, Volume 112, Issue 1, pp 273–286

Rapid evolution of wing size clines in Drosophila subobscura

  • George W. Gilchrist
  • Raymond B. Huey
  • Lluís Serra


Parallel latitudinal clines across species and continents provide dramatic evidence of the efficacy of natural selection, however little is known about the dynamics involved in cline formation. For example, several drosophilids and other ectotherms increase in body and wing size at higher latitudes. Here we compare evolution in an ancestral European and a recently introduced (North America) cline in wing size and shape in Drosophila subobscura. We show that clinal variation in wing size, spanning more than 15 degrees of latitude, has evolved in less than two decades. In females from Europe and North America, the clines are statistically indistinguishable however the cline for North American males is significantly shallower than that for European males. We document that while overall patterns of wing size are similar on two continents, the European cline is obtained largely through changing the proximal portion of the wing, whereas the North American cline is largely in the distal portion. We use data from sites collected in 1986/1988 (Pegueroles et al. 1995) and our 1997 collections to compare synchronic (divergence between contemporary populations that share a common ancestor) and allochronic (changes over time within a population) estimates of the rates of evolution. We find that, for these populations, allochronically estimated evolutionary rates within a single population are over 0.02 haldanes (2800 darwins), a value similar in magnitude to the synchronic estimates from the extremes of the cline. This paper represents an expanded analysis of data partially presented in Huey et al. (2000).

clines Drosophila subobscura evolutionary rates species introductions wing size 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Alicchio, R. & D.L. Palenzona, 1971. Changes of sexual dimorphism values in Drosophila melanogaster. Boll. Zool. 38: 75–84.Google Scholar
  2. Anderson, W.W., 1966. Genetic divergence in M. Vetukhiv' experimental populations in Drosophila pseudoobscura. 3. Divergence in body size. Gen. Res. 7: 255–266.Google Scholar
  3. Anderson, W.W., 1973. Genetic divergence in body size among experimental populations of Drosophila pseudoobscura kept at different temperatures. Evolution 27: 278–284.Google Scholar
  4. Ayala, F. J., L. Serra & A. Prevosti, 1989. A grand experiment in evolution: the Drosophila subobscura colonization of the Americas. Genome 31: 246–255.Google Scholar
  5. Baker, H.G. & G.L. Stebbins, 1965. The Genetics of Colonizing Species. Academic Press, New York.Google Scholar
  6. Beckenbach, A.T. & A. Prevosti, 1986. Colonization of North America by the European species, Drosophila subobscura and D. ambigua. Am. Midl. Nat. 115: 10–18.Google Scholar
  7. Berven, K.A., 1982. The genetic basis of altitudinal variation in the wood frog Rana sylvatica. I. An experimental analysis of life history traits. Evolution 36: 962–983.Google Scholar
  8. Boag, P.T. & P.R. Grant, 1981. Intense natural selection in a population of Darwin' finches (Geospizinae) in the Galápagos. Science 214: 82–85.Google Scholar
  9. Bock, I.R. & P.A. Parsons, 1981. Species of Australia and New Zealand, pp. 291–308 in Genetics and Biology of Drosophila, Vol. 3a, edited by M. Ashburner, H.L. Carson & J.N. Thompson. Academic Press, New York.Google Scholar
  10. Brncic, D., 1994. Colonization of Chile by Drosophila subobscura and its consequences, pp. 154–169 in Genetics of Natural Populations: The Continuing Importance of Theodosius Dobzhansky, edited by L. Levine. Columbia University Press, New York.Google Scholar
  11. Brncic, D., A. Prevosti, M. Budnik, M. Monclus & J Ocaña, 1981. Colonization of Drosophila subobscura in Chile. I. First population and cytogenetic studies. Genetica 56: 3–9.Google Scholar
  12. Bryant, E.H., 1977. Morphological adaptation of the housefly, Musca domestica L., in the United States. Evolution 31: 580–596.Google Scholar
  13. Budnik, M., L. Cifuentes & D. Brncic, 1991. Quantitative analysis of genetic differentiation among European and Chilean strains of Drosophila subobscura. Heredity 67: 29–33.Google Scholar
  14. Capy, P., E. Pla & J.R. David, 1993. Phenotypic and genetic variability of morphological traits in natural populations of Drosophila melanogaster and Drosophila simulans. 1. Geographic variations. Genet. Sel. Evol. 25: 517–536.Google Scholar
  15. Carroll, S.P., H. Dingle & S.P Klassen, 1997. Genetic differentiation of fitness-associated traits among rapidly evolving populations of the soapberry bug. Evolution 51: 1182–1188.Google Scholar
  16. Cavicchi S., G. Giorgi & M. Mochi, 1978. Investigation on early divergence between populations of Drosophila melanogaster kept at different temperatures. Genetica 48: 81–87.Google Scholar
  17. Cavicchi, S., D. Guerra, G. Giorgi & C. Pezzoli, 1985. Temperaturerelated divergence in experimental populations of Drosophila melanogaster. I. Genetic and developmental basis of wing size and shape variation. Genetics 109: 665–689.Google Scholar
  18. Constanti, M., M. Pascual, G. Ribó & A. Prevosti, 1986. Sexual isolation between populations of Drosophila subobscura. I. European strains. Genét. Ibéria 38: 213–230.Google Scholar
  19. Cowley, D.E., W.R. Atchley & J.J. Rutledge, 1986. Quantitative genetics of Drosophila melanogaster. I. Sexual dimorphism in genetic parameters for wing traits. Genetics 114: 549–566.Google Scholar
  20. Coyne, J.A. & E. Beecham, 1987. Heritability of two morphological characters within and among natural populations of Drosophila melanogaster. Genetics 117: 727–737.Google Scholar
  21. David, J.R. & C. Bocquet, 1975. Evolution in a cosmopolitan species: genetic latitudinal clines in Drosophila melanogaster wild populations. Experientia 31: 164–166.Google Scholar
  22. Dickinson, M.H., F. Lehmann & S.P. Sane, 1999. Wing rotation and the aerodynamic basis of flight. Science 284: 1954–1960.Google Scholar
  23. Endler, J.A., 1977. Geographic Variation, Speciation, and Clines. Princeton University Press, Princeton.Google Scholar
  24. Fisher, R.A., 1958. The Genetical Theory of Natural Selection. Dover, New York.Google Scholar
  25. Frankham, R., 1968. Sex and selection for a quantitative character in Drosophila. I. Single-sex selection. Aust. J. Biol. Sci. 21: 1215–1223.Google Scholar
  26. Gibbs H.L. & P.R. Grant, 1987. Oscillating selection on Darwin' finches. Nature 327: 511–513.Google Scholar
  27. Gilchrist, A.S., R.B.R. Azevedo, L. Partridge & P. O'Higgins, 2000. Adaptation and constraint in the evolution of Drosophila melanogaster wing shape. Evol. Devel. 2: 114–124.Google Scholar
  28. Grant, P.R. & B.R. Grant, 1995. Predicting microevolutionary responses to directional selection on heritable variation. Evolution 49: 241–251.Google Scholar
  29. Haldane, J.B.S., 1948. The theory of a cline. J. Genet. 48: 277–284.Google Scholar
  30. Hendry, A.P. & M.T. Kinnison, 1999. Perspective: the pace of modern life: measuring rates of contemporary microevolution. Evolution 53: 1637–1653.Google Scholar
  31. Huey, R.B., G.W. Gilchrist, M.L. Carlson, D. Berrigan & L. Serra, 2000. Rapid evolution of a geographic cline in size in an introduced fly. Science 287: 308–309.Google Scholar
  32. Huey, R.B., L. Partridge & K. Fowler, 1991. Thermal sensitivity of Drosophila melanogaster responds rapidly to laboratory natural selection. Evolution 45: 751–756.Google Scholar
  33. Huxley, J.S., 1939. Clines: an auxiliary method in taxonomy. Bijdr. Dierk. 27: 491–520.Google Scholar
  34. Imasheva, A.G., O.A. Bubli & O.E. Lazebny, 1994. Variation in wing length in Eurasian natural populations of Drosophila melanogaster. Heredity 72: 508–514.Google Scholar
  35. James, A.C., R.B.R. Azevedo & L. Partridge, 1995. Cellular basis and developmental timing in a size cline of Drosophila melanogaster. Genetics 140: 659–666.Google Scholar
  36. James, A.C. & L. Partridge, 1995. Thermal evolution of rate of larval development in Drosophila melanogaster in laboratory and field populations. J. Evol. Biol. 8: 315–330.Google Scholar
  37. Johnston, R.F. & R.K. Selander, 1964. House sparrows: rapid evolution of races in North America. Science 144: 548–550.Google Scholar
  38. Kari, J.S. & R.B. Huey, 2000. Size and seasonal temperature in freeranging Drosophila subobscura. J. Therm. Biol. 25: 267–272.Google Scholar
  39. Kinnison, M.T. & A.P. Hendry, 2001. The pace of modern life. II. from rates to pattern and process. Genetica 112-113: 145–164.Google Scholar
  40. Krimbas, C.B. & M. Loukas, 1980. The inversion polymorphism of Drosophila subobscura. Evol. Biol. 12: 163–234.Google Scholar
  41. Krimbas C.B. & J.R. Powell, 1992. The inversion polymorphism of Drosophila subobscura, pp. 127–220 in Drosophila Inversion Polymorphism, edited by C.B. Krimbas. CRC Press, Boca Raton, F.L.Google Scholar
  42. Lande, R., 1980. Sexual dimorphism, sexual selection, and adaptation in polygenic characters. Evolution 34: 292–305.Google Scholar
  43. Long A.D. & R.S. Singh, 1995. Molecules versus morphology: the detection of selection acting on morphological characters along a cline in Drosophila melanogaster. Heredity 74: 569–581.Google Scholar
  44. Lonsdale D.J. & J.S. Levinton, 1985. Latitudinal differentiation in copepod growth: an adaptation to temperature. Ecology 66: 1397–1407.Google Scholar
  45. Menozzi, P. & C.B. Krimbas, 1992. The inversion polymorphism of D. subobscura revisited: synthetic maps of gene arrangement frequencies and their interpretation. J. Evol. Biol. 5: 625–641.Google Scholar
  46. Misra, R.K. & E.C.R. Reeve, 1964. Clines in body dimensions in populations of Drosophila subobscura. Gen. Res. 5: 240–256.Google Scholar
  47. Noor, M.A., M. Pascual & K.R. Smith, 2000. Genetic variation in the spread of Drosophila subobscura from a nonequilibrium population. Evolution 54: 696–703.Google Scholar
  48. Noor, M.A.F., 1998. Diurnal activity patterns of Drosophila subobscura and D. pseudoobscura in sympatric populations. Am. Midl. Nat. 140: 34–41.Google Scholar
  49. Noor, M.A.F., J.R. Wheatley, K.A. Wetterstrand & H. Akashi, 1998. Western North America obscura-group Drosophila collection data, summer 1997. Dros. Info. Serv. 81: 136–137.Google Scholar
  50. Parsons, P.A., 1983. The Evolutionary Biology of Colonizing Species. Cambridge University Press, Cambridge.Google Scholar
  51. Partridge, L., B. Barrie, K. Fowler & V. French, 1994. Evolution and development of body size and cell size in Drosophila melanogaster in response to temperature. Evolution 48: 1269–1276.Google Scholar
  52. Partridge, L. & V. French, 1996. Thermal evolution of ectotherm body size: why get big in the cold?, pp. 265–292 in Animals and Temperature: Phenotypic and Evolutionary Adaptation, edited by I.A. Johnston & A.F. Bennett. Cambridge University Press, Cambridge, U.K.Google Scholar
  53. Pegueroles, G., M. Papaceit, A. Quintana, A. Guillén, A. Prevosti & L. Serra, 1995. An experimental study of evolution in progress: clines for quantitative traits in colonizing and Palearctic populations of Drosophila. Evol. Ecol. 9: 453–465.Google Scholar
  54. Pfriem, P., 1983. Latitudinal variation in wing size in Drosophila subobscura and its dependence on polygenes of chromosome O. Genetica 61: 221–232.Google Scholar
  55. Prevosti, A., 1955. Geographic variability in quantitative traits in populations of Drosophila subobscura. Cold Spring Harbor Symp. Quant. Biol. 20: 294–298.Google Scholar
  56. Prevosti, A., G. Ribó, L. Serra, M. Aguade, J. Balanyá, M. Monclus & F. Mestres, 1988. Colonization of America by Drosophila subobscura: experiment in natural populations that supports the adaptive role of inversion-inversion polymorphism. Proc. Natl. Acad. Sci. USA 85: 5597–5600.Google Scholar
  57. Prevosti, A., L. Serra, M Aguadé, G. Ribó, F. Mestres & J. Balanyá, 1989. Colonization and establishment of the Palearctic species Drosophila subobscura in North and South America, pp. 114–129 in Evolutionary Biology of Transient and Unstable Populations, edited by A. Fontdevila. Springer Verlag, Berlin.Google Scholar
  58. Prevosti, A., L. Serra, C. Segarra, M. Aguade, G. Ribo & M. Monclus, 1990. Clines of chromosomal arrangements of Drosophila subobscura in South America evolve closer to Old World patterns. Evolution 44: 218–221.Google Scholar
  59. Reed, S.C., C.M. Williams & L.E. Chadwick, 1942. Frequency of wingbeat as a character for separating species races and geographic varieties of Drosophila. Genetics 27: 349–361.Google Scholar
  60. Reeve, J.P. & D.J. Fairbairn, 1996. Sexual size dimorphism as a correlated response to selection on body size: an empirical test of the quantitative genetic model. Evolution 50: 1927–1938.Google Scholar
  61. Reznick, D.N., H. Bryga & J.A. Endler, 1990. Experimentally induced life-history evolution in a natural population. Nature 346: 357–359.Google Scholar
  62. Reznick, D.N., F.H. Shaw, F.H. Rodd & R.G. Shaw, 1997. Evaluation of the rate of evolution in natural populations of guppies (Poecilia reticulata). Science 275: 1934–1937.Google Scholar
  63. Riha, V.F. & K.A. Berven, 1991. An analysis of latitudinal variation in the larval development of the wood frog (Rana sylvatica). Copeia 1991: 209–221.Google Scholar
  64. Robertson, F.W. & E. Reeve, 1952. Studies of quantitative inheritance. I. The effects of selection of wing and thorax length in Drosophila melanogaster. J. Gen. 50: 414–448.Google Scholar
  65. Sokoloff, A., 1966. Morphological variation in natural and experimental populations of Drosophila pseudoobscura and Drosophila persimilis. Evolution 20: 49–71.Google Scholar
  66. Stalker, H.D., 1980. Chromosome studies in wild populations of Drosophila melanogaster. II. Relationship of inversion frequencies to latitude, season, wing-loading and flight activity. Genetics 95: 211–223.Google Scholar
  67. Stalker, H.D. & H.L. Carson, 1947. Morphological variation in natural populations of Drosophila robusta Sturtevant. Evolution 1: 237–248.Google Scholar
  68. Stalker, H.D. & H.L. Carson, 1948. An altitudinal transect of Drosophila robusta Sturtevant. Evolution 2: 295–305.Google Scholar
  69. Stalker, H.D. & H.L. Carson, 1949. Seasonal variation in the morphology of Drosophila robusta Sturtevant. Evolution 3: 330–343.Google Scholar
  70. Tantawy, A.O., 1964. Studies on natural populations of Drosophila. III. Morphological and genetic differences of wing length in Drosophila melanogaster and D. simulans in relation to season. Evolution 18: 560–570.Google Scholar
  71. van't Land, J., P. van Putten, H. Villarroel, A. Kamping & W. van Delden, 1995. Latitudinal variation in wing length and allele frequencies for Adh and ?-Gpdh in populations of Drosophila melanogaster from Ecuador and Chile. Dros. Info. Serv. 76: 156.Google Scholar
  72. van der Have, T.M. & G. de Jong, 1996. Adult size in ectotherms: temperature effects on growth and differentiation. J. Theor. Biol. 183: 329–340.Google Scholar
  73. Zwaan, B., R.B.R. Azevedo, A.C. James, J. van't Land & L. Partridge, 2000. Cellular basis of wing size variation in Drosophila melanogaster: a comparison of latitudinal clines on two continents. Heredity 84: 338–347.Google Scholar

Copyright information

© Kluwer Academic Publishers 2001

Authors and Affiliations

  • George W. Gilchrist
    • 1
  • Raymond B. Huey
    • 2
  • Lluís Serra
    • 3
  1. 1.Department of BiologyClarkson UniversityPotsdamUSA
  2. 2.Department of ZoologyUniversity of WashingtonSeattleUSA
  3. 3.Departament de GenèticaUniversitat de BarcelonaBarcelonaSpain

Personalised recommendations