Skip to main content

Thank you for visiting 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.

  • Letter
  • Published:

Pollinator shifts drive increasingly long nectar spurs in columbine flowers


Directional evolutionary trends have long garnered interest because they suggest that evolution can be predictable. However, the identification of the trends themselves and the underlying processes that may produce them have often been controversial1. In 1862, in explaining the exceptionally long nectar spur of Angraecum sesquipedale, Darwin proposed that a coevolutionary ‘race’ had driven the directional increase in length of a plant’s spur and its pollinator’s tongue2. Thus he predicted the existence of an exceptionally long-tongued moth. Though the discovery of Xanthopan morgani ssp. praedicta in 1903 with a tongue length of 22 cm validated Darwin’s prediction3, his ‘race’ model for the evolution of long-spurred flowers remains contentious4. Spurs may also evolve to exceptional lengths by way of pollinator shifts as plants adapt to a series of unrelated pollinators, each with a greater tongue length5. Here, using a species-level phylogeny of the columbine genus, Aquilegia, we show a significant evolutionary trend for increasing spur length during directional shifts to pollinators with longer tongues. In addition, we find evidence for ‘punctuated’ change in spur length during speciation events6, suggesting that Aquilegia nectar spurs rapidly evolve to fit adaptive peaks predefined by pollinator morphology. These findings show that evolution may proceed in predictable pathways without reversals and that change may be concentrated during speciation.

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

Access options

Buy this article

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

Figure 1: Two contrasting hypotheses for the evolution of exceptionally long nectar spurs.
Figure 2: Quantification of pollination syndromes and the distribution of spur lengths in Aquilegia.
Figure 3: Phylogenetic analysis of pollination syndrome evolution in Aquilegia.
Figure 4: Independent-contrasts regression analysis of pollination syndrome and spur-length evolution.

Similar content being viewed by others


  1. Gould, S. J. Cope’s rule as psychological artefact. Nature 385, 199–200 (1997)

    Article  ADS  CAS  Google Scholar 

  2. Darwin, C. The Various Contrivances by which Orchids are Fertilized by Insects (John Murray, London, 1862)

    Google Scholar 

  3. Rothschild, L. W. & Jordon, K. A revision of the lepidopterous family Sphingidae. Novit. Zool. 9, 1–972 (1903)

    Google Scholar 

  4. Nilsson, N. Deep flowers for long tongues. Trends Ecol. Evol. 13, 259–260 (1998)

    Article  Google Scholar 

  5. Wasserthal, L. T. The pollinators of the Malagasy star orchids Angraecum sesquipedale, A. sororium and A. compactum and the evolution of extremely long spurs by pollinator shift. Bot. Acta 110, 343–359 (1997)

    Article  Google Scholar 

  6. Lee, C., Blay, S., Mooers, A., Singh, A. & Oakley, T. H. . CoMET: A Mesquite package for comparing models of continuous character evolution on phylogenies. Evol. Bioinform. Online 2, 193–196 (2006); 〈〉.

    CAS  Google Scholar 

  7. Fulton, M. & Hodges, S. A. Floral isolation between Aquilegia formosa and Aquilegia pubescens. Proc. R. Soc. B 266, 2246–2252 (1999)

    Article  Google Scholar 

  8. Johnson, S. D. & Steiner, K. E. Long-tongued fly pollination and evolution of floral spur length in the Disa draconis complex (Orchidaceae). Evolution Int. J. Org. Evolution 51, 45–53 (1997)

    Article  CAS  Google Scholar 

  9. Wallace, A. R. Creation by law. Q. J. Sci. S140, 471–486 (1867)

    Google Scholar 

  10. Grant, V. & Temeles, E. J. Foraging ability of rufous hummingbirds on hummingbird flowers and hawkmoth flowers. Proc. Natl Acad. Sci. USA 89, 9400–9404 (1992)

    Article  ADS  CAS  Google Scholar 

  11. Hodges, S. A. The influence of nectar production on hawkmoth behavior, self-pollination and seed production in Mirabilis multiflora (Nyctaginaceae). Am. J. Bot. 82, 197–229 (1995)

    Article  Google Scholar 

  12. Grant, V. Pollination systems as isolating mechanisms in angiosperms. Evolution Int. J. Org. Evolution 3, 82–97 (1949)

    Article  CAS  Google Scholar 

  13. Hodges, S. A. & Arnold, M. Columbines: A geographically widespread species flock. Proc. Natl Acad. Sci. USA 91, 5129–5132 (1994)

