Evolution of the insertion-deletion mutation rate across the tree of life

G3: Genes, Genomes, Genetics

Volumn 6, Issue 8, 2016, Pages 2583-2591

  Sung, Way ^a,e   Ackerman, Matthew S ^b,e   Dillon, Marcus M ^c,e   Platt, Thomas G ^b,d,e   Fuqua, Clay ^b,e   Cooper, Vaughn S ^c,d,e   Lynch, Michael ^b,e  

^a University of North Carolina at Charlotte   (United States)

^b INDIANA UNIVERSITY   (United States)

^c UNIVERSITY OF NEW HAMPSHIRE   (United States)

^d UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^e KANSAS STATE UNIVERSITY   (United States)

Author keywords

Drift barrier; Insertion deletion mutation rate; Mutation accumulation; Mutation rate evolution

Indexed keywords

DNA METABOLISM; EFFECTIVE POPULATION SIZE; EUKARYOTE; GENETIC DRIFT; INDEL MUTATION; MUTATION ACCUMULATION; MUTATION RATE; NATURAL SELECTION; NUCLEIC ACID BASE SUBSTITUTION; SPECIES; TREE OF LIFE; AGROBACTERIUM TUMEFACIENS; EVOLUTION; GENETIC SELECTION; GENETICS; GENOME; GENOME SIZE; MOLECULAR EVOLUTION; STAPHYLOCOCCUS EPIDERMIDIS; VIBRIO CHOLERAE;

AGROBACTERIUM TUMEFACIENS; BIOLOGICAL EVOLUTION; EVOLUTION, MOLECULAR; GENETIC DRIFT; GENOME; GENOME SIZE; INDEL MUTATION; MUTATION RATE; SELECTION, GENETIC; STAPHYLOCOCCUS EPIDERMIDIS; VIBRIO CHOLERAE;

EID: 84983616784     PISSN: None     EISSN: 21601836     Source Type: Journal    
DOI: 10.1534/g3.116.030890     Document Type: Article

References (67)

1. Brandvain, Y., and S. I. Wright, 2016 The limits of natural selection in a nonequilibrium world. Trends Genet. 32: 201-210.
2. Campbell, C. D., and E. E. Eichler, 2013 Properties and rates of germline mutations in humans. Trends Genet. 29: 575-584.
3. Charlesworth, B., 2009 Fundamental concepts in genetics: effective population size and patterns of molecular evolution and variation. Nat. Rev. Genet. 10: 195-205.
4. Conrad, D. F., J. E. Keebler, M. A. DePristo, S. J. Lindsay, Y. Zhang et al., 2011 Variation in genome-wide mutation rates within and between human families. Nat. Genet. 43: 712-714.
5. Denver, D. R., K. Morris, M. Lynch, and W. K. Thomas, 2004 High mutation rate and predominance of insertions in the Caenorhabditis elegans nuclear genome. Nature 430: 679-682.
6. Denver, D. R., S. Feinberg, S. Estes, W. K. Thomas, and M. Lynch, 2005 Mutation rates, spectra and hotspots in mismatch repair-deficient Caenorhabditis elegans. Genetics 170: 107-113.
7. Denver, D. R., P. C. Dolan, L. J. Wilhelm, W. Sung, J. I. Lucas-Lledo et al., 2009 A genome-wide view of Caenorhabditis elegans base-substitution mutation processes. Proc. Natl. Acad. Sci. USA 106: 16310-16314.
8. Doroghazi, J. R., and D. H. Buckley, 2014 Intraspecies comparison of Streptomyces pratensis genomes reveals high levels of recombination and gene conservation between strains of disparate geographic origin. BMC Genomics 15: 970.
9. Drake, J. W., 1991 A constant rate of spontaneous mutation in DNA-based microbes. Proc. Natl. Acad. Sci. USA 88: 7160-7164.
10. Drake, J. W., B. Charlesworth, D. Charlesworth, and J. F. Crow, 1998 Rates of spontaneous mutation. Genetics 148: 1667-1686.
11. Eyre-Walker, A., and P. D. Keightley, 2007 The distribution of fitness effects of new mutations. Nat. Rev. Genet. 8: 610-618.
12. Feil, E. J., and B. G. Spratt, 2011 Recombination and the population structures of bacterial pathogens. Annu. Rev. Microbiol. 55: 561-590.
13. Fu, Y. X., 1995 Statistical properties of segregating sites. Theor. Popul. Biol. 48: 172-197.
14. Fu, Y. X., and W. H. Li, 1993 Statistical tests of neutrality of mutations. Genetics 133: 693-709.
15. Garland, T., A. W. Dickerman, C. M. Janis, and J. A. Jones, 1993 Phylogenetic analysis of covariance by computer-simulation. Syst. Biol. 42: 265-292.
16. Halligan, D. L., and P. D. Keightley, 2006 Ubiquitous selective constraints in the Drosophila genome revealed by a genome-wide interspecies comparison. Genome Res. 16: 875-884.
17. Halligan, D. L., A. Eyre-Walker, P. Andolfatto, and P. D. Keightley, 2004 Patterns of evolutionary constraints in intronic and intergenic DNA of Drosophila. Genome Res. 14: 273-279.
18. Haudry, A., A. E. Platts, E. Vello, D. R. Hoen, M. Leclercq et al., 2013 An atlas of over 90, 000 conserved noncoding sequences provides insight into crucifer regulatory regions. Nat. Genet. 45: 891-898.
19. Johnson, T., and N. H. Barton, 2002 The effect of deleterious alleles on adaptation in asexual populations. Genetics 162: 395-411.
20. Karasov, T., P. W. Messer, and D. A. Petrov, 2010 Evidence that adaptation in Drosophila is not limited by mutation at single sites. PLoS Genet. 6: e1000924.
21. Kibota, T. T., and M. Lynch, 1996 Estimate of the genomic mutation rate deleterious to overall fitness in E. coli. Nature 381: 694-696.
22. Kimura, M., 1967 On the evolutionary adjustment of spontaneous mutation rates. Genet. Res. 9: 23-24.
23. Kimura, M., 1983 The Neutral Theory of Molecular Evolution, Cambridge University Press, Cambridge, UK.
24. Kong, A., M. L. Frigge, G. Masson, S. Besenbacher, P. Sulem et al., 2012 Rate of de novo mutations and the importance of father's age to disease risk. Nature 488: 471-475.
25. Krokan, H. E., and M. Bjoras, 2013 Base excision repair. Cold Spring Harb. Perspect. Biol. 5: a012583.
26. Kunkel, T. A., 2009 Evolving views of DNA replication (in)fidelity. Cold Spring Harb. Symp. Quant. Biol. 74: 91-101.
27. Lassalle, F., S. Perian, T. Bataillon, X. Nesme, L. Duret et al., 2015 GCContent evolution in bacterial genomes: the biased gene conversion hypothesis expands. PLoS Genet. 11: e1004941.
28. Lee, H., E. Popodi, H. Tang, and P. L. Foster, 2012 Rate and molecular spectrum of spontaneous mutations in the bacterium Escherichia coli as determined by whole-genome sequencing. Proc. Natl. Acad. Sci. USA 109: e2774-e2783.
29. Leigh, E. G., Jr., 1970 Natural selection and mutability. Am. Nat. 104: 301-305.
30. Li, H., and R. Durbin, 2009 Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25: 1754-1760.
31. Li, H., B. Handsaker, A. Wysoker, T. Fennell, J. Ruan et al., 2009 The sequence alignment/map format and SAMtools. Bioinformatics 25: 2078-2079.
32. Lipinski, K. J., J. C. Farslow, K. A. Fitzpatrick, M. Lynch, V. Katju et al., 2011 High spontaneous rate of gene duplication in Caenorhabditis elegans. Curr. Biol. 21: 306-310.
33. Loh, E., J. J. Salk, and L. A. Loeb, 2010 Optimization of DNA polymerase mutation rates during bacterial evolution. Proc. Natl. Acad. Sci. USA 107: 1154-1159.
34. Lynch, M., 2007 The Origins of Genome Architecture, Sinauer Associates, Sunderland, Massachusetts.
35. Lynch, M., 2008 The cellular, developmental and population-genetic determinants of mutation-rate evolution. Genetics 180: 933-943.
36. Lynch, M., 2010 Evolution of the mutation rate. Trends Genet. 26: 345-352.
37. Lynch, M., 2011 The lower bound to the evolution of mutation rates. Genome Biol. Evol. 3: 1107-1118.
38. Lynch, M., and G. K. Marinov, 2015 The bioenergetic costs of a gene. Proc. Natl. Acad. Sci. USA 112: 15690-15695.
39. Lynch, M., J. Blanchard, D. Houle, T. Kibota, S. Schultz et al., 1999 Spontaneous deleterious mutation. Evolution 53: 645-663.
40. Lynch, M., W. Sung, K. Morris, N. Coffey, C. R. Landry et al., 2008 A genome-wide view of the spectrum of spontaneous mutations in yeast. Proc. Natl. Acad. Sci. USA 105: 9272-9277.
41. Martins, E. P., 2004 Compare, Version 4.6b. Computer Programs for the Statistical Analysis of Comparative Data. Department of Biology, Indiana University, Bloomington, IN. Available at: http://compare.bio.indiana.edu.
42. McCulloch, S. D., and T. A. Kunkel, 2008 The fidelity of DNA synthesis by eukaryotic replicative and translesion synthesis polymerases. Cell Res. 18: 148-161.
43. Mira, A., H. Ochman, and N. A. Moran, 2001 Deletional bias and the evolution of bacterial genomes. Trends Genet. 17: 589-596.
44. Morita, R., S. Nakane, A. Shimada, M. Inoue, H. Iino et al., 2010 Molecular mechanisms of the whole DNA repair system: a comparison of bacterial and eukaryotic systems. J. Nucleic Acids 2010: 179594.
45. Ness, R. W., A. D. Morgan, N. Colegrave, and P. D. Keightley, 2012 Estimate of the spontaneous mutation rate in Chlamydomonas reinhardtii. Genetics 192: 1447-1454.
46. Ness, R. W., S. A. Kraemer, N. Colegrave, and P. D. Keightley, 2015 Direct estimate of the spontaneous mutation rate uncovers the effects of drift and recombination in the Chlamydomonas reinhardtii plastid genome. Mol. Biol. Evol. 33: 800-808.
47. O'Roak, B. J., P. Deriziotis, C. Lee, L. Vives, J. J. Schwartz et al., 2011 Exome sequencing in sporadic autism spectrum disorders identifies severe de novo mutations. Nat. Genet. 43: 585-589.
48. O'Roak, B. J., L. Vives, S. Girirajan, E. Karakoc, N. Krumm et al., 2012 Sporadic autism exomes reveal a highly interconnected protein network of de novo mutations. Nature 485: 246-250.
49. Orr, H. A., 2000 The rate of adaptation in asexuals. Genetics 155: 961-968.
50. Ossowski, S., K. Schneeberger, J. I. Lucas-Lledo, N. Warthmann, R. M. Clark et al., 2010 The rate and molecular spectrum of spontaneous mutations in Arabidopsis thaliana. Science 327: 92-94.
51. Sancar, A., L. A. Lindsey-Boltz, K. Unsal-Kacmaz, and S. Linn, 2004 Molecular mechanisms of mammalian DNA repair and the DNA damage checkpoints. Annu. Rev. Biochem. 73: 39-85.
52. Schrider, D. R., D. Houle, M. Lynch, and M. W. Hahn, 2013 Rates and genomic consequences of spontaneous mutational events in Drosophila melanogaster. Genetics 194: 937-954.
53. Siepel, A., G. Bejerano, J. S. Pedersen, A. S. Hinrichs, M. Hou et al., 2005 Evolutionarily conserved elements in vertebrate, insect, worm, and yeast genomes. Genome Res. 15: 1034-1050.
54. Sniegowski, P., and Y. Raynes, 2013 Mutation rates: how low can you go? Curr. Biol. 23: R147-R149.
55. Sniegowski, P. D., P. J. Gerrish, T. Johnson, and A. Shaver, 2000 The evolution of mutation rates: separating causes from consequences. BioEssays 22: 1057-1066.
56. Sung, W., M. S. Ackerman, S. F. Miller, T. G. Doak, and M. Lynch, 2012a Drift-barrier hypothesis and mutation-rate evolution. Proc. Natl. Acad. Sci. USA 109: 18488-18492.
57. Sung, W., A. E. Tucker, T. G. Doak, E. Choi, W. K. Thomas et al., 2012b Extraordinary genome stability in the ciliate Paramecium tetraurelia. Proc. Natl. Acad. Sci. USA 109: 19339-19344.
58. Sung, W., M. S. Ackerman, J. F. Gout, S. F. Miller, E. Williams et al., 2015 Asymmetric context-dependent mutation patterns revealed through mutation-accumulation experiments. Mol. Biol. Evol. 32: 1672-1683.
59. Tajima, F., 1989 Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123: 585-595.
60. The 1000 Genomes Project Consortium, 2015 A global reference for human genetic variation. Nature 526: 68-74.
61. Uchimura, A., M. Higuchi, Y. Minakuchi, M. Ohno, A. Toyoda et al., 2015 Germline mutation rates and the long-term phenotypic effects of mutation accumulation in wild-type laboratory mice and mutator mice. Genome Res. 25: 1125-1134.
62. Vieira-Silva, S., M. Touchon, and E. P. Rocha, 2010 No evidence for elemental-based streamlining of prokaryotic genomes. Trends Ecol. Evol. 25: 319-320; author reply 320-311.
63. Wang, H., and X. Zhu, 2014 De novo mutations discovered in 8 Mexican American families through whole genome sequencing. BMC Proc. 8: S24.
64. Watterson, G. A., 1975 On the number of segregating sites in genetical models without recombination. Theor. Popul. Biol. 7: 256-276.
65. Whitney, K. D., and T. Garland, Jr., 2010 Did genetic drift drive increases in genome complexity? PLoS Genet. 6: e1001080.
66. Yang, S., L. Wang, J. Huang, X. Zhang, Y. Yuan et al., 2015 Parent-progeny sequencing indicates higher mutation rates in heterozygotes. Nature 523: 463-467.
67. Zhu, Y. O., M. L. Siegal, D. W. Hall, and D. A. Petrov, 2014 Precise estimates of mutation rate and spectrum in yeast. Proc. Natl. Acad. Sci. USA 111: e2310-e2318.