Hostname: page-component-cd9895bd7-dzt6s Total loading time: 0 Render date: 2024-12-26T16:42:59.516Z Has data issue: false hasContentIssue false

A comparison of genetic variability at X-linked and autosomal loci in kangaroos, man and Drosophila

Published online by Cambridge University Press:  14 April 2009

D. W. Cooper
Affiliation:
School of Biological Sciences, Macquarie University, North Ryde, N.S.W. 2113, Australia
P. G. Johnston
Affiliation:
School of Biological Sciences, Macquarie University, North Ryde, N.S.W. 2113, Australia
J. L. Vandeberg
Affiliation:
School of Biological Sciences, Macquarie University, North Ryde, N.S.W. 2113, Australia
G. M. Maynes
Affiliation:
School of Biological Sciences, Macquarie University, North Ryde, N.S.W. 2113, Australia
G. K. Chew
Affiliation:
Department of Genetics and Human Variation, La Trobe University, Bundoora, Vic. 3083, Australia
Rights & Permissions [Opens in a new window]

Summary

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

This paper tests the hypothesis that haplodiploidy or X linkage leads to less genetic variability. Although haplodiploid organisms exhibit a low level of genetic variability the wide variation existing between different diploid organisms implies that factors other than the genetical system could also be responsible. In order to test the hypothesis critically it is necessary to compare the level of genetic variability between X-linked and autosomal genes within a closely related group of organisms. For kangaroos, the ascertainment bias for X-linked loci has been removed by assuming the correctness of Ohno's law of conservation of the mammalian X, i.e. that genes found to be X-linked in man can be assumed to be X-linked in kangaroos. For Man and Drosophila, it has been assumed that the percentage of the karyotype which is X chromosome can be used as the expectation for the percentage of X-linked polymorphisms. No difference between the two classes of loci is evident in kangaroos and man for percentage polymorphism. The data however have confidence limits which would allow autosomal loci to have three times greater percentage polymorphism. In Drosophila the published data of Prakash show that autosomal loci are polymorphic about twice as frequently as are their X-linked counterparts. Thus there may be a modest reduction in percentage polymorphism as a result of X-linkage (i.e. haplodiploidy). No reduction in the number of alleles per locus or average heterozygosity at those loci which are polymorphic is evident in kangaroos, man, or Drosophila. More data on more X-linked enzymes are necessary to establish firmly that there is a real reduction in percentage polymorphism and to estimate its extent. The kangaroo data are incompatible with the hypothesis that a large fraction of the variability is maintained by simple overdominance since overdominance is very unlikely in the quasi-haploid genetical system which results from the paternal X inactivation mode of dosage compensation used by kangaroos. This is the first report on level of enzymic variability in marsupials. 17% of autosomal loci and 18% of X-linked loci are polymorphic, average heterozygosity is 4% for autosomal and 4% for X-linked loci and number of alleles per locus is 1·25 for autosomal and 1·21 for X-linked loci. These figures are somewhat lower than for eutherian mammals.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1979

References

REFERENCES

Bennett, J. H. (1958). The existence and stability of selectively balanced polymorphism at a sex-linked locus. Australian Journal of Biological Science 11, 598602.CrossRefGoogle Scholar
Beutler, E. & Yoshida, A. (1973). Human glucose-6-phosphate dehydrogenase variants: a supplementary tabulation. Annals of Human Genetics 37, 151156.CrossRefGoogle ScholarPubMed
Campbell, P. G. M., Rosenberg, L. E., Snodgrass, P. G. & Nazum, C. T. (1971). Lethal neonatal hyperammonaemia due to complete orithine transcarbamylase deficiency. Lancet ii. 217218.CrossRefGoogle Scholar
Carson, H. L. (1955). Variation in genetic recombination in natural populations. Journal of Cellular and Comparative Physiology 45 (Supplement 2), 221235. Cited by Prakash (1973).CrossRefGoogle ScholarPubMed
Cavalli-Sforza, L. L. & Bodmer, W. F. (1971). The Genetics of Human Populations. San Francisco: Freeman.Google Scholar
Chen, S. H., Malcolm, L. A., Yoshida, A. & Giblett, E. R. (1971). Phosphoglycerate kinase: an X-linked polymorphism in man. American Journal of Human Genetics 23, 8791.Google ScholarPubMed
Cooper, D. W. (1976). Studies on metatherian sex chromosomes. II. The improbability of a stable balanced polymorphism at an X-linked locus with the paternal X-inactivation systems of kangaroos. Australian Journal of Biological Science 29, 245–50.CrossRefGoogle ScholarPubMed
Cooper, D. W. (1978). Plasma protein variation in man. In The Biochemical Genetics of Man, 2nd ed. (ed. Brock, D. L. H. and Mayo, O.). New York: Academic Press.Google Scholar
Cooper, D. W., James, E. A. & Woolley, P. W. (1979). Molecular evolution in some Antechinus and related dasyurid species. (To be submitted.)Google Scholar
Cooper, D. W., Johnston, P. G., Sharman, G. B. & VandeBerg, J. L. (1977). The control of gene activity on eutherian and metatherian X-chromosomes: a comparison. In Reproduction and Evolution (ed. Calaby, J. H. and Tyndale-Biscoe, C. H.). Proceedings of the Fourth International Symposium on Comparative Biology of Reproduction, Australian Academy of Science, Canberra, 8187.Google Scholar
Crozier, R. H. (1976). Counter intuitive property of effective population size. Nature 262, 384.CrossRefGoogle ScholarPubMed
Crozier, R. H. (1977). Evolutionary genetics of the Hymenoptera. Annual Review of Entomology 22, 263288.CrossRefGoogle Scholar
Haldane, J. B. S. & Jayakar, S. D. (1964). Equilibria under natural selection at a sex linked locus. Journal of Genetics 59, 2936.CrossRefGoogle Scholar
Harris, H. (1970). The Principles of Human Biochemical Genetics, pp. 232233. Amsterdam and London: North-Holland.Google Scholar
Harris, H. & Hopkinson, D. A. (1972). Average heterozygosity per locus in man: an estimate based on the incidence of enzyme polymorphisms. Annals of Human Genetics 36, 920.CrossRefGoogle Scholar
Hartl, D. L. (1971). Some aspects of natural selection in arrhenotokus populations. American Zoologist 11, 309325.CrossRefGoogle Scholar
Johnston, P. G. & Sharman, G. B. (1975). Studies on metatherian sex chromosomes. I. Inheritance and inactivation of sex linked allelic genes determining glucose-6-phosphate dehydrogenase variation in kangaroos. Australian Journal of Biological Sciences 28, 567–564.CrossRefGoogle ScholarPubMed
Kint, J. A. (1970). Fabry's disease: alpha-galactosidase deficiency. Science 167, 1286–1269.CrossRefGoogle ScholarPubMed
Kirsch, J. A. W. & Poole, W. E. (1972). Taxonomy and distribution of the grey kangaroos, Macropus giganteus Shaw and Macropus fuliginosus (Desmarest) and their subspecies (Marsupialia: Macropodidae). Australian Journal of Zoology 20, 315339.CrossRefGoogle Scholar
Lewontin, R. C. (1974). The Genetic Basis of Evolutionary Change. Columbia: Columbia University Press.Google Scholar
Lyon, M. F. (1974). Mechanisms and evolutionary origins of variable X-chromosome activity in mammals. Proceedings of the Royal Society, Series B 187, 243268.Google ScholarPubMed
McKusick, V. A. (1975). Mendelian Inheritance in Man, 4th ed.Baltimore and London: Johns Hopkins, University Press.Google Scholar
Meera Khan, P. (1971). Enzyme electrophoresis on cellulose acetate gel: zymogram patterns in man–mouse and man–Chinese hamster somatic cell hybrids. Archives of Biochemistry and Biophysics 145, 470483.CrossRefGoogle Scholar
Metcalf, R. A., Marlin, T. C. & Whitt, G. S. (1975). Low levels of genetic heterozygosity in Hymenoptera. Nature 257, 792794.CrossRefGoogle ScholarPubMed
Milkman, R. (1973). Electrophoretic variation in Escherischia coli from natural sources. Science 182, 10241026.CrossRefGoogle Scholar
Morton, N. E. (1971). Population genetics and disease control. Social Biology 18, 243251.CrossRefGoogle ScholarPubMed
Newsome, A. E. (1977). Imbalance in the sex ratio and age structure of the red kangaroo, Macropus rufus, in Central Australia. In The Biology of Marsupials, (ed. Stonehouse, B. and Gilmore, D.). London: Macmillan Press.Google Scholar
Ohno, S. (1967). Sex Chromosomes and Sex Linked Genes. Berlin, Heidleberg and New York: Springer Verlag.CrossRefGoogle Scholar
Ohno, S. (1969). Evolution of sex chromosomes in mammals. Annual Review of Genetics 3, 495524.CrossRefGoogle Scholar
Omoto, K. & Blake, N. M. (1972). Distribution of genetic variants of erythrocyte phosphoglycerate kinase (PGK) and phosphohexose isomerase (PHI) among some population groups in south-east Asia and Oceania. Annals of Human Genetics 36, 6167.CrossRefGoogle ScholarPubMed
Pamilo, P., Varvio-Aho, S.-L. & Pekkarinen, A. (1978). Low enzyme variability in Hymenoptera as a consequence of haplodiploidy. Hereditas 88, 9399.CrossRefGoogle Scholar
Prakash, S. (1973). Patterns of gene variation in central and marginal populations of Drosophila robusta. Genetics 75, 347369.CrossRefGoogle ScholarPubMed
Prakash, S. (1977 a). Gene polymorphism in natural populations of Drosophila persimilis. Genetics 85, 513530.CrossRefGoogle ScholarPubMed
Prakash, S. (1977 b). Further studies on gene polymorphism in the mainbody and geographically isolated populations of Drosophila pseudoobscurra. Genetics 85, 713719.CrossRefGoogle Scholar
Prakash, S., Lewontin, R. C. & Hubby, J. L. (1969). A molecular approach to the study of genie heterozygosity in natural populations. IV. Patterns of genie variation in central, marginal, and isolated populations of Drosophila pseudoobscura. Genetics 61, 841858.CrossRefGoogle Scholar
Race, R. R. & Sanger, R. (1975). Blood Groups in Man, 6th ed.Oxford: Blackwell Scientific Publications.Google Scholar
Richardson, B. J. (1970). Ph.D. thesis, University of New South Wales.Google Scholar
Scott, C. R., Teng, C. C., Goodman, S. I., Greensher, A. & Mace, J. W. (1972). X-linked transmission of ornithine-transcarbamylase deficiency. Lancet ii, 1148.CrossRefGoogle Scholar
Shaw, C. R. & Prasad, R. (1970). Starch gel electrophoresis – a compilation of recipes. Biochemical Genetics 4, 297330.CrossRefGoogle ScholarPubMed
Tan, C. C. (1935). The salivary gland chromosomes in the two races of Drosophila pseudoobscura. Genetics 20, 392402.CrossRefGoogle ScholarPubMed
White, M. J. D. (1973). In Animal Cytology and Evolution, 3rd ed. p. 693. Cambridge University Press.Google Scholar