• We are sorry, but NCBI web applications do not support your browser and may not function properly. More information
Logo of geneticsGeneticsCurrent IssueInformation for AuthorsEditorial BoardSubscribeSubmit a Manuscript
Genetics. Jan 2000; 154(1): 459–473.
PMCID: PMC1460895

The probability of duplicate gene preservation by subfunctionalization.

Abstract

It has often been argued that gene-duplication events are most commonly followed by a mutational event that silences one member of the pair, while on rare occasions both members of the pair are preserved as one acquires a mutation with a beneficial function and the other retains the original function. However, empirical evidence from genome duplication events suggests that gene duplicates are preserved in genomes far more commonly and for periods far in excess of the expectations under this model, and whereas some gene duplicates clearly evolve new functions, there is little evidence that this is the most common mechanism of duplicate-gene preservation. An alternative hypothesis is that gene duplicates are frequently preserved by subfunctionalization, whereby both members of a pair experience degenerative mutations that reduce their joint levels and patterns of activity to that of the single ancestral gene. We consider the ways in which the probability of duplicate-gene preservation by such complementary mutations is modified by aspects of gene structure, degree of linkage, mutation rates and effects, and population size. Even if most mutations cause complete loss-of-subfunction, the probability of duplicate-gene preservation can be appreciable if the long-term effective population size is on the order of 10(5) or smaller, especially if there are more than two independently mutable subfunctions per locus. Even a moderate incidence of partial loss-of-function mutations greatly elevates the probability of preservation. The model proposed herein leads to quantitative predictions that are consistent with observations on the frequency of long-term duplicate gene preservation and with observations that indicate that a common fate of the members of duplicate-gene pairs is the partitioning of tissue-specific patterns of expression of the ancestral gene.

