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. 2004 Feb;166(2):779–788. doi: 10.1534/genetics.166.2.779

Effect of breeding structure on population genetic parameters in Drosophila.

Emmanuelle Gravot 1, Michèle Huet 1, Michel Veuille 1
PMCID: PMC1470752  PMID: 15020467

Abstract

The breeding structure of populations has been neglected in studies of Drosophila, even though Wright and Dobzhansky's pioneering work on the genetics of natural populations was an attempt to tackle what they regarded as an essential factor in evolution. We compared the breeding structure of sympatric populations of D. melanogaster and D. simulans, two sibling species that are widely used in evolutionary studies. We recorded changes in population density and microsatellite variation patterns for 3 years in a temperate environment of southwestern France. Results were distinctively different in the two species. Maximum population levels in summer and in autumn were similar and fluctuated greatly over years, each species being in turn the most abundant. However, genetic data showed that D. melanogaster made up a continuous breeding population in time and space of practically infinite effective size. D. simulans was fragmented into isolates with a local effective size of between 50 and 350 individuals. A consequence of this was that, while a local sample provided a reliable estimate of regional genetic variability in D. melanogaster, a sample from the same area provided an underestimate of this parameter in D. simulans. In practical terms, this means that variations in breeding structure should be accounted for in sampling schemes and in designing evolutionary genetic models. More generally, this suggests the existence of differential reactions to local environments that might contribute to several genomic differences observed between these species.

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Selected References

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  1. Agis M., Schlötterer C. Microsatellite variation in natural Drosophila melanogaster populations from New South Wales (Australia) and Tasmania. Mol Ecol. 2001 May;10(5):1197–1205. doi: 10.1046/j.1365-294x.2001.01271.x. [DOI] [PubMed] [Google Scholar]
  2. Andolfatto P. Contrasting patterns of X-linked and autosomal nucleotide variation in Drosophila melanogaster and Drosophila simulans. Mol Biol Evol. 2001 Mar;18(3):279–290. doi: 10.1093/oxfordjournals.molbev.a003804. [DOI] [PubMed] [Google Scholar]
  3. Aquadro C. F., Lado K. M., Noon W. A. The rosy region of Drosophila melanogaster and Drosophila simulans. I. Contrasting levels of naturally occurring DNA restriction map variation and divergence. Genetics. 1988 Aug;119(4):875–888. doi: 10.1093/genetics/119.4.875. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Begon M. The effective size of a natural drosophila subobscura population. Heredity (Edinb) 1977 Feb;38(1):13–18. doi: 10.1038/hdy.1977.2. [DOI] [PubMed] [Google Scholar]
  5. Begun D. J. The frequency distribution of nucleotide variation in Drosophila simulans. Mol Biol Evol. 2001 Jul;18(7):1343–1352. doi: 10.1093/oxfordjournals.molbev.a003918. [DOI] [PubMed] [Google Scholar]
  6. Bénassi V., Veuille M. Comparative population structuring of molecular and allozyme variation of Drosophila melanogaster Adh between Europe, west Africa and east Africa. Genet Res. 1995 Apr;65(2):95–103. doi: 10.1017/s0016672300033115. [DOI] [PubMed] [Google Scholar]
  7. Charlesworth B., Morgan M. T., Charlesworth D. The effect of deleterious mutations on neutral molecular variation. Genetics. 1993 Aug;134(4):1289–1303. doi: 10.1093/genetics/134.4.1289. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Charlesworth B. The effect of life-history and mode of inheritance on neutral genetic variability. Genet Res. 2001 Apr;77(2):153–166. doi: 10.1017/s0016672301004979. [DOI] [PubMed] [Google Scholar]
  9. Cobb M., Huet M., Lachaise D., Veuille M. Fragmented forests, evolving flies: molecular variation in African populations of Drosophila teissieri. Mol Ecol. 2000 Oct;9(10):1591–1597. doi: 10.1046/j.1365-294x.2000.01064.x. [DOI] [PubMed] [Google Scholar]
  10. Dobzhansky T, Wright S. Genetics of Natural Populations. V. Relations between Mutation Rate and Accumulation of Lethals in Populations of Drosophila Pseudoobscura. Genetics. 1941 Jan;26(1):23–51. doi: 10.1093/genetics/26.1.23. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Greenberg R, Crow J F. A Comparison of the Effect of Lethal and Detrimental Chromosomes from Drosophila Populations. Genetics. 1960 Aug;45(8):1153–1168. doi: 10.1093/genetics/45.8.1153. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Hamblin M. T., Veuille M. Population structure among African and derived populations of Drosophila simulans: evidence for ancient subdivision and recent admixture. Genetics. 1999 Sep;153(1):305–317. doi: 10.1093/genetics/153.1.305. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Hubby J. L., Lewontin R. C. A molecular approach to the study of genic heterozygosity in natural populations. I. The number of alleles at different loci in Drosophila pseudoobscura. Genetics. 1966 Aug;54(2):577–594. doi: 10.1093/genetics/54.2.577. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hudson R. R., Kaplan N. L. Deleterious background selection with recombination. Genetics. 1995 Dec;141(4):1605–1617. doi: 10.1093/genetics/141.4.1605. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Ives P T. The Genetic Structure of American Populations of Drosophila Melanogaster. Genetics. 1945 Mar;30(2):167–196. doi: 10.1093/genetics/30.2.167. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. KIMURA M., MARUYAMA T., CROW J. F. THE MUTATION LOAD IN SMALL POPULATIONS. Genetics. 1963 Oct;48:1303–1312. doi: 10.1093/genetics/48.10.1303. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Keightley P. D., Eyre-Walker A. Terumi Mukai and the riddle of deleterious mutation rates. Genetics. 1999 Oct;153(2):515–523. doi: 10.1093/genetics/153.2.515. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Michalakis Y., Veuille M. Length variation of CAG/CAA trinucleotide repeats in natural populations of Drosophila melanogaster and its relation to the recombination rate. Genetics. 1996 Aug;143(4):1713–1725. doi: 10.1093/genetics/143.4.1713. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Moriyama E. N., Powell J. R. Intraspecific nuclear DNA variation in Drosophila. Mol Biol Evol. 1996 Jan;13(1):261–277. doi: 10.1093/oxfordjournals.molbev.a025563. [DOI] [PubMed] [Google Scholar]
  20. Mousset Sylvain, Derome Nicolas. Molecular polymorphism in Drosophila melanogaster and D. simulans: what have we learned from recent studies? Genetica. 2004 Mar;120(1-3):79–86. doi: 10.1023/b:gene.0000017632.08718.df. [DOI] [PubMed] [Google Scholar]
  21. Mukai T., Baba M., Akiyama M., Uowaki N., Kusakabe S., Tajima F. Rapid change in mutation rate in a local population of Drosophila melanogaster. Proc Natl Acad Sci U S A. 1985 Nov;82(22):7671–7675. doi: 10.1073/pnas.82.22.7671. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Mukai T., Mettler L. E., Chigusa S. I. Linkage disequilibrium in a local population of Drosophila melanogaster. Proc Natl Acad Sci U S A. 1971 May;68(5):1065–1069. doi: 10.1073/pnas.68.5.1065. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Mukai T., Voelker R. A. The genetic structure of natural populations of Drosophila melanogaster XIII. Further studies on linkage disequilibrium. Genetics. 1977 May;86(1):175–185. doi: 10.1093/genetics/86.1.175. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Mukai T., Yamaguchi O. The genetic structure of natural populations of Drosophila melanogaster. XI. Genetic variability in a local population. Genetics. 1974 Feb;76(2):339–366. doi: 10.1093/genetics/76.2.339. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Nei M. The frequency distribution of lethal chromosomes in finite populations. Proc Natl Acad Sci U S A. 1968 Jun;60(2):517–524. doi: 10.1073/pnas.60.2.517. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Nordborg M., Charlesworth B., Charlesworth D. The effect of recombination on background selection. Genet Res. 1996 Apr;67(2):159–174. doi: 10.1017/s0016672300033619. [DOI] [PubMed] [Google Scholar]
  27. Rousset F., Raymond M. Testing heterozygote excess and deficiency. Genetics. 1995 Aug;140(4):1413–1419. doi: 10.1093/genetics/140.4.1413. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Smith D. B., Langley C. H., Johnson F. M. Variance component analysis of allozyme frequency data from eastern populations of Drosophila melanogaster. Genetics. 1978 Jan;88(1):121–137. doi: 10.1093/genetics/88.1.121. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Sturtevant A H. Genetic Studies on DROSOPHILA SIMULANS. I. Introduction. Hybrids with DROSOPHILA MELANOGASTER. Genetics. 1920 Sep;5(5):488–500. doi: 10.1093/genetics/5.5.488. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Taylor C. E., Powell J. R. Microgeographic differentiation of chromosomal and enzyme polymorphisms in Drosophila persimilis. Genetics. 1977 Apr;85(4):681–695. doi: 10.1093/genetics/85.4.681. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Veuille Michel, Baudry Emmanuelle, Cobb Matthew, Derome Nicolas, Gravot Emmanuelle. Historicity and the population genetics of Drosophila melanogaster and D. simulans. Genetica. 2004 Mar;120(1-3):61–70. doi: 10.1023/b:gene.0000017630.69020.32. [DOI] [PubMed] [Google Scholar]
  32. Wright S. Evolution in Mendelian Populations. Genetics. 1931 Mar;16(2):97–159. doi: 10.1093/genetics/16.2.97. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Wright S, Dobzhansky T, Hovanitz W. Genetics of Natural Populations. VII. the Allelism of Lethals in the Third Chromosome of Drosophila Pseudoobscura. Genetics. 1942 Jul;27(4):363–394. doi: 10.1093/genetics/27.4.363. [DOI] [PMC free article] [PubMed] [Google Scholar]

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