The effect of functional compensation among duplicate genes can constrain their evolutionary divergence.

Joseph Esfandiar Hannon Bozorgmehr
Author Information
  1. Joseph Esfandiar Hannon Bozorgmehr: bozorgmehr@tiscali.co.uk

Abstract

Gene duplicates have the inherent property of initially being functionally redundant. This means that they can compensate for the effect of deleterious variation occurring at one or more sister sites. Here, I present data bearing on evolutionary theory that illustrates the manner in which any functional adaptation in duplicate genes is markedly constrained because of the compensatory utility provided by a sustained genetic redundancy. Specifically, a two-locus epistatic model of paralogous genes was simulated to investigate the degree of purifying selection imposed, and whether this would serve to impede any possible biochemical innovation. Three population sizes were considered to see if, as expected, there was a significant difference in any selection for robustness. Interestingly, physical linkage between tandem duplicates was actually found to increase the probability of any neofunctionalization and the efficacy of selection, contrary to what is expected in the case of singleton genes. The results indicate that an evolutionary trade-off often exists between any functional change under either positive or relaxed selection and the need to compensate for failures due to degenerative mutations, thereby guaranteeing the reliability of protein production.

References

  1. Proc Natl Acad Sci U S A. 1994 Apr 12;91(8):2950-4 [PMID: 8159686]
  2. Heredity (Edinb). 2008 Jan;100(1):19-31 [PMID: 17878920]
  3. J Biochem. 2005 Feb;137(2):177-87 [PMID: 15749832]
  4. Genome Biol Evol. 2009 Oct 29;1:409-14 [PMID: 20333209]
  5. Nat Genet. 2005 Jan;37(1):73-6 [PMID: 15568024]
  6. PLoS Biol. 2006 Dec;4(12):e428 [PMID: 17238277]
  7. Heredity (Edinb). 2009 Feb;102(2):99-100 [PMID: 18971957]
  8. Mol Biol Evol. 2005 Jun;22(6):1365-74 [PMID: 15758206]
  9. Pac Symp Biocomput. 2000;:69-80 [PMID: 10902157]
  10. Genome Biol. 2007;8(5):213 [PMID: 17521457]
  11. Genome Res. 2008 Mar;18(3):449-61 [PMID: 18230802]
  12. BMC Evol Biol. 2008 Feb 08;8:43 [PMID: 18261230]
  13. Nature. 2003 Jan 2;421(6918):63-6 [PMID: 12511954]
  14. Proc Biol Sci. 2004 Jan 7;271(1534):89-96 [PMID: 15002776]
  15. Genetics. 2007 Feb;175(2):933-43 [PMID: 17151249]
  16. Science. 2000 Nov 10;290(5494):1151-5 [PMID: 11073452]
  17. BMC Evol Biol. 2004 Jul 06;4:22 [PMID: 15238160]
  18. Trends Genet. 2008 Oct;24(10):485-8 [PMID: 18786741]
  19. Genetics. 2001 Dec;159(4):1789-804 [PMID: 11779815]
  20. Genetics. 1962 Jun;47:713-9 [PMID: 14456043]
  21. Proc Natl Acad Sci U S A. 2006 Aug 1;103(31):11653-8 [PMID: 16861297]
  22. PLoS Genet. 2010 Nov 04;6(11):e1001187 [PMID: 21079672]
  23. J R Soc Interface. 2008 Nov 6;5(28):1279-89 [PMID: 18664425]
  24. J Biol Chem. 2005 Nov 25;280(47):39644-52 [PMID: 16162506]
  25. PLoS Comput Biol. 2006 Sep 29;2(9):e133 [PMID: 17009864]
  26. J Mol Evol. 2010 Oct;71(4):241-9 [PMID: 20809353]
  27. Nature. 2000 Feb 10;403(6770):661-5 [PMID: 10688203]
  28. Trends Genet. 2009 Oct;25(10):441-2 [PMID: 19783063]
  29. Genome Biol. 2002;3(5):reviews1012 [PMID: 12049669]
  30. IUBMB Life. 2006 Dec;58(12):677-85 [PMID: 17424906]
  31. Nat Genet. 2004 May;36(5):492-6 [PMID: 15107850]
  32. Mol Biol Evol. 2006 May;23(5):927-40 [PMID: 16407460]
  33. Trends Genet. 2001 May;17(5):237-9 [PMID: 11335019]
  34. Chromosome Res. 2009;17(5):699-717 [PMID: 19802709]
  35. PLoS Genet. 2008 Mar 14;4(3):e1000014 [PMID: 18369440]
  36. J Exp Zool B Mol Dev Evol. 2007 Jan 15;308(1):58-73 [PMID: 16838295]
  37. BMC Genomics. 2008 Dec 16;9:609 [PMID: 19087332]
  38. Comp Biochem Physiol B Biochem Mol Biol. 1995 Sep;112(1):1-13 [PMID: 7584839]
  39. Gene. 2000 Dec 23;259(1-2):45-52 [PMID: 11163960]
  40. Biosystems. 2011 Sep;105(3):210-5 [PMID: 21550380]
  41. PLoS Genet. 2008 Jul 04;4(7):e1000113 [PMID: 18604285]
  42. Genetics. 2006 Feb;172(2):1363-7 [PMID: 16322517]
  43. Curr Biol. 2003 Mar 18;13(6):R229-30 [PMID: 12646148]
  44. Nucleic Acids Res. 1994 Mar 25;22(6):1006-11 [PMID: 8152905]

MeSH Term

Evolution, Molecular
Genes, Duplicate
Genetic Variation
Genotype
Models, Genetic
Selection, Genetic
Terminology as Topic

Word Cloud

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