Skip to main content
Log in

Mismatch Between Ectotherm Thermal Preferenda and Optima for Swimming: A Test of the Evolutionary Pace Hypothesis

  • Research Article
  • Published:
Evolutionary Biology Aims and scope Submit manuscript

Abstract

A continuing issue in evolutionary thermal biology is the mismatch between preferred body temperatures (T pref) and optimal temperatures (T opt) for whole-animal performance. Using phylogenetic comparative analyses, I examined the hypothesis that a difference in the rates at which T pref and T opt evolve causes the mismatch in a lineage of European newts. In a laboratory thermal gradient, newts maintained body temperatures that were on average 8 °C below T opt for maximum swimming velocity. The lower boundary of the T pref range evolved faster than the mean T pref, the upper boundary of the T pref range, and T opt. The strong evolutionary co-variation between mean T pref and its boundaries prevented the shift of mean T pref away from T opt. This suggests that the variation in evolutionary rates has a limited potential to modify the disparity between thermal optima and preferenda.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Ackerly, D. (2009). Conservatism and diversification of plant functional traits: Evolutionary rates versus phylogenetic signal. Proceedings of the National Academy of Sciences of the United States of America, 106, 19699–19706.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Adams, D. C. (2013). Comparing evolutionary rates for different phenotypic traits on a phylogeny using likelihood. Systematic Biology, 62, 181–192.

    Article  PubMed  Google Scholar 

  • Angilletta, M. J., Bennett, A. F., Guderley, H., Navas, C. A., Seebacher, F., & Wilson, R. S. (2006). Coadaptation: A unifying principle in evolutionary thermal biology. Physiological and Biochemical Zoology, 79, 282–294.

    Article  PubMed  Google Scholar 

  • Angilletta, M. J., Hill, T., & Robson, M. A. (2002a). Is physiological performance optimized by thermoregulatory behavior? A case study of the eastern fence lizard, Sceloporus undulatus. Journal of Thermal Biology, 27, 199–204.

    Article  Google Scholar 

  • Angilletta, M. J., Huey, R. B., & Frazier, M. R. (2010). Thermodynamic effects on organismal performance: Is hotter better? Physiological and Biochemical Zoology, 83, 197–206.

    Article  PubMed  Google Scholar 

  • Angilletta, M. J., Niewiarowski, P. H., & Navas, C. A. (2002b). The evolution of thermal physiology in ectotherms. Journal of Thermal Biology, 27, 249–268.

    Article  Google Scholar 

  • Angilletta, M. J., Wilson, R. S., Navas, C. A., & James, R. S. (2003). Tradeoffs and the evolution of thermal reaction norms. Trends in Ecology & Evolution, 18, 234–240.

    Article  Google Scholar 

  • Arnold, S. J. (1992). Constraints on phenotypic evolution. American Naturalist, 140, S85–S107.

    Article  PubMed  Google Scholar 

  • Asbury, D. A., & Angilletta, M. J. (2010). Thermodynamic effects on the evolution of performance curves. American Naturalist, 176, E40–E49.

    Article  PubMed  Google Scholar 

  • Bauwens, D., Garland, T., Castilla, A. M., & Van Damme, R. (1995). Evolution of sprint speed in lacertid lizards: Morphological, physiological, and behavioral covariation. Evolution, 49, 848–863.

    Article  Google Scholar 

  • Beitinger, T. L., & Fitzpatrick, L. C. (1979). Physiological and ecological correlates of preferred temperature in fish. American Zoologist, 19, 319–329.

    Google Scholar 

  • Bennett, A. F., & Licht, P. (1972). Anaerobic metabolism during activity in lizards. Journal of Comparative Physiology, 81, 277–288.

    Article  Google Scholar 

  • Boettiger, C., Coop, G., & Ralph, P. (2012). Is your phylogeny informative? Measuring the power of comparative methods. Evolution, 66, 2240–2251.

