Skip to main content
NCBI home page
Genetics logoLink to Genetics
. 2000 Dec;156(4):1753–1763. doi: 10.1093/genetics/156.4.1753

A selective sweep associated with a recent gene transposition in Drosophila miranda.

S Yi 1, B Charlesworth 1
PMCID: PMC1461364  PMID: 11102371

Abstract

In Drosophila miranda, a chromosome fusion between the Y chromosome and the autosome corresponding to Muller's element C has created a new sex chromosome system. The chromosome attached to the ancestral Y chromosome is transmitted paternally and hence is not exposed to crossing over. This chromosome, conventionally called the neo-Y, and the homologous neo-X chromosome display many properties of evolving sex chromosomes. We report here the transposition of the exuperantia1 (exu1) locus from a neo-sex chromosome to the ancestral X chromosome of D. miranda. Exu1 is known to have several critical developmental functions, including a male-specific role in spermatogenesis. The ancestral location of exu1 is conserved in the sibling species of D. miranda, as well as in a more distantly related species. The transposition of exu1 can be interpreted as an adaptive fixation, driven by a selective advantage conferred by its effect on dosage compensation. This explanation is supported by the pattern of within-species sequence variation at exu1 and the nearby exu2 locus. The implications of this phenomenon for genome evolution are discussed.

Full Text

The Full Text of this article is available as a PDF (282.1 KB).

