Genetics, Vol 143, 1467-1483, Copyright © 1996

INVESTIGATIONS

Comparing Mutational Variabilities

D. Houle, B. Morikawa and M. Lynch
Department of Zoology, University of Toronto, Toronto, Ontario M5S 3G5, Canada

We have reviewed the available data on V(M), the amount of genetic variation in phenotypic traits produced each generation by mutation. We use these data to make several qualitative tests of the mutation-selection balance hypothesis for the maintenance of genetic variance (MSB). To compare V(M) values, we use three dimensionless quantities: mutational heritability, V(M)/V(E); the mutational coefficient of variation, CV(M); and the ratio of the standing genetic variance to V(M), V(G)/V(M). Since genetic coefficients of variation for life history traits are larger than those for morphological traits, we predict that under MSB, life history traits should also have larger CV(M). This is confirmed; life history traits have a median CV(M) value more than six times higher than that for morphological traits. V(G)/V(M) approximates the persistence time of mutations under MSB in an infinite population. In order for MSB to hold, V(G)/V(M) must be small, substantially less than 1000, and life history traits should have smaller values than morphological traits. V(G)/V(M) averages about 50 generations for life history traits and 100 generations for morphological traits. These observations are all consistent with the predictions of a mutation-selection balance model.

This article has been cited by other articles:

				H. Vehvilainen, A. Kause, C. Quinton, H. Koskinen, and T. Paananen Survival of the Currently Fittest: Genetics of Rainbow Trout Survival Across Time and Space Genetics, September 1, 2008; 180(1): 507 - 516. [Abstract] [Full Text] [PDF]

				J. Casellas and J. F. Medrano Within-Generation Mutation Variance for Litter Size in Inbred Mice Genetics, August 1, 2008; 179(4): 2147 - 2155. [Abstract] [Full Text] [PDF]

				X.-S. Zhang and W. G. Hill The Anomalous Effects of Biased Mutation Revisited: Mean-Optimum Deviation and Apparent Directional Selection Under Stabilizing Selection Genetics, June 1, 2008; 179(2): 1135 - 1141. [Abstract] [Full Text] [PDF]

				T. D. Weaver, C. C. Roseman, and C. B. Stringer Close correspondence between quantitative- and molecular-genetic divergence times for Neandertals and modern humans PNAS, March 25, 2008; 105(12): 4645 - 4649. [Abstract] [Full Text] [PDF]

				D. Ostrow, N. Phillips, A. Avalos, D. Blanton, A. Boggs, T. Keller, L. Levy, J. Rosenbloom, and C. F. Baer Mutational Bias for Body Size in Rhabditid Nematodes Genetics, July 1, 2007; 176(3): 1653 - 1661. [Abstract] [Full Text] [PDF]

				C. F. Baer, N. Phillips, D. Ostrow, A. Avalos, D. Blanton, A. Boggs, T. Keller, L. Levy, and E. Mezerhane Cumulative Effects of Spontaneous Mutations for Fitness in Caenorhabditis: Role of Genotype, Environment and Stress Genetics, November 1, 2006; 174(3): 1387 - 1395. [Abstract] [Full Text] [PDF]

				R. H. Wilson, T. J. Morgan, and T. F. C. Mackay High-Resolution Mapping of Quantitative Trait Loci Affecting Increased Life Span in Drosophila melanogaster Genetics, July 1, 2006; 173(3): 1455 - 1463. [Abstract] [Full Text] [PDF]

				L. Y. Yampolsky, C. Allen, S. A. Shabalina, and A. S. Kondrashov Persistence Time of Loss-of-Function Mutations at Nonessential Loci Affecting Eye Color in Drosophila melanogaster Genetics, December 1, 2005; 171(4): 2133 - 2138. [Abstract] [Full Text] [PDF]

				T. F. C. Mackay, R. F. Lyman, and F. Lawrence Polygenic Mutation in Drosophila melanogaster: Mapping Spontaneous Mutations Affecting Sensory Bristle Number Genetics, August 1, 2005; 170(4): 1723 - 1735. [Abstract] [Full Text] [PDF]

				R. C. Fuller, C. F. Baer, and J. Travis How and When Selection Experiments Might Actually be Useful Integr. Comp. Biol., June 1, 2005; 45(3): 391 - 404. [Abstract] [Full Text] [PDF]

				S. Estes, B. C. Ajie, M. Lynch, and P. C. Phillips Spontaneous Mutational Correlations for Life-History, Morphological and Behavioral Characters in Caenorhabditis elegans Genetics, June 1, 2005; 170(2): 645 - 653. [Abstract] [Full Text] [PDF]

				B. C. Ajie, S. Estes, M. Lynch, and P. C. Phillips Behavioral Degradation Under Mutation Accumulation in Caenorhabditis elegans Genetics, June 1, 2005; 170(2): 655 - 660. [Abstract] [Full Text] [PDF]

				C. F. Baer, F. Shaw, C. Steding, M. Baumgartner, A. Hawkins, A. Houppert, N. Mason, M. Reed, K. Simonelic, W. Woodard, et al. Comparative evolutionary genetics of spontaneous mutations affecting fitness in rhabditid nematodes PNAS, April 19, 2005; 102(16): 5785 - 5790. [Abstract] [Full Text] [PDF]

				J. Xu Genotype-Environment Interactions of Spontaneous Mutations for Vegetative Fitness in the Human Pathogenic Fungus Cryptococcus neoformans Genetics, November 1, 2004; 168(3): 1177 - 1188. [Abstract] [Full Text] [PDF]

				M. L. Wayne, Y.-J. Pan, S. V. Nuzhdin, and L. M. McIntyre Additivity and trans-acting Effects on Gene Expression in Male Drosophila simulans Genetics, November 1, 2004; 168(3): 1413 - 1420. [Abstract] [Full Text] [PDF]

				S. Estes, P. C. Phillips, D. R. Denver, W. K. Thomas, and M. Lynch Mutation Accumulation in Populations of Varying Size: The Distribution of Mutational Effects for Fitness Correlates in Caenorhabditis elegans Genetics, March 1, 2004; 166(3): 1269 - 1279. [Abstract] [Full Text] [PDF]

				X.-S. Zhang, J. Wang, and W. G. Hill Influence of Dominance, Leptokurtosis and Pleiotropy of Deleterious Mutations on Quantitative Genetic Variation at Mutation-Selection Balance Genetics, January 1, 2004; 166(1): 597 - 610. [Abstract] [Full Text] [PDF]

				C. Weinig, L. A. Dorn, N. C. Kane, Z. M. German, S. S. Halldorsdottir, M. C. Ungerer, Y. Toyonaga, T. F. C. Mackay, M. D. Purugganan, and J. Schmitt Heterogeneous Selection at Specific Loci in Natural Environments in Arabidopsis thaliana Genetics, September 1, 2003; 165(1): 321 - 329. [Abstract] [Full Text] [PDF]

				J. K. Kelly Deleterious Mutations and the Genetic Variance of Male Fitness Components in Mimulus guttatus Genetics, July 1, 2003; 164(3): 1071 - 1085. [Abstract] [Full Text] [PDF]

				J. Slate, P. M. Visscher, S. MacGregor, D. Stevens, M. L. Tate, and J. M. Pemberton A Genome Scan for Quantitative Trait Loci in a Wild Population of Red Deer (Cervus elaphus) Genetics, December 1, 2002; 162(4): 1863 - 1873. [Abstract] [Full Text] [PDF]

				H.-W. Deng, G. Gao, and J.-L. Li Estimation of Deleterious Genomic Mutation Parameters in Natural Populations by Accounting for Variable Mutation Effects Across Loci Genetics, November 1, 2002; 162(3): 1487 - 1500. [Abstract] [Full Text] [PDF]

				R. B. R. Azevedo, P. D. Keightley, C. Lauren-Maatta, L. L. Vassilieva, M. Lynch, and A. M. Leroi Spontaneous Mutational Variation for Body Size in Caenorhabditis elegans Genetics, October 1, 2002; 162(2): 755 - 765. [Abstract] [Full Text] [PDF]

				X.-S. Zhang and W. G. Hill Joint Effects of Pleiotropic Selection and Stabilizing Selection on the Maintenance of Quantitative Genetic Variation at Mutation-Selection Balance Genetics, September 1, 2002; 162(1): 459 - 471. [Abstract] [Full Text] [PDF]

				J. J. Welch and D. Waxman Nonequivalent Loci and the Distribution of Mutant Effects Genetics, June 1, 2002; 161(2): 897 - 904. [Abstract] [Full Text] [PDF]

				X.-S. Zhang, J. Wang, and W. G. Hill Pleiotropic Model of Maintenance of Quantitative Genetic Variation at Mutation-Selection Balance Genetics, May 1, 2002; 161(1): 419 - 433. [Abstract] [Full Text] [PDF]

				H.-P. Yang, A. Y. Tanikawa, W. A. Van Voorhies, J. C. Silva, and A. S. Kondrashov Whole-Genome Effects of Ethyl Methanesulfonate-Induced Mutation on Nine Quantitative Traits in Outbred Drosophila melanogaster Genetics, March 1, 2001; 157(3): 1257 - 1265. [Abstract] [Full Text]

				A. García-Dorado and A. Caballero On the Average Coefficient of Dominance of Deleterious Spontaneous Mutations Genetics, August 1, 2000; 155(4): 1991 - 2001. [Abstract] [Full Text]

				R. G. Shaw, D. L. Byers, and E. Darmo Spontaneous Mutational Effects on Reproductive Traits of Arabidopsis thaliana Genetics, May 1, 2000; 155(1): 369 - 378. [Abstract] [Full Text]

				J. Li and H.-W. Deng Estimation of Parameters of Deleterious Mutations in Partial Selfing or Partial Outcrossing Populations and in Nonequilibrium Populations Genetics, April 1, 2000; 154(4): 1893 - 1906. [Abstract] [Full Text]

				C. Vieira, E. G. Pasyukova, Z.-B. Zeng, J. B. Hackett, R. F. Lyman, and T. F. C. Mackay Genotype-Environment Interaction for Quantitative Trait Loci Affecting Life Span in Drosophila melanogaster Genetics, January 1, 2000; 154(1): 213 - 227. [Abstract] [Full Text]

				S. D. Pletcher, D. Houle, and J. W. Curtsinger The Evolution of Age-Specific Mortality Rates in Drosophila melanogaster: Genetic Divergence Among Unselected Lines Genetics, October 1, 1999; 153(2): 813 - 823. [Abstract] [Full Text] [PDF]

				G. Gibson, M. Wemple, and S. van Helden Potential Variance Affecting Homeotic Ultrabithorax and Antennapedia Phenotypes in Drosophila melanogaster Genetics, March 1, 1999; 151(3): 1081 - 1091. [Abstract] [Full Text]

				J.-L. Li, J. Li, and H.-W. Deng The Effect of Overdominance on Characterizing Deleterious Mutations in Large Natural Populations Genetics, February 1, 1999; 151(2): 895 - 913. [Abstract] [Full Text]

				L. L. Vassilieva and M. Lynch The Rate of Spontaneous Mutation for Life-History Traits in Caenorhabditis elegans Genetics, January 1, 1999; 151(1): 119 - 129. [Abstract] [Full Text]

				H.-W. Deng Characterization of Deleterious Mutations in Outcrossing Populations Genetics, October 1, 1998; 150(2): 945 - 956. [Abstract] [Full Text]

				M. C. Gurganus, J. D. Fry, S. V. Nuzhdin, E. G. Pasyukova, R. F. Lyman, and T. F. C. Mackay Genotype-Environment Interaction at Quantitative Trait Loci Affecting Sensory Bristle Number in Drosophila melanogaster Genetics, August 1, 1998; 149(4): 1883 - 1898. [Abstract] [Full Text] [PDF]

				E. Santiago and A. Caballero Effective Size and Polymorphism of Linked Neutral Loci in Populations Under Directional Selection Genetics, August 1, 1998; 149(4): 2105 - 2117. [Abstract] [Full Text] [PDF]

				T. Mitchell-Olds and D. Pedersen The Molecular Basis of Quantitative Genetic Variation in Central and Secondary Metabolism in Arabidopsis Genetics, June 1, 1998; 149(2): 739 - 747. [Abstract] [Full Text] [PDF]

				R. F. Lyman and T. F. C. Mackay Candidate Quantitative Trait Loci and Naturally Occurring Phenotypic Variation for Bristle Number in Drosophila melanogaster: The Delta-Hairless Gene Region Genetics, June 1, 1998; 149(2): 983 - 998. [Abstract] [Full Text] [PDF]

				P. D. Keightley Genetic Basis of Response to 50 Generations of Selection on Body Weight in Inbred Mice Genetics, April 1, 1998; 148(4): 1931 - 1939. [Abstract] [Full Text] [PDF]

				J. D. Fry, S. L. Heinsohn, and T. F. C. Mackay Heterosis for Viability, Fecundity, and Male Fertility in Drosophila melanogaster : Comparison of Mutational and Standing Variation Genetics, March 1, 1998; 148(3): 1171 - 1188. [Abstract] [Full Text] [PDF]

				P. D. Keightley and O. Ohnishi EMS-Induced Polygenic Mutation Rates for Nine Quantitative Characters in Drosophila melanogaster Genetics, February 1, 1998; 148(2): 753 - 766. [Abstract] [Full Text] [PDF]

				Quantitative Genetics of Ovariole Number in Drosophila melanogaster. II. Mutational Variation and Genotype-Environment Interaction Genetics, January 1, 1998; 148(1): 201 - 210.

				Age-Specific Properties of Spontaneous Mutations Affecting Mortality in Drosophila melanogaster Genetics, January 1, 1998; 148(1): 287 - 304.

				S. A. Shabalina, L. Yu. Yampolsky, and A. S. Kondrashov Rapid decline of fitness in panmictic populations of Drosophila melanogaster maintained under relaxed natural selection PNAS, November 25, 1997; 94(24): 13034 - 13039. [Abstract] [Full Text] [PDF]

				J. F. Crow The high spontaneous mutation rate: Is it a health risk? PNAS, August 5, 1997; 94(16): 8380 - 8386. [Abstract] [Full Text] [PDF]

				P. D. Keightley and A. Caballero Genomic mutation rates for lifetime reproductive output and lifespan in Caenorhabditis elegans PNAS, April 15, 1997; 94(8): 3823 - 3827. [Abstract] [Full Text] [PDF]