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Different growth responses to temperature and resource limitation in three fly species with similar life histories

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Abstract

Growth responses to temperature and resource limitation in three dipteran species with similar life histories were compared. With respect to current life history theory, two points are raised. First, growth rate in real time increased steeply with temperature in all species, following the standard pattern. However, when expressed in physiological time growth rate increased as temperature decreased in the yellow dung fly Scathophaga stercoraria, remained approximately constant in Sepsis cynipsea, and increased in Drosophila melanogaster. These responses can be understood as adaptations to climate and seasonality. It is concluded that some patterns of adaptation may be more easily interpreted if, and some may even go undetected unless, they are analysed in physiological time. Second, a decrease in body size, development rate and growth rate when resources are limited is believed to be nearly universal and generally predicted by life history models. Despite their similar life histories, the three species investigated showed qualitatively different growth responses to larval food shortage. At unlimited resources, yellow dung flies showed the fastest initial larval body mass gain per unit time, while those of S. cynipsea and D. melanogaster were lower and about equal. The period of no body mass gain at the end of larval development was longest in S. stercoraria and shortest in S. cynipsea. When facing resource limitation, S. stercoraria emerged smaller but earlier (thus nearly maintaining their growth rate), S. cynipsea smaller after the same development period, and D. melanogaster smaller and later (showing reduced and much reduced growth, respectively). It is concluded that whether growth really slows when resources are limited depends on the precise ecological circumstances of the species in question. More refined models, particularly those where mortality costs are independent of time, and more experiments are necessary to account for the variation in growth and size and age at maturity present in nature.

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References

  • Abrams, P.A., Leimar, O., Nylin, S. and Wiklund, C. (1996) The effect of flexible growth rates on optimal sizes and development times in a seasonal environment. Am. Nat. 147, 381–395.

    Article  Google Scholar 

  • Anholt, B.R. and Werner, E.E. (1995) Interaction between food availability and predation mortality mediated by adaptive behavior. Ecology 76, 2230–2234.

    Article  Google Scholar 

  • Arnold, C.Y. (1959) The determination and significance of the base temperature in a linear heat unit system. J. Am. Soc. Hortic. Sci. 74, 430–445.

    Google Scholar 

  • Arnold, C.Y. (1960) Maximum-minimum temperatures as a basis for computing heat units. J. Am. Soc. Hortic. Sci. 76, 682–692.

    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. (1995) Effects of temperature on the size of aquatic ectotherms: exceptions to the general rule. J. Therm. Biol. 20, 61–74.

    Article  Google Scholar 

  • Atkinson, D. and Sibly, R.M. (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 

  • Bakker, K. (1959) Feeding period, growth, and pupation in larvae of Drosophila melanogaster. Ent. Exp. Appl. 2, 171–186.

    Article  Google Scholar 

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

    Google Scholar 

  • Berrigan, D. and Koella, J.C. (1994) The evolution of reaction norms: simple models for age and size at maturity. J. Evol. Biol. 7, 549–566.

    Article  Google Scholar 

  • Blanckenhorn, W.U. (1994) Fitness consequences of alternative life histories in water striders, Aquarius remigis. Oecologia 97, 354–365.

    Google Scholar 

  • Blanckenhorn, W.U. (1997a) Effects of temperature on growth, development and diapause in the yellow dung fly — against all the rules? Oecologia 111, 318–324.

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Blanckenhorn, W.U. (1998a) Adaptive phenotypic plasticity in growth, development, and diapause in the yellow dung fly. Evolution 52, 1394–1407.

    Article  Google Scholar 

  • Blanckenhorn, W.U. (1998b) Altitudinal differentiation in diapause response in two species of dung flies. Ecol. Entomol. 23, 1–8.

    Article  Google Scholar 

  • Blanckenhorn, W.U., Reusch, T. and Mühlhäuser, C. (1998) Fluctuating asymmetry, body size and sexual selection in the dung fly Sepsis cynipsea — testing the good genes assumptions and predictions. J. Evol. Biol. 11, 735–753.

    Article  Google Scholar 

  • Church, R.B. and Robertson, F.W. (1966) Biochemical analysis of genetic differences in the growth of Drosophila. Genet. Res. Camb. 7, 383–407.

    CAS  Google Scholar 

  • Danks, H.V. (1987) Insect Dormancy: An Ecological Perspective. Biological Survey of Canada, Ottawa.

    Google Scholar 

  • David, J. and Clavel, M.-F. (1967a) Influence de la température subie au cours du développement sur divers caractères biométriques des adultes de Drosophila melanogaster. J. Ins. Physiol. 13, 717–729.

    Article  CAS  Google Scholar 

  • David, J. and Clavel, M.-F. (1967b) Influence de la température d'élévage sur la mortalité larvonymphale et la durée de développement de la Drosophile. Nat. Can. 94, 209–219.

    Google Scholar 

  • Eigenbrodt, H.J. (1930) The somatic effects of temperature on a homozygous race of Drosophila. Physiol. Zool. 3, 392–411.

    Google Scholar 

  • Fox, C.W., Martin, J.D., Thakar, M.S. and Mousseau, T.A. (1996) Clutch size manipulations in two seed beetles: consequences for progeny fitness. Oecologia 108, 88–94.

    Article  Google Scholar 

  • Fraser, D.F. and Gilliam, J.F. (1992) Nonlethal impacts of predator invasion: facultative suppression of growth and reproduction. Ecology 73, 959–970.

    Article  Google Scholar 

  • Gilbert, P., Moreteau, B. Moreteau, J.-C. and David, J.R. (1996) Growth temperature and adult pigmentation in two Drosophila sibling species: an adaptive convergence of reaction norms in sympatric populations? Evolution 50, 2346–2353.

    Article  Google Scholar 

  • Janisch, E. (1925) Über die Temperaturabhängigkeit biologischer Vorgänge und ihre kurvenmässige Analyse. Pflügers Arch. Physiol. 209, 414–436.

    Article  Google Scholar 

  • Kawecki, T.J. and Stearns, S.C. (1993) The evolution of life histories in spatially heterogeneous environments: optimal reaction norms revisited. Evol. Ecol. 7, 155–174.

    Article  Google Scholar 

  • Kozlowski, J. (1992) Optimal allocation of resources to growth and reproduction: implications for age and size at maturity. Trends Ecol. Evol. 7, 15–19.

    Article  Google Scholar 

  • Kozlowski, J. and Wiegert, R.G. (1987) Optimal age and size at maturity in annuals and perennials with determinate growth. Evol. Ecol. 1, 231–244.

    Article  Google Scholar 

  • Morf, C. (1997) Saisonale, tageszeitliche und räumliche Variation der sexuellen Selektion bei der Schwingfliege Sepsis cynipsea. Diploma Thesis, University of Zürich.

  • Møller, H., Smith, R.H. and Sibly, R.M. (1989a) Evolutionary demography of a bruchid beetle. I. Quantitative genetical analysis of the female life history. Funct. Ecol. 3, 673–681.

    Article  Google Scholar 

  • Møller, H., Smith, R.H. and Sibly, R.M. (1989b) Evolutionary demography of a bruchid beetle. II. Physiological manipulations. Funct. Ecol. 3, 683–691.

    Article  Google Scholar 

  • Mühlhäuser, C., Blanckenhorn, W.U. and Ward, P.I. (1996) The genetic component of copula duration in the yellow dung fly. Anim. Behav. 51, 1401–1407.

    Article  Google Scholar 

  • Negus, N.C., Berger, P.J. and Pinter, A.J. (1992) Phenotypic plasticity of the montane vole (Microtus montanus) in unpredictable environments. Can. J. Zool. 68, 619–640.

    Google Scholar 

  • Newman, R.A. (1992) Adaptive plasticity in amphibian metamorphosis. Bioscience 42, 671–678.

    Article  Google Scholar 

  • Nijhout, H.F. (1994) Insect Hormones. Princeton University Press, Princeton, NJ.

    Google Scholar 

  • Nunney, L. (1996) The response to selection for fast larval development in Drosophila melanogaster and its effect on adult weight: an example of a fitness trade-off. Evolution 50, 1193–1204.

    Article  Google Scholar 

  • Nylin, S., Gotthard, K. and Wiklund, C. (1996) Reaction norms for age and size at maturity in Lasiommata butterflies: predictions and tests. Evolution 50, 1351–1358.

    Article  Google Scholar 

  • Prosser, C.L. (1973) Comparative Animal Physiology. W.B. Saunders Co, Philadelphia, PA.

    Google Scholar 

  • Prowser, L. (1935) The effects of temperature on the durations of the developmental stages of Drosophila melanogaster. Physiol. Zool. 8, 474–520.

    Google Scholar 

  • Ratte, H.T. (1985) Temperature and Insect development. In K.H. Hoffman (ed.) Environmental Physiology and Biochemistry of Insects, Springer, Heidelberg, pp. 31–66.

    Google Scholar 

  • Robertson, F.W. (1963) The ecological genetics of growth in Drosophila. 6. The genetic correlation between the duration of the larval period and body size in relation to larval diet. Genet. Res. Camb. 4, 74–92.

    Google Scholar 

  • Roff, D.A. (1984) The evolution of life history parameters in teleosts. Can. J. Fish. Aquat. Sci. 41, 989–1000.

    Article  Google Scholar 

  • Roff, D.A. (1986) Predicting body size with life history models. Bioscience 36, 316–323.

    Article  Google Scholar 

  • Roff, D.A. (1992) The Evolution of Life Histories: Theory and Analysis. Chapman and Hall, New York, NY.

    Google Scholar 

  • Rowe, L. and Ludwig, D. (1991) Size and timing of metamorphosis in complex life cycles: time constraints and variation. Ecology 72, 413–427.

    Article  Google Scholar 

  • Schmidt-Nielsen, K. (1983) Animal Physiology: Adaptation and Environment, 3rd ed. Cambridge University Press, Cambridge.

    Google Scholar 

  • Schulz, K. (1989) Vergleichende Untersuchung zur Biologie einiger kuhfladenbewohnender Arten der Gattung Sepsis (Diptera, Sepsidae). Diploma thesis, Free University Berlin.

  • Shorrocks, B. (1970) Population fluctuations in the fruit fly (Drosophila melanogaster) maintained in the laboratory. J. Anim. Ecol. 39, 229–253.

    Article  Google Scholar 

  • Sibly, R.M. and Atkinson, D. (1994) How rearing temperature affects optimal adult size in ectotherms. Funct. Ecol. 8, 486–493.

    Article  Google Scholar 

  • Sokal, R.R. and Rohlf, F.J. (1995) Biometry. Freeman and Co, New York, NY.

    Google Scholar 

  • Stearns, S.C. (1992) The Evolution of Life Histories. Oxford University Press, Oxford.

    Google Scholar 

  • Stearns, S.C. and Koella, J. (1986) The evolution of phenotypic plasticity in life history traits: predictions of reaction norms for age and size at maturity. Evolution 40, 893–914.

    Article  Google Scholar 

  • Sweeney, B.W. and Vannote, R.L. (1978) Size variation and the distribution of hemimetabolous aquatic insects: two thermal equilibrium hypotheses. Science 200, 444–446.

    PubMed  Google Scholar 

  • Tabachnick, B.G. and Fidell, L.S. (1989) Using Multivariate Statistics. Harper and Row, New York, NY.

    Google Scholar 

  • Taylor, F. (1981) Ecology and evolution of physiological time in insects. Am. Nat. 117, 1–23.

    Article  Google Scholar 

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

    Article  Google Scholar 

  • van Straalen, N.M. (1983) Physiological time and time-invariance. J. Theor. Biol. 104, 349–357.

    Article  PubMed  CAS  Google Scholar 

  • Visser, M.E. (1994) The importance of being large: the relationship between size and fitness in females of the parasitoid Aphaereta minuta (Hymenoptera: Braconidae). J. Anim. Ecol. 63, 963–978.

    Article  Google Scholar 

  • Wang, J.Y. (1960) A critique of the heat unit approach to plant response studies. Ecology 41, 785–790.

    Article  Google Scholar 

  • Wigglesworth, V.B. (1972) The Principles of Insect Physiology, 7th edn. Chapman and Hall, London.

    Google Scholar 

  • Wilbur, H.M. and Collins, J.P. (1973) Ecological aspects of amphibian metamorphosis. Science 182, 1305–1314.

    PubMed  Google Scholar 

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Blanckenhorn, W.U. Different growth responses to temperature and resource limitation in three fly species with similar life histories. Evolutionary Ecology 13, 395–409 (1999). https://doi.org/10.1023/A:1006741222586

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