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.

Experimentally assessing the relative importance of predation and competition as agents of selection

This article has been updated

Abstract

Field experiments that measure natural selection in response to manipulations of the selective regime are extremely rare1, even in systems where the ecological basis of adaptation has been studied extensively. The adaptive radiation of Caribbean Anolis lizards has been studied for decades2,3,4,5, leading to precise predictions about the influence of alternative agents of selection in the wild. Here we present experimental evidence for the relative importance of two putative agents of selection in shaping the adaptive landscape for a classic island radiation. We manipulated whole-island populations of the brown anole lizard, Anolis sagrei, to measure the relative importance of predation versus competition as agents of natural selection. We excluded or included bird and snake predators across six islands that ranged from low to high population densities of lizards, then measured subsequent differences in behaviour and natural selection in each population. Predators altered the lizards’ perching behaviour and increased mortality, but predation treatments did not alter selection on phenotypic traits. By contrast, experimentally increasing population density dramatically increased the strength of viability selection favouring large body size, long relative limb length and high running stamina. Our results from A. sagrei are consistent with the hypothesis6 that intraspecific competition is more important than predation in shaping the selective landscape for traits central to the adaptive radiation of Anolis ecomorphs.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Figure 1: Differences in survival (open circles) and perching behaviour (filled circles) as a function of predator treatment.
Figure 2: Left panels show mean values (± 1 s.e.m.) of selection gradients measured in two replicates across each of three predation treatments.

Change history

  • 03 June 2010

    The penultimate sentence in the Fig. 2 legend was changed.

References

  1. 1

    Reznick, D. N. & Ghalambor, C. K. Selection in nature: experimental manipulations of natural populations. Integr. Comp. Biol. 45, 456–462 (2005)

    Article  Google Scholar 

  2. 2

    Schoener, T. W. Inferring the properties of predation and other injury producing agents from injury frequencies. Ecology 60, 1110–1115 (1979)

    ADS  Article  Google Scholar 

  3. 3

    Williams, E. E. in Lizard Ecology: Studies of a Model Organism (eds Huey, R.B., Pianka, E.R. & Schoener, T.W.) 326–370 (Harvard Univ. Press, 1983)

    Google Scholar 

  4. 4

    Langerhans, R. B., Knouft, J. H. & Losos, J. B. Shared and unique features of diversification in Greater Antillean Anolis ecomorphs. Evolution 60, 362–369 (2006)

    Article  Google Scholar 

  5. 5

    Losos, J. B. Lizards in an Evolutionary Tree: Ecology and Adaptive Radiation of Anoles (Univ. California Press, 2009)

    Google Scholar 

  6. 6

    Andrews, R. M. Evolution of life histories: a comparison of Anolis lizards from matched island and mainland habitats. Breviora 454, 1–51 (1979)

    Google Scholar 

  7. 7

    Schluter, D. Experimental evidence that competition promotes divergence in adaptive radiation. Science 266, 798–801 (1994)

    ADS  CAS  Article  Google Scholar 

  8. 8

    Reznick, D. N., Shaw, F. H., Rodd, F. H. & Shaw, R. G. Evaluation of the rate of evolution in natural populations of guppies (Poecilia reticulata). Science 275, 1934–1937 (1997)

    CAS  Article  Google Scholar 

  9. 9

    Kingsolver, J. G. H. et al. The strength of phenotypic selection in natural populations. Am. Nat. 157, 245–261 (2001)

    CAS  Article  Google Scholar 

  10. 10

    Pigliucci, M. & Kaplan, J. M. Making Sense of Evolution: The Conceptual Foundation of Evolutionary Biology (Univ. Chicago Press, 2006)

    Book  Google Scholar 

  11. 11

    Irschick, D. J., Vitt, L. J., Zani, P. A. & Losos, J. B. A comparison of evolutionary radiations in mainland and Caribbean Anolis lizards. Ecology 78, 2191–2203 (1997)

    Article  Google Scholar 

  12. 12

    Losos, J. B., Jackman, T. R., Larson, A., DeQueiroz, K. & Rodriguez-Shettino, L. Contingency and determinism in replicated adaptive radiations of island lizards. Science 279, 2115–2118 (1998)

    ADS  CAS  Article  Google Scholar 

  13. 13

    Irschick, D. J. et al. A comparison of habitat use, morphology, clinging performance and escape behaviour among two divergent green anole lizard (Anolis carolinensis) populations. Biol. J. Linn. Soc. 85, 223–234 (2005)

    Article  Google Scholar 

  14. 14

    Stamps, J. A. & Krishnan, V. V. Territory acquisition in lizards: I. First encounters. Anim. Behav. 47, 1375–1385 (1994)

