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.

Messy biology and the origins of evolutionary innovations

Nature Chemical Biology volume 6, pages 692–696 (2010)Cite this article

Biological messiness relates to infidelity, heterogeneity, stochastic noise and variation—both genetic and phenotypic—at all levels, from single proteins to organisms. Messiness comes from the complexity and evolutionary history of biological systems and from the high cost of accuracy. For better or for worse, messiness is inherent to biology. It also provides the raw material for physiological and evolutionary adaptations to new challenges.

Explaining why something happens in a given way and not in any other way is an intellectual tendency that dominates human thought in general and the biological sciences in particular. In this vein, biological systems, be they individual proteins or whole organisms, are studied with the aim of showing how their structure, function and evolution are purposely directed and optimally designed. However, although the hallmarks of optimal functionality can be seen throughout biology, there are also clear-cut indications that biology is messy and, at times, even sloppy. In other words, the accuracy and fidelity of biological systems are limited.

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

Relevant articles

Open Access articles citing this article.

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Learn more

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

Figure 1: The correlation of phenotypic and genetic variances and the origins of evolutionary innovations.
Figure 2: Promiscuous enzyme functions (protein messiness) mediate physiological and evolutionary adaptations in the arginine and proline biosynthetic pathways.

References

  1. Lynch, M. Nat. Rev. Genet. 8, 803–813 (2007).

    Article  CAS  Google Scholar 

  2. Elowitz, M.B., Levine, A.J., Siggia, E.D. & Swain, P.S. Science 297, 1183–1186 (2002).

    Article  CAS  Google Scholar 

  3. Willensdorfer, M., Burger, R. & Nowak, M.A. PLOS Comput. Biol. 3, e203 (2007).

    Article  Google Scholar 

  4. Meyerovich, M., Mamou, G. & Ben-Yehuda, S. Proc. Natl. Acad. Sci. USA 107, 11543–11548.

  5. Wang, D. & Bodovitz, S. Trends Biotechnol. 28, 281–290 (2010).

    Article  CAS  Google Scholar 

  6. Avery, S.V. Nat. Rev. Microbiol. 4, 577–587 (2006).

    Article  CAS  Google Scholar 

  7. Stern, S., Dror, T., Stolovicki, E., Brenner, N. & Braun, E. Mol. Syst. Biol. 3, 106 (2007).

    Article  Google Scholar 

  8. Cohen, A.A. et al. Science 322, 1511–1516 (2008).

    Article  CAS  Google Scholar 

  9. Kilfoil, M.L., Lasko, P. & Abouheif, E. HFSP J. 3, 379–385 (2009).

    Article  CAS  Google Scholar 

  10. Raj, A. & van Oudenaarden, A. Cell 135, 216–226 (2008).

    Article  CAS  Google Scholar 

  11. Robert, L. et al. Mol. Syst. Biol. 6, 357–368 (2010).

    Article  Google Scholar 

  12. Rotem, E. et al. Proc. Natl. Acad. Sci. USA 107, 12541–12546.

  13. Lehner, B. PLoS ONE 5, e9035 (2010).

    Article  Google Scholar 

  14. Milo, R., Hou, J.H., Springer, M., Brenner, M.P. & Kirschner, M.W. Proc. Natl. Acad. Sci. USA 104, 16998–17003 (2007).

