Skip to main content
Log in

The devil in the details of life-history evolution: Instability and reversal of genetic correlations during selection onDrosophila development

  • Published:
Journal of Genetics Aims and scope Submit manuscript

Abstract

The evolutionary relationships between three major components of Darwinian fitness, development rate, growth rate and preadult survival, were estimated using a comparison of 55 distinct populations ofDrosophila melanogaster variously selected for age-specific fertility, environmental-stress tolerance and accelerated development. Development rate displayed a strong net negative evolutionary correlation with weight at eclosion across all selection treatments, consistent with the existence of a size-versus-time tradeoff between these characters. However, within the data set, the magnitude of the evolutionary correlation depended upon the particular selection treatments contrasted. A previously proposed tradeoff between preadult viability and growth rate was apparent only under weak selection for juvenile fitness components. Direct selection for rapid development led to sharp reductions in both growth rates and viability. These data add to the mounting results from experimental evolution that illustrate the sensitivity of evolutionary correlations to (i) genotype-by-environment (G X E) interaction, (ii) complex functional-trait interactions, and (iii) character definition. Instability, disappearance and reversal of patterns of genetic covariation often occur over short evolutionary time frames and as the direct product of selection, rather than some stochastic process. We suggest that the functional architecture of fitness is a rapidly evolving matrix with reticulate properties, a matrix that we understand only poorly.

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.

Institutional subscriptions

Similar content being viewed by others

References

  • Ackermann M., Bijlsma R., James A. C., Partridge L., Zwaan B. J. and Stearns S. C. 2001 Effects of assay conditions in life-history experiments withDrosophila melanogaster.J. Evol. Biol. 14, 199–209.

    Article  Google Scholar 

  • Archer M. A., Phelan J. P., Beckman K. A. and Rose M. R. 2003 Breakdown in correlations during laboratory evolution. II. Comparative analyses ofDrosophila populations.Evolution 57, 536–543.

    PubMed  Google Scholar 

  • Bell A. E. and Burris M. J. 1973 Simultaneous selection for two correlated traits inTribolium.Genet. Res. 21, 29–46.

    Article  Google Scholar 

  • Bell G. 1997Selection: the mechanism of evolution. Chapman and Hall, New York.

    Google Scholar 

  • Cheverud J. M. 1984 Quantitative genetics and developmental constraints on evolution by selection.J. Theor. Biol. 110, 155–171.

    PubMed  CAS  Google Scholar 

  • Chippindale A. K., Leroi A. M., Kim S. B. and Rose M. R. 1993 Phenotypic plasticity and selection inDrosophila lifehistory evolution. I. Nutrition and the cost of reproduction.J. Evol. Biol. 6, 171–193.

    Article  Google Scholar 

  • Chippindale A. K., Hoang D. T., Service P. M. and Rose M. R. 1994 The evolution of development inDrosophila selected for postponed senescence.Evolution 48, 1880–1899.

    Article  Google Scholar 

  • Chippindale A. K., Chu T. J. F. and Rose M. R. 1996 Complex tradeoffs and the evolution of starvation resistance inDrosophila.Evolution 50, 753–766.

    Article  Google Scholar 

  • Chippindale A. K., Alipaz J. A., Chen H.-W. and Rose M. R. 1997 Experimental evolution of accelerated development inDrosophila. 1. Larval development speed and survival.Evolution 51, 1536–1551.

    Article  Google Scholar 

  • Chippindale A. K., Gibbs A. G., Sheik M., Yee K. J., Djawdan M., Bradley T. J. and Rose M. R. 1998 Resource acquisition and the evolution of stress resistance inDrosophila melanogaster.Evolution 52, 1342–1352.

    Article  Google Scholar 

  • Chippindale A. K., Alipaz J. A. and Rose M. R. Experimental evolution of accelerated development inDrosophila. 2. Adult fitness and the fast development syndrome. InMethuselah flies: a case study in laboratory evolution (ed. M. R. Rose, H. K. Passananti and M. Matos). World Scientific, New York (in press).

  • Clark A. G. 1987 Genetic correlations: the quantitative genetics of evolutionary constraints. InGenetic constraints on adaptive evolution (ed. V. Loeschcke), pp. 25–45. Springer, Berlin.

    Google Scholar 

  • Clayton G. A., Knight G. R., Morris J. A. and Robertson A. 1957 An experimental check on quantitative genetic theory. I. Short-term responses to selection.J. Genet. 55, 171–180.

    Google Scholar 

  • Crill W. D., Huey R. B. and Gilchrist G. W. 1996 Within- and between-generation effects of temperature on the morphology and physiology ofDrosophila melanogaster.Evolution 50, 1205–1218.

    Article  Google Scholar 

  • Djawdan M., Chippindale A. K., Rose M. R. and Bradley T. J. 1998 Metabolic reserves and evolved stress resistance inDrosophila melanogaster.Physiol. Zool. 71, 584–559.

    PubMed  CAS  Google Scholar 

  • Gibbs A. G. 1999 Laboratory selection for the comparative physiologist.J. Exp. Biol. 202, 2709–2718.

    PubMed  CAS  Google Scholar 

  • Hoffmann A. A. and Harshman L. G. 2000 Laboratory selection experiments using Drosophila: what do they really tell us?Trends Ecol. Evol. 15, 32–36.

    Article  PubMed  Google Scholar 

  • Houle D. 1991 Genetic covariance of fitness correlates: what genetic correlations are made of and why it matters.Evolution 45, 630–648.

    Article  Google Scholar 

  • Houle D. and Rowe L. 2003 Natural selection in a bottle.Am. Nat. 161, 50–67.

    Article  PubMed  Google Scholar 

  • Ives P. T. 1970 Further studies of the South Amherst population ofDrosophila melanogaster.Evolution 38, 507–518.

    Article  Google Scholar 

  • Lande R. 1982 A quantitative genetic theory of life history evolution.Ecology 63, 607–615.

    Article  Google Scholar 

  • Leroi A. M., Chippindale A. K. and Rose M. R. 1994a Longterm laboratory evolution of a genetic life-history trade-offStability of genetic inDrosophila melanogaster. 1. The role of genotype-by-environment interaction.Evolution 48, 1244–1257.

    Article  Google Scholar 

  • Leroi A. M., Chen W. R. and Rose M. R. 1994b Long-term laboratory evolution of a genetic life-history trade-off inDrosophila melanogaster. 2. Stability of genetic correlations.Evolution 48, 1258–1268.

    Article  Google Scholar 

  • Lints F. A. and Gruwez G. 1972 What determines the duration of development inDrosophila melanogaster?Mech. Ageing Dev. 1, 285–297.

    Google Scholar 

  • Matos M. and Avelar T. 2001 Adaptation to the laboratory: comments on SgrÒ and Partridge.Am. Nat. 158, 655–656.

    Article  PubMed  CAS  Google Scholar 

  • Matos M., Rose M. R., Rocha Pité M. T., Rego C. and Avelar T. 2000 Adaptation to the laboratory environment inDrosophila subobscura.J. Evol. Biol. 13, 9–19.

    Article  Google Scholar 

  • Matos M., Avelar T. and Rose M. R. 2002 Variation in the rate of convergent evolution: adaptation to a laboratory environment inDrosophila subobscura.J. Evol. Biol. 15, 673–682.

    Article  Google Scholar 

  • Maynard Smith J., Burian R., Kauffman S., Alberch P., Campbell J., Goodwin B., Lande R., Raup D. and Wolpert L. 1985 Developmental constraints and evolution.Quart. Rev. Biol. 60, 265–287.

    Article  Google Scholar 

  • Mueller L. D. 1985 The evolutionary ecology ofDrosophila.Evol. Biol. 19, 37–98.

    Google Scholar 

  • Nunney L. 1996 The response to selection for fast larval development inDrosophila and its effect on adult weight: an example of a fitness tradeoff.Evolution 50, 1193–1204.

    Article  Google Scholar 

  • Partridge L. and Farquhar M. 1983 Lifetime mating success of male fruitflies (Drosophila melanogaster) is related to their size.Anim. Behav. 31, 871–877.

    Article  Google Scholar 

  • Partridge L. and Fowler K. 1992 Direct and correlated responses to selection on age at reproduction inDrosophila melanogaster.Evolution 46, 76–91.

    Article  Google Scholar 

  • Partridge L., Hoffmann A. A. and Jones J. S. 1987 Male size and mating success inDrosophila melanogaster andDrosophila pseudoobscura under field conditions.Anim. Behav. 35, 468–476.

    Article  Google Scholar 

  • Phelan J. P., Archer M. A., Beckman K. A., Chippindale A. K. and Rose M. R. 2003 Breakdown in correlations during laboratory evolution. I. Comparative analyses ofDrosophila populations.Evolution 57, 527–535.

    PubMed  Google Scholar 

  • Prasad N. G., Shakarad M., Gohil V. M., Sheeba V., Rajamani M. and Joshi A. 2000 Evolution of reduced pre-adult viability and larval growth rate in laboratory populations ofDrosophila melanogaster selected for shorter development time.Genet. Res. 76, 249–259.

    Article  PubMed  CAS  Google Scholar 

  • Reznick D. 1992 Measuring the costs of reproduction.Trends Ecol. Evol. 7, 42–45.

    Article  Google Scholar 

  • Robertson F. W. 1957 Studies in quantitative inheritance. XI. Genetic and environmental correlation between body size and egg production inDrosophila melanogaster.J. Genet. 55, 428–443.

    Article  Google Scholar 

  • Roff D. 1992The evolution of life histories. Chapman and Hall, New York.

    Google Scholar 

  • Roper C., Pignatelli P. and Partridge L. 1993 Evolutionary effects of selection on age at reproduction in larval and adultDrosophila melanogaster.Evolution 47, 445–455.

    Article  Google Scholar 

  • Rose M. R. 1984 Laboratory evolution of postponed senescence inDrosophila melanogaster.Evolution 38, 1004–1010.

    Article  Google Scholar 

  • Rose M. R., Graves J. L. and Hutchinson E. W. 1990 The use of selection to probe patterns of fitness characters. InInsect life cycles: genetics, evolution and coordination (ed. F. Gilbert), pp. 29–41. Springer, New York.

    Google Scholar 

  • Rose M. R., Vu L. N., Park S. U. and Graves J. L. 1992 Selection on stress resistance increases longevity inDrosophila melanogaster.Exp. Gerontol. 27, 241–250.

    Article  PubMed  CAS  Google Scholar 

  • Rose M. R., Nusbaum T. J. and Chippindale A. K. 1996 Laboratory selection: the experimental wonderland and the Cheshire Cat syndrome. InAdaptation (ed. M. R. Rose and G. V. Lauder), pp. 221–242. Academic Press, San Diego.

    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 

  • Service P. M., Hutchinson E. W. and Rose M. R. 1988 Multiple genetic mechanisms for the evolution of postponed senescence inDrosophila melanogaster.Evolution 42, 708–716.

    Article  Google Scholar 

  • Sgró C. M. and Partridge L. 2000 Evolutionary responses of the life history of wild-caughtDrosophila melanogaster to two standard methods of laboratory culture.Am. Nat. 156, 341–353.

    Article  Google Scholar 

  • Sgró C. M. and Partridge L. 2001 Laboratory adaptation of life history inDrosophila.Am. Nat. 158, 657–658.

    Article  PubMed  Google Scholar 

  • Shakarad M., Prasad N. G., Rajamani M. and Joshi A. 2001 Evolution of faster development does not lead to greater fluctuating asymmetry of sternopleural bristle number inDrosophila.J. Genet. 80, 1–7.

    PubMed  CAS  Google Scholar 

  • Stearns S. C. 1992The evolution of life histories. Oxford University Press, Oxford.

    Google Scholar 

  • Wilkinson G. S., Fowler K. and Partridge L. 1990 Resistance of genetic correlation structure to directional selection inDrosophila melanogaster.Evolution 44, 1990–2003.

    Article  Google Scholar 

  • Zwaan B. J., Bijlsma R. and Hoekstra R. F. 1995 Artificial selection for developmental time inDrosophila melanogaster in relation to the evolution of aging: direct and correlated responses.Evolution 49, 635–648.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Adam K. Chippindale.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Chippindale, A.K., Ngo, A.L. & Rose, M.R. The devil in the details of life-history evolution: Instability and reversal of genetic correlations during selection onDrosophila development. J Genet 82, 133–145 (2003). https://doi.org/10.1007/BF02715814

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02715814

Keywords

Navigation