Skip to main content
PMC home page
Genetics logoLink to Genetics
. 2000 Dec;156(4):1913–1931. doi: 10.1093/genetics/156.4.1913

The population genetics of the origin and divergence of the Drosophila simulans complex species.

R M Kliman 1, P Andolfatto 1, J A Coyne 1, F Depaulis 1, M Kreitman 1, A J Berry 1, J McCarter 1, J Wakeley 1, J Hey 1
PMCID: PMC1461354  PMID: 11102384

Abstract

The origins and divergence of Drosophila simulans and close relatives D. mauritiana and D. sechellia were examined using the patterns of DNA sequence variation found within and between species at 14 different genes. D. sechellia consistently revealed low levels of polymorphism, and genes from D. sechellia have accumulated mutations at a rate that is approximately 50% higher than the same genes from D. simulans. At synonymous sites, D. sechellia has experienced a significant excess of unpreferred codon substitutions. Together these observations suggest that D. sechellia has had a reduced effective population size for some time, and that it is accumulating slightly deleterious mutations as a result. D. simulans and D. mauritiana are both highly polymorphic and the two species share many polymorphisms, probably since the time of common ancestry. A simple isolation speciation model, with zero gene flow following incipient species separation, was fitted to both the simulans/mauritiana divergence and the simulans/sechellia divergence. In both cases the model fit the data quite well, and the analyses revealed little evidence of gene flow between the species. The exception is one gene copy at one locus in D. sechellia, which closely resembled other D. simulans sequences. The overall picture is of two allopatric speciation events that occurred quite near one another in time.

Full Text

The Full Text of this article is available as a PDF (328.4 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Aguadé M., Miyashita N., Langley C. H. Polymorphism and divergence in the Mst26A male accessory gland gene region in Drosophila. Genetics. 1992 Nov;132(3):755–770. doi: 10.1093/genetics/132.3.755. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Akashi H. Inferring weak selection from patterns of polymorphism and divergence at "silent" sites in Drosophila DNA. Genetics. 1995 Feb;139(2):1067–1076. doi: 10.1093/genetics/139.2.1067. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Akashi H. Synonymous codon usage in Drosophila melanogaster: natural selection and translational accuracy. Genetics. 1994 Mar;136(3):927–935. doi: 10.1093/genetics/136.3.927. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Andolfatto P., Wall J. D., Kreitman M. Unusual haplotype structure at the proximal breakpoint of In(2L)t in a natural population of Drosophila melanogaster. Genetics. 1999 Nov;153(3):1297–1311. doi: 10.1093/genetics/153.3.1297. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Barraclough TG, Vogler AP. Detecting the Geographical Pattern of Speciation from Species-Level Phylogenies. Am Nat. 2000 Apr;155(4):419–434. doi: 10.1086/303332. [DOI] [PubMed] [Google Scholar]
  6. Begun D. J., Aquadro C. F. Levels of naturally occurring DNA polymorphism correlate with recombination rates in D. melanogaster. Nature. 1992 Apr 9;356(6369):519–520. doi: 10.1038/356519a0. [DOI] [PubMed] [Google Scholar]
  7. Berry A. J., Ajioka J. W., Kreitman M. Lack of polymorphism on the Drosophila fourth chromosome resulting from selection. Genetics. 1991 Dec;129(4):1111–1117. doi: 10.1093/genetics/129.4.1111. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Caccone A., Amato G. D., Powell J. R. Rates and patterns of scnDNA and mtDNA divergence within the Drosophila melanogaster subgroup. Genetics. 1988 Apr;118(4):671–683. doi: 10.1093/genetics/118.4.671. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Caccone A., Moriyama E. N., Gleason J. M., Nigro L., Powell J. R. A molecular phylogeny for the Drosophila melanogaster subgroup and the problem of polymorphism data. Mol Biol Evol. 1996 Nov;13(9):1224–1232. doi: 10.1093/oxfordjournals.molbev.a025688. [DOI] [PubMed] [Google Scholar]
  10. Cariou M. L. Biochemical phylogeny of the eight species in the Drosophila melanogaster subgroup, including D. sechellia and D. orena. Genet Res. 1987 Dec;50(3):181–185. doi: 10.1017/s0016672300023673. [DOI] [PubMed] [Google Scholar]
  11. Cariou M. L., Solignac M., Monnerot M., David J. R. Low allozyme and mtDNA variability in the island endemic species Drosophila sechellia (D. melanogaster complex). Experientia. 1990 Jan 15;46(1):101–104. doi: 10.1007/BF01955430. [DOI] [PubMed] [Google Scholar]
  12. 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]
  13. Clark A. G. Neutral behavior of shared polymorphism. Proc Natl Acad Sci U S A. 1997 Jul 22;94(15):7730–7734. doi: 10.1073/pnas.94.15.7730. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Cohn V. H., Thompson M. A., Moore G. P. Nucleotide sequence comparison of the Adh gene in three drosophilids. J Mol Evol. 1984;20(1):31–37. doi: 10.1007/BF02101983. [DOI] [PubMed] [Google Scholar]
  15. Cooke P. H., Oakeshott J. G. Amino acid polymorphisms for esterase-6 in Drosophila melanogaster. Proc Natl Acad Sci U S A. 1989 Feb;86(4):1426–1430. doi: 10.1073/pnas.86.4.1426. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Coyne J. A., Charlesworth B. Genetics of a pheromonal difference affecting sexual isolation between Drosophila mauritiana and D. sechellia. Genetics. 1997 Apr;145(4):1015–1030. doi: 10.1093/genetics/145.4.1015. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Coyne J. A., Crittenden A. P., Mah K. Genetics of a pheromonal difference contributing to reproductive isolation in Drosophila. Science. 1994 Sep 2;265(5177):1461–1464. doi: 10.1126/science.8073292. [DOI] [PubMed] [Google Scholar]
  18. Coyne J. A. Genetics of sexual isolation in females of the Drosophila simulans species complex. Genet Res. 1992 Aug;60(1):25–31. doi: 10.1017/s0016672300030639. [DOI] [PubMed] [Google Scholar]
  19. Da Lage J. L., Renard E., Chartois F., Lemeunier F., Cariou M. L. Amyrel, a paralogous gene of the amylase gene family in Drosophila melanogaster and the Sophophora subgenus. Proc Natl Acad Sci U S A. 1998 Jun 9;95(12):6848–6853. doi: 10.1073/pnas.95.12.6848. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Dobzhansky T. Studies on Hybrid Sterility. II. Localization of Sterility Factors in Drosophila Pseudoobscura Hybrids. Genetics. 1936 Mar;21(2):113–135. doi: 10.1093/genetics/21.2.113. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Duret L., Mouchiroud D. Expression pattern and, surprisingly, gene length shape codon usage in Caenorhabditis, Drosophila, and Arabidopsis. Proc Natl Acad Sci U S A. 1999 Apr 13;96(8):4482–4487. doi: 10.1073/pnas.96.8.4482. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Eanes W. F., Kirchner M., Yoon J., Biermann C. H., Wang I. N., McCartney M. A., Verrelli B. C. Historical selection, amino acid polymorphism and lineage-specific divergence at the G6pd locus in Drosophila melanogaster and D. simulans. Genetics. 1996 Nov;144(3):1027–1041. doi: 10.1093/genetics/144.3.1027. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Eanes W. F., Kirchner M., Yoon J. Evidence for adaptive evolution of the G6pd gene in the Drosophila melanogaster and Drosophila simulans lineages. Proc Natl Acad Sci U S A. 1993 Aug 15;90(16):7475–7479. doi: 10.1073/pnas.90.16.7475. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Hey J., Kliman R. M. Population genetics and phylogenetics of DNA sequence variation at multiple loci within the Drosophila melanogaster species complex. Mol Biol Evol. 1993 Jul;10(4):804–822. doi: 10.1093/oxfordjournals.molbev.a040044. [DOI] [PubMed] [Google Scholar]
  25. Hey J., Wakeley J. A coalescent estimator of the population recombination rate. Genetics. 1997 Mar;145(3):833–846. doi: 10.1093/genetics/145.3.833. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Hey J. The neutralist, the fly and the selectionist. Trends Ecol Evol. 1999 Jan;14(1):35–38. doi: 10.1016/s0169-5347(98)01497-9. [DOI] [PubMed] [Google Scholar]
  27. Hilton H., Hey J. DNA sequence variation at the period locus reveals the history of species and speciation events in the Drosophila virilis group. Genetics. 1996 Nov;144(3):1015–1025. doi: 10.1093/genetics/144.3.1015. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Hudson R. R. Estimating the recombination parameter of a finite population model without selection. Genet Res. 1987 Dec;50(3):245–250. doi: 10.1017/s0016672300023776. [DOI] [PubMed] [Google Scholar]
  29. Hudson R. R., Kreitman M., Aguadé M. A test of neutral molecular evolution based on nucleotide data. Genetics. 1987 May;116(1):153–159. doi: 10.1093/genetics/116.1.153. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Karotam J., Delves A. C., Oakeshott J. G. Conservation and change in structural and 5' flanking sequences of esterase 6 in sibling Drosophila species. Genetica. 1993;88(1):11–28. doi: 10.1007/BF02424448. [DOI] [PubMed] [Google Scholar]
  31. Kliman R. M., Hey J. DNA sequence variation at the period locus within and among species of the Drosophila melanogaster complex. Genetics. 1993 Feb;133(2):375–387. doi: 10.1093/genetics/133.2.375. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Kreitman M. The neutral theory is dead. Long live the neutral theory. Bioessays. 1996 Aug;18(8):678–683. doi: 10.1002/bies.950180812. [DOI] [PubMed] [Google Scholar]
  33. Leicht B. G., Muse S. V., Hanczyc M., Clark A. G. Constraints on intron evolution in the gene encoding the myosin alkali light chain in Drosophila. Genetics. 1995 Jan;139(1):299–308. doi: 10.1093/genetics/139.1.299. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Lemeunier F., Ashburner M. A. Relationships within the melanogaster species subgroup of the genus Drosophila (Sophophora). II. Phylogenetic relationships between six species based upon polytene chromosome banding sequences. Proc R Soc Lond B Biol Sci. 1976 May 18;193(1112):275–294. doi: 10.1098/rspb.1976.0046. [DOI] [PubMed] [Google Scholar]
  35. McAllister B. F., Charlesworth B. Reduced sequence variability on the Neo-Y chromosome of Drosophila americana americana. Genetics. 1999 Sep;153(1):221–233. doi: 10.1093/genetics/153.1.221. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. McDonald J. H., Kreitman M. Adaptive protein evolution at the Adh locus in Drosophila. Nature. 1991 Jun 20;351(6328):652–654. doi: 10.1038/351652a0. [DOI] [PubMed] [Google Scholar]
  37. 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]
  38. Palopoli M. F., Davis A. W., Wu C. I. Discord between the phylogenies inferred from molecular versus functional data: uneven rates of functional evolution or low levels of gene flow? Genetics. 1996 Nov;144(3):1321–1328. doi: 10.1093/genetics/144.3.1321. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Price C. S. Conspecific sperm precedence in Drosophila. Nature. 1997 Aug 14;388(6643):663–666. doi: 10.1038/41753. [DOI] [PubMed] [Google Scholar]
  40. Price C. S., Dyer K. A., Coyne J. A. Sperm competition between Drosophila males involves both displacement and incapacitation. Nature. 1999 Jul 29;400(6743):449–452. doi: 10.1038/22755. [DOI] [PubMed] [Google Scholar]
  41. R'Kha S., Capy P., David J. R. Host-plant specialization in the Drosophila melanogaster species complex: a physiological, behavioral, and genetical analysis. Proc Natl Acad Sci U S A. 1991 Mar 1;88(5):1835–1839. doi: 10.1073/pnas.88.5.1835. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Ramos-Onsins S., Aguadé M. Molecular evolution of the Cecropin multigene family in Drosophila. functional genes vs. pseudogenes. Genetics. 1998 Sep;150(1):157–171. doi: 10.1093/genetics/150.1.157. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Saitou N., Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987 Jul;4(4):406–425. doi: 10.1093/oxfordjournals.molbev.a040454. [DOI] [PubMed] [Google Scholar]
