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Energetics of embryonic development: effects of temperature on egg and hatchling composition in a butterfly

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Abstract

Phenotypic plasticity may allow an organism to adjust its phenotype to environmental needs. However, little is known about environmental effects on offspring biochemical composition and turnover rates, including energy budgets and developmental costs. Using the tropical butterfly Bicyclus anynana and employing a full-factorial design with two oviposition and two developmental temperatures, we explore the consequences of temperature variation on egg and hatchling composition, and the associated use and turnover of energy and egg compounds. At the lower temperature, larger but fewer eggs were produced. Larger egg sizes were achieved by provisioning these eggs with larger quantities of all compounds investigated (and thus more energy), whilst relative egg composition was rather similar to that of smaller eggs laid at the higher temperature. Turnover rates during embryonic development differed across developmental temperatures, suggesting an emphasis on hatchling quality (i.e. protein content) at the more stressful lower temperature, but on storage reserves (i.e. lipids) at the higher temperature. These differences may represent adaptive maternal effects. Embryonic development was much more efficient at the lower temperature, providing a possible mechanism underlying the temperature-size rule.

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References

  • Angilletta MJ, 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 

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

    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 

  • Azevedo RBR, French V, Partridge L (1997) Life-history consequences of egg size in Drosophila melanogaster. Am Nat 150:250–282

    Article  PubMed  CAS  Google Scholar 

  • Baur A, Baur B (1997) Seasonal variation in size and nutrient content of eggs of the land snail Arianta arbustorum. Inver Rep Dev 32:55–62

    Google Scholar 

  • Beenakkers AMT, Vanderhorst DJ, Vanmarrewijk WJA (1985) Insect lipids and lipoproteins, and their role in physiological processes. Prog Lipid Res 24:19–67

    Article  PubMed  CAS  Google Scholar 

  • Bernardo J (1996) The particular maternal effect of propagule size, especially egg size: patterns, models, quality of evidence and interpretations. Am Zool 36:216–236

    Google Scholar 

  • Booth DT, Kiddell K (2007) Temperature and the energetics of development in the house cricket (Acheta domesticus). J Insect Physiol 53:950–953

    Article  PubMed  CAS  Google Scholar 

  • Brakefield PM (1997) Phenotypic plasticity and fluctuating asymmetry as responses to environmental stress in the butterfly Bicyclus anynana. In: Bijlsma RR, Loeschcke V (eds) Environmental stress: adaption and evolution. Birkhäuser, Basel

    Google Scholar 

  • Brakefield PM, Mazzotta V (1995) Matching field and laboratory environments—effects of neglecting daily temperature-variation on insect reaction norms. J Evol Biol 8:559–573

    Article  Google Scholar 

  • Brakefield PM, Reitsma N (1991) Phenotypic plasticity, seasonal climate and the population biology of Bicyclus butterflies (Satyridae) in Malawi. Ecol Entomol 16:291–303

    Article  Google Scholar 

  • Chapman RF (1998) The insects: structures and function. Cambridge University Press, Cambridge

    Google Scholar 

  • Diss AL, Kunkel JG, Montgomery ME, Leonard DE (1996) Effects of maternal nutrition and egg provisioning on parameters of larval hatch, survival and dispersal in the gypsy moth, Lymantria dispar L. Oecologia 106:470–477

    Article  Google Scholar 

  • Eckert R, Randall D, Burggren W, French K (2002) Tierphysiologie. Thieme, Stuttgart

    Google Scholar 

  • Fischer K, Bot ANM, Brakefield PM, Zwaan BJ (2003a) Fitness consequences of temperature-mediated egg size plasticity in a butterfly. Funct Ecol 17:803–810

    Article  Google Scholar 

  • Fischer K, Bot ANM, Brakefield PM, Zwaan BJ (2006) Do mothers producing large offspring have to sacrifice fecundity? J Evol Biol 19:380–391

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Fox CW, Thakar MS, Mousseau TA (1997) Egg size plasticity in a seed beetle: an adaptive maternal effect. Am Nat 149:149–163

    Article  Google Scholar 

  • Ganong W (1974) Lehrbuch der medizinischen Physiologie. Springer, Berlin

    Google Scholar 

  • Garcia-Guerrero M, Villarreal H, Racotta IS (2003) Effect of temperature on lipids, proteins, and carbohydrates levels during development from egg extrusion to juvenile stage of Cherax quadricarinatus (Decapoda : Parastacidae). Comp Biochem Physiol A 135:147–154

    Article  Google Scholar 

  • Gilchrist GW, Huey RB (2001) Parental and developmental temperature effects on the thermal dependence of fitness in Drosophila melanogaster. Evolution 55:209–214

    PubMed  CAS  Google Scholar 

  • Gillot C (2005) Entomology. Springer, New York

    Google Scholar 

  • Giron D, Casas J (2003) Mothers reduce egg provisioning with age. Ecol Lett 6:273–277

    Article  Google Scholar 

  • Guisande C, Harris R (1995) Effect of total organic content of eggs on hatching success and naupliar survival in the copepod Calanus helgolandicus. Limnol Oceanogr 40:476–482

    CAS  Google Scholar 

  • Jaeckle W (1995) Variation in the size, energy content, and biochemical composition of invertebrate eggs: correlates to the mode of larval development. In: McEdward L (ed) Ecology of marine invertebrate larvae. CRC Press, Boca Raton, pp 49–77

    Google Scholar 

  • Jarošík V, Kratochvil L, Honek A, Dixon AFG (2004) A general rule for the dependence of developmental rate on temperature in ectothermic animals. Proc R Soc Lond B Biol Sci 271:S219–S221

    Article  Google Scholar 

  • Karl I, Fischer K (2008) Why get big in the cold? Towards a solution to a life-history puzzle. Oecologia 155:215–225

    Article  PubMed  Google Scholar 

  • Karl I, Lorenz MW, Fischer K (2007) Energetics of reproduction: consequences of divergent selection on egg size, food limitation, and female age for egg composition and reproductive effort in a butterfly. Biol J Linn Soc 91:403–418

    Article  Google Scholar 

  • Larsen TB (1991) The butterflies of Kenya and their natural history. Oxford University Press, Oxford

    Google Scholar 

  • Liu SS, Zhang GM, Zhu J (1995) Influence of temperature-variations on rate of development in insects—analysis of case-studies from entomological literature. Ann Entomol Soc Am 88:107–119

    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  Google Scholar 

  • Lyytinen A, Brakefield PM, Lindstrom L, Mappes J (2004) Does predation maintain eyespot plasticity in Bicyclus anynana? Proc R Soc Lond B Biol Sci 271:279–283

    Article  Google Scholar 

  • Marshall DJ, Uller T (2007) When is a maternal effect adaptive? Oikos 116:1957–1963

    Article  Google Scholar 

  • McIntyre GS, Gooding RH (2000) Egg size, contents, and quality: maternal-age and -size effects on house fly eggs. Can J Zool 78:1544–1551

    Article  Google Scholar 

  • Miner BG, Sultan SE, Morgan SG, Padilla DK, Relyea RA (2005) Ecological consequences of phenotypic plasticity. Trends Ecol Evol 20:685–692

    Article  PubMed  Google Scholar 

  • Mousseau TA, Dingle H (1991) Maternal effects in insect life histories. Annu Rev Entomol 36:511–534

    Article  Google Scholar 

  • Mousseau TA, Fox CW (1998a) The adaptive significance of maternal effects. Trends Ecol Evol 13:403–407

    Article  Google Scholar 

  • Mousseau TA, Fox CW (1998b) Maternal effects as adaptations. Oxford University Press, New York

    Google Scholar 

  • Nijhout HF (1999) Control mechanisms of polyphenic development in insects - in polyphenic development, environmental factors alter same aspects of development in an orderly and predictable way. Bioscience 49:181–192

    Article  Google Scholar 

  • Pigliucci M (2005) Evolution of phenotypic plasticity: where are we going now? Trends Ecol Evol 20:481–486

    Article  PubMed  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 

  • Rose MR, Bradley TJ (1998) Evolutionary physiology of the cost of reproduction. Oikos 83:443–451

    Article  Google Scholar 

  • Rossiter MC (1996) Incidence and consequences of inherited environmental effects. Annu Rev Ecol Syst 27:451–476

    Article  Google Scholar 

  • Sakwínska O (2004) Persistent maternal identity effects on life history traits in Daphnia. Oecologia 138:379–386

    Article  PubMed  Google Scholar 

  • Silbernagel S, Despopolos A (1991) Taschenatlas der physiologie. Thieme, Stuttgart

    Google Scholar 

  • Stearns SC (1989) The evolutionary significance of phenotypic plasticity—phenotypic sources of variation among organisms can be described by developmental switches and reaction norms. Bioscience 39:436–445

    Article  Google Scholar 

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

    Google Scholar 

  • Steigenga MJ, Zwaan BJ, Brakefield PM, Fischer K (2005) The evolutionary genetics of egg size plasticity in a butterfly. J Evol Biol 18:281–289

    Article  PubMed  CAS  Google Scholar 

  • Thompson SN, Borchardt DB, Wang LW (2003) Dietary nutrient levels regulate protein and carbohydrate intake, gluconeogenic/glycolytic flux and blood trehalose level in the insect Manduca sexta L. J Comp Physiol B 173:149–163

    PubMed  CAS  Google Scholar 

  • Van Handel E (1993) Fuel metabolism of the mosquito (Culex quinquefasciatus) embryo. J Insect Physiol 39:831–833

    Article  Google Scholar 

  • Van’t Hof AE, Zwaan BJ, Saccheri IJ, Daly D, Bot ANM, Brakefield PM (2005) Characterization of 28 microsatellite loci for the butterfly Bicyclus anynana. Mol Ecol Notes 5:169–172

    Article  Google Scholar 

  • Wagner TL, Wu HI, Sharpe PJH, Schoolfield RM, Coulson RN (1984) Modeling insect development rates—a literature-review and application of a biophysical model. Ann Entomol Soc Am 77:208–225

    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 

  • Wilson RS, Franklin CE (2002) Testing the beneficial acclimation hypothesis. Trends Ecol Evol 17:66–70

    Article  Google Scholar 

  • Windig JJ (1994) Reaction norms and the genetic-basis of phenotypic plasticity in the wing pattern of the butterfly Bicyclus anynana. J Evol Biol 7:665–695

    Article  Google Scholar 

  • Wolf JB, Brodie ED (1998) The coadaptation of parental and offspring characters. Evolution 52:299–308

    Article  Google Scholar 

  • Woods HA, Harrison JF (2002) Interpreting rejections of the beneficial acclimation hypothesis: when is physiological plasticity adaptive? Evolution 56:1863–1866

    PubMed  Google Scholar 

  • Ziegler R, Van Antwerpen R (2006) Lipid uptake by insect oocytes. Insect Biochem Mol Biol 36:264–272

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank Susann Janowitz and Jana Perlick for helping out on two occasions with the experiments. Financial support was provided by the German Research Foundation (DFG grants Fi 846/1-3 and 1-4 to KF, DFG grants Lo 697/4-3 and 4-4 to MWL and a scholarship within the Graduate College 678/2 to TLG).

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Authors and Affiliations

  1. Department of Animal Ecology I, University of Bayreuth, 95440, Bayreuth, P.O. Box 101251, Germany

    Thorin L. Geister, Matthias W. Lorenz, Klaus H. Hoffmann & Klaus Fischer

  2. Zoological Institute and Museum, University of Greifswald, 17489, Greifswald, Germany

    Klaus Fischer

Authors
  1. Thorin L. Geister
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  2. Matthias W. Lorenz
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  3. Klaus H. Hoffmann
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  4. Klaus Fischer
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Correspondence to Thorin L. Geister.

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Communicated by G. Heldmaier.

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Geister, T.L., Lorenz, M.W., Hoffmann, K.H. et al. Energetics of embryonic development: effects of temperature on egg and hatchling composition in a butterfly. J Comp Physiol B 179, 87–98 (2009). https://doi.org/10.1007/s00360-008-0293-5

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  • DOI: https://doi.org/10.1007/s00360-008-0293-5

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