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Meta-analysis reveals weak but pervasive plasticity in insect thermal limits

  • IPCC. Assessment Report 6 Climate Change 2021: The Physical Science Basis. (2021).

  • Angilletta, M. J. Thermal adaptation: a theoretical and empirical synthesis. Oxford University Press (Elsevier, 2009).

  • Sunday, J. M. et al. Thermal-safety margins and the necessity of thermoregulatory behavior across latitude and elevation. Proc. Natl Acad. Sci. USA 111, 5610–5615 (2014).

    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Hampe, A. & Petit, R. J. Conserving biodiversity under climate change: the rear edge matters. Ecol. Lett. 8, 461–467 (2005).

    PubMed 

    Google Scholar 

  • Parmesan, C. Ecological and evolutionary responses to recent climate change. Annu. Rev. Ecol. Evol. Syst. 37, 637–669 (2006).

    Google Scholar 

  • Ma, C. S., Ma, G. & Pincebourde, S. Survive a warming climate: insect responses to extreme high temperatures. Annu. Rev. Entomol. 66, 163–184 (2021).

    CAS 
    PubMed 

    Google Scholar 

  • Hoffmann, A. A., Sørensen, J. G. & Loeschcke, V. Adaptation of Drosophila to temperature extremes: Bringing together quantitative and molecular approaches. J. Therm. Biol. 28, 175–216 (2003).

    Google Scholar 

  • Oostra, V., Saastamoinen, M., Zwaan, B. J. & Wheat, C. W. Strong phenotypic plasticity limits potential for evolutionary responses to climate change. Nat. Commun. 9, 1005 (2018).

  • Štětina, T., Koštál, V. & Korbelová, J. The role of inducible Hsp70, and other heat shock proteins, in adaptive complex of cold tolerance of the fruit fly (Drosophila melanogaster). PLoS One 10, 1–22 (2015).

    Google Scholar 

  • Overgaard, J., Sørensen, J. G., Petersen, S. O., Loeschcke, V. & Holmstrup, M. Changes in membrane lipid composition following rapid cold hardening in Drosophila melanogaster. J. Insect Physiol. 51, 1173–1182 (2005).

    CAS 
    PubMed 

    Google Scholar 

  • Laland, K. N. et al. The extended evolutionary synthesis: Its structure, assumptions and predictions. Proc. R. Soc. B Biol. Sci. 282, 20151019 (2015).

  • Sánchez-Bayo, F. & Wyckhuys, K. A. G. Worldwide decline of the entomofauna: A review of its drivers. Biol. Conserv. 232, 8–27 (2019).

    Google Scholar 

  • Deutsch, C. A. et al. Increase in crop losses to insect pests in a warming climate. Science 361, 916–919 (2018).

    ADS 
    CAS 
    PubMed 

    Google Scholar 

  • Sgrò, C. M., Terblanche, J. S. & Hoffmann, A. A. What can plasticity contribute to insect responses to climate change? Annu. Rev. Entomol. 61, 433–451 (2016).

    PubMed 

    Google Scholar 

  • Sørensen, J. G., Kristensen, T. N. & Overgaard, J. Evolutionary and ecological patterns of thermal acclimation capacity in Drosophila: is it important for keeping up with climate change? Curr. Opin. Insect Sci. 17, 98–104 (2016).

    PubMed 

    Google Scholar 

  • Gunderson, A. R. & Stillman, J. H. Plasticity in thermal tolerance has limited potential to buffer ectotherms from global warming. Proc. R. Soc. B Biol. Sci. 282, 20150401 (2015).

  • Rohr, J. R. et al. The complex drivers of thermal acclimation and breadth in ectotherms. Ecol. Lett. 21, 1425–1439 (2018).

    PubMed 

    Google Scholar 

  • Gunderson, A. R., Dillon, M. E. & Stillman, J. H. Estimating the benefits of plasticity in ectotherm heat tolerance under natural thermal variability. Funct. Ecol. 31, 1529–1539 (2017).

    Google Scholar 

  • Barley, J. M. et al. Limited plasticity in thermally tolerant ectotherm populations: Evidence for a trade-off. Proc. R. Soc. B Biol. Sci. 288, 20210765 (2021).

    Google Scholar 

  • Morley, S. A., Peck, L. S., Sunday, J. M., Heiser, S. & Bates, A. E. Physiological acclimation and persistence of ectothermic species under extreme heat events. Glob. Ecol. Biogeogr. 28, 1018–1037 (2019).

    Google Scholar 

  • Kellermann, V. & van Heerwaarden, B. Terrestrial insects and climate change: adaptive responses in key traits. Physiol. Entomol. 44, 99–115 (2019).

    Google Scholar 

  • Seebacher, F., White, C. R. & Franklin, C. E. Physiological plasticity increases resilience of ectothermic animals to climate change. Nat. Clim. Chang. 5, 61–66 (2015).

