Historicity and the population genetics of Drosophila melanogaster and D. simulans

  • Michel Veuille
  • Emmanuelle Baudry
  • Matthew Cobb
  • Nicolas Derome
  • Emmanuelle Gravot
Part of the Contemporary Issues in Genetics and Evolution book series (CIGE, volume 11)


We summarize data showing that there is population structure in African populations of Drosophila from the melanogaster-simulans complex. In D. melanogaster, population structuring is found at individual loci, but is obscured by population structuring for large inversions that simultaneously affect several loci. In D. simulans, molecular polymorphism at the X-linked vermilion locus suggests that different groups of populations have been geographically isolated for some time. Invading populations are probably derived from different areas in Africa. European populations originate from an east African population that was probably not at a demographic equilibrium. The origin of the Antilles population is apparently different and is as yet unknown. In south-western France, populations from these two species undergo different population structuring at the scale of a few kilometres: D. melanogaster makes up a large panmictic population, whereas D. simulans forms a metapopulation that is divided into smaller demes.

Key words

Drosophila melanogaster Drosophila simulans metapopulation molecular polymorphism population structuring 


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  1. Alfonso, J.M., M. Hernandez, G. Padron & A.M. Gonzalez, 1985. Gametic non random association in north-west African populations of Drosophila melanogaster. Genetica 67: 3–11.CrossRefGoogle Scholar
  2. Andolfatto, P., 2001. Contrasting patterns of X-linked and autosomal nucleotide variation in Drosophila melanogaster and Drosophila simulans. Mol. Biol. Evol. 18(3): 279–290.PubMedCrossRefGoogle Scholar
  3. Andolfatto, P., J. Wall & M. Kreitman, 1999. Unusual haplotype structure at the proximal breakpoint of In(2L)t in a natural popu-lation of Drosophila melanogaster. Genetics 153: 1297–1311.Google Scholar
  4. Begun, DJ. & C.F. Aquadro, 1993. African and North American populations of Drosophila melanogaster are very different at the DNA level. Nature 365: 548–550.Google Scholar
  5. Benassi, V. & M. Veuille, 1995. Comparative population structuring of molecular and allozyme variation of Drosophila melanogaster Adh between Europe, West Africa and East Africa. Genet. Res. Camb. 65: 95–103.Google Scholar
  6. Bénassi, V., S. Aulard, S. Mazeau & M. Veuille, 1993. Molecular variation at the Alcohol dehydrogenase and the P6 loci in Drosophila melanogaster from West-Africa, and its relation to inversion polymorphism. Genetics 134: 789–799.PubMedGoogle Scholar
  7. Boulétreau-Merle, J., 1992. Two paths for geographical expansion, in Advances in Regulation of Insect Reproduction, edited by B. Bennettovà, 1. Gelbic & T. Soldän. Czech Acad. Sei.Google Scholar
  8. Capy, P., M. Veuille, M. Paillette, J.-M. Jallon, J. Vouidibio & J.R. David, 2000. Habitat races and sexual selection in Drosophila melanogaster. a step towards speciation in Brazzaville? Heredity 84: 468–475.PubMedCrossRefGoogle Scholar
  9. Cariou, M.-L., M. Solignac, M. Monnerot & J.R. David, 1990. Low allozyme and mtDNA variability in the island endemic species Drosophila sechellia (D. melanogaster complex). Experientia 46: 101–104.PubMedCrossRefGoogle Scholar
  10. Choudhary, M. & R. Singh, 1987. A comprehensive study of genetic variation in natural populations of Drosophila melanogaster. III. Variations in genetic structure and their causes between Drosophila melanogaster and its sibling species Drosophila simulans. Genetics 117: 697–710.Google Scholar
  11. Cobb, M., M. Huet, D. Lachaise & M. Veuille, 2000. Fragmented forests, evolving flies: Molecular variation in African populations of Drosophila teissieri. Mol. Ecol. 9: 1591–1987.PubMedCrossRefGoogle Scholar
  12. Depaulis, F. & M. Veuille, 1998. Neutrality tests based on the distribution of haplotypes under an infinite site model. Mol. Biol. Evol. 15: 1788–1790.PubMedCrossRefGoogle Scholar
  13. Depaulis, F., L. Brazier & M. Veuille, 1999. Selective sweep at the Drosophila melanogaster Suppressor of Hairless locus and its association with the In(2L)t inversion polymorphism. Genetics 152: 1017–1024.Google Scholar
  14. Depaulis, F., S. Mousset & M. Veuille, 2001. Haplotype tests using coalescent simulations conditional on the number of segregating sites. Mol. Biol. Evol. 18: 1136–1138.PubMedCrossRefGoogle Scholar
  15. Depaulis, F., S. Mousset & M. Veuille, 2002. Detecting selective sweeps with haplotype tests, in Selective Sweeps, edited by Nurminsky. Landes Bioscience.Google Scholar
  16. Depaulis, F., S. Mousset & M. Veuille, Power of neutrality tests to detect bottlenecks and hitchhiking. J. Mol. Evol. (in press).Google Scholar
  17. Dobzhansky, Th., 1965. Wild and domestic species of Drosophila, pp. 533-547 in The Genetics of Colonizing Species, edited byGoogle Scholar
  18. H.G. Baker & G. Leddyard Stebbins. Academic Press, New York and London.Google Scholar
  19. Dobzhansky, Th. & S. Wright, 1941. Relations between mutation rate and accumulation of lethals in populations of Drosophila pseudoobscura. Genetics 26: 23–51.PubMedGoogle Scholar
  20. Eanes, W.F., C. Wesley & B. Charlesworth, 1992. Accumulation of P elements in minority inversions in natural populations of Drosophila melanogaster. Genet Res. 59: 1–9.Google Scholar
  21. Ferveur, J.F., M. Cobb, H. Boukella & J.M. Jallon, 1996. Worldwide variation in Drosophila melanogaster sex pheromone: behavioural effects, genetic bases and potential evolutionary consequences. Genetica 97: 73–80.PubMedCrossRefGoogle Scholar
  22. Hamblin, M.T. & M. Veuille, 1999. Population structure among African and derived populations of D. simulans: evidence for ancient subdivision and recent admixture. Genetics 153: 305-317.Google Scholar
  23. Hudson, R.R. & N.L. Kaplan, 1985. Statistical properties of the number of recombination events in the history of a sample of DNA sequences. Genetics 111: 147–164.Google Scholar
  24. Hutter, CM., M.D. Schug & C.F. Aquadro, 1998. Microsatellite variation in Drosophila melanogaster and Drosophila simulans: a reciprocal test of the ascertainment bias hypothesis. Mol. Biol. Evol. 15: 1620–1636.Google Scholar
  25. Inoue, Y. & T.K. Watanabe, 1980. Inversion polymorphism in some African, New Guinean and Philippine populations of D. melanogaster. Ann. Rep. Natl. Inst. Genet. Jpn. 30: 88.Google Scholar
  26. Kauer, M., B. Zangerl, D. Dieringer& C. Schlötterer, 2002. Chromosomal patterns of microsatellite variability contrast sharply in African and non-African populations of Drosophila melanogaster. Genetics 160: 247–256.Google Scholar
  27. Kliman, R.M., P. Andolfatto, J.A. Coyne, F. Depaulis, M. Kreitman, A.J. Berry, J. McCarter, J. Wakeley & J. Hey, 2000. The population genetics of the origin and divergence of the Drosophila simulans complex species. Genetics 156: 1913–1931.PubMedGoogle Scholar
  28. Kreitman, M., 1983. Nucleotide polymorphism at the alcohol dehydrogenase gene region of Drosophila melanogaster. Nature 304: 412–417.PubMedCrossRefGoogle Scholar
  29. Kreitman, M. & R. Hudson, 1991. Inferring the evolutionary histories of the Adh and Adh-dup loci in Drosophila melanogaster from patterns of polymorphism and divergence. Genetics 127: 565-582.Google Scholar
  30. Kruglyak, S., R.T. Durrett, M.D. Schug & C.F. Aquadro, 1998. Equilibrium distributions of microsatellite repeat length resulting from a balance between slippage events and point mutations. Proc. Natl. Acad. Sci. USA 95(18): 10774-10778.Google Scholar
  31. Lachaise, D., F. Lemeunier & M. Veuille, 1981. Clinal variation in male genitalia in Drosophila teissieri Tsacas. Am. Nat. 117: 600–608.Google Scholar
  32. Lachaise, D., M.-L. Cariou, J.R. David, F. Lemeunier & L. Tsacas, 1988. Historical biogeography of the Drosophila melanogaster species subgroup. Evol. Biol. 22: 159–225.Google Scholar
  33. Lemeunier, F. & S. Aulard, 1992. Inversion polymorphism in Drosophila melanogaster, pp. 339-405 in Drosophila Inversion Polymorphism, edited by C.B. Krimbas & J.R. Powell. CRC Press, Cleveland.Google Scholar
  34. Lemeunier, F., S. Aulard, V. Benassi & M. Veuille, 1994. Scientific correspondence: fruitfly origins. Nature 371: 25.Google Scholar
  35. Lewontin, R.C., J.A. Moore, W.B. Provine & B. Wallace, 1981. Dobzhansky’s Genetics of Natural Populations, I-XLIII. Columbia University Press, New York.Google Scholar
  36. Luyten, I., 1982. Variation intraspécifique et interspéeifique des hydrocarbures cuticulaires chez Drosophila simulans et des espåces affines. C. R. Acad. Sei. Paris, Sei. Vie. 295: 733–736.Google Scholar
  37. Michalakis, Y.& M. Veuille, 1996. Length variation of CAG/CAA trinucleotide repeats in natural populations of Drosophila melanogaster and its relation to the recombination rate. Genetics 143: 1713–1725.PubMedGoogle Scholar
  38. Mousset, S. & N. Derome, Molecular polymorphism in Drosophila melanogaster and D. simulans: what have we learnt from recent studies? Genetica (in press).Google Scholar
  39. Mousset, S., L. Brazier, M.-L. Cariou, F. Chartois, F. Depaulis & M. Veuille, Evidence of multiple selective sweep events in the Drosophila melanogaster genome. Genetics (in press).Google Scholar
  40. Nei, M., 1975. Molecular Population Genetics. North-Holland, Amsterdam, Oxford.Google Scholar
  41. Nei, M., 1987. Molecular Evolutionary Genetics. Columbia Univer-sity Press, New York.Google Scholar
  42. Newfeld, S.J., A.T. Schmid and B. Yedvobnick, 1993. Homopoly-mer length variation in the Drosophila gene mastermind. J. Mol. Evol. 37: 483–495.PubMedCrossRefGoogle Scholar
  43. Newfeld, S.J., H. Tachida & B. Yedvobnick, 1994. Drive-selection equilibrium: homopolymer evolution in the Drosophila gene mastermind. J. Mol. Evol. 38: 637–641.PubMedCrossRefGoogle Scholar
  44. Petrov, D.A., T.A. Sangster, J.S. Johnston, D.L. Hard & K.L. Shaw, 2000. Evidence for DNA loss as a determinant of genome size. Science 287: 1060–1062.Google Scholar
  45. Raymond, M. & F. Rousset, 1995. Genepop (version 1.2): population genetics software for exact tests and ecumenism. J. Hered. 86: 248–249.Google Scholar
  46. Sawyer, S.A. & D.L. Hartl, 1992. Population genetics of polymorphism and divergence. Genetics 132: 1161–1176.PubMedGoogle Scholar
  47. Schlötterer, C, R. Ritter, B. Harr & G. Brem, 1998. High mutation rate of a long microsatellite allele in Drosophila melanogaster provides evidence for allele-specific mutation rates. Mol. Biol. Evol. 15(10): 1269-1274.Google Scholar
  48. Singh, R., 1989. Population genetics and evolution of species related to Drosophila melanogaster. Ann. Rev. Genet. 23: 425–453.PubMedCrossRefGoogle Scholar
  49. Veuille, M., V. Bénassi, S. Aulard & F. Depaulis, 1998. Allele-specific population structure of Drosophila melanogaster Alcohol dehydrogenase at the molecular level. Genetics 149: 971–981.Google Scholar
  50. Vouidibio, J., P. Capy, D. Defaye, E. Pia, J. Sandrin, A. Csink & J.R. David, 1989. Short-range genetic structure of Drosophila melanogaster populations in an Afrotropical urban area and its significance. Proc. Natl. Acad. Sci. USA 86: 8442–8446.PubMedCrossRefGoogle Scholar
  51. Waples, R.S., 1989. A generalized approach for estimating effective population size from temporal changes in allele frequency. Genetics 121: 379–392.Google Scholar
  52. Watanabe, T.K., Y. Inoue & M. Watada, 1984. Adaptation of Drosophila simulans in Japan. Jpn. J. Genet. 59: 225–235.CrossRefGoogle Scholar
  53. Wright, S., 1951. The genetical structure of populations. Ann. Eugen. 15:: 323–354.CrossRefGoogle Scholar
  54. Zohary, D. & M. Hopf, 2000. Domestication of Plants in the Old World. Oxford University Press, Oxford, 3rd edn.Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2004

Authors and Affiliations

  • Michel Veuille
    • 2
  • Emmanuelle Baudry
    • 2
  • Matthew Cobb
    • 1
  • Nicolas Derome
    • 2
  • Emmanuelle Gravot
    • 2
  1. 1.School of Biological SciencesUniversity of ManchesterManchesterUK
  2. 2.Laboratoire d’Ecologie (Cc237) and Ecole Pratique des Hautes EtudesUniversité Pierre et Marie CurieParis Cedex 05France

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