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The Dosage compensation of Drosophila and mammals as showing the accuracy of the normal type*

Published online by Cambridge University Press:  14 April 2009

H. J. Muller  and
W. D. Kaplan
H. J. Muller
Affiliation:
City of Hope Medical Center, Duarte, California, U.S.A.
W. D. Kaplan
Affiliation:
City of Hope Medical Center, Duarte, California, U.S.A.
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Examination, in the salivary gland nuclei of D. melanogaster males, of four cases of translocation between the X and fourth chromosome, involving breaks of the X in widely different positions, disclosed no influence of the rearrangement on the width, morphology or chromatin-staining of either of the separated parts of the X, or on the fourth chromosome. Both parts of the single X were distinctly narrower than were the double major autosomes, as is true for the X of normal males but not for the double X of females. At the junction between a portion of a translocated single X and the double fourth chromosomes the transition in width, morphology and staining was abrupt and striking. As in structurally normal males, however, the parts of a single X, here removed from one another by the translocation, did appear to be somewhat swollen, as compared with half of a double chromosome, but to be correspondingly paler in stain, so as to indicate an unaltered amount of chromatin (see also Offermann, 1936; Rudkin, 1964; Pavan & Frota-Pessoa, 1964).

The above evidence of the regional autonomy in characteristics of the different parts of the X studied by us, and also of the fourth chromosome, is in contrast to the lack of such autonomy found in translocation studies on mammals, where the X chromosome and that joined with it are subject to an influence diffusing along them and thus acting ‘wholesale’, rather than ‘piecemeal’. Likewise, a re-examination of the earlier genetic evidence on dosage compensation in Drosophila leads back again to a decidedly ‘piecemeal’ interpretation of its operation and evolution, according to which most genes in the X, and sometimes even different phases of the action of the same gene, have their own system of separately evolved, scattered compensators, which are also located in the X.

The fact that two so differently working compensation mechanisms as those in Drosophila and mammals have evolved independently to serve the same function emphasizes the importance of that function. That is, it points up the survival value of having the effectiveness of normal genes regulated to a very exact level. For the compensation enables the single representative of the X in the male cell to become equivalent to the two representatives of the X in the female cell. Moreover, this equivalence is of a considerably finer grade than that already afforded by the phenomenon termed ‘dominance’, which has evolved to meet the same basic need (that of phenotypic stabilization), and which has, incidentally, made even the uncompensated effects of one and two doses of either sex-linked or autosomal normal genes not readily distinguishable in most cases.

Taken by itself, the ‘piecemeal’ mechanism of Drosophila provides far stronger evidence for this conclusion than does the ‘wholesale’ mechanism in mammals. For the former must have required the establishment of far more numerous mutational steps and, taken individually, each of these steps was of correspondingly lesser survival value. Since they nevertheless affected fitness enough to become established, it also follows that usually a normal gene—or at any rate one of the kinds whose mutants have usually been studied—confers a significantly higher fitness when not heterozygous for such a mutation in it, despite the seeming recessiveness of most mutations. Thus, the expression ‘normal gene’ continues to have a very high validity.

Type
Research Article
Information
Genetics Research , Volume 8 , Issue 1 , August 1966 , pp. 41 - 59
Copyright
Copyright © Cambridge University Press 1966

References

REFERENCES

Altenburg, E. & Muller, H. J. (1920). The genetic basis of Truncate wing—an inconstant and modifiable character in Drosophila. Genetics, 5, 1–59.Google Scholar
Aronson, J. F., Rudkin, G. T. & Schultz, J. (1954). A comparison of giant X-chromosomes in male and female Drosophila melanogaster by cytophotometry in the ultraviolet. J. Histochem. Cytochem. 2, 452–459.Google Scholar
Cattanach, B. M. (1961). A chemically-induced variegated-type position effect in the mouse. Z. indukt. Abstamm.-u. VererbLehre, 92, 165–182.Google Scholar
Dobzhansky, Th. (1957). The X-chromosome in the larval salivary glands of hybrids Drosophila insularis × Drosophila tropicalis. Chromosoma, 8, 691–698.CrossRefGoogle ScholarPubMed
Grell, R. F. & Lewis, E. B. (1956). FM6: First multiple 6. Drosoph. Inf. Serv. No. 30, 71.Google Scholar
Littau, C. C., Burdick, C. J., Allfrey, V. G. & Mirsky, A. E. (1965). The role of histones in the maintenance of chromatin structure. Proc. natn. Acad. Sci. U.S.A. 54, 1204–1212.Google Scholar
Lyon, Mary F. (1961). Gene action in the X-chromosome of the mouse (Mus musculus L.). Nature, Lond. 190, 372–373.Google Scholar
Mackensen, O. (1934). A cytological study of short deficiencies in the X-chromosome of Drosophila melanogaster. Am. Nat. 69, 69.Google Scholar
Morgan, T. H., Bridges, C. B. & Sturtevant, A. H. (1925). The Genetics of Drosophila. Bibliographia Genetica, II, 's-Gravenhage, Martinus Nijhoff.Google Scholar
Morgan, T. H., Sturtevant, A. H., Muller, H. J. & Bridges, C. B. (1915). The Mechanism of Mendelian Heredity. New York: Henry Holt.Google Scholar
Morton, N. E., Krieger, H. & Mi, M. P. (1966). Natural selection of polymorphism in north-eastern Brazil. Am. J. hum. Genet. (in press).Google Scholar
Muller, H. J. (1914). The bearing of the selection experiments of Castle and Phillips on the variability of genes. Am. Nat. 48, 567–576.Google Scholar
Muller, H. J. (1918) Genetic variability, twin hybrids and constant hybrids, in a case of balanced lethal factors. Genetics, 3, 422–429.CrossRefGoogle Scholar
Muller, H. J. (1930). Types of visible variations induced by X-rays in Drosophila. J. Genet. 22, 299–334.Google Scholar
Muller, H. J. (1933). Further studies on the nature and causes of gene mutations. Proc. 6th Int. Congr. Genet., Ithaca, 1, 213–255.Google Scholar
Muller, H. J. (1950). Evidence of the precision of genetic adaptation. In The Harvey Lectures, Ser. XLIII, 1947–48, pp. 165–229. Springfield, I11.: Charles C. Thomas.Google Scholar
Muller, H. J. & Kaplan, W. D. (1964). Dosage compensation as an exemplification of genetic accuracy. Science, N.Y. 146, 427–428.Google Scholar
Muller, H. J., League, B. B. & Offermann, C. A. (1931). Effects of dosage changes of sex-linked genes, and the compensatory effect of other gene-differences between male and female. Anat. Rec. 51, Suppl., 110.Google Scholar
Nicoletti, Benedetto (1959). An efficient method for salivary-gland-chromosome preparations. Drosoph. Inf. Serv. No. 33, 181–182.Google Scholar
Offermann, C. A. (1936). Branched chromosomes as symmetrical duplications. J. Genet. 32, 103–116.Google Scholar
Ohno, S. & Cattanach, B. M. (1962). Cytological study of an X-autosome translocation in Mus musculus. Cytogenetics, 1, 129–140.Google Scholar
Ohno, S., Kaplan, W. D. & Kinosita, R. (1959). Formation of the sex chromatin by a single X-chromosome in liver cells of Rattus norvegicus. Expl. Cell Res. 18, 415–418.CrossRefGoogle ScholarPubMed
Pavan, C. & Basile, R. (1966). Changes in chromosomes induced by infection in various tissues of Rhynchosciara angelae. Science, N.Y. (in press).Google Scholar
Pavan, C. & Frota-Pessoa, O. (1964). O mecanismo de compensação de dose nos insetos. Ciênc. Cult. 16, No. 2, 251–252.Google Scholar
Plunkett, C. R. (1933 a). Temperature as a tool of research in phenogenetics: methods and results. Proc. 6th Int. Congr. Genet., Ithaca, 2, 158–160.Google Scholar
Plunkett, C. R. (1933 b). A contribution to the theory of dominance. Am. Nat. 67, 84–85.Google Scholar
Rudkin, G. T. (1964). The proteins of polytene chromosomes. In The Nucleohistones (Bonner, and Ts'o, , eds.), pp. 184–192. San Francisco: Holden Day.Google Scholar
Russell, Liane B. (1963). Mammalian X-chromosome action: Inactivation limited in spread and in region of origin. Science, N.Y. 140, 976–978.Google Scholar
Simões, L. C. G., Guedes, A. S. & Schreiber, G. (1962). Observações sôbre o cariotipo de Anopheles. (Nyssorhynchus) darlingi Root. Ciênc. Cult. 14, No. 1, 37.Google Scholar
Stern, C. (1929). Über die additive Wirkung multipler Allele. Biol. Zbl. 49, 261–290.Google Scholar
Stern, C. (1930). Multiple Allele. Hanb. Vererbungsw. I, (No. 14). Berlin; Gebr. Borntraeger.Google Scholar
Stern, C. & Ogura, S. (1931). Neue Untersuchungen über Aberrationen des Y-Chromosoms von Drosophila melanogaster. Z. indukt. Abstamm.-u. VererbLehre, 58, 81–121.Google Scholar