Hostname: page-component-586b7cd67f-vdxz6 Total loading time: 0 Render date: 2024-11-20T09:36:34.821Z Has data issue: false hasContentIssue false
  • English
  • Français

Can chromosomal heterosis in Drosophila be explained by deleterious recessive genes? Negative results from a dichromosomal population test

Published online by Cambridge University Press:  14 April 2009

Alan N. Wilton ,
Michael G. Joseph  and
John A. Sved
Alan N. Wilton
Affiliation:
School of Biological Sciences A12, University of Sydney, NSW 2006, Australia
Michael G. Joseph
Affiliation:
School of Biological Sciences A12, University of Sydney, NSW 2006, Australia
John A. Sved
Affiliation:
School of Biological Sciences A12, University of Sydney, NSW 2006, 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.

High levels of chromosomal heterosis have previously been detected in Drosophila using the balancer chromosome equilibration (BE) technique, in which single wild-type chromosomes are introduced into population cages along with a dominant/lethal balancer chromosome. The balancer chromosome is rarely eliminated in such populations, showing that the fitness of chromosome homozygotes must be low by comparison with chromosomal heterozygotes. As with all cases of chromosomal heterosis, the underlying cause could either be deleterious recessives at various loci or generalized overdominance. The experiment of the present paper examines the first of these explanations. Population cages containing just two wild-type chromosomes (dichromosomal populations) were set up and allowed to run for many generations. Single chromosomes were then re-extracted from these populations, and their fitness measured using the BE technique. Our expectation was that the gradual elimination of recessive genes from the dichromosomal populations ought to result in an increase in the fitness of such re-extracted chromosome homozygotes. Yet in two replicated experiments we were unable to demonstrate an; unequivocal increase in fitness. We have estimated the rate of increase of fitness under multiple locus dominance and partial dominance models. The principal unknown parameter in these calculations is the selection intensity per locus, s. The expected increase is approximately proportional to s, and we estimate that values of s around 1/64 should be detectable in our experiments. However linkage is expected to reduce the efficiency of the dichromosomal procedure We show by computer simulation that this reduction is by a factor of approximately 2, thus increasing the detectable level of s to approximately 1/32. Consideration of mutation-selection balance models shows that this is a feasible selection intensity only if dominance is nearly complete. Thus we are unable to rule out the notion that the genes responsible for heterosis are maintained by a simple mutation-selection balance, but the experimental results constrain the parameters of such a model to a narrow range.

Type
Research Article
Information
Genetics Research , Volume 53 , Issue 2 , April 1989 , pp. 129 - 140
Copyright
Copyright © Cambridge University Press 1989

References

Collins, G. N. (1921). Dominance and the vigor of first generation hybrids. American Naturalist 55, 116–133.Google Scholar
Crow, J. F. (1979). Minor viability mutants in Drosophila. Genetics 92, s165–s172.Google Scholar
Crow, J. F. & Simmons, M. J. (1983). The mutation load in Drosophila. In The Genetics and Biology of Drosophila, vol. III (ed. Ashburner, M. and Thompson, J. N.). New York: Academic Press.Google Scholar
Davenport, C. B. (1908). Degeneration, albinism and inbreeding. Science 28, 454–455.Google Scholar
Dobzhansky, Th. & Spassky, B. (1954). Genetics of natural populations. XXII. A comparison of the concealed variability in Drosophila prosaltans with that in other species. Genetics 39, 472–487.Google Scholar
East, E. M. (1908). Inbreeding Corn. Report of the Connecticut Agricultural Experimental Station for 1907, pp. 419–428.Google Scholar
East, E. M. & Hayes, H. K. (1912). Heterozygosis in evolution in plant breeding. U.S. Department of Agriculture, Bureau of Plant Industry Bulletin 243, 58.Google Scholar
Fristrom, J. W. & Clegg, M. T. (1988). Principles of Genetics, 2nd edn.New York: Chiron.Google Scholar
Gardner, C. O. (1963). Estimates of genetic parameters in cross-fertilizing plants and their implications in plant breeding. In Statistical Genetics and Plant Breeding (ed. Hanson, W. D. and Robinson, H. F.). Washington: National Academy of Sciences.Google Scholar
Gowen, J. W. (1952). Hybrid vigor in Drosophila, pp. 474–493. In Heterosis (ed. Gowen, J. W.). New York: HafnerGoogle Scholar
Hull, F. H. (1952). Recurrent selection and overdominance, pp. 451–473. In Heterosis (ed. Gowen, J. W.). New York: Hafner.Google Scholar
Haymer, D. S. & Hartl, D. L. (1982). The experimental assessment of fitness in Drosophila. I. Comparative measures of competitive reproductive success. Genetics 102, 455–466.Google Scholar
Jones, D. F. (1917). Dominance of linked factors as a means of accounting for heterosis. Genetics 2, 466–479.Google Scholar
Kidwell, M. G., Kidwell, J. F. & Sved, J. A. (1977). Hybrid dysgenesis in Drosophila melanogaster: a syndrome of aberrant traits including mutations, sterility and male recombination. Genetics 86, 813–833.CrossRefGoogle ScholarPubMed
Kimura, M. (1983). The Neutral Theory of Molecular Evolution. Cambridge University Press.Google Scholar
Kreitman, M. (1983). Nucleotide polymorphism at the alcohol dehydrogenase locus of Drosophila melanogaster. Nature 304, 412–417.Google Scholar
Lewontin, R. C. (1974). The Genetic Basis of Evolutionary Change. New York: Columbia University Press.Google Scholar
Pascoe, L. (1985). Fitness components of chromosomal homozygotes in Drosophila melanogaster in age-structured populations. PhD Thesis, The University of Sydney.Google Scholar
Prout, T. (1965). The evolution of fitnesses from genotypic frequencies. Evolution 19, 546–551.Google Scholar
Schull, G. H. (1908). The composition of a field of maize. Report of the American Breeders Association 5, 51–59.Google Scholar
Schull, G. H. (1911). The genotypes of maize. American Naturalist 45, 234–252.Google Scholar
Simmons, M. J. & Crow, J. F. (1977). Mutations affecting fitness in Drosophila populations. Annual Review of Genetics 12, 289–328.Google Scholar
Sperlich, D. & Karlik, A. (1970). The genetic conditions in heterozygous and homozygous populations of Drosophila. I. The fate of alien chromosomes. Genetica 41, 265–304.Google Scholar
Sprague, G. F., Russell, W. A. & Penny, L. H. (1959). Further studies on convergent evolution in corn. Genetics 44, 341–346.Google Scholar
Sved, J. A. (1971). An estimate of heterosis in Drosophila melanogaster. Genetical Research 18, 97–105.Google Scholar
Sved, J. A. & Ayala, F. J. (1970). A population cage test for heterosis in Drosophila pseudoobscura. Genetics 66, 97–113.Google Scholar
Sved, J. A. & Wilton, A. N. (1989). Inbreeding depression and the maintenance of deleterious genes by mutation: model of a Drosophila chromosome. Genetical Research 53, 119–128.Google Scholar
Wilton, A. N. (1980). Studies of the nature of chromosomal heterosis in Drosophila melanogaster. PhD Thesis, University of Sydney.Google Scholar
Yamazaki, T. & Maruyama, T. (1971). Evidence for the neutral hypothesis of protein polymorphism. Science 178, 56–58.Google Scholar