  44. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Satta Y., Takahata N. Evolution of Drosophila mitochondrial DNA and the history of the melanogaster subgroup. Proc Natl Acad Sci U S A. 1990 Dec;87(24):9558–9562. doi: 10.1073/pnas.87.24.9558. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Schliewen U. K., Tautz D., Päbo S. Sympatric speciation suggested by monophyly of crater lake cichlids. Nature. 1994 Apr 14;368(6472):629–632. doi: 10.1038/368629a0. [DOI] [PubMed] [Google Scholar]
  47. Shibata H., Yamazaki T. Molecular evolution of the duplicated Amy locus in the Drosophila melanogaster species subgroup: concerted evolution only in the coding region and an excess of nonsynonymous substitutions in speciation. Genetics. 1995 Sep;141(1):223–236. doi: 10.1093/genetics/141.1.223. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Smith J. M., Haigh J. The hitch-hiking effect of a favourable gene. Genet Res. 1974 Feb;23(1):23–35. [PubMed] [Google Scholar]
  49. Snook R. R., Markow T. A., Karr T. L. Functional nonequivalence of sperm in Drosophila pseudoobscura. Proc Natl Acad Sci U S A. 1994 Nov 8;91(23):11222–11226. doi: 10.1073/pnas.91.23.11222. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Tajima F. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics. 1989 Nov;123(3):585–595. doi: 10.1093/genetics/123.3.585. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Tajima F. The effect of change in population size on DNA polymorphism. Genetics. 1989 Nov;123(3):597–601. doi: 10.1093/genetics/123.3.597. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Takahata N. An attempt to estimate the effective size of the ancestral species common to two extant species from which homologous genes are sequenced. Genet Res. 1986 Dec;48(3):187–190. doi: 10.1017/s001667230002499x. [DOI] [PubMed] [Google Scholar]
  53. Ting C. T., Tsaur S. C., Wu C. I. The phylogeny of closely related species as revealed by the genealogy of a speciation gene, Odysseus. Proc Natl Acad Sci U S A. 2000 May 9;97(10):5313–5316. doi: 10.1073/pnas.090541597. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Wakeley J., Hey J. Estimating ancestral population parameters. Genetics. 1997 Mar;145(3):847–855. doi: 10.1093/genetics/145.3.847. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Wakeley J. The variance of pairwise nucleotide differences in two populations with migration. Theor Popul Biol. 1996 Feb;49(1):39–57. doi: 10.1006/tpbi.1996.0002. [DOI] [PubMed] [Google Scholar]
  56. Wang R. L., Wakeley J., Hey J. Gene flow and natural selection in the origin of Drosophila pseudoobscura and close relatives. Genetics. 1997 Nov;147(3):1091–1106. doi: 10.1093/genetics/147.3.1091. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Watterson G. A. On the number of segregating sites in genetical models without recombination. Theor Popul Biol. 1975 Apr;7(2):256–276. doi: 10.1016/0040-5809(75)90020-9. [DOI] [PubMed] [Google Scholar]
  58. Wright F. The 'effective number of codons' used in a gene. Gene. 1990 Mar 1;87(1):23–29. doi: 10.1016/0378-1119(90)90491-9. [DOI] [PubMed] [Google Scholar]
  59. Wu C. I., Li W. H. Evidence for higher rates of nucleotide substitution in rodents than in man. Proc Natl Acad Sci U S A. 1985 Mar;82(6):1741–1745. doi: 10.1073/pnas.82.6.1741. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Yanicostas C., Vincent A., Lepesant J. A. Transcriptional and posttranscriptional regulation contributes to the sex-regulated expression of two sequence-related genes at the janus locus of Drosophila melanogaster. Mol Cell Biol. 1989 Jun;9(6):2526–2535. doi: 10.1128/mcb.9.6.2526. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Zurovcova M., Eanes W. F. Lack of nucleotide polymorphism in the Y-linked sperm flagellar dynein gene Dhc-Yh3 of Drosophila melanogaster and D. simulans. Genetics. 1999 Dec;153(4):1709–1715. doi: 10.1093/genetics/153.4.1709. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES