• This record comes from PubMed

Individual variation in thermally induced plasticity of metabolic rates: ecological and evolutionary implications for a warming world

. 2024 Feb 26 ; 379 (1896) : 20220494. [epub] 20240108

Language English Country England, Great Britain Media print-electronic

Document type Journal Article, Review

Energy metabolism is a fundamental property of life providing the energy for all processes and functions within an organism. As it is temperature-dependent, it mediates the effects of changing climate on ectotherm fitness and population dynamics. Though resting metabolic rate is a highly labile trait, part of its variation is individually consistent. Recent findings show that resting metabolic rate contains consistent variation not only in the elevations (intercepts) but also in the slopes of individual thermal dependence curves, challenging the thermal dependence assumption for this trait in several ectotherm taxa. I argue that among-individual variation in thermal metabolic curves represents a previously undetected component of ectotherm response to climate change, potentially affecting their adaptive capacity and population resilience under increasing stochasticity of thermal environment. Future studies need to examine not only the amount of among-individual variation in thermal metabolic curves across phylogenetic contexts but also other aspects concerning its mechanisms and adaptive significance to improve predictions about the impact of climate change on ectotherm population dynamics. This article is part of the theme issue 'The evolutionary significance of variation in metabolic rates'.

See more in PubMed

Gillooly JF, Brown JH, West GB, Savage VM, Charnov EL. 2001. Effects of size and temperature on metabolic rate. Science 293, 2248-2251. (10.1126/science.1061967) PubMed DOI

Dell AI, Pawar S, Savage VM. 2011. Systematic variation in the temperature dependence of physiological and ecological traits. Proc. Natl Acad. Sci. USA 108, 10 591-10 596. (10.1073/pnas.1015178108) PubMed DOI PMC

Williams SE, Shoo LP, Isaac JL, Hoffmann AA, Langham G. 2008. Towards an integrated framework for assessing the vulnerability of species to climate change. PLoS Biol. 6, 2621-2626. (10.1371/journal.pbio.0060325) PubMed DOI PMC

Lopez-Sepulcre A, Kokko H. 2012. Understanding behavioural responses and their consequences. In Behavioural responses to a changing world: mechanisms and consequences (eds Candolin U, Wong BBM), pp. 3-15. Oxford, UK: Oxford University Press.

Schulte PM. 2015. The effects of temperature on aerobic metabolism: towards a mechanistic understanding of the responses of ectotherms to a changing environment. J. Exp. Biol. 218, 1856-1866. (10.1242/jeb.118851) PubMed DOI

Seebacher F, White CR, Franklin CE. 2014. Physiological plasticity increases resilience of ectothermic animals to climate change. Nat. Clim. Change 5, 61-66. (10.1038/nclimate2457) DOI

Norin T, Metcalfe NB. 2019. Ecological and evolutionary consequences of metabolic rate plasticity in response to environmental change. Phil. Trans. R. Soc. B 374, 20180180. (10.1098/rstb.2018.0180) PubMed DOI PMC

Clarke A. 1993. Seasonal acclimatization and latitudinal compensation in metabolism: do they exist? Funct. Ecol. 7, 139-149. (10.2307/2389880) DOI

Parmesan C, Yohe G. 2003. A globally coherent fingerprint of climate change impacts across natural systems. Nature 421, 37-42. (10.1038/nature01286) PubMed DOI

Colwell RK, Brehm G, Cardelus CL, Gilman AC, Longino JT. 2008. Global warming, elevational range shifts, and lowland biotic attrition in the wet tropics. Science 322, 258-261. (10.1126/science.1162547) PubMed DOI

Thomas CD, et al. 2004. Extinction risk from climate change. Nature 427, 145-148. (10.1038/nature02121) PubMed DOI

Dillon ME, Wang G, Huey RB. 2010. Global metabolic impacts of recent climate warming. Nature 467, 704-706. (10.1038/nature09407) PubMed DOI

