Skip to main content
Genetics logoLink to Genetics
. 1997 Feb;145(2):311–323. doi: 10.1093/genetics/145.2.311

Nucleotide Variation and Conservation at the Dpp Locus, a Gene Controlling Early Development in Drosophila

B Richter 1, M Long 1, R C Lewontin 1, E Nitasaka 1
PMCID: PMC1207797  PMID: 9071586

Abstract

A study of polymorphism and species divergence of the dpp gene of Drosophila has been made. Eighteen lines from a population of D. melanogaster were sequenced for 5200 bp of the Hin region of the gene, coding for the dpp polypeptide. A comparison was made with sequence from D. simulans. Ninety-six silent polymorphisms and three amino acid replacement polymorphisms were found. The overall silent polymorphism (0.0247) is low, but haplotype diversity (0.0066 for effectively silent sites and 0.0054 for all sites) is in the range found for enzyme loci. Amino acid variation is absent in the N-terminal signal peptide, the C-terminal TGF-β peptide and in the N-terminal half of the pro-protein region. At the nucleotide level there is strong conservation in the middle half of the large intron and in the 3' untranslated sequence of the last exon. The 3' untranslated conservation, which is perfect for 110 bp among all the divergent species, is unexplained. There is strong positive linkage disequilibrium among polymorphic sites, with stretches of apparent gene conversion among originally divergent sequences. The population apparently is a migration mixture of divergent clades.

Full Text

The Full Text of this article is available as a PDF (2.2 MB).

Selected References

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

  1. Begun D. J., Aquadro C. F. Evolutionary inferences from DNA variation at the 6-phosphogluconate dehydrogenase locus in natural populations of drosophila: selection and geographic differentiation. Genetics. 1994 Jan;136(1):155–171. doi: 10.1093/genetics/136.1.155. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Begun D. J., Aquadro C. F. Molecular variation at the vermilion locus in geographically diverse populations of Drosophila melanogaster and D. simulans. Genetics. 1995 Jul;140(3):1019–1032. doi: 10.1093/genetics/140.3.1019. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Berry A., Kreitman M. Molecular analysis of an allozyme cline: alcohol dehydrogenase in Drosophila melanogaster on the east coast of North America. Genetics. 1993 Jul;134(3):869–893. doi: 10.1093/genetics/134.3.869. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. 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]
  5. Gelbart W. M. The decapentaplegic gene: a TGF-beta homologue controlling pattern formation in Drosophila. Development. 1989;107 (Suppl):65–74. doi: 10.1242/dev.107.Supplement.65. [DOI] [PubMed] [Google Scholar]
  6. Gibson G., Hogness D. S. Effect of polymorphism in the Drosophila regulatory gene Ultrabithorax on homeotic stability. Science. 1996 Jan 12;271(5246):200–203. doi: 10.1126/science.271.5246.200. [DOI] [PubMed] [Google Scholar]
  7. 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]
  8. Huang J. D., Schwyter D. H., Shirokawa J. M., Courey A. J. The interplay between multiple enhancer and silencer elements defines the pattern of decapentaplegic expression. Genes Dev. 1993 Apr;7(4):694–704. doi: 10.1101/gad.7.4.694. [DOI] [PubMed] [Google Scholar]
  9. 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]
  10. Irish V. F., Gelbart W. M. The decapentaplegic gene is required for dorsal-ventral patterning of the Drosophila embryo. Genes Dev. 1987 Oct;1(8):868–879. doi: 10.1101/gad.1.8.868. [DOI] [PubMed] [Google Scholar]
  11. Kreitman M., Hudson R. R. Inferring the evolutionary histories of the Adh and Adh-dup loci in Drosophila melanogaster from patterns of polymorphism and divergence. Genetics. 1991 Mar;127(3):565–582. doi: 10.1093/genetics/127.3.565. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Kreitman M., Wayne M. L. Organization of genetic variation at the molecular level: lessons from Drosophila. EXS. 1994;69:157–183. doi: 10.1007/978-3-0348-7527-1_9. [DOI] [PubMed] [Google Scholar]
  13. 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]
  14. Lewontin R. C. Inferring the number of evolutionary events from DNA coding sequence differences. Mol Biol Evol. 1989 Jan;6(1):15–32. doi: 10.1093/oxfordjournals.molbev.a040532. [DOI] [PubMed] [Google Scholar]
  15. Lewontin R. C. The detection of linkage disequilibrium in molecular sequence data. Genetics. 1995 May;140(1):377–388. doi: 10.1093/genetics/140.1.377. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. 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]
  17. 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]
  18. Riley M. A., Hallas M. E., Lewontin R. C. Distinguishing the forces controlling genetic variation at the Xdh locus in Drosophila pseudoobscura. Genetics. 1989 Oct;123(2):359–369. doi: 10.1093/genetics/123.2.359. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Schaeffer S. W., Miller E. L. Estimates of linkage disequilibrium and the recombination parameter determined from segregating nucleotide sites in the alcohol dehydrogenase region of Drosophila pseudoobscura. Genetics. 1993 Oct;135(2):541–552. doi: 10.1093/genetics/135.2.541. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Simonsen K. L., Churchill G. A., Aquadro C. F. Properties of statistical tests of neutrality for DNA polymorphism data. Genetics. 1995 Sep;141(1):413–429. doi: 10.1093/genetics/141.1.413. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Smith S. W., Overbeek R., Woese C. R., Gilbert W., Gillevet P. M. The genetic data environment an expandable GUI for multiple sequence analysis. Comput Appl Biosci. 1994 Dec;10(6):671–675. doi: 10.1093/bioinformatics/10.6.671. [DOI] [PubMed] [Google Scholar]
  22. St Johnston R. D., Hoffmann F. M., Blackman R. K., Segal D., Grimaila R., Padgett R. W., Irick H. A., Gelbart W. M. Molecular organization of the decapentaplegic gene in Drosophila melanogaster. Genes Dev. 1990 Jul;4(7):1114–1127. doi: 10.1101/gad.4.7.1114. [DOI] [PubMed] [Google Scholar]
  23. 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]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES