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.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 51 print issues and online access
$199.00 per year
only $3.90 per issue
Buy this article
- Purchase on SpringerLink
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Rupert, J. L. The search for genotypes that underlie human performance phenotypes. Comp. Biochem. Physiol. A 136, 191–203 (2003)
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)
Arnold, S. J. Morphology, performance and fitness. Am. Zool. 23, 347–361 (1983)
Bennett, A. F. & Huey, R. B. in Oxford Surveys in Evolutionary Biology (eds Futuyma, D. J. & Antonovics, J.) 251–284, (1990)
Bouchard, C., Malina, R. M. & Pérusse, L. Human Kinetics 408 (Champaign, Illinois, 1997)
Irschick, D. J. Evolutionary approaches for studying functional morphology: examples from studies of performance capacity. Integr. Comp. Biol. 42, 278–290 (2002)
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)
Garland, T. J. Physiological correlates of locomotory performances in a lizard: an allometric approach. Am. J. Physiol. 247, R806–R815 (1984)
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)
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)
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)
Lorenzon, P., Clobert, J. & Massot, M. The contribution of phenotypic plasticity to adaptation in Lacerta vivipara. Evolution 55, 392–404 (2001)
Jayne, B. C. & Bennett, A. F. Selection of locomotor performance capacity in a natural population of garter snakes. Evolution 44, 1204–1229 (1990)
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)
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)
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)
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)
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)
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)
Riska, B. Composite traits, selection response, and evolution. Evolution 43, 1172–1191 (1986)
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)
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)
White, G. C. & Burnham, K. P. Program MARK: survival estimation from populations of marked animals. Bird Study 46, 120–138 (1999)
Avery, R. A. Estimates of food consumption by the lizard Lacerta vivipara Jacquin. J. Anim. Ecol. 40, 351–365 (1971)
Massot, M., Clobert, J., Lecomte, J. & Barbault, R. Incumbent advantage in common lizards and their colonizing ability. J. Anim. Ecol. 63, 431–440 (1994)
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)
Falconer, D. S. An Introduction to Quantitative Genetics (Longman, London, 1989)
Littell, R. C., Millinken, G. A., Stroup, W. W. & Wolfinger, R. D. SAS Systems for Mixed Models (SAS Institute, Cary, North Carolina, 1996)
Schluter, D. Estimating the form of natural selection on a quantitative trait. Evolution 42, 849–861 (1988)
Janzen, F. J. & Stern, H. S. Logistic regression for empirical studies of multivariate selection. Evolution 52, 1564–1571 (1998)
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.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Competing interests
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)
Rights and permissions
About this article
Cite this article
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
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1038/nature03057
This article is cited by
-
Transcriptomic analysis of the trade-off between endurance and burst-performance in the frog Xenopus allofraseri
BMC Genomics (2021)
-
Shrinking into the big city: influence of genetic and environmental factors on urban dragon lizard morphology and performance capacity
Urban Ecosystems (2021)
-
Recovery from discrete wound severities in side-blotched lizards (Uta stansburiana): implications for energy budget, locomotor performance, and oxidative stress
Journal of Comparative Physiology B (2021)
-
Ain’t going down without a fight: state-and environment-dependence of antipredator defensive aggressive personalities in Carpetan rock lizard
Behavioral Ecology and Sociobiology (2020)
-
Predicting adult lifespan and lifetime reproductive success from early-life reproductive events
Marine Biology (2020)
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.