Skip to main content Accessibility help
×
Hostname: page-component-76fb5796d-22dnz Total loading time: 0 Render date: 2024-04-28T14:46:34.854Z Has data issue: false hasContentIssue false

9 - Evolutionary physiology of insect thermal adaptation to cold environments

from PART II - ECOLOGICAL AND EVOLUTIONARY RESPONSES

Published online by Cambridge University Press:  04 May 2010

David L. Denlinger
Affiliation:
Ohio State University
Richard E. Lee, Jr
Affiliation:
Miami University
Get access

Summary

Introduction

Body temperature influences all aspects of the physiology and ecology of insects and indeed of all other ectotherms (Cossins and Bowler, 1987; Chown and Nicolson, 2004; Angilletta, 2009). Extreme low or high temperatures are physiologically damaging or even lethal, but temperatures well within those critical limits have profound effects on performance and fitness. Not surprisingly, an insect's thermal sensitivity plays a key role in its behavior, ecology and fitness.

Here I review several consequences of insect adaptation to low temperature. My focus is largely on organismal and population-level consequences. I take a macrophysiological approach (Chown et al., 2004) and focus on four key issues: some are classical, but others have only recently received attention: (a) Do optimal and critical temperatures correlate inversely with latitude, indicating that high-latitude species have adapted evolutionarily to low temperatures? (b) Are high-latitude species, which live in seasonal environments, physiologically adapted to a broader range of temperatures than are low-latitude species? (c) Do species with low optimal temperatures have the same maximal rates of population growth as do species with high optimal temperatures, as might occur if biochemical adaptation compensates fully for the thermodynamically depressing effects of low temperature? (d) Are cold-adapted, high-latitude species at greater risk from climate warming than are warm-adapted, low-latitude species, as might be expected given the faster rate of climate warming at high latitudes?

Type
Chapter
Information
Publisher: Cambridge University Press
Print publication year: 2010

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Addo-Bediako, A., Chown, S. L. and Gaston, K. J. (2000). Thermal tolerance, climatic variability and latitude. Proceedings of the Royal Society, Series B 267, 739–745.CrossRefGoogle ScholarPubMed
Angilletta, M. J. (2009). Thermal Adaptation: A Theoretical and Empirical Synthesis. Oxford, U.K.: Oxford University Press.CrossRefGoogle Scholar
Angilletta, M. J., Bennett, A. F., Guderley, H., Navas, C. A., Seebacher, F. and Wilson, R. S. (2006). Coadapation: a unifying principle in evolutionary thermal biology. Physiological and Biochemical Zoology 79, 282–294.CrossRefGoogle Scholar
Angilletta, M. J., Hill, T. and Robson, M. A. (2002). Is physiological performance optimized by thermoregulatory behavior?: a case study of the eastern fence lizard, Sceloporus undulatus. Journal of Thermal Biology 27, 199–204.CrossRefGoogle Scholar
Bakken, G. S. (1992). Measurement and application of operative and standard operative temperatures in ecology. American Zoologist 32, 194–216.CrossRefGoogle Scholar
Beck, S. D. (1980). Insect Photoperiodism. New York: Academic Press.Google Scholar
Bennett, A. F. (1987). Evolution of the control of body temperature: is warmer better? In Comparative Physiology: Life in Water and on Land, ed. Dejours, P., Taylor, C. R. and Weibel, E. R.. Padova, Italy: Liviana Press, pp. 421–431.Google Scholar
Bennett, A. F., Lenski, R. E. and Mittler, J. E. (1992). Evolutionary adaptation to temperature. I. Fitness responses of Escherichia coli to changes in its thermal environment. Evolution 46, 16–30.CrossRefGoogle ScholarPubMed
Bogert, C. M. (1949). Thermoregulation in reptiles, a factor in evolution. Evolution 3, 195–211.CrossRefGoogle Scholar
Bradshaw, W. E. and Holzapfel, C. M. (2001). Genetic shift in photoperiodic response correlated with global warming. Proceedings of the National Academy of Sciences, USA 98, 14509–14511.CrossRefGoogle ScholarPubMed
Bradshaw, W. E. and Holzapfel, C. M. (2006). Evolutionary response to rapid climate change. Science 312, 1477–1478.CrossRefGoogle ScholarPubMed
Bradshaw, W. E., Zani, P. A. and Holzapfel, C. M. (2004). Adaptation to temperate climates. Evolution 58, 1748–1762.CrossRefGoogle ScholarPubMed
Brett, J. R. (1970). Temperature, fishes. In Marine Ecology vol. 1, ed. Kinne, O.. New York, NY: John Wiley & Sons, pp. 515–560.Google Scholar
Carey, J. R. (1993). Applied Demography for Biologists. Oxford: Oxford University Press.Google Scholar
Charlesworth, B. (1994). Evolution in Age-structured Populations, 2nd edn. Cambridge, UK: Cambridge University Press.CrossRefGoogle Scholar
Chen, C.-P., Lee, R. E. and Denlinger, D. L. (1990). A comparison of the responses of tropical and temperate flies (Diptera: Sarcophagidae) to cold and heat stress. Journal of Comparative Physiology B 160, 543–547.CrossRefGoogle Scholar
Chown, S. L., Gaston, K. J. and Robinson, D. (2004). Macrophysiology: large-scale patterns in physiological traits and their ecological implications. Functional Ecology 18, 159–167.CrossRefGoogle Scholar
Chown, S. L., Jumbam, K. R., Sørensen, J. G. and Terblanche, J. S. (2008). Phenotypic variance, plasticity and heritability estimates of critical thermal limits depend on methodological context. Functional Ecology 22, 1–8.Google Scholar
Chown, S. L. and Nicolson, S. W. (2004). Insect Physiological Ecology. Mechanisms and Patterns. Oxford: Oxford University Press.CrossRefGoogle Scholar
Clarke, A. (2006). Temperature and the metabolic theory of ecology. Functional Ecology 20, 405–412.CrossRefGoogle Scholar
Cossins, A. R. and Bowler, K. (1987). Temperature Biology of Animals. New York, NY: Chapman & Hall.CrossRefGoogle Scholar
Crozier, L. and Dwyer, G. (2006). Combining population-dynamic and ecophysiological models to predict climate-induced insect range shifts. American Naturalist 167, 853–866.Google ScholarPubMed
Davis, A., Lawton, J., Shorrocks, B. and Jenkinson, L. (1998). Individualistic species responses invalidate simple physiological models of community dynamics under global environmental change. Journal of Animal Ecology 67, 600–612.CrossRefGoogle Scholar
Denlinger, D. L., Giebultowicz, J. M. and Saunders, D. S. (eds.) (2001). Insect Timing: Circadian Rhythmicity to Seasonality. Amsterdam: Elsevier.
Deutsch, C. A., Tewksbury, J. J., Huey, R. B., Sheldon, K. S., Ghalambor, C. K., Haak, D. C. and Martin, P. R. (2008). Impacts of climate warming on terrestrial ectotherms across latitude. Proceedings of the National Academy of Sciences, USA. 105, 6668–6672.CrossRefGoogle ScholarPubMed
Frazier, M. R., Huey, R. B. and Berrigan, D. (2006). Thermodynamics constrains the evolution of insect population growth rates: “warmer is better”. American Naturalist 168, 512–520.CrossRefGoogle Scholar
Garland, T. (1994). Phylogenetic analyses of lizard endurance capacity in relation to body size and body temperature. In Lizard Ecology: Historical and Experimental Perspectives, ed. Vitt, L. J. and Pianka, E. R.. Princeton, NJ: Princeton University Press, pp. 237–259.Google Scholar
Ghalambor, C. K., Huey, R. B., Martin, P. R., Tewksbury, J. J. and Wang, G. (2006). Are mountain passes higher in the tropics? Janzen's hypothesis revisited. Integrative and Comparative Biology 46, 5–17.CrossRefGoogle ScholarPubMed
Gibert, P., Moreteau, B., Pla, E., Petavy, G., Karan, D. and David, J. R. (2001). Chill-coma tolerance, a major climatic adaptation among Drosophila species. Evolution 55, 1063–1068.CrossRefGoogle Scholar
Gilchrist, G. W. (1995). Specialists and generalists in changing environments. I. Fitness landscapes of thermal sensitivity. American Naturalist 146, 252–270.CrossRefGoogle Scholar
Gilchrist, G. W. (1996). Quantitative genetic analysis of the thermal sensitivity of locomotory performance curve of Aphidius ervi. Evolution 50, 1560–1572.CrossRefGoogle Scholar
Goto, S. G. and Kimura, M. T. (1988). Heat- and cold-shock responses and temperature adaptations in subtropical and temperate species of Drosophila. Journal of Insect Physiology 44, 1233–1239.CrossRefGoogle Scholar
Gould, S. J. and Lewontin, R. C. (1979). The spandrels of San Marcos and the Panglossian paradigm – a critique of the adaptationist program. Proceedings of the Royal Society, Series B 205, 581–598.CrossRefGoogle Scholar
Hamilton, W. J. (1973). Life's Color Code. New York, NY: McGraw Hill.Google Scholar
Heinrich, B. (1981). Insect Thermoregulation. New York: John Wiley & Sons, Inc.Google Scholar
Helmuth, B., Kingsolver, J. G. and Carrington, E. (2005). Biophysics, physiological ecology and climate change: does mechanism matter?Annual Review of Physiology 67, 177–201.CrossRefGoogle ScholarPubMed
Hertz, P. E., Huey, R. B. and Nevo, E. (1983). Homage to Santa Anita: thermal sensitivity of sprint speed in agamid lizards. Evolution 37, 1075–1084.CrossRefGoogle ScholarPubMed
Hochachka, P. W. and Somero, G. N. (2002). Biochemical Adaptation: Mechanism and Process in Physiological Evolution. New York: Oxford University Press.Google Scholar
Hoffmann, A. A. and Blows, M. W. (1993). Evolutionary genetics and climate change: will animals adapt to global warming? In Biotic Interactions and Global Change, ed. Kareiva, P. M., Kingsolver, J. G. and Huey, R. B.. Sunderland., MA: Sinauer Assoc., pp. 165–178.Google Scholar
Hoffmann, A. A., Sørensen, J. G. and Loeschcke, V. (2003). Adaptation of Drosophila to temperature extremes: bringing together quantitative and molecular approaches. Journal of Thermal Biology 26, 175–216.CrossRefGoogle Scholar
Hoffmann, A. A. and Watson, M. (1993). Geographical variation in the acclimation responses of Drosophila to temperature extremes. American Naturalist 142, S93–S113.CrossRefGoogle ScholarPubMed
Huey, R. B. (1987). Phylogeny, history and the comparative method. In New Directions in Ecological Physiology, ed. Feder, M. E., Bennett, A. F., Burggren, W. W. and Huey, R. B.. Cambridge, UK: Cambridge University Press, pp. 76–98.Google Scholar
Huey, R. B. and Bennett, A. F. (1987). Phylogenetic studies of coadaptation: preferred temperatures versus optimal performance temperatures of lizards. Evolution 41, 1098–1115.CrossRefGoogle ScholarPubMed
Huey, R. B. and Berrigan, D. (2001). Temperature, demography and ectotherm fitness. American Naturalist 158, 204–210.CrossRefGoogle ScholarPubMed
Huey, R. B. and Hertz, P. E. (1984). Is a jack-of-all-temperatures a master of none?Evolution 38, 41–50.CrossRefGoogle ScholarPubMed
Huey, R. B., Hertz, P. E. and Sinervo, B. (2003). Behavioral drive versus behavioral inertia: a null model approach. American Naturalist 161, 357–366.CrossRefGoogle ScholarPubMed
Huey, R. B. and Kingsolver, J. G. (1989). Evolution of thermal sensitivity of ectotherm performance. Trends in Ecology and Evolution 4, 131–135.CrossRefGoogle ScholarPubMed
Huey, R. B. and Rosenzweig, F. (2009). Laboratory evolution meets Catch 22: balancing simplicity and realism. In Experimental Evolution: Concepts, Methods and Applications, ed. Garland, Jr. T. and Rose, M. R.. Berkeley: University of California Press, pp. 671–701.Google Scholar
Huey, R. B. and Slatkin, M. (1976). Costs and benefits of lizard thermoregulation. Quarterly Review of Biology 51, 363–384.CrossRefGoogle ScholarPubMed
Huey, R. B. and Stevenson, R. D. (1979). Integrating thermal physiology and ecology of ectotherms: a discussion of approaches. American Zoologist 19, 357–366.CrossRefGoogle Scholar
,IPPC (2007). Climate Change 2007: The Physical Science Basis. Cambridge: Cambridge University Press.Google Scholar
Irwin, J. T. and Lee, R. E.. (2003). Cold winter microenvironments conserve energy and improve overwintering survival and potential fecundity of the goldenrod gall fly, Eurosta solidaginis. Oikos 100, 71–78.CrossRefGoogle Scholar
Izem, R. and Kingsolver, J. G. (2005). Variation in continuous reaction norms: quantifying directions of biological interest. American Naturalist 166, 277–289.CrossRefGoogle ScholarPubMed
Janzen, D. H. (1967). Why mountain passes are higher in the tropics. American Naturalist 101, 233–249.CrossRefGoogle Scholar
Kingsolver, J. G. and Gomulkiewicz, R. (2004). Environmental variation and selection on performance curves. Integrative and Comparative Biology 43, 470–477.CrossRefGoogle Scholar
Kingsolver, J. G. and Huey, R. B. (1998). Evolutionary analyses of morphological and physiological plasticity in thermally variable environments. American Zoologist 38, 323–336.CrossRefGoogle Scholar
Kingsolver, J. G. and Huey, R. B. (2008). Size, temperature, and fitness: three rules. Evolutionary Ecology Research 10, 251–268.Google Scholar
Kingsolver, J. G. and Nagle, A. M. (2007). Rapid divergence of thermal sensitivity and diapause in field and laboratory populations of Manduca sexta. Physiological and Biochemical Zoology 80, 473–479.CrossRefGoogle Scholar
Kingsolver, J. G., Ragland, G. J. and Shlichta, J. G. (2004). Quantitative genetics of continuous reaction norms: thermal sensitivity of caterpillar growth rates. Evolution 58, 1521–1529.CrossRefGoogle ScholarPubMed
Klok, C. J. and Chown, S. L. (1997). Critical thermal limits, temperature tolerance and water balance of a sub-Antarctic caterpillar, Pringleophaga marioni Viette (Lepidoptera: Tineidae). Journal of Insect Physiology 43, 685–694.CrossRefGoogle Scholar
Lee, R. E. and Denlinger, D. L. (1991). Insects at Low Temperature. New York: Chapman & Hall.CrossRefGoogle Scholar
Lee, R. E. and Denlinger, D. L. (2006). Entomology on the Antarctic Peninsula: the southernmost insect. American Entomologist 52, 84–89.CrossRefGoogle Scholar
Levins, R. (1968). Evolution in Changing Environments. Princeton, NJ: Princeton University Press.Google Scholar
MacArthur, R. H. (1984). Geographical Ecology: Patterns in the Distribution of Species. Princeton, NJ: Princeton University Press.Google Scholar
Palaima, A. and Spitze, K. (2004). Is a jack-of-all temperatures a master of none? An experimental test with Daphnia pulicaria (Crustacea: Cladocera). Evolutionary Ecology Research 6, 215–225.Google Scholar
Parmesan, C. (2006). Ecological and evolutionary responses to recent climate change. Annual Review of Ecology and Systematics 37, 637–669.CrossRefGoogle Scholar
Pörtner, H. O. (2002). Climate variations and the physiological basis of temperature dependent biogeography: tradeoffs in muscle design and performance in polar ectotherms. Journal of Experimental Biology 205, 2217–2254.Google Scholar
Pörtner, H. O., Peck, L. and Somero, G. (2007). Thermal limits and adaptation in marine Antarctic ectotherms: an integrative view. Philosophical Transactions of the Royal Society B 362, 2233–2258.CrossRefGoogle Scholar
Price, P. W., Fernandes, G. W., Lara, A. C. F. and Brawn, J. (1998). Global patterns in the local number of insect galling species. Journal of Biogeography 25, 581–591.CrossRefGoogle Scholar
Ragland, G. J. and Kingsolver, J. G. (2008). Evolution of thermotolerance in seasonal environments: the effects of annual temperature variation and life-history timing in Wyeomyia smithii. Evolution 62, 1345–1357.CrossRefGoogle ScholarPubMed
Root, T. L., Price, J. T., Hall, K. R., Schneider, S. H., Rosenzweig, C. and Pounds, J. L. (2003). Fingerprints of global warming on wild animals and plants. Nature 421, 37–42.CrossRefGoogle ScholarPubMed
Savage, V. M., Gillooly, J. F., Brown, J. H., West, G. B. and Charnov, E. L. (2004). Effects of body size and temperature on population growth. American Naturalist 163, 429–441.CrossRefGoogle ScholarPubMed
Tewksbury, J. J., Huey, R. B. and Deutsch, C. A. (2008). Putting the heat on tropical animals. Science 320, 1296–1297.CrossRefGoogle ScholarPubMed
Asch, M. and Visser, M. E. (2007). Phenology of forest caterpillars and their host trees: the importance of synchrony. Annual Review of Entomology 52, 37–55.CrossRefGoogle Scholar
Berkum, F. H. (1988). Latitudinal patterns of the thermal sensitivity of sprint speed in lizards. American Naturalist 132, 327–343.CrossRefGoogle Scholar
Williams, J. B., Shorthouse, J. D. and Lee, R. E.. (2003). Deleterious effects of mild simulated overwintering temperatures on survival and potential fecundity of rose-galling Diplolepis wasps (Hymenoptera: Cynipidae). Journal of Experimental Zoology 298A, 23–31.CrossRefGoogle Scholar
Williams, S. E., Shoo, L. P., Isaac, J. L., Hoffmann, A. A. and Langham, G. (2008). Toward an integrated framework for assessing the vulnerability of species to climate change. PLoS Biology 6, 2621–2626.CrossRefGoogle Scholar
Wilson, B. S. and Cooke, D. E. (2001). Latitudinal variation in rates of overwinter mortality in the lizard Uta stansburiana. Ecology 85, 3406–3417.CrossRefGoogle Scholar
Zani, P. A. (2008). Climate-change trade-offs in the side-blotched lizard (Uta stansburiana): effects of growing-season length and mild temperatures on winter survival. Physiological and Biochemical Zoology 81, 797–809.CrossRefGoogle ScholarPubMed
Zani, P. A., Swanson, S. E. T., Corbin, D., Cohnstaedt, L. W., Agotsch, M. D., Bradshaw, W. E. and Holzapfel, C. M. (2005). Geographic variation in tolerance of transient thermal stress in the mosquito Wyeomyia smithii. Ecology 86, 1206–1211.CrossRefGoogle Scholar

Save book to Kindle

To save this book to your Kindle, first ensure coreplatform@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Available formats
×

Save book to Dropbox

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Dropbox.

Available formats
×

Save book to Google Drive

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Google Drive.

Available formats
×