Full Text

The Full Text of this article is available as a PDF (191K).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Graf JD, Kobel HR. Genetics of Xenopus laevis. Methods Cell Biol. 1991;36:19–34. [PubMed]
  • Henikoff S, Greene EA, Pietrokovski S, Bork P, Attwood TK, Hood L. Gene families: the taxonomy of protein paralogs and chimeras. Science. 1997 Oct 24;278(5338):609–614. [PubMed]
  • Hill WG, Robertson A. The effect of linkage on limits to artificial selection. Genet Res. 1966 Dec;8(3):269–294. [PubMed]
  • Huang JD, Schwyter DH, Shirokawa JM, Courey AJ. The interplay between multiple enhancer and silencer elements defines the pattern of decapentaplegic expression. Genes Dev. 1993 Apr;7(4):694–704. [PubMed]
  • Hughes MK, Hughes AL. Evolution of duplicate genes in a tetraploid animal, Xenopus laevis. Mol Biol Evol. 1993 Nov;10(6):1360–1369. [PubMed]
  • Jack J, DeLotto Y. Structure and regulation of a complex locus: the cut gene of Drosophila. Genetics. 1995 Apr;139(4):1689–1700. [PMC free article] [PubMed]
  • Kammandel B, Chowdhury K, Stoykova A, Aparicio S, Brenner S, Gruss P. Distinct cis-essential modules direct the time-space pattern of the Pax6 gene activity. Dev Biol. 1999 Jan 1;205(1):79–97. [PubMed]
  • Kimura M, King JL. Fixation of a deleterious allele at one of two "duplicate" loci by mutation pressure and random drift. Proc Natl Acad Sci U S A. 1979 Jun;76(6):2858–2861. [PMC free article] [PubMed]
  • Kimura M, Ohta T. The Average Number of Generations until Fixation of a Mutant Gene in a Finite Population. Genetics. 1969 Mar;61(3):763–771. [PMC free article] [PubMed]
  • Kirchhamer CV, Yuh CH, Davidson EH. Modular cis-regulatory organization of developmentally expressed genes: two genes transcribed territorially in the sea urchin embryo, and additional examples. Proc Natl Acad Sci U S A. 1996 Sep 3;93(18):9322–9328. [PMC free article] [PubMed]
  • Amores A, Force A, Yan YL, Joly L, Amemiya C, Fritz A, Ho RK, Langeland J, Prince V, Wang YL, et al. Zebrafish hox clusters and vertebrate genome evolution. Science. 1998 Nov 27;282(5394):1711–1714. [PubMed]
  • Arnone MI, Davidson EH. The hardwiring of development: organization and function of genomic regulatory systems. Development. 1997 May;124(10):1851–1864. [PubMed]
  • Bailey GS, Poulter RT, Stockwell PA. Gene duplication in tetraploid fish: model for gene silencing at unlinked duplicated loci. Proc Natl Acad Sci U S A. 1978 Nov;75(11):5575–5579. [PMC free article] [PubMed]
  • Nadeau JH, Sankoff D. Comparable rates of gene loss and functional divergence after genome duplications early in vertebrate evolution. Genetics. 1997 Nov;147(3):1259–1266. [PMC free article] [PubMed]
  • Birky CW, Jr, Walsh JB. Effects of linkage on rates of molecular evolution. Proc Natl Acad Sci U S A. 1988 Sep;85(17):6414–6418. [PMC free article] [PubMed]
  • Brookfield JF. Genetic redundancy. Adv Genet. 1997;36:137–155. [PubMed]
  • Nornes S, Clarkson M, Mikkola I, Pedersen M, Bardsley A, Martinez JP, Krauss S, Johansen T. Zebrafish contains two pax6 genes involved in eye development. Mech Dev. 1998 Oct;77(2):185–196. [PubMed]
  • Nowak MA, Boerlijst MC, Cooke J, Smith JM. Evolution of genetic redundancy. Nature. 1997 Jul 10;388(6638):167–171. [PubMed]
  • Clark AG, Wang L, Hulleberg T. Spontaneous mutation rate of modifiers of metabolism in Drosophila. Genetics. 1995 Feb;139(2):767–779. [PMC free article] [PubMed]
  • Ohta T. Simulating evolution by gene duplication. Genetics. 1987 Jan;115(1):207–213. [PMC free article] [PubMed]
  • DiLeone RJ, Russell LB, Kingsley DM. An extensive 3' regulatory region controls expression of Bmp5 in specific anatomical structures of the mouse embryo. Genetics. 1998 Jan;148(1):401–408. [PMC free article] [PubMed]
  • Postlethwait JH, Yan YL, Gates MA, Horne S, Amores A, Brownlie A, Donovan A, Egan ES, Force A, Gong Z, et al. Vertebrate genome evolution and the zebrafish gene map. Nat Genet. 1998 Apr;18(4):345–349. [PubMed]
  • Donnelly P, Tavaré S. Coalescents and genealogical structure under neutrality. Annu Rev Genet. 1995;29:401–421. [PubMed]
  • Ramos-Onsins S, Aguadé M. Molecular evolution of the Cecropin multigene family in Drosophila. functional genes vs. pseudogenes. Genetics. 1998 Sep;150(1):157–171. [PMC free article] [PubMed]
  • Sidow A. Gen(om)e duplications in the evolution of early vertebrates. Curr Opin Genet Dev. 1996 Dec;6(6):715–722. [PubMed]
  • Slusarski DC, Motzny CK, Holmgren R. Mutations that alter the timing and pattern of cubitus interruptus gene expression in Drosophila melanogaster. Genetics. 1995 Jan;139(1):229–240. [PMC free article] [PubMed]
  • Stoltzfus A. On the possibility of constructive neutral evolution. J Mol Evol. 1999 Aug;49(2):169–181. [PubMed]
  • Takahata N, Maruyama T. Polymorphism and loss of duplicate gene expression: a theoretical study with application of tetraploid fish. Proc Natl Acad Sci U S A. 1979 Sep;76(9):4521–4525. [PMC free article] [PubMed]
  • Watterson GA. On the time for gene silencing at duplicate Loci. Genetics. 1983 Nov;105(3):745–766. [PMC free article] [PubMed]
  • Xu PX, Zhang X, Heaney S, Yoon A, Michelson AM, Maas RL. Regulation of Pax6 expression is conserved between mice and flies. Development. 1999 Jan;126(2):383–395. [PubMed]

Articles from Genetics are provided here courtesy of Genetics Society of America

Formats:

Related citations in PubMed

See reviews...See all...

Cited by other articles in PMC

See all...

Links

  • PubMed
    PubMed
    PubMed citations for these articles

Recent Activity

Your browsing activity is empty.

Activity recording is turned off.

Turn recording back on

See more...