they are derived. Numerous theories have been proposed for the evolution of genomic imprinting: one theory is that it is an intra-individual manifestation of classical parent -offspring conflict. This theory is unique in predicting that an arms race may develop between maternally and paternally derived genes for the control of foetal growth demands. Such antagonistic coevolution may be mediated through changes in the structure of the proteins concerned. Comparable coevolution is the most likely explanation for the rapid changes seen in antigenic components of parasites and antigen recognition components of immune systems. We have examined the evolution of insulin-like growth factor Igf2, and its antagonistic receptor Igf2r) and find that in contrast to immune genes, at the sites of mutual binding they are highly conserved. In addition, we have analysed the rate of molecular evolution of seven imprinted genes including Igf2 and Igf2r), sequenced in both mouse and rat, and had that this is the same as that of nonimprinted receptors and significantly lower than that of immune genes controlling for differences in mutation rates. Contrary to the expectations of the conflict hypothesis, we hence find no evidence for antagonistic coevolution of imprinted genes mediated by changes in sequence.

Full Text

The Full Text of this article is available as a PDF (273.4 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Efstratiadis A. Parental imprinting of autosomal mammalian genes. Curr Opin Genet Dev. 1994 Apr;4(2):265–280. doi: 10.1016/s0959-437x(05)80054-1. [DOI] [PubMed] [Google Scholar]
  2. Endo T., Ikeo K., Gojobori T. Large-scale search for genes on which positive selection may operate. Mol Biol Evol. 1996 May;13(5):685–690. doi: 10.1093/oxfordjournals.molbev.a025629. [DOI] [PubMed] [Google Scholar]
  3. Guillemot F., Caspary T., Tilghman S. M., Copeland N. G., Gilbert D. J., Jenkins N. A., Anderson D. J., Joyner A. L., Rossant J., Nagy A. Genomic imprinting of Mash2, a mouse gene required for trophoblast development. Nat Genet. 1995 Mar;9(3):235–242. doi: 10.1038/ng0395-235. [DOI] [PubMed] [Google Scholar]
  4. 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]
  5. Haig D. Genetic conflicts in human pregnancy. Q Rev Biol. 1993 Dec;68(4):495–532. doi: 10.1086/418300. [DOI] [PubMed] [Google Scholar]
  6. 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]
  7. Haraguchi Y., Sasaki A. Host-parasite arms race in mutation modifications: indefinite escalation despite a heavy load? J Theor Biol. 1996 Nov 21;183(2):121–137. doi: 10.1006/jtbi.1996.9999. [DOI] [PubMed] [Google Scholar]
  8. Hashimoto R., Fujiwara H., Higashihashi N., Enjoh-Kimura T., Terasawa H., Fujita-Yamaguchi Y., Inagaki F., Perdue J. F., Sakano K. N-terminal deletion mutants of insulin-like growth factor-II (IGF-II) show Thr7 and Leu8 important for binding to insulin and IGF-I receptors and Leu8 critical for all IGF-II functions. J Biol Chem. 1995 Jul 28;270(30):18013–18018. doi: 10.1074/jbc.270.30.18013. [DOI] [PubMed] [Google Scholar]
  9. Hughes A. L. Circumsporozoite protein genes of malaria parasites (Plasmodium spp.): evidence for positive selection on immunogenic regions. Genetics. 1991 Feb;127(2):345–353. doi: 10.1093/genetics/127.2.345. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Hughes A. L. Evidence of positive selection at the Lyb-2 locus of the mouse. Immunogenetics. 1993;38(1):54–56. doi: 10.1007/BF00216391. [DOI] [PubMed] [Google Scholar]
  11. Hughes A. L., Nei M. Pattern of nucleotide substitution at major histocompatibility complex class I loci reveals overdominant selection. Nature. 1988 Sep 8;335(6186):167–170. doi: 10.1038/335167a0. [DOI] [PubMed] [Google Scholar]
  12. Hughes A. L., Ota T., Nei M. Positive Darwinian selection promotes charge profile diversity in the antigen-binding cleft of class I major-histocompatibility-complex molecules. Mol Biol Evol. 1990 Nov;7(6):515–524. doi: 10.1093/oxfordjournals.molbev.a040626. [DOI] [PubMed] [Google Scholar]
  13. Hurst L. D., Atlan A., Bengtsson B. O. Genetic conflicts. Q Rev Biol. 1996 Sep;71(3):317–364. doi: 10.1086/419442. [DOI] [PubMed] [Google Scholar]
  14. Hurst L. D. Embryonic growth and the evolution of the mammalian Y chromosome. II. Suppression of selfish Y-linked growth factors may explain escape from X-inactivation and rapid evolution of Sry. Heredity (Edinb) 1994 Sep;73(Pt 3):233–243. doi: 10.1038/hdy.1994.128. [DOI] [PubMed] [Google Scholar]
