Mutation load: The fitness of individuals in populations where deleterious alleles are abundant

Annual Review of Ecology, Evolution, and Systematics

Volumn 43, Issue , 2012, Pages 115-135

  Agrawal, Aneil F ^a   Whitlock, Michael C ^b  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

evolutionary theory; genetic load; population ecology

Indexed keywords

ALLELE; EPISTASIS; EUKARYOTE; EVOLUTIONARY THEORY; EXTINCTION; FITNESS; INBREEDING; INTERSPECIFIC COMPETITION; MUTATION; NATURAL SELECTION; POPULATION ECOLOGY;

EID: 84876823246     PISSN: 1543592X     EISSN: 15452069     Source Type: Book Series    
DOI: 10.1146/annurev-ecolsys-110411-160257     Document Type: Review

References (142)

1. 1000 Genomes Project Consortium. 2010. Amap of human genome variation from population-scale sequencing. Nature 467:1061-73
2. Abrams PA. 2003. Effects of altered resource consumption rates by one consumer species on a competitor. Ecol. Lett. 6:550-55
3. Abrams PA, Brassil CE, Holt RD. 2003. Dynamics and responses to mortality rates of competing predators undergoing predator-prey cycles. Theor. Popul. Biol. 64:163-76
4. Agrawal AF. 2001. Sexual selection and the maintenance of sexual reproduction. Nature 411:692-95
5. Agrawal AF. 2002. Genetic loads under fitness-dependent mutation rates. J. Evol. Biol. 15:1004-10
6. Agrawal AF. 2010. Ecological determinants of mutation load and inbreeding depression in subdivided populations. Am. Nat. 176:111-22
7. Agrawal AF, Chasnov JR. 2001. Recessive mutations and the maintenance of sex in structured populations. Genetics 158:913-17
8. Agrawal AF, Wang AD. 2008. Increased transmission of mutations by low-condition females: evidence for condition-dependent DNA repair. PLoS Biol. 6:e30
9. Agrawal AF, Whitlock MC. 2010. Environmental duress and epistasis: How does stress affect the strength of selection on new mutations Trends Ecol. Evol. 25:450-58
10. Agrawal AF, Whitlock MC. 2011. Inferences about the distribution of dominance drawn from yeast gene knockout data. Genetics 187:553-66
11. Anderson JP, Daifuku R, Loeb LA. 2004. Viral error catastrophe by mutagenic nucleosides. Annu. Rev. Microbiol. 58:183-205
12. Baer CF, Miyamoto MM, Denver DR. 2007. Mutation rate variation in multicellular eukaryotes: causes and consequences. Nat. Rev. Genet. 8:619-31
13. Baer CF, Shaw F, Steding C, Baumgartner M, Hawkins A, et al. 2005. Comparative evolutionary genetics of spontaneous mutations affecting fitness in rhabditid nematodes. Proc. Natl. Acad. Sci. USA 102:5785-90
14. Bataillon T, Kirkpatrick M. 2000. Inbreeding depression due to mildly deleterious mutations in finite populations: Size does matter. Genet. Res. 75:75-81
15. B́egin M, Schoen DJ. 2006. Low impact of germline transposition on the rate of mildly deleterious mutation in Caenorhabditis elegans. Genetics 174:2129-36
16. Boyko AR, Williamson SH, Indap AR, Degenhardt JD, Hernandez RD, et al. 2008. Assessing the evolutionary impact of amino acid mutations in the human genome. PLoS Genet. 4:e1000083
17. Bull JJ, Sanjúan R, Wilke CO. 2007. Theory of lethal mutagenesis for viruses. J. Virol. 81:2930-39
18. Bull JJ, Wilke CO. 2008. Lethal mutagenesis of bacteria. Genetics 180:1061-70
19. Charlesworth B. 1990. Mutation-selection balance and the evolutionary advantage of sex and recombination. Genet. Res. 55:199-221
20. Charlesworth B. 2012. The effects of deleterious mutations on evolution at linked sites. Genetics 190:5-22
21. Charlesworth B, Charlesworth D. 2010. Elements of Evolutionary Genetics. Greenwood Village, CO: Roberts and Co.
22. Charlesworth B, Hughes KA. 1999. The maintenance of genetic variation in life-history traits. In Evolutionary Genetics: From Molecules to Morphology, ed. RS Singh, CB Krimbas, pp. 369-92. Cambridge, UK: Cambridge Univ. Press
23. Charlesworth D, Morgan MT, Charlesworth B. 1990. Inbreeding depression, genetic load, and the evolution of outcrossing rates in a multilocus system with no linkage. Evolution 44:1469-89
24. Clarke B. 1973a. Effect of mutation on population size. Nature 242:196-97
25. Clarke B. 1973b. Mutation and population size. Heredity 31:367-79
26. Conrad DF, Keebler JEM, DePristo MA, Lindsay SJ, Zhang YJ, et al. 2011. Variation in genome-wide mutation rates within and between human families. Nat. Genet. 43:712-14
27. Crotty S, Cameron CE, Andino R. 2001. RNA virus error catastrophe: direct molecular test by using ribavirin. Proc. Natl. Acad. Sci. USA 98:6895-900
28. Crow JF. 1970. Genetic loads and the cost of natural selection. In Mathematical Topics in Population Genetics, ed. K-I Kojima, pp. 128-77. Berlin: Springer-Verlag
29. Crow JF. 1993. Mutation, mean fitness, and genetic load. In Oxford Surveys in Evolutionary Biology, ed. D Futuyma, J Antonovics, pp. 3-42. Oxford, UK: Oxford Univ. Press
30. Crow JF. 1997. The high spontaneous mutation rate: Is it a health risk Proc. Natl. Acad. Sci. USA 94:8380-86
31. Crow JF, Kimura M. 1970. An Introduction to Population Genetics Theory. Minneapolis: Burgess Publ.
32. Cutter AD. 2008. Divergence times in Caenorhabditis and Drosophila inferred from direct estimates of the neutral mutation rate. Mol. Biol. Evol. 25:778-86
33. Davies EK, Peters AD, Keightley PD. 1999. High frequency of cryptic deleterious mutations in Caenorhabditis elegans. Science 285:1748-51
34. de Visser JAGM, Hoekstra RF, van den Ende H. 1997a. An experimental test for synergistic epistasis and its application in Chlamydomonas. Genetics 145:815-19
35. de Visser JAGM, Hoekstra RF, van den Ende H. 1997b. Test of interaction between genetic markers that affect fitness in Aspergillus niger. Evolution 51:1499-505
36. Denver DR, Dolan PC,Wilhelm LJ, Sung W, Lucas-Lledo JI, et al. 2009. A genome-wide view of Caenorhabditis elegans base-substitution mutation processes. Proc. Natl. Acad. Sci. USA 106:16310-14
37. Denver DR, Morris K, Lynch M, Thomas WK. 2004. High mutation rate and predominance of insertions in the Caenorhabditis elegans nuclear genome. Nature 430:679-82
38. Drake JW, Charlesworth B, Charlesworth D, Crow JF. 1998. Rates of spontaneous mutation. Genetics 148:1667-86
39. Eigen M. 2002. Error catastrophe and antiviral strategy. Proc. Natl. Acad. Sci. USA 99:13374-76
40. Elena SF, Lenski RE. 1997. Test of synergistic interactions among deleterious mutations in bacteria. Nature 390:395-98
41. Ë ory L, Halligan DL, Keightley PD. 2010. Distributions of selectively constrained sites and deleterious mutation rates in the hominid and murid genomes. Mol. Biol. Evol. 27:177-92
42. Estes S, Phillips PC, Denver DR, Thomas WK, Lynch M. 2004. Mutation accumulation in populations of varying size: the distribution of mutational effects for fitness correlates in Caenorhabditis elegans. Genetics 166:1269-79
43. Eyre-Walker A, Woolfit M, Phelps T. 2006. The distribution of fitness effects of new deleterious amino acid mutations in humans. Genetics 173:891-900
44. Fawcett TW, Johnstone RA. 2003. Mate choice in the face of costly competition. Behav. Ecol. 14:771-79
45. Freistadt MS, Meades GD, Cameron CE. 2004. Lethal mutagens: broad-spectrum antivirals with limited potential for development of resistance Drug Resist. Updat. 7:19-24
46. Fry JD. 1996. The evolution of host specialization: Are trade-offs overrated Am. Nat. 148:S84-107
47. Gĺemin S. 2003.Howare deleterious mutations purged Drift versus nonrandom mating. Evolution 57:2678-87
48. Gĺemin S, Ronfort J, Bataillon T. 2003. Patterns of inbreeding depression and architecture of the load in subdivided populations. Genetics 165:2193-212
49. Glenday C, ed. 2010. Guinness World Records 2011. New York: Bantam Books.
50. Goho S, Bell G. 2000. Mild environmental stress elicits mutations affecting fitness in Chlamydomonas. Proc. R. Soc. B 267:123-29
51. Haag CR, Roze D. 2007. Genetic load in sexual and asexual diploids: segregation, dominance and genetic drift. Genetics 176:1663-78
52. Haag-Liautard C, Dorris M, Maside X, Macaskill S, Halligan DL, et al. 2007. Direct estimation of per nucleotide and genomic deleterious mutation rates in Drosophila. Nature 445:82-85
53. Haldane JBS. 1937. The effect of variation on fitness. Am. Nat. 71:337-49
54. Haldane JBS. 1957. The cost of natural selection. J. Genet. 55:511-24
55. Halligan DL,Keightley PD. 2009. Spontaneous mutation accumulation studies in evolutionary genetics. Annu. Rev. Ecol. Evol. Syst. 40:151-72
56. Hansen TF,WagnerGP. 2001. Epistasis and the mutation load: a measurement-theoretical approach. Genetics 158:477-85
57. Holsinger KE, Pacala SW. 1990. Multiple-niche polymorphisms in plant populations. Am. Nat. 135:301-9
58. Holt RD. 1996. Adaptive evolution in source-sink environments: direct and indirect effects of densitydependence on niche evolution. Oikos 75:182-92
59. Houle D, Kondrashov AS. 2002. Coevolution of costly mate choice and condition-dependent display of good genes. Proc. R. Soc. B 269:97-104
60. Howard RS, Lively CM. 1998. The maintenance of sex by parasitism and mutation accumulation under epistatic fitness functions. Evolution 52:604-10
61. Jasnos L, Korona R. 2007. Epistatic buffering of fitness loss in yeast double deletion strains. Nat. Genet. 39:550-54
62. Jasnos L, Tomala K, Paczesniak D, Korona R. 2008. Interactions between stressful environment and gene deletions alleviate the expected average loss of fitness in yeast. Genetics 178:2105-11
63. Kawecki TJ. 1994. Accumulation of deleterious mutations and the evolutionary cost of being a generalist. Am. Nat. 144:833-38
64. Kawecki TJ. 1995. Demography of source-sink populations and the evolution of ecological niches. Evol. Ecol. 9:38-44
65. Kawecki TJ, Barton NH, Fry JD. 1997. Mutational collapse of fitness in marginal habitats and the evolution of ecological specialisation. J. Evol. Biol. 10:407-29
66. Keightley PD. 1996. Metabolic models of selection response. J. Theor. Biol. 182:311-16
67. Keightley PD. 2012. Rates and fitness consequences of new mutations in humans. Genetics 190:295-304
68. Keightley PD, Eyre-Walker A. 2007. Joint inference of the distribution of fitness effects of deleterious mutations and population demography based on nucleotide polymorphism frequencies. Genetics 177:2251-61
69. Keightley PD, Halligan DL. 2009. Analysis and implications of mutational variation. Genetica 136:359-69
70. Keightley PD, Lynch M. 2003. Toward a realistic model of mutations affecting fitness. Evolution 57:683-85
71. Keightley PD, Otto SP. 2006. Interference among deleterious mutations favours sex and recombination in finite populations. Nature 443:89-92
72. Kimura M, Maruyama T. 1966. The mutational load with epistatic interactions in fitness. Genetics 54:1337-51
73. Kimura M, Maruyama T, Crow JF. 1963. Mutation load in small populations. Genetics 48:1303-12
74. King JL. 1966. The gene interaction component of genetic load. Genetics 53:403-13
75. King JL. 1967. Continuously distributed factors affecting fitness. Genetics 55:483-92
76. Kishony R, Leibler S. 2003. Environmental stresses can alleviate the average deleterious effect of mutations. J. Biol. 2:14
77. Kondrashov AS. 1982. Selection against harmful mutations in large sexual and asexual populations. Genet. Res. 40:325-32
78. Kondrashov AS. 1988. Deleterious mutations and the evolution of sexual reproduction. Nature 336:435-40
79. Kondrashov AS. 1995. Contamination of the genome by very slightly deleterious mutations: Why have we not died 100 times over J. Theor. Biol. 175:583-94
80. Kondrashov AS, Crow JF. 1988. King's formula for the mutation load with epistasis. Genetics 120:853-56
81. Kondrashov AS, Crow JF. 1993. A molecular approach to estimating the human deleterious mutation rate. Hum. Mutat. 2:229-34
82. Laffafian A, King JD, Agrawal AF. 2010. Variation in the strength and softness of selection on deleterious mutations. Evolution 64:3232-41
83. Lande R, Schemske DW. 1985. The evolution of self-fertilization and inbreeding depression in plants. I. Genetic models. Evolution 39:24-40
84. Loeb LA, Essigmann JM, Kazazi F, Zhang J, Rose KD, Mullins JI. 1999. Lethal mutagenesis of HIV with mutagenic nucleoside analogs. Proc. Natl. Acad. Sci. USA 96:1492-97
85. Lynch M. 2007. The Origins of Genome Architecture. Sunderland, MA: Sinauer Assoc.
86. Lynch M. 2010. Rate, molecular spectrum, and consequences of human mutation. Proc. Natl. Acad. Sci. USA 107:961-68
87. Lynch M, Conery JS. 2003. The origins of genome complexity. Science 302:1401-4
88. Lynch M, Conery J, B̈ urger R. 1995. Mutation accumulation and the extinction of small populations. Am. Nat. 146:489-518
89. MacArthur RH. 1972. Geographical Ecology. New York: Harper and Row.
90. Mack PD,LesterVK, PromislowDEL. 2000. Age-specific effects of novel mutations in Drosophila melanogaster. II. Fecundity and male mating ability. Genetica 110:31-41
91. Mallet MA, Bouchard JM, Kimber CM, Chippindale AK. 2011. Experimental mutation-accumulation on the X chromosome of Drosophila melanogaster reveals stronger selection on males than females. BMC Evol. Biol. 11:156
92. Manna F, Martin G, Lenormand T. 2012. Fitness landscapes: an alternative theory for the dominance of a mutation. Genetics 189:923-37
93. Martin G, Elena SF, Lenormand T. 2007. Distributions of epistasis in microbes fit predictions from a fitness landscape model. Nat. Genet. 39:555-60
94. Martin G, Gandon S. 2010. Lethal mutagenesis and evolutionary epidemiology. Philos. Trans. R. Soc. B 365:1953-63
95. Martin G, Lenormand T. 2006. The fitness effect ofmutations across environments: a survey in light of fitness landscape models. Evolution 60:2413-27
96. Matessi C, Gatto M. 1984. Does K-selection imply prudent predation Theor. Popul. Biol. 25:347-63
97. Mather K. 1969. Selection through competition. Heredity 24:529-49
98. MukaiT. 1969. Genetic structure of natural populations of Drosophila melanogaster.VII. Synergistic interaction of spontaneous mutant polygenes controlling viability. Genetics 61:749-61
99. Muller HJ. 1950. Our load of mutations. Am. J. Hum. Genet. 2:111-76
100. NachmanMW, Crowell SL. 2000. Estimate of the mutation rate per nucleotide in humans. Genetics 156:297-304
101. Nothel H. 1987. Adaptation of Drosophila melanogaster populations to high mutation pressure: evolutionary adjustment of mutation rates. Proc. Natl. Acad. Sci. USA 84:1045-49
102. Otto SP, Goldstein DB. 1992. Recombination and the evolution of diploidy. Genetics 131:745-51
103. Peck JR,Waxman D. 2000. Mutation and sex in a competitive world. Nature 406:399-404
104. Peters AD, Keightley PD. 2000. A test for epistasis among induced mutations in Caenorhabditis elegans. Genetics 156:1635-47
105. PhadnisN, Fry JD. 2005. Widespread correlations between dominance and homozygous effects of mutations: implications for theories of dominance. Genetics 171:385-92
106. Phillips N, Salomon M, Custer A, Ostrow D, Baer CF. 2009. Spontaneous mutational and standing genetic (co)variation at dinucleotide microsatellites in Caenorhabditis briggsae and Caenorhabditis elegans. Mol. Biol. Evol. 26:659-69
107. Reed FA, Aquadro CF. 2006. Mutation, selection and the future of human evolution. Trends Genet. 22:479-84
108. Rice WR. 1998. Requisite mutational load, pathway epistasis and deterministic mutation accumulation in sexual versus asexual populations. Genetica 102-103:71-81
109. Rowe L, Houle D. 1996. The lek paradox and the capture of genetic variance by condition dependent traits. Proc. R. Soc. B 263:1415-21
110. Roze D. 2012. Spatial heterogeneity in the strength of selection against deleterious allelesmay strongly reduce the mutation load. Heredity 109:137-45
111. Roze D, Rousset FO. 2004. Joint effects of self-fertilization and population structure on mutation load, inbreeding depression and heterosis. Genetics 167:1001-15
112. Sanjúan R, Elena SF. 2006. Epistasis correlates to genomic complexity. Proc. Natl. Acad. Sci. USA 103:14402-5
113. Sanjúan R, Moya A, Elena SF. 2004. The contribution of epistasis to the architecture of fitness in an RNA virus. Proc. Natl. Acad. Sci. USA 101:15376-79
114. Sanjúan R, Nebot MR. 2008. A network model for the correlation between epistasis and genomic complexity. PLoS ONE 3:e2663
115. Sankaranarayanan K. 1964. Genetic loads in irradiated experimental populations of Drosophila melanogaster. Genetics 50:131-50
116. Sankaranarayanan K. 1965. Further data on the genetic loads in irradiated experimental populations of Drosophila melanogaster. Genetics 52:153-64
117. Schoener TW. 1973. Population growth regulated by intraspecific competition for energy or time: some simple representations. Theor. Popul. Biol. 4:56-84
118. Schoener TW. 1976. Alternatives to Lotka-Volterra competition: models of intermediate complexity. Theor. Popul. Biol. 10:309-33
119. Schreiber S, Rudolf VHW. 2008. Crossing habitat boundaries: coupling dynamics of ecosystems through complex life cycles. Ecol. Lett. 11:576-87
120. Segr̀e D, DeLuna A, Church GM, Kishony R. 2005. Modular epistasis in yeast metabolism. Nat. Genet. 37:77-83
121. Sharp NP, Agrawal AF. 2009. Sexual selection and the random union of gametes: testing for a correlation in fitness between mates in Drosophila melanogaster. Am. Nat. 174:613-22
122. Sharp NP, Agrawal AF. 2012. Evidence for elevated mutation rates in low-quality genotypes. Proc. Natl. Acad. Sci. USA 109(16):6142-46
123. Shaw FH, Baer CF. 2011. Fitness-dependent mutation rates in finite populations. J. Evol. Biol. 24:1677-84
124. Siller S. 2001. Sexual selection and the maintenance of sex. Nature 411:689-92
125. Simmons MJ,Crow JF. 1977. Mutations affecting fitness in Drosophila populations. Annu. Rev. Genet. 11:49-78
126. Springman R, Keller T, Molineux IJ, Bull JJ. 2010. Evolution at a high imposed mutation rate: adaptation obscures the load in phage T7. Genetics 184:221-32
127. Szathḿary E. 1993. Do deleterious mutations act synergistically Metabolic control theory provides a partial answer. Genetics 133:127-32
128. Tobari I, Murata M. 1970a. Changes of genetic loads in experimental populations of Drosophila melanogaster with radiation histories. Jpn. J. Genet. 45:387-97
129. Tobari I, Murata M. 1970b. Effects of X-rays on genetic loads in a cage population of Drosophila melanogaster. Genetics 65:107-19
130. Turner JRG, Williamson MH. 1968. Population size, natural selection and genetic load. Nature 218:700
131. Wallace B. 1956. Studies on irradiated populations of Drosophila melanogaster. J. Genet. 54:280-93
132. Wallace B. 1959. Studies of the relative fitnesses of experimental populations of Drosophila melanogaster. Am. Nat. 93:295-314
133. Wallace B. 1968. Polymorphism, population size, and genetic load. In Population Biology and Evolution, ed.RC Lewontin, pp. 87-108. Syracuse, NY: Syracuse Univ. Press
134. Wallace B. 1970. Genetic Load. Its Biological and Conceptual Aspects. Englewood Cliffs, NJ: Prentice-Hall.
135. Wallace B. 1975. Hard and soft selection revisited. Evolution 29:465-73
136. Wallace B. 1991. Fifty Years of Genetic Load: An Odyssey. Ithaca, NY: Cornell Univ. Press
137. Wang AD, Sharp NP, Spencer CC, Tedman-Aucoin K, Agrawal AF. 2009. Selection, epistasis, and parent-oforigin effects on deleterious mutations across environments in Drosophila melanogaster. Am. Nat. 174:863-74
138. West SA, Peters AD, Barton NH. 1998. Testing for epistasis between deleterious mutations. Genetics 149:435-44
139. Whitlock MC. 1996. The Red Queen beats the Jack-of-All-Trades: the limitations on the evolution of phenotypic plasticity and niche breadth. Am. Nat. 148:S65-77
140. Whitlock MC. 2002. Selection, load, and inbreeding depression in a large metapopulation. Genetics 160:1191-202
141. Whitlock MC, Agrawal AF. 2009. Purging the genome with sexual selection: reducingmutational load through selection on males. Evolution 63:569-82
142. Whitlock MC, Bourguet D. 2000. Factors affecting the genetic load in Drosophila: synergistic epistasis and correlations among fitness components. Evolution 54:1654-60