Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Perspective
  • Published:

An adaptive radiation model for the origin of new gene functions

Nature Genetics volume 37, pages 573–578 (2005)Cite this article

A Corrigendum to this article was published on 01 August 2005

Abstract

Current models for the evolution of new gene functions after gene duplication presume that the duplication events themselves have no effect on fitness. But those duplications that result in new gene functions are likely to be positively selected from their inception. The evolution of new function may start with the amplification of an existing gene with some level of preadaptation for that function, followed by a period of competitive evolution among the gene copies, resulting in the preservation of the most effective variant and the 'pseudogenization' and eventual loss of the rest.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Hypothetical course of events illustrating the adaptive radiation model for the evolution of new gene functions.

Similar content being viewed by others

References

  1. Ohno, S. Evolution by Gene Duplication (Springer, Heidelberg, Germany, 1970).

    Book  Google Scholar 

  2. Force, A. et al. Preservation of duplicate genes by complementary degenerative mutations. Genetics 151, 1531–1545 (1999).

    CAS  PubMed Central  PubMed  Google Scholar 

  3. Hendrickson, H., Slechta, E.S., Bergthorsson, U., Andersson, D.I. & Roth, J.R. Amplification–mutagenesis: Evidence that 'directed' adaptive mutation and general hypermutability result from growth with a selected gene amplification. Proc. Natl. Acad. Sci. 99, 2164–2169 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Kondrashov, F.A., Rogozin, I.B., Wolf, Y.I. & Koonin, E.V. Selection in the evolution of gene duplications. Genome Biol. 3, RESEARCH0008 (2002).

    Article  PubMed  PubMed Central  Google Scholar 

  5. Hooper, S.D. & Berg, O.G. On the nature of gene innovation: duplication patterns in microbial genomes. Mol. Biol. Evol. 20, 945–954 (2003).

    Article  CAS  PubMed  Google Scholar 

  6. Roth, J.R. & Andersson, D.I. Adaptive mutation: how growth under selection stimulates Lac(+) reversion by increasing target copy number. J. Bacteriol. 186, 4855–4860 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Cairns, J. & Foster, P.L. Adaptive radiation of a frameshift mutation in Escherichia coli. Genetics 128, 695–701 (1991).

    CAS  PubMed Central  PubMed  Google Scholar 

  8. Romero, D. & Palacios, R. Gene amplification and genomic plasticity in prokaryotes. Annu. Rev. Genet. 31, 91–111 (1997).

    Article  CAS  PubMed  Google Scholar 

  9. Riehle, M.M., Bennett, A.F. & Long, A.D. Genetic architecture of thermal adaptation in Escherichia coli. Proc. Natl. Acad. Sci. USA 98, 525–530 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Zhong, S., Khodursky, A., Dykhuizen, D.E. & Dean, A.M. Evolutionary genomics of ecological specialization. Proc. Natl. Acad. Sci. USA 101, 11719–11724 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Reams, A.B. & Neidle, E.L. Genome plasticity in Acinetobacter: new degradative capabilities acquired by the spontaneous amplification of large chromosomal segments. Mol. Microbiol. 47, 1291–1304 (2003).

    Article  CAS  PubMed  Google Scholar 

  12. Dunham, M.J. et al. Characteristic genome rearrangements in experimental evolution of Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 99, 16144–16149 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Guillemaud, T. et al. Quantitative variation and selection of esterase gene amplification in Culex pipiens. Heredity 83, 87–99 (1999).

    Article  CAS  PubMed  Google Scholar 

  14. Kim, S.J. & Lee, G.M. Cytogenetic analysis of chimeric antibody-producing CHO cells in the course of dihydrofolate reductase-mediated gene amplification and their stability in the absence of selective pressure. Biotechnol. Bioeng. 64, 741–749 (1999).

    Article  CAS  PubMed  Google Scholar 

  15. Roth, J.R. & Andersson, D.I. Amplification-mutagenesis--how growth under selection contributes to the origin of genetic diversity and explains the phenomenon of adaptive mutation. Res. Microbiol. 155, 342–351 (2004).

    Article  CAS  PubMed  Google Scholar 

  16. Hall, B.G. The EBG system of E. coli: origin and evolution of a novel beta-galactosidase for the metabolism of lactose. Genetica 118, 143–156 (2003).

    Article  CAS  PubMed  Google Scholar 

  17. Aharoni, A. et al. The 'evolvability' of promiscuous protein functions. Nat. Genet. 37, 73–76 (2005).

    Article  CAS  PubMed  Google Scholar 

  18. Gevers, D., Vandepoele, K., Simillion, C. & Van de Peer, Y. Gene duplication and biased functional retention of paralogs in bacterial genomes. Trends Microbiol. 12, 148–154 (2004).

    Article  CAS  PubMed  Google Scholar 

  19. Hooper, S.D. & Berg, O.G. Duplication is more common among laterally transferred genes than among indigenous genes. Genome Biol. 4, R48 (2003).

    Article  Google Scholar 

  20. Dujon, B. et al. Genome evolution in yeasts. Nature 430, 35–44 (2004).

    Article  PubMed  Google Scholar 

  21. Lespinet, O., Wolf, Y.I., Koonin, E.V. & Aravind, L. The role of lineage-specific gene family expansion in the evolution of eukaryotes. Genome Res. 12, 1048–1059 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Jordan, I.K., Makarova, K.S., Spouge, J.L., Wolf, Y.I. & Koonin, E.V. Lineage-specific gene expansions in bacterial and archaeal genomes. Genome Res. 11, 555–565 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Fortna, A. et al. Lineage-Specific Gene Duplication and Loss in Human and Great Ape Evolution. PLOS Biol. 2, 0937–0954 (2004).

    Article  CAS  Google Scholar 

  24. Trask, B.J. et al. Large multi-chromosomal duplications encompass many members of the olfactory receptor gene family in the human genome. Hum. Mol. Genet. 7, 2007–2020 (1998).

    Article  CAS  PubMed  Google Scholar 

  25. Mefford, H.C. et al. Comparative sequencing of a multicopy subtelomeric region containing olfactory receptor genes reveals multiple interactions between non-homologous chromosomes. Hum. Mol. Genet. 10, 2363–2372 (2001).

    Article  CAS  PubMed  Google Scholar 

  26. Sebat, J. et al. Large-scale copy number polymorphism in the human genome. Science 305, 525–528 (2004).

    Article  CAS  PubMed  Google Scholar 

  27. Huynen, M.A. & van Nimwegen, E. The frequency distribution of gene family sizes in complete genomes. Mol. Biol. Evol. 15, 583–589 (1998).

    Article  CAS  PubMed  Google Scholar 

  28. Harrison, P.M. & Gerstein, M. Studying genomes through the aeons: protein families, pseudogenes and proteome evolution. J. Mol. Biol. 318, 1155–1174 (2002).

    Article  CAS  PubMed  Google Scholar 

  29. Qian, J., Luscombe, N.M. & Gerstein, M. Protein family and fold occurrence in genomes: power-law behaviour and evolutionary model. J. Mol. Biol. 313, 673–681 (2001).

    Article  CAS  PubMed  Google Scholar 

  30. Karev, G.P., Wolf, Y.I. & Koonin, E.V. Simple stochastic birth and death models of genome evolution: was there enough time for us to evolve? Bioinformatics 19, 1889–1900 (2003).

    Article  CAS  PubMed  Google Scholar 

  31. Karev, G.P., Wolf, Y.I., Rzhetsky, A.Y., Berezovskaya, F.S. & Koonin, E.V. Birth and death of protein domains: A simple model of evolution explains power law behavior. BMC Evol. Biol. 2, 18 (2002).

    Article  PubMed  PubMed Central  Google Scholar 

  32. Lynch, M. & Conery, J.S. The evolutionary fate and consequences of duplicate genes. Science 290, 1151–1155 (2000).

    Article  CAS  PubMed  Google Scholar 

  33. Hughes, A.L. The evolution of functionally novel proteins after gene duplication. Proc. R. Soc. Lond. B Biol. Sci. 256, 119–124 (1994).

    Article  CAS  Google Scholar 

  34. Wagner, A. Selection and gene duplication: a view from the genome. Genome Biol. 3, 1012.1–1012.3 (2002).

    Article  Google Scholar 

  35. Hughes, A.L. Evolutionary diversification of the mammalian defensins. Cell Mol. Life Sci. 56, 94–103 (1999).

    Article  CAS  PubMed  Google Scholar 

  36. Gilad, Y., Bustamante, C.D., Lancet, D. & Paabo, S. Natural selection on the olfactory receptor gene family in humans and chimpanzees. Am. J. Hum. Genet. 73, 489–501 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Gilad, Y. et al. Dichotomy of single-nucleotide polymorphism haplotypes in olfactory receptor genes and pseudogenes. Nat. Genet. 26, 221–224 (2000).

    Article  CAS  PubMed  Google Scholar 

  38. Johnson, M.E. et al. Positive selection of a gene family during the emergence of humans and African apes. Nature 413, 514–519 (2001).

    Article  CAS  PubMed  Google Scholar 

  39. Zhang, J., Rosenberg, H.F. & Nei, M. Positive Darwinian selection after gene duplication in primate ribonuclease genes. Proc. Natl. Acad. Sci. USA 95, 3708–3713 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Holloway, A.K. & Begun, D.J. Molecular evolution and population genetics of duplicated accessory gland protein genes in Drosophila. Mol. Biol. Evol. 21, 1625–1628 (2004).

