Skip to main content
Log in

Why get big in the cold? Towards a solution to a life-history puzzle

  • Physiology Ecology - Original Paper
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

The temperature–size rule (TSR), which states that body size increases at lower developmental temperatures, appears to be a near-universal law for ectotherms. Although recent studies seem to suggest that the TSR might be adaptive, the underlying developmental mechanisms are thus far largely unknown. Here, we investigate temperature effects on life-history traits, behaviour and physiology in the copper butterfly Lycaena tityrus in order to disentangle the mechanistic basis for the above rule. In L. tityrus the larger body size produced at a lower temperature was proximately due to a greater increase in mass, which was caused by both behavioural and physiological mechanisms: a much-increased food intake and a higher efficiency in converting ingested food into body matter. These mechanisms, combined with temperature-induced changes at the cellular level, may provide general explanations for the TSR. Body fat and protein content increased in butterflies reared at the higher temperature, indicating favourable growth conditions. As predicted from protandry theory, males showed reduced development times, caused by higher growth rates compared to females. The latter was itself related to a higher daily food consumption, while the total food consumption (due to the females’ longer developmental period) and assimilation was higher in females and may underly the sexual body size dimorphism.

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. 1a–l

Similar content being viewed by others

References

  • Angilletta MJ Jr, Dunham AE (2003) The temperature–size rule in ectotherms: simple evolutionary explanations may not be general. Am Nat 162:332–342

    Article  PubMed  Google Scholar 

  • Angilletta MJ Jr, Steury TD, Sears MW (2004) Temperature, growth rate, and body size in ectotherms: fitting pieces of a life-history puzzle. Integr Comp Biol 44:498–509

    Article  Google Scholar 

  • Arendt JD (1997) Adaptive intrinsic growth rates: an integration across taxa. Q Rev Biol 72:149–177

    Article  Google Scholar 

  • Arnett AE, Gotelli NJ (1999) Geographic variation in life-history traits of the ant lion, Myrmeleon immaculatus: evolutionary implications of Bergmann’s rule. Evolution 53:1180–1188

    Article  Google Scholar 

  • Atkinson D (1994) Temperature and organism size—a biological law for ectotherms? Adv Ecol Res 25:1–58

    Article  Google Scholar 

  • Atkinson D, Sibly RM (1997) Why are organisms usually bigger in colder environments? Making sense of a life history puzzle. Trends Ecol Evol 12:235–239

    Article  Google Scholar 

  • Atkinson D, Morley SA, Hughes RN (2006) From cells to colonies: at what levels of body organization does the ‘temperature–size rule’ apply? Evol Dev 8:202–214

    Article  PubMed  Google Scholar 

  • Bauerfeind SS, Fischer K (2005) Effects of adult-derived carbohydrates, amino acids and micronutrients on female reproduction in a fruit-feeding butterfly. J Insect Physiol 51:545–554

    Article  PubMed  CAS  Google Scholar 

  • Berrigan D (1997) Acclimation of metabolic rate in response to developmental temperature in Drosophila melanogaster. J Therm Biol 22:213–218

    Article  Google Scholar 

  • Berrigan D, Charnov EL (1994) Reaction norms for age and size at maturity in response to temperature: a puzzle for life historians. Oikos 70:474–478

    Article  Google Scholar 

  • Blackburn TM, Gaston KJ (2001) Linking patterns in macroecology. J Anim Ecol 70:338–352

    Article  Google Scholar 

  • Blanckenhorn WU (1997) Altitudinal life history variation in the dung flies Scathophaga stercoraria and Sepsis cynipsea. Oecologia 109:342–352

    Article  Google Scholar 

  • Blanckenhorn WU (1999) Different growth responses to temperature and resource limitation in three fly species with similar life histories. Evol Ecol 13:395–409

    Article  Google Scholar 

  • Blanckenhorn WU, Llaurens V (2005) Effects of temperature on cell size and number in the yellow dung fly Scathophaga stercoraria. J Therm Biol 30:213–219

    Article  Google Scholar 

  • Blanckenhorn WU, Stillwell RC, Young KA, Fox CW, Ashton KG (2006) When Rensch meets Bergmann: does sexual size dimorphism change systematically with latitude? Evolution 60:2004–2011

    PubMed  Google Scholar 

  • Bochdanovits Z, de Jong G (2003) Temperature dependence of fitness components in geographical populations of Drosophila melanogaster: changing the association between size and fitness. Biol J Linn Soc 80:717–725

    Article  Google Scholar 

  • Cabanita R, Atkinson D (2006) Seasonal time constraints do not explain exceptions to the temperature size rule in ectotherms. Oikos 114:431–440

