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Physical performance and darwinian fitness in lizards

Nature volume 432, pages 502–505 (2004)Cite this article

Abstract

Strong evidence for a genetic basis of variation in physical performance has accumulated1,2. Considering one of the basic tenets of evolutionary physiology—that physical performance and darwinian fitness are tightly linked3—one may expect phenotypes with exceptional physiological capacities to be promoted by natural selection. Why then does physical performance remain considerably variable in human and other animal populations1,2,4? Our analysis of locomotor performance in the common lizard (Lacerta vivipara) demonstrates that initial endurance (running time to exhaustion measured at birth) is indeed highly heritable, but natural selection in favour of this trait can be unexpectedly weak. A manipulation of dietary conditions unravels a proximate mechanism explaining this pattern. Fully fed individuals experience a marked reversal of performance within only one month after birth: juveniles with low endurance catch up, whereas individuals with high endurance lose their advantage. In contrast, dietary restriction allows highly endurant neonates to retain their locomotor superiority as they age. Thus, the expression of a genetic predisposition to high physical performance strongly depends on the environment experienced early in life.

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Figure 1
Figure 2: Fitness functions of initial endurance during the first summer (triangles pointing down) and the whole year (triangles pointing up) following birth.
Figure 3: Ontogenic change in endurance depending on diet and initial endurance.
Figure 4: Fitness functions of initial endurance depending on dietary conditions experienced during the first month following birth (filled circles and solid line, full feeding; open circles and dashed line, dietary restriction).

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References

  1. Rupert, J. L. The search for genotypes that underlie human performance phenotypes. Comp. Biochem. Physiol. A 136, 191–203 (2003)

    Article  Google Scholar 

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

    Google Scholar 

  3. Arnold, S. J. Morphology, performance and fitness. Am. Zool. 23, 347–361 (1983)

    Article  Google Scholar 

  4. Bennett, A. F. & Huey, R. B. in Oxford Surveys in Evolutionary Biology (eds Futuyma, D. J. & Antonovics, J.) 251–284, (1990)

    Google Scholar 

  5. Bouchard, C., Malina, R. M. & Pérusse, L. Human Kinetics 408 (Champaign, Illinois, 1997)

    Google Scholar 

  6. Irschick, D. J. Evolutionary approaches for studying functional morphology: examples from studies of performance capacity. Integr. Comp. Biol. 42, 278–290 (2002)

    Article  Google Scholar 

  7. Irschick, D. J. & Garland, T. J. Integrating function and ecology in studies of adaptation: investigations of locomotor capacity as a model system. Annu. Rev. Ecol. Syst. 32, 367–396 (2001)

    Article  Google Scholar 

  8. Garland, T. J. Physiological correlates of locomotory performances in a lizard: an allometric approach. Am. J. Physiol. 247, R806–R815 (1984)

    CAS  PubMed  Google Scholar 

  9. Clobert, J. et al. Trade-offs in phenotypic traits: endurance at birth, growth, survival, predation and susceptibility to parasitism in a lizard, Lacerta vivipara. Funct. Ecol. 14, 675–684 (2000)

    Article  Google Scholar 

  10. Le Galliard, J.-F., Ferrière, R. & Clobert, J. Mother–offspring interactions affect natal dispersal in a lizard. Proc. R. Soc. Lond. B 270, 1163–1169 (2003)

    Article  Google Scholar 

  11. Sorci, G., Swallow, J. G., Garland, T. J. & Clobert, J. Quantitative genetics of locomotor speed and endurance in the lizard Lacerta vivipara. Physiol. Zool. 68, 698–720 (1995)

    Article  Google Scholar 

  12. Lorenzon, P., Clobert, J. & Massot, M. The contribution of phenotypic plasticity to adaptation in Lacerta vivipara. Evolution 55, 392–404 (2001)

    Article  CAS  Google Scholar 

  13. Jayne, B. C. & Bennett, A. F. Selection of locomotor performance capacity in a natural population of garter snakes. Evolution 44, 1204–1229 (1990)

    Article  Google Scholar 

  14. Sorci, G. & Clobert, J. Natural selection on hatchling body size and mass in two environments in the common lizard (Lacerta vivipara). Evol. Ecol. Res. 1, 303–316 (1999)

    Google Scholar 

  15. Janzen, F. J., Tucker, J. K. & Paukstis, G. L. Experimental analysis of an early life-history stage: selection on size of hatchling turtles. Ecology 81, 2290–2304 (2000)

    Article  Google Scholar 

  16. Cureton, K. J. & Sparling, P. B. Distance running performance and metabolic responses to running in men and women with excess weight experimentally equated. Med. Sci. Sports Exerc. 12, 288–294 (1980)

    Article  CAS  Google Scholar 

  17. Swallow, J. G., Koteja, P., Carter, P. A. & Garland, T. Jr. Food consumption and body composition in mice selected for high wheel-running activity. J. Comp. Physiol. B 171, 651–659 (2001)

    Article  CAS  Google Scholar 

  18. Khodadoost, M., Pilorge, T. & Ortega, A. Variations de la densité et de la taille corporelle en fonction de la composition du peuplement de proies de trois populations de lézards vivipares du Mont Lozère. Revue d'Ecologie (Terre Vie) 42, 193–201 (1987)

    Google Scholar 

  19. Price, T. D. & Grant, P. R. Life history traits and natural selection for small body size in a population of Darwin's finches. Evolution 38, 483–494 (1984)

    Article  Google Scholar 

  20. Riska, B. Composite traits, selection response, and evolution. Evolution 43, 1172–1191 (1986)

    Article  Google Scholar 

  21. Le Galliard, J.-F., Le Bris, M. & Clobert, J. Timing of locomotor impairment and shift in thermal preferences during gravidity in a viviparous lizard. Funct. Ecol. 17, 877–885 (2003)

    Article  Google Scholar 

  22. Huey, R. B., Bennett, A. F., John-Alder, H. & Nagy, K. A. Locomotor capacity and foraging behaviour of Kalahari lacertid lizards. Anim. Behav. 32, 41–50 (1984)

    Article  Google Scholar 

  23. White, G. C. & Burnham, K. P. Program MARK: survival estimation from populations of marked animals. Bird Study 46, 120–138 (1999)

    Article  Google Scholar 

  24. Avery, R. A. Estimates of food consumption by the lizard Lacerta vivipara Jacquin. J. Anim. Ecol. 40, 351–365 (1971)

    Article  Google Scholar 

  25. Massot, M., Clobert, J., Lecomte, J. & Barbault, R. Incumbent advantage in common lizards and their colonizing ability. J. Anim. Ecol. 63, 431–440 (1994)

    Article  Google Scholar 

  26. Rice, W. R. & Gaines, S. D. ‘Heads I win, tails you lose’: testing directional alternative hypotheses in ecological and evolutionary research. Trends Ecol. Evol. 9, 235–237 (1994)

    Article  CAS  Google Scholar 

  27. Falconer, D. S. An Introduction to Quantitative Genetics (Longman, London, 1989)

    Google Scholar 

  28. Littell, R. C., Millinken, G. A., Stroup, W. W. & Wolfinger, R. D. SAS Systems for Mixed Models (SAS Institute, Cary, North Carolina, 1996)

    Google Scholar 

  29. Schluter, D. Estimating the form of natural selection on a quantitative trait. Evolution 42, 849–861 (1988)

    Article  Google Scholar 

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

    Article  Google Scholar 

Download references

Acknowledgements

We are grateful to A. Badyaev, A. Burke and T. Markow for comments, to P. Cassey, M. Massot, M. Nachman, D. Papaj, M. Saunders and T. van Dooren for discussions, and to J. Cote, B. Decencière, M.-L. Jarzat, M. Le Bris, D. Mersch and S. Testard for assistance. Financial support was received from the French Ministry of Education and Research, the French Ministry of Environment, the European Research Training Network ‘ModLife’, and the NSF Biomath REU programme.

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Author notes

  1. Jean-François Le Galliard

    Present address: Centre for Ecological and Evolutionary Synthesis, Department of Biology, University of Oslo, P.O. Box 1050, Blindern, 0316, Oslo, Norway

Authors and Affiliations

  1. Laboratoire Fonctionnement et Evolution des Systèmes Ecologiques, CNRS UMR 7625, Ecole Normale Supérieure, 46 rue d'Ulm, 75230, cedex 05, Paris, France

    Jean-François Le Galliard, Jean Clobert & Régis Ferrière

  2. Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, Arizona, 85721, USA

    Régis Ferrière

Authors
  1. Jean-François Le Galliard
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  2. Jean Clobert
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  3. Régis Ferrière
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Corresponding author

Correspondence to Jean-François Le Galliard.

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The authors declare that they have no competing financial interests.

Supplementary information

Supplementary Discussion

The Discussion explains that the semi-natural conditions of our enclosures mimic the social selection acting on lizards in the wild. (DOC 23 kb)

Supplementary Table S1

Describes the effect of removing individuals from the original sample on the statistical relationship between morphology and endurance on one side, and annual survival on the other side. (DOC 34 kb)

Supplementary Table S2

Table S2 shows that the relationship between morphology and endurance on one side, and annual survival on the other side is not confounded by the effect of the behavioural motivation. (DOC 36 kb)

Supplementary Table S3

Table S3 shows that the body growth observed under the ‘Full feeding’ treatment matched the body growth observed in the wild during the course of the selection study. (DOC 29 kb)

Supplementary Table S4

The Table S4 illustrates the food delivery per lizard per day during the course of the feeding manipulation. (DOC 31 kb)

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Le Galliard, JF., Clobert, J. & Ferrière, R. Physical performance and darwinian fitness in lizards. Nature 432, 502–505 (2004). https://doi.org/10.1038/nature03057

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