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. 1978 Nov;75(11):5618–5622. doi: 10.1073/pnas.75.11.5618

Model for evolution of Y chromosomes and dosage compensation.

B Charlesworth
PMCID: PMC393018  PMID: 281711

Abstract

Some difficulties with the classical model for the evolution of a genetically invert Y chromosome are discussed. An alternative model is proposed, which is based on the principle of Mullers ratchet; this involves the accumulation of chromosomes bearing deleterious mutant genes in a finite population in the absence of crossing-over. This process would result in the gradual increase, with time, in the number of mutant loci carried in an average Y chromosome, although the frequency of individual deleterious alleles at most loci remains low. It is shown that this creates a selection pressure for differentially increasing the activity of the X chromosome in heterogametic individuals at the expense of that of the Y, leading eventually to a genetically inert Y chromosome and to the evolution of dosage compensation.

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Selected References

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

  1. Abraham I., Lucchesi J. C. Dosage compensation of genes on the left and right arms of the X chromosome of Drosophila pseudoobscura and Drosophila willistoni. Genetics. 1974 Dec;78(4):1119–1126. doi: 10.1093/genetics/78.4.1119. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Brown S. W., Chandra H. S. Inactivation system of the mammalian X chromosome. Proc Natl Acad Sci U S A. 1973 Jan;70(1):195–199. doi: 10.1073/pnas.70.1.195. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Cooper D. W. Directed genetic change model for X chromosome inactivation in eutherian mammals. Nature. 1971 Apr 2;230(5292):292–294. doi: 10.1038/230292a0. [DOI] [PubMed] [Google Scholar]
  4. Cooper D. W., VandeBerg J. L., Sharman G. B., Poole W. E. Phosphoglycerate kinase polymorphism in kangaroos provides further evidence for paternal X inactivation. Nat New Biol. 1971 Mar 31;230(13):155–157. doi: 10.1038/newbio230155a0. [DOI] [PubMed] [Google Scholar]
  5. Dronamraju K. R. The function of the y-chromosome in man, animals, and plants. Adv Genet. 1965;13:227–310. [PubMed] [Google Scholar]
  6. Felsenstein J. The evolutionary advantage of recombination. Genetics. 1974 Oct;78(2):737–756. doi: 10.1093/genetics/78.2.737. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Felsenstein J., Yokoyama S. The evolutionary advantage of recombination. II. Individual selection for recombination. Genetics. 1976 Aug;83(4):845–859. doi: 10.1093/genetics/83.4.845. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Hamilton W. D. Extraordinary sex ratios. A sex-ratio theory for sex linkage and inbreeding has new implications in cytogenetics and entomology. Science. 1967 Apr 28;156(3774):477–488. doi: 10.1126/science.156.3774.477. [DOI] [PubMed] [Google Scholar]
  9. Lakhotia S. C., Mukherjee A. S. Chromosomal basis of dosage compensation in Drosophila. I. Cellular autonomy of hyperactivity of the male X-chromosome in salivary glands and sex differentiation. Genet Res. 1969 Oct;14(2):137–150. doi: 10.1017/s001667230000197x. [DOI] [PubMed] [Google Scholar]
  10. Lifschytz E., Lindsley D. L. The role of X-chromosome inactivation during spermatogenesis (Drosophila-allocycly-chromosome evolution-male sterility-dosage compensation). Proc Natl Acad Sci U S A. 1972 Jan;69(1):182–186. doi: 10.1073/pnas.69.1.182. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Lucchesi J. C. Dosage compensation in Drosophila. Annu Rev Genet. 1973;7:225–237. doi: 10.1146/annurev.ge.07.120173.001301. [DOI] [PubMed] [Google Scholar]
  12. Lyon M. F. Mechanisms and evolutionary origins of variable X-chromosome activity in mammals. Proc R Soc Lond B Biol Sci. 1974 Nov 5;187(1088):243–268. doi: 10.1098/rspb.1974.0073. [DOI] [PubMed] [Google Scholar]
  13. MULLER H. J. Our load of mutations. Am J Hum Genet. 1950 Jun;2(2):111–176. [PMC free article] [PubMed] [Google Scholar]
  14. MULLER H. J. THE RELATION OF RECOMBINATION TO MUTATIONAL ADVANCE. Mutat Res. 1964 May;106:2–9. doi: 10.1016/0027-5107(64)90047-8. [DOI] [PubMed] [Google Scholar]
  15. 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]
  16. Maroni G., Plaut W. Dosage Compensation in DROSOPHILA MELANOGASTER Triploids. II. Glucose-6-Phosphate Dehydrogenase Activity. Genetics. 1973 Jun;74(2):331–342. doi: 10.1093/genetics/74.2.331. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Mukai T., Chigusa S. I., Mettler L. E., Crow J. F. Mutation rate and dominance of genes affecting viability in Drosophila melanogaster. Genetics. 1972 Oct;72(2):335–355. doi: 10.1093/genetics/72.2.335. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Mukherjee A. S., Beermann W. Synthesis of ribonucleic acid by the X-chromosomes of Drosophila melanogaster and the problem of dosage compensation. Nature. 1965 Aug 14;207(998):785–786. doi: 10.1038/207785a0. [DOI] [PubMed] [Google Scholar]
  19. Mukherjee A. S., Chatterjee S. N. Chromosomal basis of dosage compensation in Drosophila VIII. Faster replication and hyperactivity of both arms of the X-chromosome in males of Drosophila pseudoobscura and their possible significance. Chromosoma. 1975 Nov 24;53(2):91–105. doi: 10.1007/BF00333038. [DOI] [PubMed] [Google Scholar]
  20. Muller H J. Genetic Variability, Twin Hybrids and Constant Hybrids, in a Case of Balanced Lethal Factors. Genetics. 1918 Sep;3(5):422–499. doi: 10.1093/genetics/3.5.422. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Richardson B. J., Czuppon A. B., Sharman G. B. Inheritance of glucose-6-phosphate dehydrogenase variation in kangaroos. Nat New Biol. 1971 Mar 31;230(13):154–155. doi: 10.1038/newbio230154a0. [DOI] [PubMed] [Google Scholar]
  22. Schwartz D. The application of the maize-derived gene competition model to the problem of dosage compensation in Drosophila. Genetics. 1973 Dec;75(4):639–641. doi: 10.1093/genetics/75.4.639. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. 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]
  24. Stewart B. R., Merriam J. R. Regulation of gene activity by dosage compensation at the chromosomal level in drosophila. Genetics. 1975 Apr;79(4):635–647. doi: 10.1093/genetics/79.4.635. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. 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]

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