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. 1997 Apr;145(4):989–1002. doi: 10.1093/genetics/145.4.989

Lack of Degeneration of Loci on the Neo-Y Chromosome of Drosophila Americana Americana

B Charlesworth 1, D Charlesworth 1, J Hnilicka 1, A Yu 1, D S Guttman 1
PMCID: PMC1207902  PMID: 9093852

Abstract

The extent of genetic degeneration of the neo-Y chromosome of Drosophila americana americana has been investigated. Three loci, coding for the enzymes enolase, phosphoglycerate kinase and alcohol dehydrogenase, have been localized to chromosome 4 of D. a. americana, which forms the neo-Y and neo-X chromosomes. Crosses between D. a. americana and D. virilis or D. montana showed that the loci coding for these enzymes carry active alleles on the neo-Y chromosome in all wild-derived strains of americana that were tested. Intercrosses between a genetically marked stock of virilis and strains of americana were carried out, creating F(3) males that were homozygous for sections of the neo-Y chromosome. The sex ratios in the F(3) generation of the intercrosses showed that no lethal alleles have accumulated on any of the neo-Y chromosomes tested. There was evidence for more minor reductions in fitness, but this seems to be mainly caused by deleterious alleles that are specific to each strain. A similar picture was provided by examination of the segregation ratios of two marker genes among the F(3) progeny. Overall, the data suggest that the neo-Y chromosome has undergone very little degeneration, certainly not to the extent of having lost the functions of vital genes. This is consistent with the recent origin of the neo-Y and neo-X chromosomes, and the slow rates at which the forces that cause Y chromosome degeneration are likely to work.

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Selected References

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  1. 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]
  2. 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]
  3. 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]
  4. 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]
  5. Charlesworth B. The evolution of sex chromosomes. Science. 1991 Mar 1;251(4997):1030–1033. doi: 10.1126/science.1998119. [DOI] [PubMed] [Google Scholar]
  6. Coyne J. A. Do males of Drosophila littoralis have free recombination? Hereditas. 1988;109(2):281–283. doi: 10.1111/j.1601-5223.1988.tb00366.x. [DOI] [PubMed] [Google Scholar]
  7. Graves J. A. The origin and function of the mammalian Y chromosome and Y-borne genes--an evolving understanding. Bioessays. 1995 Apr;17(4):311–320. doi: 10.1002/bies.950170407. [DOI] [PubMed] [Google Scholar]
  8. 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]
  9. Kreitman M. Nucleotide polymorphism at the alcohol dehydrogenase locus of Drosophila melanogaster. Nature. 1983 Aug 4;304(5925):412–417. doi: 10.1038/304412a0. [DOI] [PubMed] [Google Scholar]
  10. Krishnan R., Swanson K. D., Ganguly R. Dosage compensation of a retina-specific gene in Drosophila miranda. Chromosoma. 1991 Feb;100(2):125–133. doi: 10.1007/BF00418246. [DOI] [PubMed] [Google Scholar]
  11. LYON M. F. Gene action in the X-chromosome of the mouse (Mus musculus L.). Nature. 1961 Apr 22;190:372–373. doi: 10.1038/190372a0. [DOI] [PubMed] [Google Scholar]
  12. Lumme J., Lankinen P. Comments to Jerry A. Coyne: Do males of Drosophila littoralis have free recombination? Hereditas. 1988;109(2):283–283. doi: 10.1111/j.1601-5223.1988.tb00367.x. [DOI] [PubMed] [Google Scholar]
  13. 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]
  14. Norman R. A., Doane W. W. Dosage compensation and dietary glucose repression of larval amylase activity in Drosophila miranda. Biochem Genet. 1990 Dec;28(11-12):601–613. doi: 10.1007/BF00553953. [DOI] [PubMed] [Google Scholar]
  15. Nurminsky D. I., Moriyama E. N., Lozovskaya E. R., Hartl D. L. Molecular phylogeny and genome evolution in the Drosophila virilis species group: duplications of the alcohol dehydrogenase gene. Mol Biol Evol. 1996 Jan;13(1):132–149. doi: 10.1093/oxfordjournals.molbev.a025551. [DOI] [PubMed] [Google Scholar]
  16. Orr H. A., Coyne J. A. The genetics of postzygotic isolation in the Drosophila virilis group. Genetics. 1989 Mar;121(3):527–537. doi: 10.1093/genetics/121.3.527. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Rice W. R. Degeneration of a nonrecombining chromosome. Science. 1994 Jan 14;263(5144):230–232. doi: 10.1126/science.8284674. [DOI] [PubMed] [Google Scholar]
  18. Roberts D. B., Evans-Roberts S. The genetic and cytogenetic localization of the three structural genes coding for the major protein of drosophila larval serum. Genetics. 1979 Nov;93(3):663–679. doi: 10.1093/genetics/93.3.663. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Russo C. A., Takezaki N., Nei M. Molecular phylogeny and divergence times of drosophilid species. Mol Biol Evol. 1995 May;12(3):391–404. doi: 10.1093/oxfordjournals.molbev.a040214. [DOI] [PubMed] [Google Scholar]
  20. Simmons M. J., Crow J. F. Mutations affecting fitness in Drosophila populations. Annu Rev Genet. 1977;11:49–78. doi: 10.1146/annurev.ge.11.120177.000405. [DOI] [PubMed] [Google Scholar]
  21. Sniegowski P. D., Charlesworth B. Transposable element numbers in cosmopolitan inversions from a natural population of Drosophila melanogaster. Genetics. 1994 Jul;137(3):815–827. doi: 10.1093/genetics/137.3.815. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Sperlich D., Feuerbach-Mravlag H., Lange P., Michaelidis A., Pentzos-Daponte A. Genetic Load and Viability Distribution in Central and Marginal Populations of DROSOPHILA SUBOBSCURA. Genetics. 1977 Aug;86(4):835–848. doi: 10.1093/genetics/86.4.835. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Stalker H. D. CHROMOSOME HOMOLOGIES IN TWO SUB-SPECIES OF DROSOPHILA VIRILIS. Proc Natl Acad Sci U S A. 1940 Sep 15;26(9):575–578. doi: 10.1073/pnas.26.9.575. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Steinemann M., Steinemann S., Lottspeich F. How Y chromosomes become genetically inert. Proc Natl Acad Sci U S A. 1993 Jun 15;90(12):5737–5741. doi: 10.1073/pnas.90.12.5737. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Stephan W. An improved method for estimating the rate of fixation of favorable mutations based on DNA polymorphism data. Mol Biol Evol. 1995 Sep;12(5):959–962. doi: 10.1093/oxfordjournals.molbev.a040274. [DOI] [PubMed] [Google Scholar]
  26. 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]
  27. Tominaga H., Narise S. Sequence evolution of the Gpdh gene in the Drosophila virilis species group. Genetica. 1995;96(3):293–302. doi: 10.1007/BF01439583. [DOI] [PubMed] [Google Scholar]

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