Letter | Published:

Predator-induced behaviour shifts and natural selection in field-experimental lizard populations

Naturevolume 432pages505508 (2004) | Download Citation

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Abstract

The role of behaviour in evolutionary change has long been debated. On the one hand, behavioural changes may expose individuals to new selective pressures by altering the way that organisms interact with the environment, thus driving evolutionary divergence1,2,3. Alternatively, behaviour can act to retard evolutionary change4,5,6: by altering behavioural patterns in the face of new environmental conditions, organisms can minimize exposure to new selective pressures. This constraining influence of behaviour has been put forward as an explanation for evolutionary stasis within lineages4,7,8,9 and niche conservatism within clades10,11. Nonetheless, the hypothesis that behavioural change prevents natural selection from operating in new environments has never been experimentally tested. We conducted a controlled and replicated experimental study of selection in entirely natural populations; we demonstrate that lizards alter their habitat use in the presence of an introduced predator, but that these behavioural shifts do not prevent patterns of natural selection from changing in experimental populations.

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References

  1. 1

    Wyles, J. S., Kunkel, J. G. & Wilson, A. C. Birds, behavior, and anatomical evolution. Proc. Natl Acad. Sci. USA 80, 4394–4397 (1983)

  2. 2

    Wcislo, W. T. Behavioral environments and evolutionary change. Annu. Rev. Ecol. Syst. 20, 137–169 (1989)

  3. 3

    West-Eberhard, M. J. Phenotypic plasticity and the origins of diversity. Annu. Rev. Ecol. Syst. 20, 249–278 (1989)

  4. 4

    Wake, D. B., Roth, G. & Wake, M. H. On the problem of stasis in organismal evolution. J. Theor. Biol. 101, 211–224 (1983)

  5. 5

    Brandon, R. in The Role of Behavior in Evolution (ed. Plotkin, H. C.) 51–71 (MIT Press, Cambridge, USA, 1988)

  6. 6

    Huey, R. B., Hertz, P. E. & Sinervo, B. Behavioral drive versus behavioral inertia in evolution: A null model approach. Am. Nat. 161, 357–366 (2003)

  7. 7

    Eldredge, N. Macroevolutionary Dynamics: Species, Niches, & Adaptive Peaks (McGraw-Hill, New York, 1989)

  8. 8

    Coope, G. R. in Extinction Rates (eds Lawton, J. H. & May, R. M.) 55–74 (Oxford Univ. Press, Oxford, 1995)

  9. 9

    Leviton, J. S. Genetics, Paleontology, and Macroevolution 2nd edn (Cambridge Univ. Press, Cambridge, UK, 2001)

  10. 10

    Harvey, P. H. & Pagel, M. D. The Comparative Method in Evolutionary Biology (Oxford Univ. Press, Oxford, 1991)

  11. 11

    Webb, C. O., Ackerly, D. D., McPeek, M. A. & Donoghue, M. J. Phylogenies and community ecology. Annu. Rev. Ecol. Syst. 33, 475–505 (2003)

  12. 12

    Schoener, T. W. Presence and absence of habitat shift in some widespread lizard species. Ecol. Monogr. 45, 233–258 (1975)

  13. 13

    Pacala, S. W. & Roughgarden, J. Population experiments with the Anolis lizards of St. Maarten and St. Eustatius. Ecology 66, 129–141 (1985)

  14. 14

    Losos, J. B. & Spiller, D. Differential colonization success and asymmetrical interactions between two lizard species. Ecology 80, 252–258 (1999)

  15. 15

    Losos, J. B. Integrative approaches to evolutionary ecology: Anolis lizards as model systems. Annu. Rev. Ecol. Syst. 25, 467–493 (1994)

  16. 16

    Schoener, T. W., Spiller, D. A. & Losos, J. B. Predators increase the risk of catastrophic extinction of prey populations. Nature 412, 183–186 (2001)

  17. 17

    Schoener, T. W., Spiller, D. A. & Losos, J. B. Predation on a common Anolis lizard: Can the food-web effects of a devastating predator be reversed? Ecol. Monogr. 72, 383–408 (2002)

  18. 18

    Schoener, T. W., Slade, J. B. & Stinson, C. H. Diet and sexual dimorphism in the very catholic lizard genus Leiocephalus of the Bahamas. Oecologia 53, 160–169 (1982)

  19. 19

    Garland, T. Jr & Losos, J. B. in Ecological Morphology: Integrative Organismal Biology (eds Wainwright, P. C. & Reilly, S.) 240–302 (Univ. Chicago Press, Chicago, USA, 1994)

  20. 20

    Lande, R. & Arnold, S. J. The measurement of selection on correlated characters. Evolution 37, 1210–1226 (1983)

  21. 21

    Brodie, E. D. III, Moore, A. J. & Janzen, F. J. Visualizing and quantifying natural selection. Trends Ecol. Evol. 10, 313–318 (1995)

  22. 22

    Schoener, T. W. & Schoener, A. The ecological correlates of survival in some Bahamian Anolis lizards. Oikos 39, 1–16 (1982)

  23. 23

    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, Cambridge, USA, 1983)

  24. 24

    Irschick, D. J. & Losos, J. B. Do lizards avoid habitats in which performance is submaximal?: The relationship between sprinting capabilities and structural habitat use in Caribbean anoles. Am. Nat. 154, 293–305 (1999)

  25. 25

    Hurlbert, S. H. Pseudoreplication and the design of ecological field experiments. Ecol. Monogr. 54, 187–211 (1984)

  26. 26

    Janzen, F. J. & Stern, H. S. Logistic regression for empirical studies of multivariate selection. Evolution 52, 1564–1571 (1998)

  27. 27

    DeWitt, T. J. & Langerhans, R. B. Multiple prey traits, multiple predators: keys to understanding complex community dynamics. J. Sea Res. 49, 143–155 (2003)

  28. 28

    Rundle, H. D., Vamosi, S. M. & Schluter, D. Experimental test of predation's effect on divergent selection during character displacement in sticklebacks. Proc. Natl Acad. Sci. USA 100, 14943–14948 (2003)

  29. 29

    Bolnick, D. I. Can intraspecific competition drive disruptive selection? An experimental test in natural populations of sticklebacks. Evolution 58, 608–618 (2004)

  30. 30

    Littell, R. C., Freund, R. J. & Spector, P. C. SAS System for Linear Models 3rd edn (SAS Institute Inc., Cary, North Carolina, 1999)

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Acknowledgements

We thank the National Science Foundation and the National Geographic Society for support, J. Chase, T. Knight and B. Pinder for assistance, R. B. Langerhans for suggesting the approach to study selection and helping in its implementation, D. Bolnick, J. Chase, B. Fitzpatrick, F. Janzen, T. Knight, B. Langerhans, M. Leal, M. Turelli and the Turelli labgroup, for constructive comments on previous drafts, and the Bahamian government for permission to conduct this research.

Author information

Affiliations

  1. Department of Biology, Washington University, Campus Box 1137, St Louis, Missouri, 63130, USA

    • Jonathan B. Losos
  2. Section of Ecology and Evolution and Center for Population Biology, University of California, Davis, California, 95616, USA

    • Thomas W. Schoener
    •  & David A. Spiller

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Competing interests

The authors declare that they have no competing financial interests.

Corresponding author

Correspondence to Jonathan B. Losos.

Supplementary information

  1. Supplementary Methods

    This file provides information on how marginal recapture rates were calculated. (DOC 23 kb)

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https://doi.org/10.1038/nature03039

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