Molecular Clock of Neutral Mutations in a Fitness-Increasing Evolutionary Process

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Mutations that have little influence on biological function are referred to as neutral mutations and frequently appear in molecular phylogenetic analyses. The fixation of neutral mutations in populations has been attributed to genetic drift in fitness-steady evolutionary processes or hitchhiking in adaptive evolution. We examined the fitness-increasing evolution of Escherichia coli for thermal adaptation to observe the fixation dynamics of genome-wide mutations. In the adaptive evolution, all genomes in the population equally accumulated neutral mutations by replication errors. The infrequent occurrence of an adaptive mutation on one of the genomes by chance resulted in the fixation of the neutral mutations that had pre-accumulated in the same genome by hitchhiking. Via successive hitchhiking events, the neutral mutations were fixed in the population linearly over generations at the same rate as the spontaneous mutation accumulation rate in the genome. The molecular clock of neutral mutations thus functions even in adaptive evolution. The evolutionary period characterized by the accumulation of numerous neutral mutations observed in molecular phylogenetic trees may not be specific to neutral evolution but may occur in adaptive evolution as well.

Vyšlo v časopise: Molecular Clock of Neutral Mutations in a Fitness-Increasing Evolutionary Process. PLoS Genet 11(7): e32767. doi:10.1371/journal.pgen.1005392
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1005392

Souhrn

Zdroje

1. Barrick JE, Lenski RE (2013) Genome dynamics during experimental evolution. Nat Rev Genet 14: 827–839. doi: 10.1038/nrg3564 24166031

2. Ohta T, Kimura M (1971) On the constancy of the evolutionary rate of cistrons. J Mol Evol 1: 18–25. 4377445

3. Drake JW, Charlesworth B, Charlesworth D, Crow JF (1998) Rates of spontaneous mutation. Genetics 148: 1667–1686. 9560386

4. Elena SF, Ekunwe L, Hajela N, Oden SA, Lenski RE (1998) Distribution of fitness effects caused by random insertion mutations in Escherichia coli. Genetica 102–103: 349–358. 9720287

5. Wloch DM, Szafraniec K, Borts RH, Korona R (2001) Direct estimate of the mutation rate and the distribution of fitness effects in the yeast Saccharomyces cerevisiae. Genetics 159: 441–452. 11606524

6. Joseph SB, Hall DW (2004) Spontaneous mutations in diploid Saccharomyces cerevisiae: more beneficial than expected. Genetics 168: 1817–1825. 15611159

7. Sanjuan R, Moya A, Elena SF (2004) The distribution of fitness effects caused by single-nucleotide substitutions in an RNA virus. Proc Natl Acad Sci U S A 101: 8396–8401. 15159545

8. Kassen R, Bataillon T (2006) Distribution of fitness effects among beneficial mutations before selection in experimental populations of bacteria. Nat Genet 38: 484–488. 16550173

9. Arjan JA, Visser M, Zeyl CW, Gerrish PJ, Blanchard JL, et al. (1999) Diminishing returns from mutation supply rate in asexual populations. Science 283: 404–406. 9888858

10. Sanjuan R, Elena SF (2006) Epistasis correlates to genomic complexity. Proc Natl Acad Sci U S A 103: 14402–14405. 16983079

11. Khan AI, Dinh DM, Schneider D, Lenski RE, Cooper TF (2011) Negative epistasis between beneficial mutations in an evolving bacterial population. Science 332: 1193–1196. doi: 10.1126/science.1203801 21636772

12. Smith JM, Haigh J (1974) The hitch-hiking effect of a favourable gene. Genet Res 23: 23–35. 4407212

13. Desai MM, Fisher DS (2011) The balance between mutators and nonmutators in asexual populations. Genetics 188: 997–1014. doi: 10.1534/genetics.111.128116 21652523

14. Lang GI, Rice DP, Hickman MJ, Sodergren E, Weinstock GM, et al. (2013) Pervasive genetic hitchhiking and clonal interference in forty evolving yeast populations. Nature 500: 571–574. doi: 10.1038/nature12344 23873039

