Journal of Genetics

, Volume 82, Issue 3, pp 179–189 | Cite as

Thermal adaptation inDrosophila serrata under conditions linked to its southern border: Unexpected patterns from laboratory selection suggest limited evolutionary potential

  • Andréa Magiafoglou
  • Ary Hoffmann


To investigate the ability ofDrosophila serrata to adapt to thermal conditions over winter at the species southern border, replicate lines from three source locations were held as discrete generations over three years at either 19‡C (40 generations) or temperatures fluctuating between 7‡C and 18δC (20 generations). Populations in the fluctuating environment were maintained either with an adult 0‡C cold shock or without a shock. These conditions were expected to result in temperature-specific directional selection for increased viability and productivity under both temperature regimes, and reduced development time under the fluctuating-temperature regime. Selection responses of all lines were tested under both temperature regimes after controlling for carry-over effects by rearing lines in these environments for two generations. When tested in the 19‡C environment, lines evolving at 19‡C showed a faster development time and a lower productivity relative to the other lines, while cold shock reduced development time and productivity of all lines. When tested in the fluctuating environment, productivity of the 7–18‡C lines selected with a cold shock was relatively lower than that of lines selected without a shock, but this pattern was not observed in the other populations. Viability and body size as measured by wing length were not altered by selection or cold shock, although there were consistent effects of source population on wing length. These results provide little evidence for temperature-specific adaptation inD. serrata —although the lines had diverged for some traits, these changes were not consistent with a priori predictions. In particular, there was no evidence for life-history changes reflecting adaptation to winter conditions at the southern border. The potential forD. serrata to adapt to winter conditions may therefore be limited.


species borders central and marginal populations cold shock selection thermal adaptation 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Arnold S. J. 1992 Constraints on phenotypic evolution.Am. Nat. 140, S85-S107.CrossRefGoogle Scholar
  2. Azevedo R. B. R., French V. and Partridge L. 1996 Thermal evolution of egg size inDrosophila melanogaster.Evolution 50, 2338–2345.CrossRefGoogle Scholar
  3. Baer C. F. and Travis J. 2000 Direct and correlated responses to artificial selection on acute thermal stress tolerance in a livebearing fish.Evolution 54, 238–244.PubMedGoogle Scholar
  4. Barton N. H. and Turelli M. 1989 Evolutionary quantitative genetics: how little do we know?Annu. Rev. Genet. 23, 337–370.PubMedGoogle Scholar
  5. Blows M. W. 1993 The genetics of central and marginal populations ofDrosophila serrata. 2. Hybrid breakdown in fitness components as a correlated response to selection for desiccation resistance.Evolution 47, 1271–1285.CrossRefGoogle Scholar
  6. Blows M. W. and Hoffmann A. A. 1993 The genetics of central and marginal populations ofDrosophila serrata. 1. Genetic variation for stress resistance and species borders.Evolution 47, 1255–1270.CrossRefGoogle Scholar
  7. Blows M. W. and Hoffmann A. A. 1996 Evidence for an association between nonadditive genetic variation and extreme expression of a trait.Am. Nat. 148, 576–587.CrossRefGoogle Scholar
  8. Brussard P. F. 1984 Geographic patterns and environmental gradients: the central-marginal model inDrosophila revisited.Annu. Rev. Ecol. Syst. 15, 25–64.CrossRefGoogle Scholar
  9. Bubliy O. A., Riihimaa A., Norry F. M. and Loeschcke V. 2002 Variation in resistance and acclimation to low-temperature stress among three geographical strains ofDrosophila melanogaster.J. Therm. Biol. 27, 337–344.CrossRefGoogle Scholar
  10. Case T. J. and Taper M. L. 2000 Interspecific competition, environmental gradients, gene flow, and the coevolution of species’ borders.Am. Nat. 155, 583–605.PubMedCrossRefGoogle Scholar
  11. Cavicchi S., Guerra D., Natali V., Pezzoli C. and Giorgi G. 1989 Temperature-related divergence in experimental populations ofDrosophila melanogaster. II. Correlation between fitness and body dimensions.J. Evol. Biol. 2, 235–251.CrossRefGoogle Scholar
  12. Cavicchi S., Gianfranco G., Natali V. and Guerra D. 1991 Temperature-related divergence in experimental populations ofDrosophila melanogaster. III. Fourier and centroid analysis of wing shape and relationship between shape variation and fitness.J. Evol. Biol. 4, 141–159.CrossRefGoogle Scholar
  13. Cheverud J. M. 1984 Quantitative genetics and developmental constraints on evolution by selection.J. Theor. Biol. 110, 155–171.PubMedGoogle Scholar
  14. Cohan F. M. and Graf J.-D. 1985 Latitudinal cline inDrosophila melanogaster for knockdown resistance to ethanol fumes and for rates of response to selection for further resistance.Evolution 39, 278–293.CrossRefGoogle Scholar
  15. Crespi B. J. 2000 The evolution of maladaptation.Heredity 84, 623–629.PubMedCrossRefGoogle Scholar
  16. Dhondt A. A., Adriaensen F., Matthysen E. and Kempenaers B. 1990 Non-adaptive clutch sizes in tits.Nature 348, 723–725.CrossRefGoogle Scholar
  17. Foley P. A. and Luckinbill L. S. 2001 The effects of selection for larval behavior on adult life-history features inDrosophila melanogaster.Evolution 55, 2493–2502.PubMedGoogle Scholar
  18. Garcia-Ramos G. and Kirkpatrick M. 1997 Genetic models of adaptation and gene flow in peripheral populations.Evolution 51, 21–28.CrossRefGoogle Scholar
  19. Gibbs A. G., Chippindale A. K. and Rose M. R. 1997 Physiological mechanisms of evolved desiccation resistance inDrosophila melanogaster.J. Exp. Biol. 200, 1821–1832.PubMedGoogle Scholar
  20. Gilchrist G. W., Huey R. B. and Partridge L. 1997 Thermal sensitivity ofDrosophila melanogaster-evolutionary responses of adults and eggs to laboratory natural selection at different temperatures.Physiol. Zool. 70, 403–414.PubMedCrossRefGoogle Scholar
  21. Harshman L. G. and Hoffmann A. A. 2000 Laboratory selection experiments using Drosophila: what do they really tell us?Trends Ecol. Evol. 15, 32–36.PubMedCrossRefGoogle Scholar
  22. Hercus M. J. and Hoffmann A. A. 1999 Does interspecific hybridization influence evolutionary rates? An experimental study of laboratory adaptation in hybrids betweenDrosophila serrata andDrosophila birchii.Proc. R. Soc. London B266, 2195–2200.CrossRefGoogle Scholar
  23. Hicks C. R. 1973Fundamental concepts in the design of experiments, 2nd edition. Holt, Rinehart and Winston, New York.Google Scholar
  24. Hoffmann A. A. and Blows M. W. 1994 Species borders — ecological and evolutionary perspectives.Trends Ecol. Evol. 9, 223–227.CrossRefGoogle Scholar
  25. Hoffmann A. A. and Hercus M. J. 2000 Environmental stress as an evolutionary force.Bioscience 50, 217–226.CrossRefGoogle Scholar
  26. Hoffmann A. A., Sgró C. M. and Lawler S. H. 1995 Ecological population genetics — the interface between genes and the environment.Annu. Rev. Genet. 29, 349–370.PubMedCrossRefGoogle Scholar
  27. Hoffmann A. A., Hallas R., Sinclair C. and Partridge L. 2001 Rapid loss of stress resistance inDrosophila melanogaster under adaptation to laboratory culture.Evolution 55, 436–438.PubMedGoogle Scholar
  28. Hoffmann A. A., Hallas R., Dean J. A. and Schiffer M. 2003 Low potential for climatic stress adaptation in a rainforestDrosophila species.Science 301, 100–102.PubMedCrossRefGoogle Scholar
  29. Holt R. D. and Gomulkiewicz R. 1997 How does immigration influence local adaptation — a reexamination of a familiar paradigm.Am. Nat. 149, 563–572.CrossRefGoogle Scholar
  30. Huey R. B., Partridge L. and Fowler K. 1991 Thermal sensitivity ofDrosophila melanogaster responds rapidly to laboratory natural selection.Evolution 45, 751–756.CrossRefGoogle Scholar
  31. James A. C. and Partridge L. 1995 Thermal evolution of rate of larval development inDrosophila melanogaster in laboratory and field populations.J. Evol. Biol. 8, 315–330.CrossRefGoogle Scholar
  32. Jenkins N. L. 1999 Testing species borders hypotheses usingDrosophila serrata. Ph.D. thesis, La Trobe University, Melbourne, Australia.Google Scholar
  33. Jenkins N. L. and Hoffmann A. A. 1999 Limits to the southern border ofDrosophila serrata: cold resistance, heritable variation, and trade-offs.Evolution 53, 1823–1834.CrossRefGoogle Scholar
  34. Jenkins N. L. and Hoffmann A. A. 2000 Variation in morphological traits and trait asymmetry in fieldDrosophila serrata from marginal populations.J. Evol. Biol. 13, 113–130.CrossRefGoogle Scholar
  35. Jenkins N. L. and Hoffmann A. A. 2001 Distribution ofDrosophila serrata Malloch (Diptera: Drosophilidae) in Australia with particular reference to the southern border.Aust. J. Entomol. 40, 41–48.CrossRefGoogle Scholar
  36. Jenkins N. L., Sgró C. M. and Hoffmann A. A. 1997 Environmental stress and the expression of genetic variation. InEnvironmental stress, adaptation and evolution (ed. R. Bijlsma and V. Loeschcke), pp. 79–96. BirkhÄuser, Boston.Google Scholar
  37. Kennington W. J., Killeen J. R., Goldstein D. B. and Partridge L. 2003 Rapid laboratory evolution of adult wing area inDrosophila melanogaster in response to humidity.Evolution 57, 932–936.PubMedGoogle Scholar
  38. Kern S., Ackermann M., Stearns S. C. and Kawecki T. J. 2001 Decline in offspring viability as a manifestation of aging inDrosophila melanogaster.Evolution 55, 1822–1831.PubMedGoogle Scholar
  39. Kirkpatrick M. and Barton N. H. 1997 Evolution of a species range.Am. Nat. 150, 1–23.CrossRefGoogle Scholar
  40. Krebs R. A. and Loeschcke V. 1994a Costs and benefits of activation of the heat-shock response inDrosophila melanogaster.Funct. Ecol. 8, 730–737.CrossRefGoogle Scholar
  41. Krebs R. A. and Loeschcke V. 1994b Effects of exposure to short-term heat stress on fitness components inDrosophila melanogaster.J. Evol. Biol. 7, 39–49.CrossRefGoogle Scholar
  42. Krebs R. A. and Loeschcke V. 1996 Acclimation and selection for increased resistance to thermal stress inDrosophila buzzatii.Genetics 142, 471–479.PubMedGoogle Scholar
  43. Krebs R. A. and Loeschcke V. 1999 A genetic analysis of the relationship between life-history variation and heat-shock tolerance inDrosophila buzzatii.Heredity 83, 46–53.PubMedCrossRefGoogle Scholar
  44. Lammi A., Siikamaki P. and Mustajarvi K. 1999 Genetic diversity, population size, and fitness in central and peripheral populations of a rare plantLychnis viscaria.Conserv. Biol. 13, 1069–1078.CrossRefGoogle Scholar
  45. Lenormand T. 2002 Gene flow and the limits to natural selection.Trends Ecol. Evol. 17, 183–189.CrossRefGoogle Scholar
  46. Lenski R. E. and Bennett A. F. 1993 Evolutionary response ofEscherichia coli to thermal stress.Am. Nat. 142, S47-S64.CrossRefGoogle Scholar
  47. Linnen C., Tatar M. and Promislow D. 2001 Cultural artifacts: a comparison of senescence in natural, laboratory-adapted and artificially selected lines ofDrosophila melanogaster.Evol. Ecol. Res. 3, 877–888.Google Scholar
  48. Magiafoglou A. and Hoffmann A. A. 2003 Cross-generation effects due to cold exposure inDrosophila serrata.Funct. Ecol. 17, 664–672.CrossRefGoogle Scholar
  49. Magiafoglou A., Carew M. E. and Hoffmann A. A. 2002 Shifting clinal patterns and microsatellite variation inDrosophila serrata populations: a comparison of populations near the southern border of the species range.J. Evol. Biol. 15, 763–774.CrossRefGoogle Scholar
  50. 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.CrossRefGoogle Scholar
  51. Mayr E. 1963Animal species and evolution. Harvard University Press, Cambridge.Google Scholar
  52. Mockett R. J., Orr W. C., Rahmandar J. J., Sohal B. H. and Sohal R. S. 2001 Antioxidant status and stress resistance in long- and short-lived lines ofDrosophila melanogaster.Exp. Gerontol. 36, 441–463.PubMedCrossRefGoogle Scholar
  53. Partridge L. and Sibly R. 1991 Constraints in the evolution of life histories.Philos. Trans. R. Soc. London B332, 3–13.Google Scholar
  54. Partridge L., Barrie B., Fowler K. and French V. 1994a Thermal evolution of pre-adult life history traits inDrosophila melanogaster.J. Evol. Biol. 7, 645–663.CrossRefGoogle Scholar
  55. Partridge L., Barrie B., Fowler K. and French V. 1994b Evolution and development of body size and cell size inDrosophila melanogaster in response to temperature.Evolution 48, 1269–1276.CrossRefGoogle Scholar
  56. Partridge L., Barrie B., Barton N. H., Fowler K. and French V. 1995 Rapid laboratory evolution of adult life-history traits inDrosophila melanogaster in response to temperature.Evolution 49, 538–544.CrossRefGoogle Scholar
  57. Patton Z. J. and Krebs R. A. 2001 The effect of thermal stress on the mating behaviour of threeDrosophila species.Physiol. Biochem. Zool. 74, 783–788.PubMedCrossRefGoogle Scholar
  58. Prasad N. G., Shakarad M., Anitha D., Rajamani M. and Joshi A. 2001 Correlated responses to selection for faster development and early reproduction in Drosophila: the evolution of larval traits.Evolution 55, 1363–1372.PubMedGoogle Scholar
  59. Reeve J. P. and Fairbairn D. J. 1999 Change in sexual size dimorphism as a correlated response to selection on fecundity.Heredity 83, 697–706.PubMedCrossRefGoogle Scholar
  60. Scheiner S. M. 2002 Selection experiments and the study of phenotypic plasticity.J. Evol. Biol. 15, 889–898.CrossRefGoogle Scholar
  61. Sgró C. M. and Hoffmann A. A. 1998 Effects of stress combinations on the expression of additive genetic variation for fecundity inDrosophila melanogaster.Genet. Res. 72, 13–18.PubMedCrossRefGoogle Scholar
  62. Sgró C. M. and Partridge L. 2001 Laboratory adaptation of life history inDrosophila.Am. Nat. 158, 657–658.CrossRefPubMedGoogle Scholar
  63. Sheeba V., Sharma V. K., Shubha K., Chandrashekaran M. K. and Joshi A. 2000 The effect of different light regimes on adult life span inDrosophila melanogaster is partly mediated through reproductive output.J. Biol. Rhythms 15, 380–392.PubMedCrossRefGoogle Scholar
  64. van Klinken R. D. and Walter G. H. 2001 Larval hosts of Australian Drosophilidae (Diptera): A field survey in subtropical and tropical Australia.Aust. J. Entomol. 40, 163–179.CrossRefGoogle Scholar
  65. Watson M. J. O. and Hoffmann A. A. 1996 Acclimation, crossgeneration effects, and the response to selection for increased cold resistance inDrosophila.Evolution 50, 1182–1192.CrossRefGoogle Scholar
  66. Zamudio K. R., Huey R. B. and Crill W. D. 1995 Bigger isn’t always better — body size, developmental and parental temperature and male territorial success inDrosophila melanogaster.Anim. Behav. 49, 671–677.Google Scholar
  67. Zar J. H. 1996Biostatistical analysis. Prentice-Hall, Upper Saddle River.Google Scholar

Copyright information

© Indian Academy of Sciences 2003

Authors and Affiliations

  1. 1.Centre for Environmental Stress and Adaptation ResearchLa Trobe UniversityBundooraAustralia

Personalised recommendations