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Recombination load associated with selection for increased recombination

Published online by Cambridge University Press:  14 April 2009

B. Charlesworth  and
N. H. Barton
B. Charlesworth*
Affiliation:
Department of Ecology and Evolution, The University of Chicago, 1101 E. 57th St., Chicago, IL 60637-1573, U.S.A.
N. H. Barton
Affiliation:
Institute of Cell, Animal and Population Biology, University of Edinburgh, King's Buildings, West Mains Road, Edinburgh EH9 3JT, UK
*
* B. Charlesworth, Department of Ecology and Evolution, The University of Chicago, 1101 E. 57th St., Chicago, IL 60637-1573, U.S.A. Phone: 312-702-8942; Fax: 312- 702-9740; E-mail: [email protected].
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Summary

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Experiments on Drosophila suggest that genetic recombination may result in lowered fitness of progeny (a ‘recombination load’). This has been interpreted as evidence either for a direct effect of recombination on fitness, or for the maintenance of linkage disequilibria by epistatic selection. Here we show that such a recombination load is to be expected even if selection favours increased genetic recombination. This is because of the fact that, although a modifier may suffer an immediate loss of fitness if it increases recombination, it eventually becomes associated with a higher additive genetic variance in fitness, which allows a faster response to directionselection. This argument applies to mutation-selection balance with synergistic epistasis, directional selection on quantitative traits, and ectopic exchange among transposable elements. Further experiments are needed to determine whether the selection against recombination due to trie immediate load is outweighed by the increased additive variance in fitness produced by recombination.

Type
Research Article
Information
Genetics Research , Volume 67 , Issue 1 , February 1996 , pp. 27 - 41
Copyright
Copyright © Cambridge University Press 1996