    Article  CAS  Google Scholar 

  15. Landry, C.R., Lemos, B., Rifkin, S.A., Dickinson, W.J. & Hartl, D.L. Science 317, 118–121 (2007).

    Article  CAS  Google Scholar 

  16. Tirosh, I., Weinberger, A., Carmi, M. & Barkai, N. Nat. Genet. 38, 830–834 (2006).

    Article  CAS  Google Scholar 

  17. Kaneko, K. & Furusawa, C. J. Theor. Biol. 240, 78–86 (2006).

    Article  Google Scholar 

  18. Khersonsky, O. & Tawfik, D.S. Annu. Rev. Biochem. 79, 471–505 (2010).

    Article  CAS  Google Scholar 

  19. Amitai, G., Gupta, R.D. & Tawfik, D.S. HFSP J. 1, 67–78 (2007).

    Article  CAS  Google Scholar 

  20. D'Ari, R. & Casadesus, J. Bioessays 20, 181–186 (1998).

    Article  CAS  Google Scholar 

  21. McLoughlin, S.Y. & Copley, S.D. Proc. Natl. Acad. Sci. USA 105, 13497–13502 (2008).

    Article  CAS  Google Scholar 

  22. Masel, J. & Trotter, M.V. Trends Genet. 26, 406–414 (2010).

    Article  CAS  Google Scholar 

  23. Lehner, B. Mol. Syst. Biol. 4, 170–175 (2008).

    Article  Google Scholar 

  24. Kovács, K., Hurst, L.D. & Papp, B. PLoS Biol. 7, e1000115 (2009).

    Article  Google Scholar 

  25. Galhardo, R.S., Hastings, P.J. & Rosenberg, S.M. Crit. Rev. Biochem. Mol. Biol. 42, 399–435 (2007).

    Article  CAS  Google Scholar 

  26. Masel, J. & Bergman, A. Evolution 57, 1498–1512 (2003).

    Article  Google Scholar 

  27. Fraser, D. & Kaern, M. Mol. Microbiol. 71, 1333–1340 (2009).

    Article  CAS  Google Scholar 

  28. Radman, M., Matic, I. & Taddei, F. Ann. NY Acad. Sci. 870, 146–155 (1999).

    Article  CAS  Google Scholar 

  29. Vignuzzi, M., Stone, J.K., Arnold, J.J., Cameron, C.E. & Andino, R. Nature 439, 344–348 (2006).

    Article  CAS  Google Scholar 

  30. Zhang, Z. & Zhang, J. PLoS ONE 4, e5686 (2009).

    Article  Google Scholar 

  31. Greenspan, R.J. Nat. Rev. Genet. 2, 383–387 (2001).

    Article  CAS  Google Scholar 

  32. Gould, S.J. The Panda's Thumb: More Reflections in Natural History (W. W. Norton & Company, 1980).

    Google Scholar 

  33. Jacob, F. Science 196, 1161–1166 (1977).

    Article  CAS  Google Scholar 

  34. Austin, M.B., O'Maille, P.E. & Noel, J.P. Nat. Chem. Biol. 4, 217–222 (2008).

    Article  CAS  Google Scholar 

  35. Goldsmith, M. & Tawfik, D.S. Proc. Natl. Acad. Sci. USA 106, 6197–6202 (2009).

    Article  CAS  Google Scholar 

  36. Süel, G.M., Kulkarni, R.P., Dworkin, J., Garcia-Ojalvo, J. & Elowitz, M.B. Science 315, 1716–1719 (2007).

    Article  Google Scholar 

Download references

Acknowledgements

The author is grateful to J. Noel for inspirational discussions and for a comment he made in the opening of his seminar at the Weizmann Institute—“Biology is messy”—used in this article. He is also grateful to R. Milo, E. Braun, N. Balaban, B. Lehner and S. Stern for insightful and enjoyable discussions and valuable comments. Financial support from the Israel Science Foundation and the Sasson and Marjorie Peress Foundation are gratefully acknowledged. The author is the Nella and Leon Benoziyo Professor of Biochemistry.

Author information

Authors and Affiliations

  1. Dan S. Tawfik is in the Department of Biological Chemistry, Weizmann Institute of Science, Rehovot, Israel.,

    Dan S Tawfik

Authors
  1. Dan S Tawfik
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Dan S Tawfik.

Ethics declarations

Competing interests

The author declares no competing financial interests.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Tawfik, D. Messy biology and the origins of evolutionary innovations. Nat Chem Biol 6, 692–696 (2010). https://doi.org/10.1038/nchembio.441

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nchembio.441

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