Selected References

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

  1. Anderson W. W., Ayala F. J., Michod R. E. Chromosomal and allozymic diagnosis of three species of Drosophila. Drosophila pseudoobscura, D. persimilis, and D. miranda. J Hered. 1977 Mar-Apr;68(2):71–74. doi: 10.1093/oxfordjournals.jhered.a108793. [DOI] [PubMed] [Google Scholar]
  2. Bachtrog D., Charlesworth B. Reduced levels of microsatellite variability on the neo-Y chromosome of Drosophila miranda. Curr Biol. 2000 Sep 7;10(17):1025–1031. doi: 10.1016/s0960-9822(00)00656-4. [DOI] [PubMed] [Google Scholar]
  3. Barrio E., Ayala F. J. Evolution of the Drosophila obscura species group inferred from the Gpdh and Sod genes. Mol Phylogenet Evol. 1997 Feb;7(1):79–93. doi: 10.1006/mpev.1996.0375. [DOI] [PubMed] [Google Scholar]
  4. Baverstock P. R., Adams M., Polkinghorne R. W., Gelder M. A sex-linked enzyme in birds--Z-chromosome conservation but no dosage compensation. Nature. 1982 Apr 22;296(5859):763–766. doi: 10.1038/296763a0. [DOI] [PubMed] [Google Scholar]
  5. 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]
  6. Blackman R. K., Meselson M. Interspecific nucleotide sequence comparisons used to identify regulatory and structural features of the Drosophila hsp82 gene. J Mol Biol. 1986 Apr 20;188(4):499–515. doi: 10.1016/s0022-2836(86)80001-8. [DOI] [PubMed] [Google Scholar]
  7. Bone J. R., Kuroda M. I. Dosage compensation regulatory proteins and the evolution of sex chromosomes in Drosophila. Genetics. 1996 Oct;144(2):705–713. doi: 10.1093/genetics/144.2.705. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Braverman J. M., Hudson R. R., Kaplan N. L., Langley C. H., Stephan W. The hitchhiking effect on the site frequency spectrum of DNA polymorphisms. Genetics. 1995 Jun;140(2):783–796. doi: 10.1093/genetics/140.2.783. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Brock H. W., Roberts D. B. Location of the LSP-1 Genes in Drosophila Species by IN SITU Hybridization. Genetics. 1983 Jan;103(1):75–92. doi: 10.1093/genetics/103.1.75. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Charlesworth B. Model for evolution of Y chromosomes and dosage compensation. Proc Natl Acad Sci U S A. 1978 Nov;75(11):5618–5622. doi: 10.1073/pnas.75.11.5618. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Charlesworth B. The evolution of chromosomal sex determination and dosage compensation. Curr Biol. 1996 Feb 1;6(2):149–162. doi: 10.1016/s0960-9822(02)00448-7. [DOI] [PubMed] [Google Scholar]
  12. Comeron J. M. K-Estimator: calculation of the number of nucleotide substitutions per site and the confidence intervals. Bioinformatics. 1999 Sep;15(9):763–764. doi: 10.1093/bioinformatics/15.9.763. [DOI] [PubMed] [Google Scholar]
  13. Fu Y. X., Li W. H. Statistical tests of neutrality of mutations. Genetics. 1993 Mar;133(3):693–709. doi: 10.1093/genetics/133.3.693. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Fu Y. X. Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics. 1997 Oct;147(2):915–925. doi: 10.1093/genetics/147.2.915. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Hazelrigg T., Tu C. Sex-specific processing of the Drosophila exuperantia transcript is regulated in male germ cells by the tra-2 gene. Proc Natl Acad Sci U S A. 1994 Oct 25;91(22):10752–10756. doi: 10.1073/pnas.91.22.10752. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Hazelrigg T., Watkins W. S., Marcey D., Tu C., Karow M., Lin X. R. The exuperantia gene is required for Drosophila spermatogenesis as well as anteroposterior polarity of the developing oocyte, and encodes overlapping sex-specific transcripts. Genetics. 1990 Nov;126(3):607–617. doi: 10.1093/genetics/126.3.607. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. 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]
  18. 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]
  19. Jegalian K., Page D. C. A proposed path by which genes common to mammalian X and Y chromosomes evolve to become X inactivated. Nature. 1998 Aug 20;394(6695):776–780. doi: 10.1038/29522. [DOI] [PubMed] [Google Scholar]
  20. Kaplan N. L., Hudson R. R., Langley C. H. The "hitchhiking effect" revisited. Genetics. 1989 Dec;123(4):887–899. doi: 10.1093/genetics/123.4.887. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Kress H. The salivary gland chromosomes of Drosophila virilis: a cytological map, pattern of transcription and aspects of chromosome evolution. Chromosoma. 1993 Dec;102(10):734–742. doi: 10.1007/BF00650901. [DOI] [PubMed] [Google Scholar]
  22. Luk S. K., Kilpatrick M., Kerr K., Macdonald P. M. Components acting in localization of bicoid mRNA are conserved among Drosophila species. Genetics. 1994 Jun;137(2):521–530. doi: 10.1093/genetics/137.2.521. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Macdonald P. M., Luk S. K., Kilpatrick M. Protein encoded by the exuperantia gene is concentrated at sites of bicoid mRNA accumulation in Drosophila nurse cells but not in oocytes or embryos. Genes Dev. 1991 Dec;5(12B):2455–2466. doi: 10.1101/gad.5.12b.2455. [DOI] [PubMed] [Google Scholar]
  24. Macknight R H. The Sex-Determining Mechanism of Drosophila Miranda. Genetics. 1939 Mar;24(2):180–201. doi: 10.1093/genetics/24.2.180. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Marín I., Franke A., Bashaw G. J., Baker B. S. The dosage compensation system of Drosophila is co-opted by newly evolved X chromosomes. Nature. 1996 Sep 12;383(6596):160–163. doi: 10.1038/383160a0. [DOI] [PubMed] [Google Scholar]
  26. Miller D. D., Sanger W. G. Salivary gland chromosome variation in the Drosophila affinis subgroup. II. Comparison of C-chromosome patterns in D. athabasca and five related species. J Hered. 1968 Nov-Dec;59(6):323–327. doi: 10.1093/oxfordjournals.jhered.a107734. [DOI] [PubMed] [Google Scholar]
  27. Montgomery E., Charlesworth B., Langley C. H. A test for the role of natural selection in the stabilization of transposable element copy number in a population of Drosophila melanogaster. Genet Res. 1987 Feb;49(1):31–41. doi: 10.1017/s0016672300026707. [DOI] [PubMed] [Google Scholar]
  28. 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]
  29. Segarra C., Aguadé M. Molecular organization of the X chromosome in different species of the obscura group of Drosophila. Genetics. 1992 Mar;130(3):513–521. doi: 10.1093/genetics/130.3.513. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. 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]
  31. Smith J. M., Haigh J. The hitch-hiking effect of a favourable gene. Genet Res. 1974 Feb;23(1):23–35. [PubMed] [Google Scholar]
  32. Steinemann M. Analysis of chromosomal homologies between two species of the subgenus Sophophora: D. miranda and D. melanogaster using cloned DNA segments. Chromosoma. 1982;87(1):77–88. doi: 10.1007/BF00333510. [DOI] [PubMed] [Google Scholar]
  33. Steinemann M. Multiple sex chromosomes in Drosophila miranda: a system to study the degeneration of a chromosome. Chromosoma. 1982;86(1):59–76. doi: 10.1007/BF00330730. [DOI] [PubMed] [Google Scholar]
  34. Steinemann M., Steinemann S. Enigma of Y chromosome degeneration: neo-Y and neo-X chromosomes of Drosophila miranda a model for sex chromosome evolution. Genetica. 1998;102-103(1-6):409–420. [PubMed] [Google Scholar]
  35. Steinemann S., Steinemann M. The Amylase gene cluster on the evolving sex chromosomes of Drosophila miranda. Genetics. 1999 Jan;151(1):151–161. doi: 10.1093/genetics/151.1.151. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Stone W. S., Guest W. C., Wilson F. D. THE EVOLUTIONARY IMPLICATIONS OF THE CYTOLOGICAL POLYMORPHISM AND PHYLOGENY OF THE VIRILIS GROUP OF DROSOPHILA. Proc Natl Acad Sci U S A. 1960 Mar;46(3):350–361. doi: 10.1073/pnas.46.3.350. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Strobel E., Pelling C., Arnheim N. Incomplete dosage compensation in an evolving Drosophila sex chromosome. Proc Natl Acad Sci U S A. 1978 Feb;75(2):931–935. doi: 10.1073/pnas.75.2.931. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Suzuki M. G., Shimada T., Kobayashi M. Absence of dosage compensation at the transcription level of a sex-linked gene in a female heterogametic insect, Bombyx mori. Heredity (Edinb) 1998 Sep;81(Pt 3):275–283. doi: 10.1046/j.1365-2540.1998.00356.x. [DOI] [PubMed] [Google Scholar]
  39. Suzuki M. G., Shimada T., Kobayashi M. Bm kettin, homologue of the Drosophila kettin gene, is located on the Z chromosome in Bombyx mori and is not dosage compensated. Heredity (Edinb) 1999 Feb;82(Pt 2):170–179. doi: 10.1038/sj.hdy.6884570. [DOI] [PubMed] [Google Scholar]
  40. Tajima F. Relationship between DNA polymorphism and fixation time. Genetics. 1990 Jun;125(2):447–454. doi: 10.1093/genetics/125.2.447. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Tajima F. Simple methods for testing the molecular evolutionary clock hypothesis. Genetics. 1993 Oct;135(2):599–607. doi: 10.1093/genetics/135.2.599. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. 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]
  43. Theurkauf W. E., Hazelrigg T. I. In vivo analyses of cytoplasmic transport and cytoskeletal organization during Drosophila oogenesis: characterization of a multi-step anterior localization pathway. Development. 1998 Sep;125(18):3655–3666. doi: 10.1242/dev.125.18.3655. [DOI] [PubMed] [Google Scholar]
  44. Tonzetich J., Hayashi S., Grigliatti T. A. Conservatism of sites of tRNA loci among the linkage groups of several Drosophila species. J Mol Evol. 1990 Feb;30(2):182–188. doi: 10.1007/BF02099944. [DOI] [PubMed] [Google Scholar]
  45. Vieira C. P., Vieira J., Hartl D. L. The evolution of small gene clusters: evidence for an independent origin of the maltase gene cluster in Drosophila virilis and Drosophila melanogaster. Mol Biol Evol. 1997 Oct;14(10):985–993. doi: 10.1093/oxfordjournals.molbev.a025715. [DOI] [PubMed] [Google Scholar]
  46. Wall J. D. A comparison of estimators of the population recombination rate. Mol Biol Evol. 2000 Jan;17(1):156–163. doi: 10.1093/oxfordjournals.molbev.a026228. [DOI] [PubMed] [Google Scholar]
  47. 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]
  48. 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]
  49. Yi S., Charlesworth B. Contrasting patterns of molecular evolution of the genes on the new and old sex chromosomes of Drosophila miranda. Mol Biol Evol. 2000 May;17(5):703–717. doi: 10.1093/oxfordjournals.molbev.a026349. [DOI] [PubMed] [Google Scholar]
  50. Younger-Shepherd S., Vaessin H., Bier E., Jan L. Y., Jan Y. N. deadpan, an essential pan-neural gene encoding an HLH protein, acts as a denominator in Drosophila sex determination. Cell. 1992 Sep 18;70(6):911–922. doi: 10.1016/0092-8674(92)90242-5. [DOI] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES