Journal of Genetics

, Volume 82, Issue 3, pp 207–223 | Cite as

Latitudinal clines inDrosophila melanogaster: Body size, allozyme frequencies, inversion frequencies, and the insulin-signalling pathway

  • Gerdien de JongEmail author
  • Zoltán Bochdanovits


Many latitudinal clines exist inDrosophila melanogaster: in adult body size, in allele frequency at allozyme loci, and in frequencies of common cosmopolitan inversions. The question is raised whether these latitudinal clines are causally related. This review aims to connect data from two very different fields of study, evolutionary biology and cell biology, in explaining such natural genetic variation inD. melanogaster body size and development time. It is argued that adult body size clines, inversion frequency clines, and clines in allele frequency at loci involved in glycolysis and glycogen storage are part of the same adaptive strategy. Selection pressure is expected to differ at opposite ends of the clines. At high latitudes, selection onD. melanogaster would favour high larval growth rate at low temperatures, and resource storage in adults to survive winter. At low latitudes selection would favour lower larval critical size to survive crowding, and increased male activity leading to high male reproductive success. Studies of the insulin-signalling pathway inD. melanogaster point to the involvement of this pathway in metabolism and adult body size. The genes involved in the insulin-signalling pathway are associated with common cosmopolitan inversions that show latitudinal clines. Each chromosome region connected with a large common cosmopolitan inversion possesses a gene of the insulin transmembrane complex, a gene of the intermediate pathway and a gene of the TOR branch. The hypothesis is presented that temperateD. melanogaster populations have a higher frequency of a ’thrifty’ genotype corresponding to high insulin level or high signal level, while tropical populations possess a more ’spendthrift’ genotype corresponding to low insulin or low signal level.


Drosophila insulin body size latitudinal cline inversion polymorphism 


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  1. 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.Google Scholar
  2. Agis M. and Schlotterer C. 2001 Microsatellite variation in naturalDrosophila melanogaster populations from New South Wales (Australia) and Tasmania.Mol. Ecol. 10, 1197–1205.PubMedGoogle Scholar
  3. Arbeitman M. N., Furlong E. E. M., Imam F., Johnson E., Null B. H., Baker B. S., Krasnow M. A., Scott M. P., Davis R. W. and White K. P. 2002 Gene expression during the life cycle ofDrosophila melanogaster.Science 297, 2270–2275.PubMedGoogle Scholar
  4. Azevedo R. B. R., French V. and Partridge L. 1996 Thermal evolution of egg size inDrosophila melanogaster.Evolution 50, 2338–2345.Google Scholar
  5. Berrigan D. and Partridge L. 1997 Influence of temperature and activity on the metabolic rate of adultDrosophila melanogaster.Comp. Biochem. Physiol. A118, 1301–1307.Google Scholar
  6. Betran E., Santos M. and Ruiz A. 1998 Antagonistic pleiotropic effect of second-chromosome inversions on body size and early life-history traits inDrosophila buzzatii.Evolution 52, 144–154.Google Scholar
  7. Blanckenhorn W. U. 2000 The evolution of body size: What keeps organisms small?Q. Rev. Biol. 75, 385–407.PubMedGoogle Scholar
  8. Bochdanovits Z. and de Jong G. 2003a Co-variation of larval gene expression and adult body size in natural populations ofDrosophila melanogaster.Mol. Biol. Evol. 20, 1760–1766.PubMedGoogle Scholar
  9. Bochdanovits Z. and de Jong G. 2003b Experimental evolution inDrosophila melanogaster: interaction of temperature and food quality selection regimes.Evolution 57, 1829–1836.PubMedGoogle Scholar
  10. Bochdanovits Z. and de Jong G. 2003c Temperature dependence of fitness components in geographical populations ofDrosophila melanogaster: Changing the association between size and fitness.Biol. J. Linn. Soc. 80, 717–725.Google Scholar
  11. Bochdanovits Z. and de Jong G. 2003d Temperature dependent larval resource allocation shaping adult body size inDrosophila melanogaster.J. Evol. Biol. 16, 1159–1167.PubMedGoogle Scholar
  12. Britton J. S. and Edgar B. A. 1998 Environmental control of the cell cycle in Drosophila: nutrition activates mitotic and endoreplicative cells by distinct mechanisms.Development 125, 2149–2158.PubMedGoogle Scholar
  13. Britton J. S., Lockwood W. K., Li L., Cohen S. M. and Edgar B. A. 2002 Drosophila’s insulin/PI3-kinase pathway coordinates cellular metabolism with nutritional conditions.Dev. Cell 2, 239–249.PubMedGoogle Scholar
  14. Brogiolo W., Stocker H., Ikeya T., Rintelen F., Fernandez R. and Hafen E. 2001 An evolutionarily conserved function of theDrosophila insulin receptor and insulin-like peptides in growth control.Curr. Biol. 11, 213–221.PubMedGoogle Scholar
  15. Bryant P. J. 2001 Growth factors controlling imaginal disc growth inDrosophila.Cell Cycle Dev. 237, 182–199.Google Scholar
  16. Caceres M., Barbadilla A. and Ruiz A. 1997 Inversion length and breakpoint distribution in theDrosophila buzzatii species complex: Is inversion length a selected trait?Evolution 51, 1149–1155.Google Scholar
  17. Caceres M., Barbadilla A. and Ruiz A. 1999 Recombination rate predicts inversion size in diptera.Genetics 153, 251–259.PubMedGoogle Scholar
  18. Calboli F. C. F., Kennington W. J. and Partridge L. 2003 QTL mapping reveals a striking coincidence in the positions of genomic regions associated with adaptive variation in body size in parallel clines ofDrosophila melanogaster on different continents.Evolution 57, 2653–2658.PubMedGoogle Scholar
  19. Capy P., Pla E. and David J. R. 1993 Phenotypic and genetic variability of morphometrical traits in natural populations ofDrosophila melanogaster andDrosophila simulans. 1. Geographic variations.Genet. Sel. Evol. 25, 517–536.Google Scholar
  20. Caracristi G. and Schlotterer C. 2003 Genetic differentiation between American and EuropeanDrosophila melanogaster populations could be attributed to admixture of African alleles.Mol. Biol. Evol. 20, 792–799.PubMedGoogle Scholar
  21. Cardenas M. E., Cutler N. S., Lorenz M. C., Di Como C. J. and Heitman J. 1999 The TOR signaling cascade regulates gene expression in response to nutrients.Genes Dev. 13, 3271–3279.PubMedGoogle Scholar
  22. Cavicchi S. 1978 Investigation on early divergence between populations ofDrosophila melanogaster kept at different temperatures.Genetica 48, 81–87.Google Scholar
  23. Cavicchi S., Giorgi G., Natali V. and Guerra D. 1991 Temperature related divergence in experimental populations ofDrosophila melanogaster. 4. Fourier and centroid analysis of wing shape and relationship between shape variation and fitness.J. Evol. Biol. 4, 141–159.Google Scholar
  24. Chippindale A. K., Chu T. J. F. and Rose M. R. 1996 Complex trade-offs and the evolution of starvation resistance inDrosophila melanogaster.Evolution 50, 753–766.Google Scholar
  25. Chippindale A. K., Alipaz J. A., Chen H. W. and Rose M. R. 1997 Experimental evolution of accelerated development in Drosophila.1. Developmental speed and larval survival.Evolution 51, 1536–1551.Google Scholar
  26. Chippindale A. K., Ngo A. and Rose M. R. 2003 The devil in the details of life-history evolution: instability and reversal of genetic correlations during selection onDrosophila development.J. Genet. 82, 133–145 (this issue).PubMedGoogle Scholar
  27. Clancy D. J., Gems D., Harshman L. G., Oldham S., Stocker H., Hafen E., Leevers S. J. and Partridge L. 2001 Extension of life-span by loss of CHICO, aDrosophila insulin receptor substrate protein.Science 292, 104–106.PubMedGoogle Scholar
  28. Conlon I. and Raff M. 1999 Size control in animal development.Cell 96, 235–244.PubMedGoogle Scholar
  29. Coyne J. A. and Beecham E. 1987 Heritability of two morphological characters within and among natural populations ofDrosophila melanogaster.Genetics 117, 727–737.PubMedGoogle Scholar
  30. Coyne J. A., Wicker-Thomas C. and Jallon J. M. 1999 A gene responsible for a cuticular hydrocarbon polymorphism inDrosophila melanogaster.Genet. Res. 73, 189–203.PubMedGoogle Scholar
  31. David J. R. 1975 Evolution of a cosmopolitan species: genetic latitudinal clines inDrosophila melanogaster wild populations.Experientia 31, 164–166.PubMedGoogle Scholar
  32. David J. R. and Capy P. 1988 Genetic variation ofDrosophila melanogaster natural populations.Trends Genet. 4, 106–111.PubMedGoogle Scholar
  33. David J. R., Bocquet C. and Pla E. 1976 New results on the genetic characteristic of the Far East race ofDrosophila melanogaster.Genet. Res. 28, 253–260.PubMedGoogle Scholar
  34. David J. R., Allemand R., Van Herrewege J. and Cohet Y. 1983 Ecophysiology: abiotic factors. InThe genetics and biology of Drosophila (ed. M. Ashburner, H. L. Carson and J. N. Thompson), vol. 3d, pp. 105–170. Academic Press, London.Google Scholar
  35. De Moed G. H., de Jong G. and Scharloo W. 1997 The phenotypic plasticity of wing size inDrosophila melanogaster: the cellular basis of its genetic variation.Heredity 79, 260–267.PubMedGoogle Scholar
  36. De Moed G. H., de Jong G. and Scharloo W. 1998 The energetics of growth inDrosophila melanogaster: Effect of temperature and food conditions.Neth. J. Zool. 48, 169–188.Google Scholar
  37. De Moed G. H., Kruitwagen C. L. J. J., de Jong G. and Scharloo W. 1999 Critical weight for the induction of pupariation inDrosophila melanogaster: genetic and environmental variation.J. Evol. Biol. 12, 852–858.Google Scholar
  38. Delpuech J., Moreteau B., Chice J., Pla E., Vouidibio J. and David J. R. 1995 Phenotypic plasticity and reaction norms in temperate and tropical populations ofDrosophila melanogaster: ovarian size and developmental temperature.Evolution 49, 670–675.Google Scholar
  39. Djawdan M., Chippindale A. K., Rose M. R. and Bradley T. J. 1998 Metabolic reserves and evolved stress resistance inDrosophila melanogaster.Physiol. Zool. 71, 584–594.PubMedGoogle Scholar
  40. Drummond-Barbosa D. and Spradling A. C. 2001 Stem cells and their progeny respond to nutritional changes duringDrosophila oogenesis.Dev. Biol. 231, 265–278.PubMedGoogle Scholar
  41. Eanes W. F. 1999 Analysis of selection on enzyme polymorphisms.Annu. Rev. Ecol. Syst. 30, 301–326.Google Scholar
  42. Ferveur J. F., Cobb M., Boukella H. and Jallon J. M. 1996 World-wide variation inDrosophila melanogaster sex pheromone: Behavioural effects, genetic bases and potential evolutionary consequences.Genetica 97, 73–80.PubMedGoogle Scholar
  43. Gao X. S. and Pan D. J. 2001 TSC1 and TSC2 tumour suppressors antagonize insulin signaling in cell growth.Genes Dev. 15, 1383–1392.PubMedGoogle Scholar
  44. Garofalo R. S. 2002 Genetic analysis of insulin signaling inDrosophila.Trends Endocrinol. Metab. 13, 156–162.PubMedGoogle Scholar
  45. Gasser M., Kaiser M., Berrigan D. and Stearns S. C. 2000 Life-history correlates of evolution under high and low adult mortality.Evolution 54, 1260–1272.PubMedGoogle Scholar
  46. Gilchrist A. S. and Partridge L. 1999 A comparison of the genetic basis of wing size divergence in three parallel body size clines ofDrosophila melanogaster.Genetics 153, 1775–1787.PubMedGoogle Scholar
  47. Gockel J., Kennington W. J., Hoffmann A., Goldstein D. B. and Partridge L. 2001 Nonclinality of molecular variation implicates selection in maintaining a morphological cline ofDrosophila melanogaster.Genetics 158, 319–323.PubMedGoogle Scholar
  48. Gockel J., Robinson S. J. W., Kennington W. J., Goldstein D. B. and Partridge L. 2002 Quantitative genetic analysis of natural variation in body size inDrosophila melanogaster.Heredity 89, 145–153.PubMedGoogle Scholar
  49. Harshman L. G., Hoffmann A. A. and Clark A. G. 1999 Selection for starvation resistance inDrosophila melanogaster: physiological correlates, enzyme activities and multiple stress responses.J. Evol. Biol. 12, 370–379.Google Scholar
  50. Hasson E. and Eanes W. F. 1996 Contrasting histories of three gene regions associated with In(3L)Payne ofDrosophila melanogaster.Genetics 144, 1565–1575.PubMedGoogle Scholar
  51. Hipfner D. R. and Cohen S. M. 1999 New growth factors for imaginal discs.BioEssays 21, 718–720.PubMedGoogle Scholar
  52. Hoffmann A. A., Hallas R., Sinclair C. and Mitrovski P. 2001 Levels of variation in stress resistance inDrosophila among strains, local populations and geographic regions: Patterns for desiccation, starvation, cold resistance, and associated traits.Evolution 55, 1621–1630.PubMedGoogle Scholar
  53. Hoffmann A. A., Scott M., Partridge L. and Hallas R. 2003 Overwintering inDrosophila melanogaster: outdoor field cage experiments on clinal and laboratory selected populations help to elucidate traits under selection.J. Evol. Biol. 16, 614–623.PubMedGoogle Scholar
  54. Huey R. B., Partridge L. and Fowler K. 1989 Natural selection on thermal sensitivity ofDrosophila melanogaster.Am. Zool. 29, A141.Google Scholar
  55. Huey R. B., Partridge L. and Fowler K. 1991 Thermal sensitivity ofDrosophila melanogaster responds rapidly to laboratory natural selection.Evolution 45, 751–756.Google Scholar
  56. Huey R. B., Gilchrist G. W., Carlson M. L., Berrigan D. and Serra L. 2000 Rapid evolution of a geographic cline in size in an introduced fly.Science 287, 308–309.PubMedGoogle Scholar
  57. Ikeya T., Galic M., Belawat P., Nairz K. and Hafen E. 2002 Nutrient-dependent expression of insulin-like peptides from neuroendocrine cells in the CNS contributes to growth regulation inDrosophila.Curr. Biol. 12, 1293–1300.PubMedGoogle Scholar
  58. Imasheva A. G., Bubli O. A. and Lazebny O. E. 1994 Variation in wing length in Eurasian natural populations ofDrosophila melanogaster.Heredity 72, 508–514.PubMedGoogle Scholar
  59. Izquieredo J. 1991 How doesDrosophila melanogaster overwinter?Entomol. Exp. Appl. 59, 51–58.Google Scholar
  60. 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.Google Scholar
  61. James A. C. and Partridge L. 1998 Geographic variation in competitive ability inDrosophila melanogaster.Am. Nat. 151, 530–537.Google Scholar
  62. James A. C., Azevedo R. B. R. and Partridge L. 1995 Cellular basis and developmental timing in a size cline ofDrosophila melanogaster.Genetics 140, 659–666.PubMedGoogle Scholar
  63. James A. C., Azevedo R. B. R. and Partridge L. 1997 Genetic and environmental responses to temperature ofDrosophila melanogaster from a latitudinal cline.Genetics 146, 881–890.PubMedGoogle Scholar
  64. Johnston L. A. and Gallant P. 2002 Control of growth and organ size inDrosophila.BioEssays 24, 54–64.PubMedGoogle Scholar
  65. Kamping A. and van Delden W. 1999a A long-term study on interactions between the Adh and alpha Gpdh allozyme polymorphisms and the chromosomal inversion In(2L)t in a seminatural population ofD. melanogaster.J. Evol. Biol. 12, 809–821.Google Scholar
  66. Kamping A. and van Delden W. 1999b The role of fertility restoration in the maintenance of the inversion In(2L)t polymorphism inDrosophila melanogaster.Heredity 83, 460–468.PubMedGoogle Scholar
  67. Karan D., Dahiya N., Munjal A. K., Gibert P., Moreteau B., Parkash R. and David J. R. 1998 Desiccation and starvation tolerance of adult Drosophila: Opposite latitudinal clines in natural populations of three different species.Evolution 52, 825–831.Google Scholar
  68. Kauer M., Zangerl B., Dieringer D. and Schlotterer C. 2002 Chromosomal patterns of microsatellite variability contrast sharply in African and non-African populations ofDrosophila melanogaster.Genetics 160, 247–256.PubMedGoogle Scholar
  69. Kawamura K., Shibata T., Saget O., Peel D. and Peter J. 1999 A new family of growth factors produced by the fat body and active onDrosophila imaginal disc cells.Development 126, 211–219.PubMedGoogle Scholar
  70. Knibb W., Oakeshott J. and Gibson J. 1981 Chromosome inversion polymorphism inDrosophila melanogaster. I. Latitudinal clines and associations between inversions in Australasian populations.Genetics 98, 833–837.PubMedGoogle Scholar
  71. Lachaise D., Cariou M. L., David J. R., Lemeunier F., Tsacas L. and Ashburner M. 1988 Historical biogeography of theDrosophila melanogaster species subgroup.Evol. Biol. 22, 159–225.Google Scholar
  72. Leips J. and MacKay T. F. C. 2000 Quantitative trait loci for life span inDrosophila melanogaster: Interactions with genetic background and larval density.Genetics 155, 1773–1788.PubMedGoogle Scholar
  73. Leips J. and MacKay T. F. C. 2002 The complex genetic architecture ofDrosophila life span.Exp. Aging Res. 28, 361–390.PubMedGoogle Scholar
  74. Lemeunier F. and Aulard S. 1992 Inversion polymorphism inDrosophila melanogaster. InDrosophila inversion polymorphism (ed. C. Krimbas and J. R. Powell), pp. 339–405. CRC Press, Boca Raton.Google Scholar
  75. Lemeunier F., David J. R. and Tsacas L. 1986 Themelanogaster species group. InThe geneticsand biology of Drosophila. (ed. M. Ashburner, H. L. Carson and J. N. Thompson), vol. 3e, pp. 147–256. Academic Press, London.Google Scholar
  76. McCabe J. and Partridge L. 1997 An interaction between environmental temperature and genetic variation for body size for the fitness of adult femaleDrosophila melanogaster.Evolution 51, 1164–1174.Google Scholar
  77. Malpica J., Vasallo J., Frias A. and Fuentes-Bol F. 1987 On recombination amongIn(2L)t, aGpdh andAdh inDrosophila melanogaster.Genetics 115, 141–142.PubMedGoogle Scholar
  78. Mettler L., Voelker R. and Mukai T. 1977 Inversion clines in populations ofDrosophila melanogaster.Genetics 87, 169–176.PubMedGoogle Scholar
  79. Mitrovski P. and Hoffmann A. A. 2001 Postponed reproduction as an adaptation to winter conditions inDrosophila melanogaster: evidence for clinal variation under semi-natural conditions.Proc. R. Soc. London B268, 2163–2168.Google Scholar
  80. Neat F., Fowler K., French V. and Partridge L. 1995 Thermal evolution of growth efficiency inDrosophila melanogaster.Proc. R. Soc. London B260, 73–78.Google Scholar
  81. Nijhout H. 2003 The control of body size in insects.Dev. Biol. 261, 1–9.PubMedGoogle Scholar
  82. Nijhout, H. F. 1994.Insect hormones. Princeton University Press, Princeton.Google Scholar
  83. Noach E. J. K., de Jong G. and Scharloo W. 1996 Phenotypic plasticity in morphological traits in two populations ofDrosophila melanogaster.J. Evol. Biol. 9, 831–844.Google Scholar
  84. Nunney L. 1996 The response to selection for fast larval development inDrosophila melanogaster and its effect on adult weight: An example of a fitness trade-off.Evolution 50, 1193–1204.Google Scholar
  85. Nunney L. and Cheung W. 1997 The effect of temperature on body size and fecundity in femaleDrosophila melanogaster: Evidence for adaptive plasticity.Evolution 51, 1529–1535.Google Scholar
  86. Oldham S. and Hafen E. 2003 Insulin/IGF and target of rapamycin signaling: a TOR de force in growth control.Trends Cell Biol. 13, 79–85.PubMedGoogle Scholar
  87. Oldham S., Montagne J., Radimerski T., Thomas G. and Hafen E. 2000 Genetic and biochemical characterization of dTOR, theDrosophila homolog of the target of rapamycin.Genes Dev. 14, 2689–2694.PubMedGoogle Scholar
  88. Oudman L., van Delden W., Kamping A. and Bijlsma R. 1991 Polymorphism at the Adh and a-Gpdh loci inDrosophila melanogaster: effects of rearing temperature on developmental rate, body weight and some biochemical parameters.Heredity 67, 103–115.PubMedGoogle Scholar
  89. Oudman L., van Delden W., Kamping A. and Bijlsma R. 1992 Interaction between theAdh and a-Gpdh loci inDrosophila melanogaster: adult survival at high temperature.Heredity 68, 289–297.PubMedGoogle Scholar
  90. Oudman L., van Delden W., Kamping A. and Bijlsma R. 1994 Starvation resistance inDrosophila melanogaster in relation to the polymorphisms at theAdh and a-Gpdh loci.J. Insect Physiol. 40, 709–713.Google Scholar
  91. Partridge L., Barrie B., Fowler K. and French V. 1994a Evolution and development of body size and cell size inDrosophila melanogaster in response to temperature.Evolution 48, 1269–1276.Google Scholar
  92. Partridge L., Barrie B., Fowler K. and French V. 1994b Thermal evolution of pre-adult life-history traits inDrosophila melanogaster.J. Evol. Biol. 7, 645–663.Google Scholar
  93. 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.Google Scholar
  94. Partridge L., Langelan R., Fowler K., Zwaan B. and French V. 1999 Correlated responses to selection on body size inDrosophila melanogaster.Genet. Res. 74, 43–54.PubMedGoogle Scholar
  95. Petavy G., Morin J. P., Moreteau B. and David J. R. 1997 Growth temperature and phenotypic plasticity in twoDrosophila sibling species: probable adaptive changes in flight capacities.J. Evol. Biol. 10, 875–887.Google Scholar
  96. 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.PubMedGoogle Scholar
  97. Reeve M. W., Fowler K. and Partridge L. 2000 Increased body size confers greater fitness at lower experimental temperature in maleDrosophila melanogaster.J. Evol. Biol. 13, 836–844.Google Scholar
  98. Robinson S. J. W. and Partridge L. 2001 Temperature and clinal variation in larval growth efficiency inDrosophila melanogaster.J. Evol. Biol. 14, 14–21.Google Scholar
  99. Robinson S. J. W., Zwaan B. and Partridge L. 2000 Starvation resistance and adult body composition in a latitudinal cline ofDrosophila melanogaster.Evolution 54, 1819–1824.PubMedGoogle Scholar
  100. Rulifson E. J., Kim S. K. and Nusse R. 2002 Ablation of insulin-producing neurons in flies: Growth and diabetic phenotypes.Science 296, 1118–1120.PubMedGoogle Scholar
  101. Saltiel A. R. and Kahn C. R. 2001 Insulin signalling and the regulation of glucose and lipid metabolism.Nature 414, 799–806.PubMedGoogle Scholar
  102. Santos M., Fowler K. and Partridge L. 1994 Gene-environment interaction for body size and larval density inDrosophila melanogaster: an investigation of effects on development time, thorax length and adult sex ratio.Heredity 72, 515–521.PubMedGoogle Scholar
  103. Santos M., Borash D. J., Joshi A., Bounlutay N. and Mueller L. D. 1997 Density-dependent natural selection in Drosophila: Evolution of growth rate and body size.Evolution 51, 420–432.Google Scholar
  104. Saucedo L. J. and Edgar B. A. 2002 Why size matters: altering cell size.Curr. Opin. Genet. Dev. 12, 565–571.PubMedGoogle Scholar
  105. Schmelzle T. and Hall M. N. 2000 TOR, a central controller of cell growth.Cell 103, 253–262.PubMedGoogle Scholar
  106. Stearns S. C., Ackermann M., Doebeli M. and Kaiser M. 2000 Experimental evolution of aging, growth and reproduction in fruitflies.Proc. Natl. Acad. Sci. USA 97, 3309–3313.PubMedGoogle Scholar
  107. Stern D. 2001 Body-size evolution: How to evolve a mammoth moth.Curr. Biol. 11, R917-R919.PubMedGoogle Scholar
  108. Stern D. 2003 Body-size control: How an insect knows it has grown enough.Curr. Biol. 13, R267-R269.PubMedGoogle Scholar
  109. Tatar M., Kopelman A., Epstein D., Tu M. P., Yin C. M. and Garofalo R. S. 2001 A mutantDrosophila insulin receptor homolog that extends life-span and impairs neuroendocrine function.Science 292, 107–110.PubMedGoogle Scholar
  110. Tatar M., Bartke A. and Antebi A. 2003 The endocrine regulation of aging by insulin-like signals.Science 299, 1346–1351.PubMedGoogle Scholar
  111. van Delden W. and Kamping A. 1989 The association between the polymorphisms at theAdh and a-Gpdh loci and theIn(2L)t inversion inDrosophila melanogaster in relation to temperature.Evolution 43, 775–793.Google Scholar
  112. van Delden W. and Kamping A. 1991 Changes in relative fitness with temperature among 2nd chromosome arrangements inDrosophila melanogaster.Genetics 127, 507–514.PubMedGoogle Scholar
  113. van Dijken F., Stolwijk H. and Scharloo W. 1985 Locomotor activity inDrosophila melanogaster.Neth. J. Zool. 35, 438–454.Google Scholar
  114. van’t Land J., Van Putten P., Zwaan B., Kamping A. and van Delden W. 1999 Latitudinal variation in wild populations ofDrosophila melanogaster: heritabilities and reaction norms.J. Evol. Biol. 12, 222–232.Google Scholar
  115. van’t Land J., Van Putten W. F., Villarroel H., Kamping A. and van Delden W. 2000 Latitudinal variation for two enzyme loci and an inversion polymorphism inDrosophila melanogaster from Central and South America.Evolution 54, 201–209.Google Scholar
  116. Verrelli B. C. and Eanes W. F. 2000 Extensive amino acid polymorphism at thePgm locus is consistent with adaptive protein evolution inDrosophila melanogaster.Genetics 156, 1737–1752.PubMedGoogle Scholar
  117. Verrelli B. C. and Eanes W. F. 2001a Clinal variation for amino acid polymorphisms at thePgm locus inDrosophila melanogaster.Genetics 157, 1649–1663.PubMedGoogle Scholar
  118. Verrelli B. C. and Eanes W. F. 2001b The functional impact ofPgm amino acid polymorphism on glycogen content inDrosophila melanogaster.Genetics 159, 201–210.PubMedGoogle Scholar
  119. Wayne M. L., Hackett J. B., Dilda C. L., Nuzhdin S. V., Pasyukova E. G. and MacKay T. F. C. 2001 Quantitative trait locus mapping of fitness-related traits inDrosophila melanogaster.Genet. Res. 77, 107–116.PubMedGoogle Scholar
  120. Weeks A. R., McKechnie S. W. and Hoffmann A. A. 2002 Dissecting adaptive clinal variation: markers, inversions and size/ stress associations inDrosophila melanogaster from a central field population.Ecol. Lett. 5, 756–763.Google Scholar
  121. Worthen W. B. 1996 Latitudinal variation in developmental time and mass inDrosophila melanogaster.Evolution 50, 2523–2529.Google Scholar
  122. Zhang H. B., Stallock J. P., Ng J. C., Reinhard C. and Neufeld T. P. 2000 Regulation of cellular growth by theDrosophila target of rapamycin dTOR.Genes Dev. 14, 2712–2724.PubMedGoogle Scholar
  123. Zurovcova M. and Ayala F. J. 2002 Polymorphism patterns in two tightly linked developmental genes,Idgf1 andIdgf3, ofDrosophila melanogaster.Genetics 162, 177–188.PubMedGoogle Scholar
  124. Zwaan B. J., Azevedo R. B. R., James A. C., van’t Land J. and Partridge L. 2000 Cellular basis of wing size variation inDrosophila melanogaster: a comparison of latitudinal clines on two continents.Heredity 84, 338–347.PubMedGoogle Scholar

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© Indian Academy of Sciences 2003

Authors and Affiliations

  1. 1.Evolutionary Population BiologyUtrecht UniversityCH UtrechtNetherlands

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