References

Altenberg, L., & Feldman, M. W., (1987). Selection, generalized transmission and the evolution of modifier genes. I. The reduction principle. Genetics 117, 559–572.CrossRefGoogle ScholarPubMed
Baker, B. S., Carpenter, A. T. C., Esposito, M. S., Esposito, R. E., & Sandier, L., (1976). The genetic control of meiosis. Annual Review of Genetics 10, 53–134.CrossRefGoogle ScholarPubMed
Barton, N. H., (1995). A general theory for the evolution of recombination. Genetical Research 65, 123–144.CrossRefGoogle Scholar
Barton, N. H., & Turelli, M., (1991). Natural and sexual selection on many loci. Genetics 127, 229–255.CrossRefGoogle ScholarPubMed
Begun, D. J., & Aquadro, C. F., (1992). Levels of naturally occurring DNA polymorphism correlate with recombination rate in Drosophila melanogaster. Nature 356, 519–520.CrossRefGoogle Scholar
Berg, P., & Howe, M. M., (1989). Mobile DNA. Washington D.C.: American Society for Microbiology.Google Scholar
Bernstein, H., Hopf, F. A., & Michod, R. E., (1988). Is meiotic recombination an adaptation for repairing DNA, producing genetic variation, or both? In The Evolution of Sex (ed. Michod, R. E. and Levin, B. R.), pp. 139–160. Sunderland, Massachusetts: Sinauer Press.Google Scholar
Brooks, L. D., (1988). The evolution of recombination rates. In The Evolution of Sex (ed. Michod, R. E. and Levin, B. R.), pp. 87–105. Sunderland, Massachusetts: Sinauer Press.Google Scholar
Bulmer, M. G., (1985). The Mathematical Theory of Quantitative Genetics. Oxford: Oxford University Press.Google Scholar
Charlesworth, B., (1976). Recombination modification in a fluctuating environment. Genetics 83, 181–195.CrossRefGoogle Scholar
Charlesworth, B., (1985). The population genetics of transposable elements. In Population Genetics and Molecular Evolution (ed. Ohta, T. and Aoki, K.), pp. 213–232. Berlin: Springer-Verlag.Google Scholar
Charlesworth, B., (1987). The heritability of fitness. In Sexual Selection: Testing the Alternatives (ed. Bradbury, J. W. and Andersson, M. B.), pp. 21–40. Chichester: John Wiley.Google Scholar
Charlesworth, B., (1989). The evolution of sex and recombination. Trends in Ecology & Evolution 4, 264–267.CrossRefGoogle ScholarPubMed
Charlesworth, B., (1990). Mutation-selection balance and the evolutionary advantage of sex and recombination. Genetical Research 55, 199–221.CrossRefGoogle ScholarPubMed
Charlesworth, B., (1993). Directional selection and the evolution of sex and recombination. Genetical Research 61, 205–224.CrossRefGoogle ScholarPubMed
Charlesworth, B., & Charlesworth, D., (1975). An experiment on recombination load in Drosophila melanogaster. Genetical Research 25, 267–274.CrossRefGoogle Scholar
Charlesworth, B., & Langley, C. H., (1989). The population genetics of Drosophila transposable elements. Annual Reviews of Genetics 23, 251–287.CrossRefGoogle ScholarPubMed
Charlesworth, B., Lapid, A., & Canada, D., (1992). The distribution of transposable elements within and between chromosomes in a population of Drosophila melanogaster. II. Inferences on the nature of selection against elements. Genetical Research 60, 115–130.CrossRefGoogle Scholar
Coyne, J. A., Meyers, W., Crittenden, A. P., & Sniegowski, P., (1993). The fertility effects of pericentric inversions in Drosophila melanogaster. Genetics 134, 487–496.CrossRefGoogle ScholarPubMed
Crow, J. F., (1970). Genetic loads and the cost of natural selection. In Mathematical Topics in Population Genetics (ed. Kojima, K. I.), pp. 128–177. Berlin: Springer Verlag.CrossRefGoogle Scholar
Davis, P. S., Shen, M. W., & Judd, B. H., (1987). Asymmetrical pairing of transposons in and proximal to the white locus of Drosophila accounts for four classes of regularly occurring exchange products. Proceedings of the National Academy of Science U.S.A. 84, 174–178.CrossRefGoogle Scholar
Dobzhansky, T., Levene, H., Spassky, B., & Spassky, N., (1959). Release of genetic variability through recombination. III. Drosophila prosaltans. Genetics 44, 75–92.CrossRefGoogle ScholarPubMed
Eanes, W. F., Wesley, C., & Charlesworth, B., (1992). Accumulation of P elements in minority inversions in natural populations of Drosophila melanogaster. Genetical Research 59, 1–9.CrossRefGoogle ScholarPubMed
Falconer, D. S., (1985). A note on Fisher's ‘average effect’ and ‘average excess’. Genetical Research 46, 337–348.CrossRefGoogle ScholarPubMed
Feldman, M. W., Christiansen, F. B., & Brooks, L. D., (1980). Evolution of recombination in a constant environment. Proceedings of the National Academy of Sciences U.S.A. 77, 4838–4841.CrossRefGoogle Scholar
Felsenstein, J., (1974). The evolutionary advantage of recombination. Genetics 78, 737–756.CrossRefGoogle ScholarPubMed
Fisher, R. A., (1930). The Genetical Theory of Natural Selection. Oxford: Oxford University Press.CrossRefGoogle Scholar
Hamilton, W. D., (1980). Sex vs non-sex vs parasite. Oikos 35, 282–290.CrossRefGoogle Scholar
Hamilton, W. D., (1993). Haploid dynamic polymorphism in a host with matching parasites: effects of mutation/subdivision, linkage and patterns of selection. Journal of Heredity 84, 328–338.CrossRefGoogle Scholar
Houle, D., (1992). Comparing evolvability and variability of quantitative traits. Genetics 130, 195–204.CrossRefGoogle ScholarPubMed
Keightley, P. D., (1994). The distribution of mutation effects on viability in Drosophila. Genetics 138, 1315–1322.CrossRefGoogle ScholarPubMed
Kimura, M., & Maruyama, T., (1966). Mutational load with epistatic gene interactions in fitness. Genetics 54, 1337–1351.CrossRefGoogle ScholarPubMed
Kondrashov, A. S., (1984). Deleterious mutations as an evolutionary factor. I. The advantage of recombination. Genetical Research 44, 199–218.CrossRefGoogle Scholar
Kondrashov, A. S., (1995). Dynamics of unconditionally deleterious mutations: Gaussian approximation and soft selection. Genetical Research 65, 113–122.CrossRefGoogle ScholarPubMed
Langley, C. H., Montgomery, E., Hudson, R., Kaplan, N., & Charlesworth, B., (1988). On the role of unequal exchange in the containment of transposable element copy number. Genetical Research 52, 223–235.CrossRefGoogle ScholarPubMed
Levene, H., (1959). Release of genetic variability through recombination. IV. Statistical theory. Genetics 44, 93–104.CrossRefGoogle ScholarPubMed
Smith, J. Maynard, (1978). The Evolution of Sex. Cambridge: Cambridge University Press.Google Scholar
Smith, J. Maynard, (1980). Selection for recombination in a polygenic model. Genetical Research 33, 121–128.CrossRefGoogle Scholar
Smith, J. Maynard, (1988). Selection for recombination in a polygenic model: the mechanism. Genetical Research 51, 59–63.CrossRefGoogle Scholar
Montgomery, E. A., Huang, S. M., Langley, C. H., & Judd, B. H., (1991). Chromosome rearrangement by ectopic recombination in Drosophila melanogaster: genome structure and evolution. Genetics 129, 1085–1098.CrossRefGoogle ScholarPubMed
Mukai, T., (1969). The genetic structure of natural populations of D. melanogaster. VIII. Synergistic interactions of spontaneous mutant polygenes controlling viability. Genetics 61, 149–161.CrossRefGoogle Scholar
Mukai, T., & Yamaguchi, O., (1974). The genetic structure of natural populations of D. melanogaster. XI. Genetic variability in a local population. Genetics 76, 339–366.CrossRefGoogle Scholar
Nee, S., (1989). Antagonistic coevolution and the evolution of genotypic randomisation. Journal of Theoretical Biology 140, 499–518.CrossRefGoogle Scholar
Nuzhdin, S. V., & Mackay, T. F. C., (1995). The genomic rate of transposable element movement in Drosophila melanogaster. Molecular Biology and Evolution 12, 180–181.CrossRefGoogle ScholarPubMed
Radman, M., & Wagner, M., (1993). Mismatch recognition in chromosomal interactions and speciation. Chromosoma 102, 369–373.CrossRefGoogle ScholarPubMed
Shnol, E. E., & Kondrashov, A. S., (1993). The effect of selection on the phenotypic variance. Genetics 134, 995–996.CrossRefGoogle ScholarPubMed
Sniegowski, P. D., & Charlesworth, B., (1994). Transposable element numbers in cosmopolitan inversions from a natural population of Drosophila melanogaster. Genetics 137, 815–827.CrossRefGoogle ScholarPubMed
Spassky, B., Spassky, N., Levene, H., & Dobzhansky, T., (1958). Release of genetic variability through recombination. I. Drosophila pseudoobscura. Genetics 43, 844–865.CrossRefGoogle ScholarPubMed
Spiess, E. B. (1958 a). The effect of genetic recombination on viability in Drosophila. Cold Spring Harbor Symposium on Quantitative Biology 23, 239–250.CrossRefGoogle ScholarPubMed
Spiess, E. B. (1958 b). Release of genetic variability through recombination. II. Drosophila persimilis. Genetics 44, 43–58.CrossRefGoogle Scholar
Tucic, N., Ayala, F. J., & Marinkovic, D., (1981). Correlation between recombination frequency and fitness in Drosophila melanogaster. Genetica 56, 61–69.CrossRefGoogle Scholar
Turelli, M., (1984). Lerch's zeta meets the abdominal bristle. Theoretical Population Biology 25, 138–193.CrossRefGoogle Scholar
Turner, J. R. G., (1967). Why does the genotype not congeal? Evolution 21, 645–656.CrossRefGoogle Scholar
Wasserman, M., (1972). Factors influencing fitness in chromosomal strains in Drosophila subobscura. Genetics 72, 691–708.CrossRefGoogle ScholarPubMed
Woodruff, R. C., Slatko, B. E., & Thompson, J. R., (1983). Factors affecting mutation rate in natural populations. In The Genetics and Biology of Drosophila, Vol. 3c (ed. Ashburner, M., Carson, H. L. and Thompson, J. N.), pp. 37–124. London: Academic Press.Google Scholar
Zhivotovsky, L. A., Feldman, M. W., & Christiansen, F. B., (1994). Evolution of recombination among multiple selected loci: a generalized reduction principle. Proceedings of the National Academy of Sciences U.S.A. 91, 1079–1083.CrossRefGoogle ScholarPubMed