    Article  Google Scholar 

  • Chown SL, Klok CJ (2003) Altitudinal body size clines: latitudinal effects associated with changing seasonality. Ecography 26:445–455

    Article  Google Scholar 

  • Clarke A (2003) Costs and consequences of evolutionary temperature adaptation. Trends Ecol Evol 18:573–581

    Article  Google Scholar 

  • Clarke A (2006) Temperature and the metabolic theory of ecology. Funct Ecol 20:405–412

    Article  Google Scholar 

  • Clarke A, Fraser KPP (2004) Why does metabolism scale with temperature? Funct Ecol 18:243–251

    Article  Google Scholar 

  • Davidowitz G, D’Amico LJ, Nijhout HF (2003) Critical weight in the development of body size. Evol Dev 5:188–197

    Article  PubMed  Google Scholar 

  • Davidowitz G, D’Amico LJ, Nijhout HF (2004) The effects of environmental variation on a mechanism that controls insect body size. Evol Ecol Res 6:49–62

    Google Scholar 

  • Ebert G, Rennwald E (1991) Die Schmetterlinge Baden-Württembergs, vol 2. Ulmer, Stuttgart

    Google Scholar 

  • Elliot JM, Hurley MA (1997) A functional model of optimal growth of Atlantic salmon parr, Salmo salar, from two populations in Northwest England. Funct Ecol 11:592–603

    Article  Google Scholar 

  • Elliot JM, Hurley MA (1999) A new energetics model for brown trout, Salmo trutta. Freshwater Biol 39:339–349

    Article  Google Scholar 

  • Elliot JM, Hurley MA (2000) Daily energy intake and growth of piscivorous trout, Salmo trutta. Freshwater Biol 44:237–246

    Article  Google Scholar 

  • Fagerström T, Wiklund C (1982) Why do males emerge before females? Protandry as a mating strategy in male and female butterflies. Oecologia 52:164–166

    Article  Google Scholar 

  • Fischer K, Fiedler K (2000) Sex-related differences in reaction norms in the butterfly Lycaena tityrus (Lepidoptera: Lycaenidae). Oikos 90:372–380

    Article  Google Scholar 

  • Fischer K, Fiedler K (2001) Sexual differences in life-history traits in the butterfly Lycaena tityrus: a comparison between direct and diapause development. Entomol Exp Appl 100:325–330

    Article  Google Scholar 

  • Fischer K, Fiedler K (2002) Reaction norms for age and size at maturity in response to temperature: a test of the compound interest hypothesis. Evol Ecol 16:333–349

    Article  Google Scholar 

  • Fischer K, Brakefield PM, Zwaan BJ (2003) Plasticity in butterfly egg size: why larger offspring at lower temperatures? Ecology 84:3138–3147

    Article  Google Scholar 

  • Fischer K, Zeilstra I, Hetz SK, Fiedler K (2004) Physiological costs of growing fast: does accelerated growth reduce pay-off in adult fitness? Evol Ecol 18:343–353

    Article  Google Scholar 

  • Frazier MR, Raymond BH, Berrigan D (2001) Thermodynamic constrains the evolution of insect population growth rates: Warmer is better. Am Nat 168:512–520

    Article  Google Scholar 

  • French V, Feast M, Partridge L (1998) Body size and cell size in Drosophila: the developmental response to temperature. J Insect Physiol 44:1081–1089

    Article  PubMed  CAS  Google Scholar 

  • Gibert P, de Jong G (2001) Temperature dependence of development rate and adult size in Drosophila species: biophysical parameters. J Evol Biol 14:267–276

    Article  Google Scholar 

  • Gotthard K, Nylin S, Wiklund C (2000) Individual state controls temperature dependence in a butterfly (Lassiommata maera). Proc R Soc Lond B 267:589–593

    Article  CAS  Google Scholar 

  • Gunnarsson B, Johnsson J (1990) Protandry and moulting to maturity in the spider Pitophantes phrygianus. Oikos 59:205–212

    Article  Google Scholar 

  • Hoffmann KH (1973) Effects of temperature on chemical composition of crickets (Gryllus, Orthopt.) Oecologia 13:147–175

    Article  Google Scholar 

  • Hoffmann KH (1974) Effects of constant and varying temperatures on life-span, food utilization and fertility. Oecologia 17:39–54

    Article  Google Scholar 

  • Johnston IA, Bennett AF (1996) Animals and temperature. Cambridge University Press, Cambridge

    Google Scholar 

  • Jonsson B, Forseth T, Jensen AJ, Naesje TF (2001) Thermal performance of juvenile Atlantic salmon, Salmo salar L. Funct Ecol 15:701–711

    Article  Google Scholar 

  • Kingsolver JG, Woods HA (1997) Thermal sensitivity of growth and feeding in Manduca sexta caterpillars. Physiol Zool 70:631–638

    PubMed  CAS  Google Scholar 

  • Kingsolver JG, Woods HA (1998) Interactions of temperature and dietary protein concentration in growth and feeding in Manduca sexta caterpillars. Physiol Entomol 23:3554–3559

    Article  Google Scholar 

  • Kingsolver JG, Massie KR, Ragland GJ, Smith MH (2007) Rapid population divergence in thermal reaction norms for an invading species: breaking the temperature–size rule. J Evol Biol 20:892–900

    Article  PubMed  CAS  Google Scholar 

  • Koskela J, Pirhonen J, Jobling M (1997) Feed intake, growth rate and body composition of juvenile Baltic salmon exposed to different constant temperatures. Aquacult Int 5:351–360

    Article  Google Scholar 

  • Kozłowski J, Czarnołęski M, Dańko (2004) Can optimal resource allocation models explain why ectotherms grow larger in the cold? Int Comp Biol 44:480–493

    Article  Google Scholar 

  • Larsson S, Berglund I (2005) The effect of temperature on the energetic growth efficiency of Arctic Charr (Salvelinus alpinus L.) from four Swedish populations. J Therm Biol 30:29–36

    Article  Google Scholar 

  • Lindgren B, Laurila A (2005) Proximate causes of adaptive growth rates: growth efficiency variation among latitudinal populations of Rana temporaria. J Evol Biol 18:820–828

    Article  PubMed  CAS  Google Scholar 

  • Lorenz MW (2003) Adipokinetic hormone inhibits the formation of energy stores and egg production in the cricket Gryllus bimaculatus. Comp Biochem Physiol B 136:197–206

    Article  PubMed  CAS  Google Scholar 

  • Moed GH, Kruitwagen CLJJ, de Jong G, Scharloo W (1999) Critical weight for the induction of pupariation in Drosophila melanogaster: genetic and environmental variation. J Evol Biol 12:852–858

    Article  Google Scholar 

  • Neat F, Fowler K, French V, Partridge L (1995) Thermal evolution of growth efficiency in Drosophila melanogaster. Proc R Soc Lond B 260:73–78

    Article  CAS  Google Scholar 

  • Nylin S (1992) Seasonal plasticity in life history traits: growth and development in Polygonia c-album (Lepidoptera: Nymphalidae). Biol J Linn Soc 47:301–323

    Article  Google Scholar 

  • Nylin S, Wiklund C, Wickman PO, Garcia-Barros E (1993) Absence of trade-offs between sexual size dimorphism and early male emergence in a butterfly. Ecology 74:1414–1427

    Article  Google Scholar 

  • Partridge L, Coyne JA (1997) Bergmann’s rule in ectotherms: is it adaptive? Evolution 51:632–635

    Article  Google Scholar 

  • Partridge L, Barrie B, Fowler K, French V (1994) Evolution and development of body size and cell size in Drosophila melanogaster in response to temperature. Evolution 48:1269–1276

    Article  Google Scholar 

  • Partridge L, French V (1996) Thermal evolution of ectotherm body size: why get big in the cold? In: Johnston IA, Bennett AF (eds) Animals and temperature: Phenotypic and evolutionary adaptation. Cambridge University Press, Cambridge, pp 265–292

    Google Scholar 

  • Perrin N (1995) About Berrigan and Charnov’s life history puzzle. Oikos 73:137–139

    Article  Google Scholar 

  • Petersen C, Woods HA, Kingsolver JG (2000) Stage-specific effects of temperature and dietary protein on growth and survival of Manduca sexta caterpillars. Physiol Entomol 25:35–40

    Article  CAS  Google Scholar 

  • Pörtner HO (2002) Climate variations and the physiological basis of temperature dependent biogeography: systemic to molecular hierarchy of thermal tolerance in animals. Comp Biochem Phys A 132:739–761

    Google Scholar 

  • Present TMC, Conover DO (1992) Physiological basis of latitudinal growth differences in Menidia menidia: variation in consumption or efficiency? Funct Ecol 6:23–31

    Article  Google Scholar 

  • Raubenheimer D, Simpson SJ (1992) Analysis of covariance: an alternate to nutritional indices. Entomol Exp Appl 62:221–231

    Article  Google Scholar 

  • Renault D, Hervant F, Vernon P (2002) Comparative study of the metabolic responses during food shortage and subsequent recovery at different temperatures in the adult lesser mealworm, Alphitobius diaperinus (Coleoptera: Tenebrionidae). Physiol Entomol 27:291–301

    Article  Google Scholar 

  • Robinson SJW, Partridge L (2001) Temperature and clinal variation in larval growth efficiency in Drosophila melanogaster. J Evol Biol 14:14–21

    Article  Google Scholar 

  • Roff DA (1992) The evolution of life-histories. Theory and analysis. Chapman and Hall, New York

    Google Scholar 

  • Santos M, Brites D, Laayouni H (2006) Thermal evolution of pre-adult life history traits, geometric size and shape, and developmental stability in Drosophila obscura. Evol Ecol 19:2006–2021

    CAS  Google Scholar 

  • SBN (Schweizerischer Bund für Naturschutz) (1987) Tagfalter und ihre Lebensräume. Fotorotar, Basel

    Google Scholar 

  • Sinclair B, Vernon P, Klok CL, Chown SL (2003) Insects at low temperatures: an ecological perspective. Trends Ecol Evol 18:257–262

    Article  Google Scholar 

  • Sørensen JG, Kristensen TN, Loeschke V (2003) The evolutionary and ecological role of heat shock proteins. Ecol Lett 6:1025–1037

    Article  Google Scholar 

  • Stearns SC (1992) The evolution of life-histories. Oxford University Press, Oxford

    Google Scholar 

  • Stelzer CP (2002) Phenotypic plasticity of body size at different temperatures in a planktonic rotifer: mechanisms and adaptive significance. Funct Ecol 16:835–841

    Article  Google Scholar 

  • Teuschl Y, Reim C, Blanckenhorn WU (2007) Correlated responses to artificial body size selection in growth, development, phenotypic plasticity and juvenile viability in yellow dung flies. J Evol Biol 20:87–103

    Article  PubMed  CAS  Google Scholar 

  • Tolman T, Lewington R (1998) Die Tagfalter Europas und Nordwestafrikas. Franckh-Kosmos, Stuttgart

    Google Scholar 

  • Van der Have TM, de Jong G (1996) Adult size in ectotherms: temperature effects on growth and differentiation. J Theor Biol 183:329–340

    Article  Google Scholar 

  • Van Doorslaer W, Stoks R (2005) Growth rate plasticity to temperature in two damselfly species differing in latitude: contributions of behaviour and physiology. Oikos 111:599–605

    Article  Google Scholar 

  • Von Bertalanffy L (1960) Principles and theory of growth. In: Nowinski WW (ed) Fundamental aspects of normal and malignant growth. Elsevier, New York

    Google Scholar 

  • Walters RJ, Hassall M (2006) The temperature–size rule in ectotherms: may a general explanation exist after all? Am Nat 167:510–523

    Article  PubMed  Google Scholar 

  • Weetman D, Atkinson D (2004) Evaluation of alternative hypotheses to explain temperature-induced life history shifts in Daphnia. J Plankt Res 26:107–116

    Article  Google Scholar 

  • Wiklund C, Nylin S, Forsberg J (1991) Sex-related variation in growth rate as a result of selection for large size and protandry in a bivoltine butterfly (Pieris napi L.). Oikos 60:241–250

    Article  Google Scholar 

  • Woods HA, Makino W, Cotner JB, Hobbie SE, Harrison JF, Acharya K, Elsers JJ (2003) Temperature and the chemical composition of poikilothermic organisms. Funct Ecol 17:237–245

    Article  Google Scholar 

  • Yahara I (1999) The role of HSP90 in evolution. Genes Cells 4:375–379

    Article  PubMed  CAS  Google Scholar 

  • Yamahira K, Conover DO (2002) Intra- vs. interspecific latitudinal variation in growth: adaptation to temperature or seasonality? Ecology 83:1252–1262

    Article  Google Scholar 

  • Zera AJ, Potts J, Kobus K (1998) The physiology of life-history trade-offs: experimental analysis of hormonally induced life-history trade-off in Gryllus assimilis. Am Nat 152:7–23

    Article  CAS  PubMed  Google Scholar 

  • Zwaan BJ, Bijlsma R, Hoekstra RF (1991) On the developmental theory of ageing. 1. Starvation resistance and longevity in Drosophila melanogaster in relation to pre-adult breeding conditions. Heredity 66:29–39

    Google Scholar 

Download references

Acknowledgments

We thank Dr. M.W. Lorenz for help with protein analyses and J. Perlick for technical assistance. Insightful comments provided by two anonymous reviewers substantially improved the quality of this manuscript. Financial support was provided by the German Research Council (DFG grant no. Fi 846/1–2 and 1–3 to KF).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Isabell Karl.

Additional information

Communicated by Thomas Hoffmeister.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Karl, I., Fischer, K. Why get big in the cold? Towards a solution to a life-history puzzle. Oecologia 155, 215–225 (2008). https://doi.org/10.1007/s00442-007-0902-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-007-0902-0

Keywords

Navigation