Pörtner HO, Knust R. 2007. Climate change affects marine fishes through the oxygen limitation of thermal tolerance. Science 315, 95-97. (10.1126/science.1135471) PubMed DOI

Briscoe NJ, et al. 2023. Mechanistic forecasts of species responses to climate change: the promise of biophysical ecology. Glob. Change Biol. 29, 1451-1470. (10.1111/gcb.16557) PubMed DOI

Dingemanse NJ, Kazem AJ, Reále D, Wright J. 2010. Behavioural reaction norms: animal personality meets individual plasticity. Trends Ecol. Evol. 25, 81-89. (10.1016/j.tree.2009.07.013) PubMed DOI

Nussey DH, Wilson AJ, Brommer JE. 2007. The evolutionary ecology of individual phenotypic plasticity in wild populations. J. Evol. Biol. 20, 831-844. (10.1111/j.1420-9101.2007.01300.x) PubMed DOI

Roche DG, Careau V, Binning SA. 2016. Demystifying animal 'personality' (or not): why individual variation matters to experimental biologists. J. Exp. Biol. 219, 3832-3843. (10.1242/jeb.146712) PubMed DOI

Careau V, Thomas D, Humphries MM, Reále D. 2008. Energy metabolism and animal personality. Oikos 117, 641-653. (10.1111/j.0030-1299.2008.16513.x) DOI

Burton T, Killen SS, Armstrong JD, Metcalfe NB. 2011. What causes intraspecific variation in resting metabolic rate and what are its ecological consequences? Proc. R. Soc. B 278, 3465-3473. (10.1098/rspb.2011.1778) PubMed DOI PMC

Nespolo RF, Franco M. 2007. Whole-animal metabolic rate is a repeatable trait: a meta-analysis. J. Exp. Biol. 210, 3877-3878. (10.1242/jeb.02780) PubMed DOI

White CR, Schimpf NG, Cassey P. 2013. The repeatability of metabolic rate declines with time. J. Exp. Biol. 216, 1763-1765. (10.1242/jeb.076562) PubMed DOI

Ponzi E, Keller LF, Bonnet T, Muff S. 2018. Heritability, selection, and the response to selection in the presence of phenotypic measurement error: effects, cures, and the role of repeated measurements. Evolution 72, 1992-2004. (10.1111/evo.13573) PubMed DOI

Baškiera S, Gvoždík L. 2021. Repeatability and heritability of resting metabolic rate in a long-lived amphibian. Comp. Biochem. Physiol. A 253, 110858. (10.1016/j.cbpa.2020.110858) PubMed DOI

Dezetter M, Dupoué A, Le Galliard JF, Lourdais O. 2021. Additive effects of developmental acclimation and physiological syndromes on lifetime metabolic and water loss rates of a dry-skinned ectotherm. Funct. Ecol. 36, 432-445. (10.1111/1365-2435.13951) DOI

Dingemanse NJ, Wolf M. 2013. Between-individual differences in behavioural plasticity within populations: causes and consequences. Anim. Behav. 85, 1031-1039. (10.1016/j.anbehav.2012.12.032) DOI

Careau V, Gifford ME, Biro PA. 2014. Individual (co)variation in thermal reaction norms of standard and maximal metabolic rates in wild-caught slimy salamanders. Funct. Ecol. 28, 1175-1186. (10.1111/1365-2435.12259) DOI

Norin T, Malte H, Clark TD, Konarzewski M. 2015. Differential plasticity of metabolic rate phenotypes in a tropical fish facing environmental change. Funct. Ecol. 30, 369-378. (10.1111/1365-2435.12503) DOI

Auer SK, Salin K, Anderson GJ, Metcalfe NB. 2018. Individuals exhibit consistent differences in their metabolic rates across changing thermal conditions. Comp. Biochem. Physiol. A 217, 1-6. (10.1016/j.cbpa.2017.11.021) PubMed DOI PMC

Kar F, Nakagawa S, Friesen CR, Noble DWA. 2021. Individual variation in thermal plasticity and its impact on mass-scaling. Oikos 130, 1131-1142. (10.1111/oik.08122) DOI

Araya-Ajoy YG, Mathot KJ, Dingemanse NJ, O'Hara RB. 2015. An approach to estimate short-term, long-term and reaction norm repeatability. Methods Ecol. Evol. 6, 1462-1473. (10.1111/2041-210x.12430) DOI

Réveillon T, Rota T, Chauvet É, Lecerf A, Sentis A. 2019. Repeatable inter-individual variation in the thermal sensitivity of metabolic rate. Oikos 128, 1633-1640. (10.1111/oik.06392) DOI

Baškiera S, Gvoždík L. 2022. Individual variation in thermal reaction norms reveals metabolic-behavioral relationships in an ectotherm. Front. Ecol. Evol. 10, 850941. (10.3389/fevo.2022.850941) DOI

Kar F, Nakagawa S, Noble DWA. 2022. Impact of developmental temperatures on thermal plasticity and repeatability of metabolic rate. Evol. Ecol. 36, 199-216. (10.1007/s10682-022-10160-1) DOI

Winterová B, Gvoždík L. 2021. Individual variation in seasonal acclimation by sympatric amphibians: a climate change perspective. Funct. Ecol. 35, 117-126. (10.1111/1365-2435.13705) DOI

Huey RB, Kearney MR, Krockenberger A, Holtum JA, Jess M, Williams SE. 2012. Predicting organismal vulnerability to climate warming: roles of behaviour, physiology and adaptation. Phil. Trans. R. Soc. B 367, 1665-1679. (10.1098/rstb.2012.0005) PubMed DOI PMC

Killen SS, Adriaenssens B, Marras S, Claireaux G, Cooke SJ. 2016. Context dependency of trait repeatability and its relevance for management and conservation of fish populations. Conserv. Physiol. 4, cow007. (10.1093/conphys/cow007) PubMed DOI PMC

Dohm MR. 2002. Repeatability estimates do not always set an upper limit to heritability. Funct. Ecol. 16, 273-280. (10.1046/j.1365-2435.2002.00621.x) DOI

Hoffmann AA, Sgro CM. 2011. Climate change and evolutionary adaptation. Nature 470, 479-485. (10.1038/nature09670) PubMed DOI

Dall SR. 2010. Managing risk: the perils of uncertainty. In Evolutionary behavioral ecology (eds Westneat DF, Fox CW), pp. 194-206. New York: NY: Oxford University Press.

IPCC. 2021. Climate Change 2021: The Physical Science Basis. In Contribution of Working Group I to the Sixth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge, UK, and New York, NY: Cambridge University Press.

Williams CM, Henry HA, Sinclair BJ. 2015. Cold truths: how winter drives responses of terrestrial organisms to climate change. Biol. Rev. 90, 214-235. (10.1111/brv.12105) PubMed DOI

Sinclair BJ. 2015. Linking energetics and overwintering in temperate insects. J. Therm. Biol. 54, 5-11. (10.1016/j.jtherbio.2014.07.007) PubMed DOI

Huey RB, Ma L, Levy O, Kearney MR. 2021. Three questions about the eco-physiology of overwintering underground. Ecol. Lett. 24, 170-185. (10.1111/ele.13636) PubMed DOI

Podhajský L, Gvoždík L. 2016. Variation in winter metabolic reduction between sympatric amphibians. Comp. Biochem. Physiol. A 201, 110-114. (10.1016/j.cbpa.2016.07.003) PubMed DOI

Rall BC, Vucic-Pestic O, Ehnes RB, Emmerson M, Brose U. 2010. Temperature, predator-prey interaction strength and population stability. Glob. Change Biol. 16, 2145-2157. (10.1111/j.1365-2486.2009.02124.x) DOI

Uszko W, Diehl S, Englund G, Amarasekare P. 2017. Effects of warming on predator-prey interactions - a resource-based approach and a theoretical synthesis. Ecol. Lett. 20, 513-523. (10.1111/ele.12755) PubMed DOI

Starrfelt J, Kokko H. 2012. Bet-hedging: a triple trade-off between means, variances and correlations. Biol. Rev. Camb. Philos. Soc. 87, 742-755. (10.1111/j.1469-185X.2012.00225.x) PubMed DOI

Agrawal AF, Stinchcombe JR. 2009. How much do genetic covariances alter the rate of adaptation? Proc. R. Soc. B 276, 1183-1191. (10.1098/rspb.2008.1671) PubMed DOI PMC

Tufto J. 2015. Genetic evolution, plasticity, and bet-hedging as adaptive responses to temporally autocorrelated fluctuating selection: a quantitative genetic model. Evolution 69, 2034-2049. (10.1111/evo.12716) PubMed DOI

Botero CA, Weissing FJ, Wright J, Rubenstein DR. 2015. Evolutionary tipping points in the capacity to adapt to environmental change. Proc. Natl Acad. Sci. USA 112, 184-189. (10.1073/pnas.1408589111) PubMed DOI PMC

DeWitt TJ, Langerhans RB. 2004. Integrated solutions to environmental heterogeneity: theory of multimoment reaction norms. In Phenotypic plasticity: functional and conceptual approaches (eds DeWitt TJ, Scheiner SM), pp. 98-111. New York, NY: Oxford University Press.

Xue B, Sartori P, Leibler S. 2019. Environment-to-phenotype mapping and adaptation strategies in varying environments. Proc. Natl Acad. Sci. USA 116, 13 847-13 855. (10.1073/pnas.1903232116) PubMed DOI PMC

Haaland TR, Wright J, Ratikainen II. 2021. Individual reversible plasticity as a genotype-level bet-hedging strategy. J. Evol. Biol. 34, 1022-1033. (10.1111/jeb.13788) PubMed DOI

Pincebourde S. 2016. Fine-scale microclimatic variation can shape the responses of organisms to global change in both natural and urban environments. Integr. Comp. Biol. 56, 45-61. (10.1093/icb/icw016) PubMed DOI

Lighton JRB. 2008. Measuring metabolic rates: a manual for scientists. Oxford, UK: Oxford University Press.

Killen SS, et al. 2021. Guidelines for reporting methods to estimate metabolic rates by aquatic intermittent-flow respirometry. J. Exp. Biol. 224, jeb242522. (10.1242/jeb.242522) PubMed DOI PMC

Koch RE, et al. 2021. Integrating mitochondrial aerobic metabolism into ecology and evolution. Trends Ecol. Evol. 36, 321-332. (10.1016/j.tree.2020.12.006) PubMed DOI

Massot M, Clobert J, Montes-Poloni L, Haussy C, Cubo J, Meylan S. 2011. An integrative study of ageing in a wild population of common lizards. Funct. Ecol. 25, 848-858. (10.1111/j.1365-2435.2011.01837.x) DOI

Moe B, Ronning B, Verhulst S, Bech C. 2009. Metabolic ageing in individual zebra finches. Biol. Lett. 5, 86-89. (10.1098/rsbl.2008.0481) PubMed DOI PMC

Seebacher F, Brand MD, Else PL, Guderley H, Hulbert AJ, Moyes CD. 2010. Plasticity of oxidative metabolism in variable climates: molecular mechanisms. Physiol. Biochem. Zool. 83, 721-732. (10.1086/649964) PubMed DOI

Maxwell CS, Magwene PM. 2017. When sensing is gambling: an experimental system reveals how plasticity can generate tunable bet-hedging strategies. Evolution 71, 859-871. (10.1111/evo.13199) PubMed DOI PMC

Abram PK, Boivin G, Moiroux J, Brodeur J. 2017. Behavioural effects of temperature on ectothermic animals: unifying thermal physiology and behavioural plasticity. Biol. Rev. 92, 1859-1876. (10.1111/brv.12312) PubMed DOI

Pettersen AK, Hall MD, White CR, Marshall DJ. 2020. Metabolic rate, context-dependent selection, and the competition-colonization trade-off. Evol. Lett. 4, 333-344. (10.1002/evl3.174) PubMed DOI PMC

Artacho P, Nespolo RF. 2009. Natural selection reduces energy metabolism in the garden snail, Helix aspersa (Cornu aspersum). Evolution 63, 1044-1050. (10.1111/j.1558-5646.2008.00603.x) PubMed DOI

Auer SK, et al. 2018. Nutrients from salmon parents alter selection pressures on their offspring. Ecol. Lett. 21, 287-295. (10.1111/ele.12894) PubMed DOI PMC

Schulte PM, Healy TM, Fangue NA. 2011. Thermal performance curves, phenotypic plasticity, and the time scales of temperature exposure. Integr. Comp. Biol. 51, 691-702. (10.1093/icb/icr097) PubMed DOI

Seebacher F, Little AG. 2021. Plasticity of performance curves in ectotherms: individual variation modulates population responses to environmental change. Front. Physiol. 12, 733305. (10.3389/fphys.2021.733305) PubMed DOI PMC

Sokolova I. 2021. Bioenergetics in environmental adaptation and stress tolerance of aquatic ectotherms: linking physiology and ecology in a multi-stressor landscape. J. Exp. Biol. 224, jeb236802. (10.1242/jeb.236802) PubMed DOI

Killen SS, Marras S, Metcalfe NB, McKenzie DJ, Domenici P. 2013. Environmental stressors alter relationships between physiology and behaviour. Trends Ecol. Evol. 28, 651-658. (10.1016/j.tree.2013.05.005) PubMed DOI

Millidine KJ, Metcalfe NB, Armstrong JD. 2009. Presence of a conspecific causes divergent changes in resting metabolism, depending on its relative size. Proc. R. Soc. B 276, 3989-3993. (10.1098/rspb.2009.1219) PubMed DOI PMC

Janča M, Gvoždík L. 2017. Costly neighbours: heterospecific competitive interactions increase metabolic rates in dominant species. Sci. Rep. 7, 5177. (10.1038/s41598-017-05485-9) PubMed DOI PMC

Blouin-Demers G, Nadeau P. 2005. The cost-benefit model of thermoregulation does not predict lizard thermoregulatory behavior. Ecology 86, 560-566. (10.1890/04-1403) DOI

Tüzün N, Stoks R. 2022. A fast pace-of-life is traded off against a high thermal performance. Proc. R. Soc. B 289, 20212414. (10.1098/rspb.2021.2414) PubMed DOI PMC

Goulet CT, Thompson MB, Chapple DG. 2017. Repeatability and correlation of physiological traits: do ectotherms have a "thermal type"? Ecol. Evol. 7, 710-719. (10.1002/ece3.2632) PubMed DOI PMC

Urban MC, et al. 2016. Improving the forecast for biodiversity under climate change. Science 353, aad8466. (10.1126/science.aad8466) PubMed DOI

Kearney M, Porter WP, Williams C, Ritchie S, Hoffmann AA. 2009. Integrating biophysical models and evolutionary theory to predict climatic impacts on species' ranges: the dengue mosquito Aedes aegypti in Australia. Funct. Ecol. 23, 528-538. (10.1111/j.1365-2435.2008.01538.x) DOI

Bush A, Mokany K, Catullo R, Hoffmann A, Kellermann V, Sgro C, McEvey S, Ferrier S. 2016. Incorporating evolutionary adaptation in species distribution modelling reduces projected vulnerability to climate change. Ecol. Lett. 19, 1468-1478. (10.1111/ele.12696) PubMed DOI

Catullo RA, Ferrier S, Hoffmann AA. 2015. Extending spatial modelling of climate change responses beyond the realized niche: estimating, and accommodating, physiological limits and adaptive evolution. Glob. Ecol. Biogeogr. 24, 1192-1202. (10.1111/geb.12344) DOI

Find record

Citation metrics

Loading data ...

Archiving options

Loading data ...