    Article  Google Scholar 

  15. 15

    Rand, A. S. Ecology and social organization in the iguanid lizard, Anolis lineatopus . Proc. US Natl Mus. 122, 1–79 (1967)

    Article  Google Scholar 

  16. 16

    Butler, M. A., Sawyer, S. A. & Losos, J. B. Sexual dimorphism and adaptive radiation in Anolis lizards. Nature 447, 202–205 (2007)

    ADS  CAS  Article  Google Scholar 

  17. 17

    Losos, J. B., Schoener, T. W. & Spiller, D. A. Predator-induced behaviour shifts and natural selection in field-experimental lizard populations. Nature 432, 505–508 (2004)

    ADS  CAS  Article  Google Scholar 

  18. 18

    Schoener, T. W. Ecological significance of sexual dimorphism in size in lizard Anolis conspersus . Science 155, 474–477 (1967)

    ADS  CAS  Article  Google Scholar 

  19. 19

    Calsbeek, R. & Irschick, D. J. The quick and the dead: correlational selection on morphology, performance, and habitat use in island lizards. Evolution 61, 2493–2503 (2007)

    Article  Google Scholar 

  20. 20

    MacArthur, R. H. & Wilson, E. O. The Theory of Island Biogeography (Princeton Univ. Press, 1967)

    Google Scholar 

  21. 21

    Calsbeek, R. & Smith, T. B. Experimentally replicated disruptive selection on performance traits in a Caribbean lizard. Evolution 62, 478–484 (2008)

    Article  Google Scholar 

  22. 22

    Schoener, T. W. The Anolis lizards of Bimini: resource partitioning in a complex fauna. Ecology 49, 704–726 (1968)

    Article  Google Scholar 

  23. 23

    Calsbeek, R. Sex-specific adult dispersal and its selective consequences in the brown anole, Anolis sagrei . J. Anim. Ecol. 78, 617–624 (2009)

    Article  Google Scholar 

  24. 24

    Lailvaux, S. P., Herrel, A., VanHooydonck, B., Meyers, J. J. & Irschick, D. J. Performance capacity, fighting tactics and the evolution of life-stage male morphs in the green anole lizard (Anolis carolinensis). Proc. R. Soc. Lond. B 271, 2501–2508 (2004)

    Article  Google Scholar 

  25. 25

    Anderson, D. R. Model Based Inference in the Life Sciences: A Primer on Evidence (Springer, 2008)

    Book  Google Scholar 

  26. 26

    Losos, J. B., Schoener, T. W., Langerhans, R. B. & Spiller, D. A. Rapid temporal reversal in predator-driven natural selection. Science 314, 1111 (2006)

    ADS  CAS  Article  Google Scholar 

  27. 27

    Cox, R. M. & Calsbeek, R. Sexually antagonistic selection, sexual dimorphism, and the resolution of intralocus sexual conflict. Am. Nat. 173, 176–187 (2009)

    Article  Google Scholar 

  28. 28

    Calsbeek, R. & Smith, T. B. Probing the adaptive landscape on experimental islands: density dependent selection on lizard body-size. Evolution 61, 1052–1061 (2007)

    Article  Google Scholar 

  29. 29

    Perry, G., Levering, K., Girard, I. & Garland, T. Jr. Locomotor performance and social dominance in male Anolis cristatellus . Anim. Behav. 67, 37–47 (2004)

    Article  Google Scholar 

  30. 30

    Cox, R. M. & Calsbeek, R. Severe costs of reproduction persist in Anolis lizards despite the evolution of single-egg clutch. Evolution (in the press)

Download references

Acknowledgements

We thank T. B. Smith for suggestions about experimental design, and B. Calsbeek and A. Gasc for help with predator manipulations. M. C. Duryea, S. Kuchta, M. Logan, M. Najarro and D. Urbach helped to clarify the manuscript. This research was conducted under permits from The Bahamas Ministry of Agriculture and approval from the Dartmouth College Institutional Animal Care and Use Committee. An award from the National Science Foundation to R. Calsbeek, and funding from Dartmouth College, provided financial support.

Author information

Affiliations

Authors

Contributions

Both authors contributed equally to study design, fieldwork and data analysis. R.C. prepared the manuscript with assistance from R.M.C.

Corresponding author

Correspondence to Ryan Calsbeek.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Information

This file contains Supplementary Methods, Supplementary Tables S1-S2 and Supplementary Figures S1-S2 with legends. Supplementary Table 1 was amended on 3 June 2010. (PDF 550 kb)

PowerPoint slides

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Calsbeek, R., Cox, R. Experimentally assessing the relative importance of predation and competition as agents of selection. Nature 465, 613–616 (2010). https://doi.org/10.1038/nature09020

Download citation

Further reading

Comments

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.

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