    Article  CAS  PubMed  Google Scholar 

  41. Moore, R.C. & Purugganan, M.D. The early stages of duplicate gene evolution. Proc. Natl. Acad. Sci. USA 100, 15682–15687 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Newman, T. & Trask, B.J. Complex Evolution of 7E Olfactory Receptor Genes in Segmental Duplications. Genome Res. 13, 781–793 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Liu, Y., Harrison, P.M., Kunin, V. & Gerstein, M. Comprehensive analysis of pseudogenes in prokaryotes: widespread gene decay and failure of putative horizontally transferred genes. Genome Biol. 5, R64 (2004).

    Article  PubMed  PubMed Central  Google Scholar 

  44. Mira, A., Ochman, H. & Moran, N.A. Deletional bias and the evolution of bacterial genomes. Trends Genet. 17, 589–596 (2001).

    Article  CAS  PubMed  Google Scholar 

  45. Young, J.M. & Trask, B.J. The sense of smell: genomics of vertebrate odorant receptors. Hum. Mol. Genet. 11, 1153–1160 (2002).

    Article  CAS  PubMed  Google Scholar 

  46. Gilad, Y. & Lancet, D. Population differences in the human functional olfactory repertoire. Mol. Biol. Evol. 20, 307–314 (2003).

    Article  CAS  PubMed  Google Scholar 

  47. Clark, A.G. Inferring nonneutral evolution from human-chimp-mouse orthologous gene trios. Science 302, 1960–1963 (2003).

    Article  CAS  PubMed  Google Scholar 

  48. Schluter, D. The Ecology of Adaptive Radiation (Oxford University Press, Oxford, UK, 2000).

    Google Scholar 

  49. Simpson, G. Tempo and Mode in Evolution (Columbia University Press, New York, 1944).

    Google Scholar 

  50. Eldredge, N. & Gould, S.J. Punctuated equilibria: an alternative to phyletic gradualism. in Models in Paleobiology (ed. Schopf, T.) 82–115 (Freeman, Cooper & Co., San Francisco, California, 1972).

    Google Scholar 

  51. Stanley, S. Macroevolution: Pattern and Process (W. H. Freeman, San Francisco, California, 1979).

    Google Scholar 

  52. Simpson, G. The Major Features of Evolution (Columbia University Press, New York, 1953).

    Google Scholar 

  53. Lande, R. Natural selection and random genetic drift in phenotypic evolution. Evolution 30, 314–334 (1976).

    Article  PubMed  Google Scholar 

  54. Gingerich, P.D. Rates of evolution: effects of time and temporal scaling. Science 222, 159–161 (1983).

    Article  CAS  PubMed  Google Scholar 

  55. Lynch, M. The rate of morphological evolution in mammals from the standpoint of the neutral expectation. Am. Nat. 136, 727–741 (1990).

    Article  Google Scholar 

  56. Turelli, M., Gillespie, J.H. & Lande, R. Rate tests for selection on quantitative characters during macroevolution and microevolution. Evolution 42, 1085–1089 (1988).

    Article  PubMed  Google Scholar 

  57. Chan, K.M. & Moore, B.R. Whole-tree methods for detecting differential diversification rates. Syst. Biol. 51, 855–865 (2002).

    Article  PubMed  Google Scholar 

  58. Wagner, P.J. Contrasting the underlying patterns of active trends in morphologic evolution. Evolution 50, 990–1007 (1996).

    Article  PubMed  Google Scholar 

  59. Jablonski, D. Body size and macroevolution. in Evolutionary Paleobiology (eds. Jablonski, D., Erwin, D.H. & Lipps, J.H.) 256–289 (University of Chicago Press, Chicago, Illinois, 1996).

    Google Scholar 

Download references

Acknowledgements

Early discussions on the parallels between gene and organismal evolution with M. Medina prompted the development of this model. This manuscript was improved by comments from H. Ochman, U. Bergthorsson, R. Baker, J. Morgan, G. Moreno-Hagelsieb and E. Branscomb. The figure was designed with input from M. Posada-Buitrago, Y. Vallès, P. Dehal and E. Alm. I thank F. Kondrashov for constructive review of the manuscript. I also thank the US Department of Energy, Office of Biological and Environmental Research, and the Joint Genome Institute, Department of Evolutionary Genomics, for support during the writing of this paper.

Author information

Authors and Affiliations

  1. the Evolutionary Genomics Department, DOE Joint Genome Institute and Genomics Division, Lawrence Berkeley National Laboratory, 2800 Mitchell Dr, Walnut Creek, California, USA

    M Pilar Francino

Authors
  1. M Pilar Francino
    View author publications

    You can also search for this author in PubMed Google Scholar

Ethics declarations

Competing interests

The author declares no competing financial interests.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Francino, M. An adaptive radiation model for the origin of new gene functions. Nat Genet 37, 573–578 (2005). https://doi.org/10.1038/ng1579

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/ng1579

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing