Skip to main content

Disentangling the Consequences of Growth Temperature and Adult Acclimation Temperature on Starvation and Thermal Tolerance in the Red Flour Beetle

Abstract

Temperature affects most aspects of animal life, and impacts particularly strongly on ectotherms. We studied the combined effects of growth temperature and adult acclimation temperature on starvation tolerance, cold tolerance, and heat tolerance in the red flour beetle. A lower adult acclimation temperature enhanced starvation tolerance and cold tolerance and impaired heat tolerance. This is an expected outcome of short-term plasticity and of the beneficial acclimation hypothesis. The higher growth temperature led to improved performance of all three measured traits: beetles raised under higher temperature tolerated starvation longer and showed better cold and heat tolerance. While this result fits well the rule “hotter is better”, it is nonetheless surprising that the same temperature had opposite effects when experienced by juveniles and adults (i.e., the effect of the warm temperature on cold tolerance). We emphasize the importance of separating between the juvenile growth temperature (developmental plasticity) and adult temperature (acclimation), as they can have opposite effects on adult performance.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3

References

  • Abramoff, M. D., Magalhaes, P. J., & Ram, S. J. (2004). Image processing with ImageJ. Biophotonics International, 11, 36–42.

    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 

  • Bowler, K. (2005). Acclimation, heat shock and hardening. Journal of Thermal Biology, 30, 125–130.

    Article  Google Scholar 

  • Bradley, B. P. (1978). Increase in range of temperature tolerance by acclimation in the copepod Eurytemora affinis. Biological Bulletin, 154, 177–187.

    Article  Google Scholar 

  • Bubliy, O. A., Kristensen, T. N., Kellermann, V., & Loeschcke, V. (2012). Plastic responses to four environmental stresses and cross-resistance in a laboratory population of Drosophila melanogaster. Functional Ecology, 26, 245–253.

    Article  Google Scholar 

  • Campbell, J. F., & Runnion, C. (2003). Patch exploitation by female red flour beetles, Tribolium castaneum. Journal of Insect Science, 3, 20.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Campbell, J. F., Toews, M. D., Arthur, F. H., & Arbogast, R. T. (2010). Long-term monitoring of Tribolium castaneum in two flour mills: Seasonal patterns and impact of fumigation. Journal of Economic Entomology, 103, 991–1001.

    Article  PubMed  Google Scholar 

  • Chen, C. P., Lee, R. E., & Denlinger, D. L. (1991). Cold shock and heat shock: A comparison of the protection generated by brief pretreatment at less severe temperatures. Physiological Entomology, 16, 19–26.

    Article  Google Scholar 

  • Clark, M. S., & Worland, M. R. (2008). How insects survive the cold: Molecular mechanisms—A review. Journal of Comparative Physiology B, 178, 917–933.

    Article  CAS  Google Scholar 

  • Colinet, H., & Hoffmann, A. A. (2012). Comparing phenotypic effects and molecular correlates of developmental, gradual and rapid cold acclimation responses in Drosophila melanogaster. Functional Ecology, 26, 84–93.

    Article  Google Scholar 

  • David, R. J., Gibert, P., Pla, E., Petavy, G., Karan, D., & Moreteau, B. (1998). Cold stress tolerance in Drosophila: Analysis of chill coma recovery in D. melanogaster. Journal of Thermal Biology, 23, 291–299.

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • DeWitt, T. S., & Scheiner, S. M. (2004). Phenotypic variation from single genotypes: A primer. In T. S. DeWitt & S. M. Scheiner (Eds.), Phenotypic plasticity: Functional and conceptual approaches (pp. 1–9). Oxford, UK: Oxford University Press.

    Google Scholar 

  • Dhileepan, K., Treviño, M., & Raghu, S. (2005). Effect of temperature on the survival of Aconophora compressa Walker (Hemiptera: Membracidae): Implications for weed biocontrol. Australian Journal of Entomology, 44, 457–462.

    Article  Google Scholar 

  • Edwards, D. K. (1958). Effects of acclimitization and sex on respiration and thermal resistance in Tribolium (Coleoptera: Tenebrionidae). Canadian Journal of Zoology, 36, 363–382.

    Article  Google Scholar 

  • Fischer, K., Eenhoorn, E., Bot, A. N. M., Brakefield, P. M., & Zwaan, B. J. (2003). Cooler butterflies lay larger eggs: Developmental plasticity versus acclimation. Proceedings of the Royal Society of London, Series B: Biological Sciences, 270, 2051–2056.

    Article  Google Scholar 

  • Geister, T. L., & Fischer, K. (2007). Testing the beneficial acclimation hypothesis: Temperature effects on mating success in a butterfly. Behavioral Ecology, 18, 658–664.

    Article  Google Scholar 

  • Gibert, P., Huey, R. B., & Gilchrist, G. W. (2001a). Locomotor performance of Drosophila melanogaster: Interactions among developmental and adult temperatures, age, and geography. Evolution, 55, 205–209.

    Article  CAS  PubMed  Google Scholar 

  • Gibert, P., Moreteau, B., Petavy, G., Karan, D., & David, J. R. (2001b). Chill-coma tolerance, a major climatic adaptation among Drosophila species. Evolution, 55, 1063–1068.

    Article  CAS  PubMed  Google Scholar 

  • Gilchrist, G. W., & Huey, R. B. (2001). Parental and developmental temperature effects on the thermal dependence of fitness in Drosophila melanogaster. Evolution, 55, 209–214.

    Article  CAS  PubMed  Google Scholar 

  • Grazer, V. M., & Martin, O. Y. (2012). Elevated temperature changes female costs and benefits of reproduction. Evolutionary Ecology, 26, 625–637.

    Article  Google Scholar 

  • Hoffmann, A. A., Dagher, H., Hercus, M., & Berrigan, D. (1997). Comparing different measures of heat resistance in selected lines of Drosophila melanogaster. Journal of Insect Physiology, 43, 393–405.

    Article  CAS  PubMed  Google Scholar 

  • Hoffmann, A. A., Hallas, R., Anderson, A. R., & Telonis-Scott, M. (2005). Evidence for a robust sex-specific trade-off between cold resistance and starvation resistance in Drosophila melanogaster. Journal of Evolutionary Biology, 18, 804–810.

    Article  CAS  PubMed  Google Scholar 

  • Huey, R. B., & Berrigan, D. (1996). Testing evolutionary hypotheses of acclimation. In I. S. Johnston & A. F. Bennett (Eds.), Animals and temperature: Phenotypic and evolutionary adaptation (pp. 205–237). Cambridge, UK: Cambridge University Press.

    Chapter  Google Scholar 

  • Huey, R. B., Berrigan, D., Gilchrist, G. W., & Herron, J. C. (1999). Testing the adaptive significance of acclimation: A strong inference hypothesis. American Zoologist, 39, 323–336.

    Google Scholar 

  • Huey, R. B., Crill, W. D., Kingsolver, J. G., & Weber, K. E. (1992). A method for rapid measurement of heat or cold resistance of small insects. Functional Ecology, 6, 489–494.

    Article  Google Scholar 

  • Huey, R. B., Wakefield, T., Crill, W. D., & Gilchrist, G. W. (1995). Within- and between-generation effects of temperature on early fecundity of Drosophila melanogaster. Heredity, 74, 216–223.

  • Jensen, D., Overgaard, J., & Sørensen, J. G. (2007). The influence of developmental stage on cold shock resistance and ability to cold-harden in Drosophila melanogaster. Journal of Insect Physiology, 53, 186–197.

    Article  Google Scholar 

  • Karl, I., & Fischer, K. (2009). Altitudinal and environmental variation in lifespan in the Copper butterfly Lycaena tityrus. Functional Ecology, 23, 1132–1138.

    Article  Google Scholar 

  • Kenny, M. C., Wilton, A., & Ballard, J. W. O. (2008). Seasonal trade-off between starvation resistance and cold resistance in temperate wild-caught Drosophila simulans. Australian Journal of Entomology, 47, 20–23.

    Article  Google Scholar 

  • Kingsolver, J. G., & Huey, R. B. (2008). Size, temperature, and fitness: Three rules. Evolutionary Ecology Research, 10, 251–268.

    Google Scholar 

  • Krasnov, B., Ward, D., & Shenbrot, G. (1996). Body size and leg length variation in several species of darkling beetles (Coleoptera: Tenebrionidae) along a rainfall and altitudinal gradient in the Negev Desert (Israel). Journal of Arid Environments, 34, 477–489.

    Article  Google Scholar 

  • Leroi, A. M., Bennett, A. F., & Lenski, R. E. (1994). Temperature acclimation and competitive fitness: An experimental test of the beneficial acclimation assumption. Proceedings of the National Academy of Sciences of the United States of America, 91, 1917–1921.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • MacMillan, H. A., & Sinclair, B. J. (2011). Mechanisms underlying insect chill-coma. Journal of Insect Physiology, 57, 12–20.

    Article  CAS  PubMed  Google Scholar 

  • MacMillan, H. A., Walsh, J. P., & Sinclair, B. J. (2009). The effects of selection for cold tolerance on cross-tolerance to other environmental stressors in Drosophila melanogaster. Insect Science, 16, 263–276.

    Article  Google Scholar 

  • MacMillan, H. A., Williams, C. M., Staples, J. F., & Sinclair, B. J. (2012). Reestablishment of ion homeostasis during chill-coma recovery in the cricket Gryllus pennsylvanicus. Proceedings of the National Academy of Sciences of the United States of America, 109, 20750–20755.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Maysov, A., & Kipyatkov, V. E. (2009). Critical thermal minima, their spatial and temporal variation and response to hardening in Myrmica ants. CryoLetters, 30, 29–40.

    PubMed  Google Scholar 

  • Milutinović, B., Stolpe, C., Peuß, R., Armitage, S. A. O., & Kurtz, J. (2013). The red flour beetle as a model for bacterial oral infections. PLoS One, 8, e64638.

    Article  PubMed Central  PubMed  Google Scholar 

  • Modlmeier, A. P., Foitzik, S., & Scharf, I. (2013). Starvation endurance in the ant Temnothorax nylanderi depends on group size, body size and access to larvae. Physiological Entomology, 38, 89–94.

    Article  Google Scholar 

  • Modlmeier, A. P., Pamminger, T., Foitzik, S., & Scharf, I. (2012). Cold resistance depends on acclimation and behavioral caste in a temperate ant. Naturwissenschaften, 99, 811–819.

    Article  CAS  PubMed  Google Scholar 

  • Pijpe, J., Brakefield, P. M., & Zwaan, B. J. (2007). Phenotypic plasticity of starvation resistance in the butterfly Bicyclus anynana. Evolutionary Ecology, 21, 589–600.

    Article  Google Scholar 

  • Ransberry, V. E., MacMillan, H. A., & Sinclair, B. J. (2011). The relationship between chill-coma onset and recovery at the extremes of the thermal window of Drosophila melanogaster. Physiological and Biochemical Zoology, 84, 553–559.

    Article  PubMed  Google Scholar 

  • Relyea, R. A., & Auld, J. R. (2004). Having the guts to compete: How intestinal plasticity explains costs of inducible defences. Ecology Letters, 7, 869–875.

    Article  Google Scholar 

  • Renault, D., Salin, C., Vannier, G., & Vernon, P. (2002). Survival at low temperatures in insects: What is the ecological significance of the supercooling point? CryoLetters, 23, 217–228.

    CAS  PubMed  Google Scholar 

  • Rion, S., & Kawecki, T. J. (2007). Evolutionary biology of starvation resistance: What we have learned from Drosophila. Journal of Evolutionary Biology, 20, 1655–1664.

    Article  CAS  PubMed  Google Scholar 

  • Robinson, S. J. W., Zwaan, B., & Partridge, L. (2000). Starvation resistance and adult body composition in a latitudinal cline of Drosophila melanogaster. Evolution, 54, 1819–1824.

    Article  CAS  PubMed  Google Scholar 

  • Santos, M. (2007). Evolution of total net fitness in thermal lines: Drosophila subobscura likes it “warm”. Journal of Evolutionary Biology, 20, 2361–2370.

    Article  CAS  PubMed  Google Scholar 

  • Scharf, I., Filin, I., Ben-Yehoshua, D., & Ovadia, O. (2009). Phenotypic plasticity and variation in morphological and life-history traits of antlion adults across a climatic gradient. Zoology, 112, 139–150.

    Article  PubMed  Google Scholar 

  • Scharf, I., Sbilordo, S. H., & Martin, O. Y. (2014). Cold tolerance in flour beetle species differing in body size and selection temperature. Physiol Entomol, 39, 80–87.

    Article  Google Scholar 

  • Sejerkilde, M., Sørensen, J. G., & Loeschcke, V. (2003). Effects of cold- and heat hardening on thermal resistance in Drosophila melanogaster. Journal of Insect Physiology, 49, 719–726.

    Article  CAS  PubMed  Google Scholar 

  • Sokoloff, A. (1974). The Biology of Tribolium (Vol. 2). Oxford: Oxford University Press.

    Google Scholar 

  • Teets, N. M., & Denlinger, D. L. (2013). Physiological mechanisms of seasonal and rapid cold-hardening in insects. Physiological Entomology, 38, 105–116.

    Article  CAS  Google Scholar 

  • Terblanche, J. S., & Chown, S. L. (2006). The relative contributions of developmental plasticity and adult acclimation to physiological variation in the tsetse fly, Glossina pallidipes (Diptera, Glossinidae). Journal of Experimental Biology, 209, 1064–1073.

    Article  PubMed Central  PubMed  Google Scholar 

  • Van Buskirk, J. (2002). A comparative test of the adaptive plasticity hypothesis: Relationships between habitat and phenotype in Anuran larvae. The American Naturalist, 160, 87–102.

    Article  PubMed  Google Scholar 

  • Van Dijk, P. L. M., Staaks, G., & Hardewig, I. (2002). The effect of fasting and refeeding on temperature preference, activity and growth of roach, Rutilus rutilus. Oecologia, 130, 496–504.

    Article  Google Scholar 

  • Wang, T., Hung, C. C. Y., & Randall, D. J. (2006). The comparative physiology of food deprivation: From feast to famine. Annual Review of Physiology, 68, 223–251.

    Article  PubMed  Google Scholar 

  • Wilson, R. S., & Franklin, C. E. (2002). Testing the beneficial acclimation hypothesis. Trends in Ecology & Evolution, 17, 66–70.

    Article  Google Scholar 

  • Woods, H. A., & Harrison, J. F. (2001). The beneficial acclimation hypothesis versus acclimation of specific traits: Physiological change in water-stressed Manduca sexta caterpillars. Physiological and Biochemical Zoology, 74, 32–44.

    Article  CAS  PubMed  Google Scholar 

  • Woods, H. A., & Harrison, J. F. (2002). Interpreting rejections of the beneficial acclimation hypothesis: When is physiological plasticity adaptive? Evolution, 56, 1863–1866.

    Article  PubMed  Google Scholar 

  • Young, A. M. (1970). Predation and abundance in populations of flour beetles. Ecology, 51, 602–619.

    Article  Google Scholar 

  • Zamudio, K. R., Huey, R. B., & Crill, W. D. (1995). Bigger isn’t always better: Body-size, developmental and parental temperature and male territorial success in Drosophila melanogaster. Animal Behaviour, 49, 671–677.

    Article  Google Scholar 

  • Zehnder, C. B., Parris, M. A., & Hunter, M. D. (2007). Effects of maternal age and environment on offspring vital rates in the Oleander Aphid (Hemiptera: Aphididae). Environmental Entomology, 36, 910–917.

    Article  PubMed  Google Scholar 

  • Zeilstra, I., & Fischer, K. (2005). Cold tolerance in relation to developmental and adult temperature in a butterfly. Physiological Entomology, 30, 92–95.

    Article  Google Scholar 

Download references

Acknowledgments

The research leading to these results received funding from the People Programme (Marie Curie Actions) of the European Union’s Seventh Framework Programme (FP7/2007-2013) under REA Grant agreement no [333442]. We are also grateful to Aziz Subach, Oliver Martin, Ofer Ovadia and Roi Dor for their assistance in the laboratory and/or for thorough discussions, which helped with the design and interpretation of this study. We are grateful too to Naomi Paz for English editing, and to Moshe Kostyukovsky for kindly supplying the initial stock of flour beetles.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Inon Scharf.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 12 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Scharf, I., Galkin, N. & Halle, S. Disentangling the Consequences of Growth Temperature and Adult Acclimation Temperature on Starvation and Thermal Tolerance in the Red Flour Beetle. Evol Biol 42, 54–62 (2015). https://doi.org/10.1007/s11692-014-9298-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11692-014-9298-z

Keywords

  • Chill-coma recovery
  • Heat knockdown
  • Hotter is better
  • Starvation endurance
  • Stress
  • Survival
  • Tribolium