    Article  PubMed Central  PubMed  Google Scholar 

  • Castañeda, L. E., Lardies, M. A., & Bozinovic, F. (2004). Adaptive latitudinal shifts in the thermal physiology of a terrestrial isopod. Evolutionary Ecology Research, 6, 579–593.

    Google Scholar 

  • Cossins, A. R., & Bowler, K. (1987). Temperature biology of animals. New York: Chapman and Hall.

    Book  Google Scholar 

  • Dawson, W. R. (1975). On the physiological significance of the preferred body temperatures of reptiles. In D. M. Gates & R. B. Schmerl (Eds.), Perspectives of biophysical ecology (pp. 443–473). New York: Springer.

    Chapter  Google Scholar 

  • Deere, J. A., & Chown, S. L. (2006). Testing the beneficial acclimation hypothesis and its alternatives for locomotor performance. American Naturalist, 168, 630–644.

    Article  PubMed  Google Scholar 

  • DiCiccio, T. J., & Efron, B. (1996). Bootstrap confidence intervals. Statistical Science, 11, 189–212.

    Article  Google Scholar 

  • Dvořák, J., & Gvoždík, L. (2010). Adaptive accuracy of temperature oviposition preferences in newts. Evolutionary Ecology, 24, 1115–1127.

    Article  Google Scholar 

  • Felsenstein, J. (2008). Comparative methods with sampling error and within-species variation: Contrasts revisited and revised. American Naturalist, 171, 713–725.

    Article  PubMed  Google Scholar 

  • Gilchrist, G. W. (1995). Specialists and generalists in changing environments. 1. Fitness landscapes of thermal sensitivity. American Naturalist, 146, 252–270.

    Article  Google Scholar 

  • Gilchrist, G. W. (1996). A quantitative genetic analysis of thermal sensitivity in the locomotor performance curve of Aphidius ervi. Evolution, 50, 1560–1572.

    Article  Google Scholar 

  • Gittleman, J. L., Anderson, C. G., Kot, M., & Luh, H.-K. (1996). Phylogenetic lability and rates of evolution: A comparison of behavioral, morphological and life history traits. In E. P. Martins (Ed.), Phylogenies and the comparative method in animal behavior (pp. 166–205). Oxford: Oxford University Press.

    Google Scholar 

  • Griffiths, R. A. (1996). Newts and salamanders of Europe. London: Academic Press.

    Google Scholar 

  • Gvoždík, L. (2003). Postprandial thermophily in the Danube crested newt, Triturus dobrogicus. Journal of Thermal Biology, 28, 545–550.

    Article  Google Scholar 

  • Gvoždík, L. (2005). Does reproduction influence temperature preferences in newts? Canadian Journal of Zoology, 83, 1038–1044.

    Article  Google Scholar 

  • Gvoždík, L., Puky, M., & Šugerková, M. (2007). Acclimation is beneficial at extreme test temperatures in the Danube crested newt, Triturus dobrogicus (Caudata, Salamandridae). Biological Journal of the Linnean Society, 90, 627–636.

    Article  Google Scholar 

  • Gvoždík, L., & Van Damme, R. (2008). The evolution of thermal performance curves in semi-aquatic newts: Thermal specialists on land and thermal generalists in water? Journal of Thermal Biology, 33, 395–403.

    Article  Google Scholar 

  • Hadamová, M., & Gvoždík, L. (2011). Seasonal acclimation of preferred body temperatures improves the opportunity for thermoregulation in newts. Physiological and Biochemical Zoology, 84, 166–174.

    Article  PubMed  Google Scholar 

  • Hertz, P. E., Huey, R. B., & Stevenson, R. D. (1993). Evaluating temperature regulation by field-active ectotherms: The fallacy of the inappropriate question. American Naturalist, 142, 796–818.

    Article  CAS  PubMed  Google Scholar 

  • Hochachka, P. W., & Somero, G. N. (2002). Biochemical adaptation: Mechanism and process in physiological evolution. Oxford: Oxford University Press.

    Google Scholar 

  • Huey, R. B. (1982). Temperature, physiology, and the ecology of reptiles. In C. Gans & F. H. Pough (Eds.), Biology of the reptilia, Physiology C, Physiological ecology (Vol. 12, pp. 25–91). London: Academic Press.

    Google Scholar 

  • Huey, R. B., & Bennett, A. F. (1987). Phylogenetic studies of coadaptation: Preferred temperatures versus optimal performance temperatures of lizards. Evolution, 41, 1098–1115.

    Article  Google Scholar 

  • Huey, R. B., & Bennett, A. F. (1990). Physiological adjustments to fluctuating thermal environments: An ecological and evolutionary perspective. In A. Morimoto, A. Tissieres, & C. Georgopoulus (Eds.), Stress proteins in biology and medicine (pp. 37–59). Spring: Cold Spring Harbor Laboratory Press.

    Google Scholar 

  • Huey, R. B., Kearney, M. R., Krockenberger, A., Holtum, J. A. M., Jess, M. & Williams S. E. (2012). Predicting organismal vulnerability to climate warming: Roles of behaviour, physiology, and adaptation. Philosophical Transactions of the Royal Society B, 367, 1665–1679.

    Article  Google Scholar 

  • Huey, R. B., & Stevenson, R. D. (1979). Integrating thermal physiology and ecology of ectotherms: A discussion of approaches. American Zoologist, 19, 357–366.

    Google Scholar 

  • Johnston, I. A., & Temple, G. K. (2002). Thermal plasticity of skeletal muscle phenotype in ectothermic vertebrates and its significance for locomotory behaviour. Journal of Experimental Biology, 205, 2305–2322.

    PubMed  Google Scholar 

  • Kelsch, S. W., & Neill, W. H. (1990). Temperature preference vs. acclimation in fishes: Selection for changing metabolic optima. Transactions of the American Fisheries Society, 119, 601–610.

    Article  Google Scholar 

  • Kurdíková, V., Smolinský, R., & Gvoždík, L. (2011). Mothers matter too: Benefits of temperature oviposition preferences in newts. PLoS ONE, 6, e23842.

    Article  PubMed Central  PubMed  Google Scholar 

  • Marek, V., & Gvoždík, L. (2012). The insensitivity of thermal preferences to various thermal gradient profiles in newts. Journal of Ethology, 30, 35–41.

    Article  Google Scholar 

  • Martin, T. L., & Huey, R. B. (2008). Why “suboptimal” is optimal: Jensen’s inequality and ectotherm thermal preferences. American Naturalist, 171, E102–E118.

    Article  PubMed  Google Scholar 

  • Muñoz, M. M., Stimola, M. A., Algar, A. C., Conover, A., Rodriguez, A. J., Landestoy, M. A., et al. (2014). Evolutionary stasis and lability in thermal physiology in a group of tropical lizards. Proceedings of the Royal Society B, 281, 20132433.

    Article  PubMed Central  PubMed  Google Scholar 

  • O’Meara, B. C., Ane, C., Sanderson, M. J., & Wainwright, P. C. (2006). Testing for different rates of continuous trait evolution using likelihood. Evolution, 60, 922–933.

    Article  PubMed  Google Scholar 

  • Paradis, E. (2006). Analysis of phylogenetics and evolution with R. New York: Springer.

    Google Scholar 

  • Pitchers, W., Wolf, J. B., Tregenza, T., Hunt, J., & Dworkin, I. (2014). Evolutionary rates for multivariate traits: The role of selection and genetic variation. Philosophical Transactions of the Royal Society B, 369, 20130252.

    Article  Google Scholar 

  • Pörtner, H. O. (2001). Climate change and temperature-dependent biogeography: Oxygen limitation of thermal tolerance in animals. Naturwissenschaften, 88, 137–146.

    Article  PubMed  Google Scholar 

  • Revell, L. J. (2012). Phytools: An R package for phylogenetic comparative biology (and other things). Methods in Ecology and Evolution, 3, 217–223.

    Article  Google Scholar 

  • Šamajová, P., & Gvoždík, L. (2009). The influence of temperature on diving behaviour in the alpine newt, Triturus alpestris. Journal of Thermal Biology, 34, 401–405.

    Article  Google Scholar 

  • Smolinský, R., & Gvoždík, L. (2009). The ontogenetic shift in thermoregulatory behaviour of newt larvae: Testing the ‘enemy-free temperatures’ hypothesis. Journal of Zoology, 279, 180–186.

    Article  Google Scholar 

  • Somero, G. N., Dahlhoff, E., & Lin, J. J. (1996). Stenotherms and eurytherms: Mechanisms establishing thermal optima and tolerance ranges. In I. A. Johnston & A. F. Bennett (Eds.), Animals and temperature: Phenotypic and evolutionary adaptation (pp. 53–78). Cambridge: Cambridge University Press.

    Chapter  Google Scholar 

  • Stevenson, R. D., Peterson, C. R., & Tsuji, J. S. (1985). The thermal dependence of locomotion, tongue flicking, digestion, and oxygen consumption in the wandering garter snake. Physiological Zoology, 58, 46–57.

    Google Scholar 

  • Van Damme, R., Bauwens, D., & Verheyen, R. F. (1991). The thermal dependence of feeding behaviour, food consumption and gut-passage time in the lizard Lacerta vivipara Jacquin. Functional Ecology, 5, 507–517.

    Article  Google Scholar 

  • Venables, W. N., & Ripley, B. D. (2002). Modern applied statistics with S. New York: Springer.

    Book  Google Scholar 

  • Vieites, D. R., Nieto-Roman, S., & Wake, D. B. (2009). Reconstruction of the climate envelopes of salamanders and their evolution through time. Proceedings of the National Academy of Sciences of the United States of America, 106, 19715–19722.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Vinšálková, T., & Gvoždík, L. (2007). Mismatch between temperature preferences and morphology in F1 hybrid newts (Triturus carnifex × T. dobrogicus). Journal of Thermal Biology, 32, 433–439.

    Article  Google Scholar 

  • Wiens, J. J., Sparreboom, M., & Arntzen, J. W. (2011). Crest evolution in newts: Implications for reconstruction methods, sexual selection, phenotypic plasticity and the origin of novelties. Journal of Evolutionary Biology, 24, 2073–2086.

    Article  CAS  PubMed  Google Scholar 

  • Williams, S. E., Shoo, L. P., Isaac, J. L., Hoffmann, A. A., & Langham, G. (2008). Towards an integrated framework for assessing the vulnerability of species to climate change. PLoS Biology, 6, 2621–2626.

    Article  CAS  PubMed  Google Scholar 

  • Yamamoto, A. H. (1994). Temperature preference of Drosophila immigrans and D. virilis: Intra- and inter-population genetic variation. Japanese Journal of Genetics, 69, 67–76.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

I thank the anonymous reviewers for their comments on the previous versions of this manuscript, R. Van Damme for a detailed presubmission review, and D. Adams for help with his R script. This study was funded by a grant from the Czech Science Foundation (P506/10/2170) and institutional support (RVO: 68081766).

Conflict of interest

The author declares that he has no conflicts of interest.

Ethical standard

The author declares that this paper complies with the current laws of the Czech Republic.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Lumír Gvoždík.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gvoždík, L. Mismatch Between Ectotherm Thermal Preferenda and Optima for Swimming: A Test of the Evolutionary Pace Hypothesis. Evol Biol 42, 137–145 (2015). https://doi.org/10.1007/s11692-015-9305-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11692-015-9305-z

Keywords

Navigation