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. 2004 Jul;167(3):1475–1492. doi: 10.1534/genetics.103.025874

Redistribution of gene frequency and changes of genetic variation following a bottleneck in population size.

Xu-Sheng Zhang 1, Jinliang Wang 1, William G Hill 1
PMCID: PMC1470934  PMID: 15280256

Abstract

Although the distribution of frequencies of genes influencing quantitative traits is important to our understanding of their genetic basis and their evolution, direct information from laboratory experiments is very limited. In theory, different models of selection and mutation generate different predictions of frequency distributions. When a large population at mutation-selection balance passes through a rapid bottleneck in size, the frequency distribution of genes is dramatically altered, causing changes in observable quantities such as the mean and variance of quantitative traits. We investigate the gene frequency distribution of a population at mutation-selection balance under a joint-effect model of real stabilizing and pleiotropic selection and its redistribution and thus changes of the genetic properties of metric and fitness traits after the population passes a rapid bottleneck and expands in size. If all genes that affect the trait are neutral with respect to fitness, the additive genetic variance (VA) is always reduced by a bottleneck in population size, regardless of their degree of dominance. For genes that have been under selection, VA increases following a bottleneck if they are (partially) recessive, while the dominance variance increases substantially for any degree of dominance. With typical estimates of mutation parameters, the joint-effect model can explain data from laboratory experiments on the effect of bottlenecking on fitness and morphological traits, providing further support for it as a plausible mechanism for maintenance of quantitative genetic variation.

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Selected References

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  1. Avery P. J., Hill W. G. Variability in genetic parameters among small populations. Genet Res. 1977 Jun;29(3):193–213. doi: 10.1017/s0016672300017286. [DOI] [PubMed] [Google Scholar]
  2. Avery P. J., Hill W. G. Variance in quantitative traits due to linked dominant genes and variance in heterozygosity in small populations. Genetics. 1979 Apr;91(4):817–844. doi: 10.1093/genetics/91.4.817. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Barton N. H., Keightley P. D. Understanding quantitative genetic variation. Nat Rev Genet. 2002 Jan;3(1):11–21. doi: 10.1038/nrg700. [DOI] [PubMed] [Google Scholar]
  4. Barton N. H. Pleiotropic models of quantitative variation. Genetics. 1990 Mar;124(3):773–782. doi: 10.1093/genetics/124.3.773. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Barton N. H., Turelli M. Evolutionary quantitative genetics: how little do we know? Annu Rev Genet. 1989;23:337–370. doi: 10.1146/annurev.ge.23.120189.002005. [DOI] [PubMed] [Google Scholar]
  6. Bryant E. H., McCommas S. A., Combs L. M. The Effect of an Experimental Bottleneck upon Quantitative Genetic Variation in the Housefly. Genetics. 1986 Dec;114(4):1191–1211. doi: 10.1093/genetics/114.4.1191. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Caballero A., Keightley P. D. A pleiotropic nonadditive model of variation in quantitative traits. Genetics. 1994 Nov;138(3):883–900. doi: 10.1093/genetics/138.3.883. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Charlesworth B., Charlesworth D. The genetic basis of inbreeding depression. Genet Res. 1999 Dec;74(3):329–340. doi: 10.1017/s0016672399004152. [DOI] [PubMed] [Google Scholar]
  9. Davies E. K., Peters A. D., Keightley P. D. High frequency of cryptic deleterious mutations in Caenorhabditis elegans. Science. 1999 Sep 10;285(5434):1748–1751. doi: 10.1126/science.285.5434.1748. [DOI] [PubMed] [Google Scholar]
  10. Deng Hong-Wen, Gao Guimin, Li Jin-Long. Estimation of deleterious genomic mutation parameters in natural populations by accounting for variable mutation effects across loci. Genetics. 2002 Nov;162(3):1487–1500. doi: 10.1093/genetics/162.3.1487. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Gavrilets S., de Jong G. Pleiotropic models of polygenic variation, stabilizing selection, and epistasis. Genetics. 1993 Jun;134(2):609–625. doi: 10.1093/genetics/134.2.609. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Hill W. G., Weir B. S. Variances and covariances of squared linkage disequilibria in finite populations. Theor Popul Biol. 1988 Feb;33(1):54–78. doi: 10.1016/0040-5809(88)90004-4. [DOI] [PubMed] [Google Scholar]
  13. Keightley P. D., Eyre-Walker A. Terumi Mukai and the riddle of deleterious mutation rates. Genetics. 1999 Oct;153(2):515–523. doi: 10.1093/genetics/153.2.515. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Kimura M. The number of heterozygous nucleotide sites maintained in a finite population due to steady flux of mutations. Genetics. 1969 Apr;61(4):893–903. doi: 10.1093/genetics/61.4.893. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Kirkpatrick M, Jarne P. The Effects of a Bottleneck on Inbreeding Depression and the Genetic Load. Am Nat. 2000 Feb;155(2):154–167. doi: 10.1086/303312. [DOI] [PubMed] [Google Scholar]
  16. Lyman R. F., Lawrence F., Nuzhdin S. V., Mackay T. F. Effects of single P-element insertions on bristle number and viability in Drosophila melanogaster. Genetics. 1996 May;143(1):277–292. doi: 10.1093/genetics/143.1.277. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. López-Fanjul Carlos, Fernández Almudena, Toro Miguel A. The effect of epistasis on the excess of the additive and nonadditive variances after population bottlenecks. Evolution. 2002 May;56(5):865–876. doi: 10.1111/j.0014-3820.2002.tb01400.x. [DOI] [PubMed] [Google Scholar]
  18. López-Fanjul Carlos, Fernández Almudena, Toro Miguel A. The effect of neutral nonadditive gene action on the quantitative index of population divergence. Genetics. 2003 Aug;164(4):1627–1633. doi: 10.1093/genetics/164.4.1627. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Meffert L. M. Bottleneck effects on genetic variance for courtship repertoire. Genetics. 1995 Jan;139(1):365–374. doi: 10.1093/genetics/139.1.365. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Naciri-Graven Yamama, Goudet Jérôme. The additive genetic variance after bottlenecks is affected by the number of loci involved in epistatic interactions. Evolution. 2003 Apr;57(4):706–716. doi: 10.1111/j.0014-3820.2003.tb00284.x. [DOI] [PubMed] [Google Scholar]
  21. Ohta T., Tachida H. Theoretical study of near neutrality. I. Heterozygosity and rate of mutant substitution. Genetics. 1990 Sep;126(1):219–229. doi: 10.1093/genetics/126.1.219. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Otto S. P., Jones C. D. Detecting the undetected: estimating the total number of loci underlying a quantitative trait. Genetics. 2000 Dec;156(4):2093–2107. doi: 10.1093/genetics/156.4.2093. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Paterson A. H., DeVerna J. W., Lanini B., Tanksley S. D. Fine mapping of quantitative trait loci using selected overlapping recombinant chromosomes, in an interspecies cross of tomato. Genetics. 1990 Mar;124(3):735–742. doi: 10.1093/genetics/124.3.735. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Robertson A. The Effect of Inbreeding on the Variation Due to Recessive Genes. Genetics. 1952 Mar;37(2):189–207. doi: 10.1093/genetics/37.2.189. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Roff Derek A. Inbreeding depression: tests of the overdominance and partial dominance hypotheses. Evolution. 2002 Apr;56(4):768–775. doi: 10.1111/j.0014-3820.2002.tb01387.x. [DOI] [PubMed] [Google Scholar]
  26. Saccheri I. J., Nichols R. A., Brakefield P. M. Effects of bottlenecks on quantitative genetic variation in the butterfly Bicyclus anynana. Genet Res. 2001 Apr;77(2):167–181. doi: 10.1017/s0016672301004906. [DOI] [PubMed] [Google Scholar]
  27. Turelli M. Effects of pleiotropy on predictions concerning mutation-selection balance for polygenic traits. Genetics. 1985 Sep;111(1):165–195. doi: 10.1093/genetics/111.1.165. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Wang J., Caballero A., Keightley P. D., Hill W. G. Bottleneck effect on genetic variance. A theoretical investigation of the role of dominance. Genetics. 1998 Sep;150(1):435–447. doi: 10.1093/genetics/150.1.435. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Whitlock M. C., Fowler K. The changes in genetic and environmental variance with inbreeding in Drosophila melanogaster. Genetics. 1999 May;152(1):345–353. doi: 10.1093/genetics/152.1.345. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Wloch D. M., Szafraniec K., Borts R. H., Korona R. Direct estimate of the mutation rate and the distribution of fitness effects in the yeast Saccharomyces cerevisiae. Genetics. 2001 Oct;159(2):441–452. doi: 10.1093/genetics/159.2.441. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Zhang Xu-Sheng, Wang Jinliang, Hill William G. Influence of dominance, leptokurtosis and pleiotropy of deleterious mutations on quantitative genetic variation at mutation-selection balance. Genetics. 2004 Jan;166(1):597–610. doi: 10.1534/genetics.166.1.597. [DOI] [PMC free article] [PubMed] [Google Scholar]

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