    Article  ADS  CAS  Google Scholar 

  14. Hodges, S. A. & Arnold, M. Spurring plant diversification: Are floral nectar spurs a key evolutionary innovation? Proc. R. Soc. Lond. B 262, 343–348 (1995)

    Article  ADS  Google Scholar 

  15. Huelsenbeck, J. P. & Ronquist, F. MRBAYES: Bayesian inference of phylogeny. Bioinformatics 17, 754–755 (2001)

    Article  CAS  Google Scholar 

  16. Grant, V. Isolation and hybridization between Aquilegia formosa and A. pubescens. Aliso 2, 341–360 (1952)

    Google Scholar 

  17. Hodges, S. A., Fulton, M., Yang, J. Y. & Whittall, J. B. Verne Grant and evolutionary studies of Aquilegia. New Phytol. 161, 113–120 (2004)

    Article  Google Scholar 

  18. Pagel, M., Meade, A. & Barker, D. Bayesian estimation of ancestral character states on phylogenies. Syst. Biol. 53, 673–684 (2004)

    Article  Google Scholar 

  19. Felsenstein, J. Phylogenies and the comparative method. Am. Nat. 125, 1–15 (1985)

    Article  Google Scholar 

  20. Butler, M. A. & King, A. A. Phylogenetic comparative analysis: A modelling approach for adaptive evolution. Am. Nat. 164, 683–695 (2004)

    Article  Google Scholar 

  21. Miller, W. E. Diversity and evolution of tongue length in hawkmoths (Sphingidae). J. Lepid. Soc 5, 9–31 (1997)

    Google Scholar 

  22. Hundsdoerfer, A. K., Kitching, I. J. & Wink, M. A molecular phylogeny of the hawkmoth genus Hyles (Lepidoptera: Sphingidae, Macroglossinae). Mol. Phylogenet. Evol. 35, 442–458 (2005)

    Article  CAS  Google Scholar 

  23. Kay, K., Whittall, J. B. & Hodges, S. A. A survey of nrITS substitution rates across angiosperms: An approximate molecular clock with life history effects. BMC Evol. Biol. 6, 36 (2006)

    Article  Google Scholar 

  24. Vos, P. et al. AFLP: A new technique for DNA fingerprinting. Nucleic Acids Res. 23, 4407–4414 (1995)

    Article  CAS  Google Scholar 

  25. Sanderson, M. J. r8s: inferring absolute rates of molecular evolution and divergence times in the absence of a molecular clock. Bioinformatics 19, 301–302 (2003)

    Article  CAS  Google Scholar 

  26. Pagel, M. The maximum likelihood approach to reconstructing ancestral character states of discrete characters on phylogenies. Syst. Biol. 48, 612–622 (1999)

    Article  Google Scholar 

  27. Midford, P., Garland, T. Jr. & Maddison, W. P. PDAP package of Mesquite. Version 1.07 (2005); 〈〉.

  28. Maddison, W. P. & Maddison, D. R. . Mesquite: A modular system for evolutionary analysis. Version 1.05 (2004); 〈〉.

  29. Garland, T., Harvey, P. H. & Ives, A. R. Procedures for the analysis of comparative data using phylogenetically independent contrasts. Syst. Biol. 41, 18–32 (1992)

    Article  Google Scholar 

Download references


We thank D. Bush and B. Counterman for laboratory assistance; J. Yang, M. Fulton, S. Schaefer, Y. Kisel and J. Bean for greenhouse and field help; T. Oakley and B. O’Meara for technical assistance; C. Voelkel and C. Eckert for comments on earlier versions of this manuscript; and M. Hodges for help with the figures. Funding was provided by the Botanical Society of America, UCSB’s Olivia Long Converse Fellowship, the National Science Foundation, UC Davis’ Comparative Biology Postdoctoral Fellowship, and the Native Plant Societies of Wyoming, Colorado, and northern Nevada.

Author Contributions J.B.W. and S.A.H. designed the study and collected the samples; J.B.W. collected and analysed the phylogenetic and comparative data; J.B.W. and S.A.H. wrote the paper.

Author information

Authors and Affiliations


Corresponding authors

Correspondence to Justen B. Whittall or Scott A. Hodges.

Ethics declarations

Competing interests

Reprints and permissions information is available at The authors declare no competing financial interests.

Supplementary information

Supplementary Information

This file contains Supplementary Methods, Supplementary Discussion, Supplementary Figure 1 with Legend, Supplementary Tables 1-5 and additional references. (PDF 481 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Whittall, J., Hodges, S. Pollinator shifts drive increasingly long nectar spurs in columbine flowers. Nature 447, 706–709 (2007).

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI:

This article is cited by


By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.


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