  15. Hurst L. D. Further evidence consistent with Stellate's involvement in meiotic drive. Genetics. 1996 Feb;142(2):641–643. doi: 10.1093/genetics/142.2.641. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Hurst L. D. Is Stellate a relict meiotic driver? Genetics. 1992 Jan;130(1):229–230. doi: 10.1093/genetics/130.1.229. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Hurst L. D., McVean G., Moore T. Imprinted genes have few and small introns. Nat Genet. 1996 Mar;12(3):234–237. doi: 10.1038/ng0396-234. [DOI] [PubMed] [Google Scholar]
  18. Kuma K., Iwabe N., Miyata T. Functional constraints against variations on molecules from the tissue level: slowly evolving brain-specific genes demonstrated by protein kinase and immunoglobulin supergene families. Mol Biol Evol. 1995 Jan;12(1):123–130. doi: 10.1093/oxfordjournals.molbev.a040181. [DOI] [PubMed] [Google Scholar]
  19. Li W. H., Wu C. I., Luo C. C. A new method for estimating synonymous and nonsynonymous rates of nucleotide substitution considering the relative likelihood of nucleotide and codon changes. Mol Biol Evol. 1985 Mar;2(2):150–174. doi: 10.1093/oxfordjournals.molbev.a040343. [DOI] [PubMed] [Google Scholar]
  20. Lyon M. F. Epigenetic inheritance in mammals. Trends Genet. 1993 Apr;9(4):123–128. doi: 10.1016/0168-9525(93)90206-w. [DOI] [PubMed] [Google Scholar]
  21. Maiti S., Doskow J., Sutton K., Nhim R. P., Lawlor D. A., Levan K., Lindsey J. S., Wilkinson M. F. The Pem homeobox gene: rapid evolution of the homeodomain, X chromosomal localization, and expression in reproductive tissue. Genomics. 1996 Jun 15;34(3):304–316. doi: 10.1006/geno.1996.0291. [DOI] [PubMed] [Google Scholar]
  22. McVean G. T., Hurst L. D., Moore T. Genomic evolution in mice and men: imprinted genes have little intronic content. Bioessays. 1996 Sep;18(9):773–775. doi: 10.1002/bies.950180913. [DOI] [PubMed] [Google Scholar]
  23. 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]
  24. 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]
  25. Palumbo G., Bonaccorsi S., Robbins L. G., Pimpinelli S. Genetic analysis of Stellate elements of Drosophila melanogaster. Genetics. 1994 Dec;138(4):1181–1197. doi: 10.1093/genetics/138.4.1181. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Ronni T., Matikainen S., Lehtonen A., Palvimo J., Dellis J., Van Eylen F., Goetschy J. F., Horisberger M., Content J., Julkunen I. The proximal interferon-stimulated response elements are essential for interferon responsiveness: a promoter analysis of the antiviral MxA gene. J Interferon Cytokine Res. 1998 Sep;18(9):773–781. doi: 10.1089/jir.1998.18.773. [DOI] [PubMed] [Google Scholar]
  27. Sakano K., Enjoh T., Numata F., Fujiwara H., Marumoto Y., Higashihashi N., Sato Y., Perdue J. F., Fujita-Yamaguchi Y. The design, expression, and characterization of human insulin-like growth factor II (IGF-II) mutants specific for either the IGF-II/cation-independent mannose 6-phosphate receptor or IGF-I receptor. J Biol Chem. 1991 Nov 5;266(31):20626–20635. [PubMed] [Google Scholar]
  28. Schmidt B., Kiecke-Siemsen C., Waheed A., Braulke T., von Figura K. Localization of the insulin-like growth factor II binding site to amino acids 1508-1566 in repeat 11 of the mannose 6-phosphate/insulin-like growth factor II receptor. J Biol Chem. 1995 Jun 23;270(25):14975–14982. doi: 10.1074/jbc.270.25.14975. [DOI] [PubMed] [Google Scholar]
  29. Szebenyi G., Rotwein P. The mouse insulin-like growth factor II/cation-independent mannose 6-phosphate (IGF-II/MPR) receptor gene: molecular cloning and genomic organization. Genomics. 1994 Jan 1;19(1):120–129. doi: 10.1006/geno.1994.1021. [DOI] [PubMed] [Google Scholar]
  30. Wallis M. Remarkably high rate of molecular evolution of ruminant placental lactogens. J Mol Evol. 1993 Jul;37(1):86–88. doi: 10.1007/BF00170466. [DOI] [PubMed] [Google Scholar]
  31. Wallis M. Variable evolutionary rates in the molecular evolution of mammalian growth hormones. J Mol Evol. 1994 Jun;38(6):619–627. doi: 10.1007/BF00175882. [DOI] [PubMed] [Google Scholar]
  32. Williamson C. M., Schofield J., Dutton E. R., Seymour A., Beechey C. V., Edwards Y. H., Peters J. Glomerular-specific imprinting of the mouse gsalpha gene: how does this relate to hormone resistance in albright hereditary osteodystrophy? Genomics. 1996 Sep 1;36(2):280–287. doi: 10.1006/geno.1996.0463. [DOI] [PubMed] [Google Scholar]
  33. Wolfe K. H., Sharp P. M. Mammalian gene evolution: nucleotide sequence divergence between mouse and rat. J Mol Evol. 1993 Oct;37(4):441–456. doi: 10.1007/BF00178874. [DOI] [PubMed] [Google Scholar]

Articles from Proceedings of the Royal Society B: Biological Sciences are provided here courtesy of The Royal Society

RESOURCES