    ADS 

    Google Scholar 

  • Pincebourde, S. & Woods, H. A. There is plenty of room at the bottom: microclimates drive insect vulnerability to climate change. Curr. Opin. Insect Sci. 41, 63–70 (2020).

    PubMed 

    Google Scholar 

  • van Heerwaarden, B. & Kellermann, V. Does plasticity trade off with basal heat tolerance? Trends Ecol. Evol. 35, 874–885 (2020).

    PubMed 

    Google Scholar 

  • Stevenson, R. D. The relative importance of behavioral and physiological adjustments controlling body temperature in terrestrial ectotherms. Am. Nat. 126, 362–386 (1985).

    Google Scholar 

  • Donelson, J. M., Salinas, S., Munday, P. L. & Shama, L. N. S. Transgenerational plasticity and climate change experiments: Where do we go from here? Glob. Chang. Biol. 24, 13–34 (2018).

    ADS 
    PubMed 

    Google Scholar 

  • Kristensen, T. N. et al. Costs and benefits of cold acclimation in field-released Drosophila. Proc. Natl Acad. Sci. 105, 216–221 (2008).

    ADS 
    CAS 
    PubMed 

    Google Scholar 

  • Bozinovic, F., Calosi, P. & Spicer, J. I. Physiological correlates of geographic range in animals. Annu. Rev. Ecol. Evol. Syst. 42, 155–179 (2011).

    Google Scholar 

  • Chown, S. L., Gaston, K. J. & Robinson, D. Macrophysiology: large-scale patterns in physiological traits and their ecological implications. Funct. Ecol. 18, 159–167 (2004).

    Google Scholar 

  • Overgaard, J., Hoffmann, A. A. & Kristensen, T. N. Assessing population and environmental effects on thermal resistance in Drosophila melanogaster using ecologically relevant assays. J. Therm. Biol. 36, 409–416 (2011).

    Google Scholar 

  • Sgrò, C. M. et al. A comprehensive assessment of geographic variation in heat tolerance and hardening capacity in populations of Drosophila melanogaster from Eastern Australia. J. Evol. Biol. 23, 2484–2493 (2010).

    PubMed 

    Google Scholar 

  • Kingsolver, J. G. & Huey, R. B. Size, temperature, and fitness: three rules. Evol. Ecol. Res. 10, 251–268 (2008).

    Google Scholar 

  • Brown, J., Gillooly, J. F., Allen, A. P., Savage, V. M. & West, G. Toward a metabolic theory of ecology. Ecology 85, 1771–1789 (2004).

    Google Scholar 

  • Stillwell, R. C., Blanckenhorn, W. U., Teder, T., Davidowitz, G. & Fox, C. W. Sex differences in phenotypic plasticity affect variation in sexual size dimorphism in insects: from physiology to evolution. Annu. Rev. Entomol. 55, 227 (2010).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Tarka, M., Guenther, A., Niemelä, P. T., Nakagawa, S. & Noble, D. W. A. Sex differences in life history, behavior, and physiology along a slow-fast continuum: a meta-analysis. Behav. Ecol. Sociobiol. 72, 1–13 (2018).

    Google Scholar 

  • Pottier, P., Burke, S., Drobniak, S. M., Lagisz, M. & Nakagawa, S. Sexual (in)equality? A meta-analysis of sex differences in thermal acclimation capacity across ectotherms. Funct. Ecol. 35, 2663–2678 (2021).

    Google Scholar 

  • Bowler, K. & Terblanche, J. S. Insect thermal tolerance: what is the role of ontogeny, ageing and senescence? Biol. Rev. 83, 339–355 (2008).

    PubMed 

    Google Scholar 

  • Fawcett, T. W. & Frankenhuis, W. E. Adaptive explanations for sensitive windows in development. Front. Zool. 12, 1–14 (2015).

    Google Scholar 

  • English, S. & Barreaux, A. M. The evolution of sensitive periods in development: insights from insects. Curr. Opin. Behav. Sci. 36, 71–78 (2020).

    Google Scholar 

  • Overgaard, J., Kristensen, T. N. & Sørensen, J. G. Validity of thermal ramping assays used to assess thermal tolerance in arthropods. PLoS One 7, e32758 (2012).

    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Bak, C. W. et al. Comparison of static and dynamic assays when quantifying thermal plasticity of drosophilids. Insects 11, 1–11 (2020).

    Google Scholar 

  • Rodrigues, Y. K. & Beldade, P. Thermal plasticity in insects’ response to climate change and to multifactorial environments. Front. Ecol. Evol. 8, 271 (2020).

    Google Scholar 

  • Terblanche, J. S. & Hoffmann, A. Validating measurements of acclimation for climate change adaptation. Curr. Opin. Insect Sci. 41, 7–16 (2020).

    PubMed 

    Google Scholar 

  • Loeschcke, V. & Hoffmann, A. A. The detrimental acclimation hypothesis. Trends Ecol. Evol. 17, 407–408 (2002).

    Google Scholar 

  • Cossins, A. R. & Bowler, K. Temperature Biology of Animals. (Chapman and Hall, 1987).

  • Pintor, A. F. V., Schwarzkopf, L. & Krockenberger, A. K. Extensive acclimation in ectotherms conceals interspecific variation in thermal tolerance limits. PLoS One 11, e0150408 (2016).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Rezende, E. L., Tejedo, M. & Santos, M. Estimating the adaptive potential of critical thermal limits: methodological problems and evolutionary implications. Funct. Ecol. 25, 111–121 (2011).

    Google Scholar 

  • Allen, J. L., Chown, S. L., Janion-Scheepers, C. & Clusella-Trullas, S. Interactions between rates of temperature change and acclimation affect latitudinal patterns of warming tolerance. Conserv. Physiol. 4, cow053 (2016).

  • Lutterschmidt, W. I. & Hutchison, V. H. The critical thermal maximum: History and critique. Can. J. Zool. 75, 1561–1574 (1997).

    Google Scholar 

  • Terblanche, J. S. et al. Phenotypic plasticity and geographic variation in thermal tolerance and water loss of the tsetse Glossina pallidipes (Diptera: Glossinidae): Implications for distribution modelling. Am. J. Trop. Med. Hyg. 74, 786–794 (2006).

    PubMed 

    Google Scholar 

  • Koricheva, J., Gurevitch, J. & Mengersen, K. Handbook of meta-analysis in ecology and evolution. Handbook of Meta-analysis in Ecology and Evolution (Princeton University Press, 2013).

  • Suggitt, A. J. et al. Habitat microclimates drive fine-scale variation in extreme temperatures. Oikos 120, 1–8 (2011).

    Google Scholar 

  • Oyen, K. J. & Dillon, M. E. Critical thermal limits of bumblebees (Bombus impatiens) are marked by stereotypical behaviors and are unchanged by acclimation, age or feeding status. J. Exp. Biol. 221, jeb165589 (2018).

  • Bennett, J. M. et al. The evolution of critical thermal limits of life on Earth. Nat. Commun. 12, 1–9 (2021).

    Google Scholar 

  • Bowler, K. Heat death in poikilotherms: Is there a common cause? J. Therm. Biol. 76, 77–79 (2018).

    PubMed 

    Google Scholar 

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

    CAS 
    PubMed 

    Google Scholar 

  • Hoffmann, A. A., Chown, S. L. & Clusella-Trullas, S. Upper thermal limits in terrestrial ectotherms: How constrained are they? Funct. Ecol. 27, 934–949 (2013).

    Google Scholar 

  • Sandblom, E. et al. Physiological constraints to climate warming in fish follow principles of plastic floors and concrete ceilings. Nat. Commun. 7, 1–8 (2016).

    Google Scholar 

  • Maclean, H. J. et al. Evolution and plasticity of thermal performance: An analysis of variation in thermal tolerance and fitness in 22 Drosophila species. Philos. Trans. R. Soc. B Biol. Sci. 374, 20180548 (2019).

  • Addo-Bediako, A., Chown, S. L. & Gaston, K. J. Thermal tolerance, climatic variability and latitude. Proc. R. Soc. B Biol. Sci. 267, 739–745 (2000).

    CAS 

    Google Scholar 

  • Sales, K. et al. Experimental heatwaves compromise sperm function and cause transgenerational damage in a model insect. Nat. Commun. 9, 1–11 (2018).

    ADS 
    CAS 

    Google Scholar 

  • Walsh, B. S. et al. Integrated approaches to studying male and female thermal fertility limits. Trends Ecol. Evol. 34, 492–493 (2019).

    PubMed 

    Google Scholar 

  • Moher, D. et al. Preferred reporting items for systematic reviews and meta-analyses: The PRISMA statement. PLoS Med. 6, e1000097 (2009).

  • Hadley, N. F. Water relations of terrestrial arthropods. (Academic Press, 1994).

  • Hinchliff, C. E. et al. Synthesis of phylogeny and taxonomy into a comprehensive tree of life. PNAS. 112, 12764–12769 (2015).

    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Viechtbauer, W. Conducting meta-analyses in R with the metafor. J. Stat. Softw. 36, 1–48 (2010).

    Google Scholar 

  • Barton, K. MuMIn: Multi-Model Inference. (2020).

  • Nakagawa, S. et al. Methods for testing publication bias in ecological and evolutionary meta-analyses. Methods Ecol. Evol. 13, 4–21 (2022).

    Google Scholar 

  • Macartney, E. L., Crean, A. J., Nakagawa, S. & Bonduriansky, R. Effects of nutrient limitation on sperm and seminal fluid: a systematic review and meta-analysis. Biol. Rev. 94, 1722–1739 (2019).

    PubMed 

    Google Scholar 


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