15. Wiser MJ, Ribeck N, Lenski RE (2013) Long-term dynamics of adaptation in asexual populations. Science 342: 1364–1367. doi: 10.1126/science.1243357 24231808

16. Herron MD, Doebeli M (2013) Parallel evolutionary dynamics of adaptive diversification in Escherichia coli. PLoS Biol 11: e1001490. doi: 10.1371/journal.pbio.1001490 23431270

17. Masel J (2011) Genetic drift. Curr Biol 21: R837–838. doi: 10.1016/j.cub.2011.08.007 22032182

18. Zuckerkandl E, Pauling L (1965) Molecules as documents of evolutionary history. J Theor Biol 8: 357–366. 5876245

19. Bromham L, Penny D (2003) The modern molecular clock. Nat Rev Genet 4: 216–224. 12610526

20. Peterson GI, Masel J (2009) Quantitative prediction of molecular clock and ka/ks at short timescales. Mol Biol Evol 26: 2595–2603. doi: 10.1093/molbev/msp175 19661199

21. Gillooly JF, Allen AP, West GB, Brown JH (2005) The rate of DNA evolution: effects of body size and temperature on the molecular clock. Proc Natl Acad Sci U S A 102: 140–145. 15618408

22. Li WH, Makova KD (2008) Molecular Clocks. In: Encyclopedia of Life Sciences (ELS). Chichester: John Wiley & Sons.

23. Kimura M (1968) Evolutionary rate at the molecular level. Nature 217: 624–626. 5637732

24. Schiffels S, Szollosi GJ, Mustonen V, Lassig M (2011) Emergent neutrality in adaptive asexual evolution. Genetics 189: 1361–1375. doi: 10.1534/genetics.111.132027 21926305

25. Gillespie JH (2000) Genetic drift in an infinite population. The pseudohitchhiking model. Genetics 155: 909–919. 10835409

26. Birky CW Jr., Walsh JB (1988) Effects of linkage on rates of molecular evolution. Proc Natl Acad Sci U S A 85: 6414–6418. 3413105

27. Kimura M (1984) The neutral theory of molecular evolution: Cambridge University Press.

28. Buri P (1956) Gene Frequency in Small Populations of Mutant Drosophila. Evolution 10: 367–402.

29. Kishimoto T, Iijima L, Tatsumi M, Ono N, Oyake A, et al. (2010) Transition from positive to neutral in mutation fixation along with continuing rising fitness in thermal adaptive evolution. PLoS Genet 6: e1001164. doi: 10.1371/journal.pgen.1001164 20975944

30. Barrick JE, Yu DS, Yoon SH, Jeong H, Oh TK, et al. (2009) Genome evolution and adaptation in a long-term experiment with Escherichia coli. Nature 461: 1243–1247. doi: 10.1038/nature08480 19838166

31. Denamur E, Matic I (2006) Evolution of mutation rates in bacteria. Mol Microbiol 60: 820–827. 16677295

32. Taddei F, Radman M, Maynard-Smith J, Toupance B, Gouyon PH, et al. (1997) Role of mutator alleles in adaptive evolution. Nature 387: 700–702. 9192893

33. Gerrish PJ, Lenski RE (1998) The fate of competing beneficial mutations in an asexual population. Genetica 102–103: 127–144. 9720276

34. Miralles R, Gerrish PJ, Moya A, Elena SF (1999) Clonal interference and the evolution of RNA viruses. Science 285: 1745–1747. 10481012

35. Hegreness M, Shoresh N, Hartl D, Kishony R (2006) An equivalence principle for the incorporation of favorable mutations in asexual populations. Science 311: 1615–1617. 16543462

36. Kao KC, Sherlock G (2008) Molecular characterization of clonal interference during adaptive evolution in asexual populations of Saccharomyces cerevisiae. Nat Genet 40: 1499–1504. doi: 10.1038/ng.280 19029899

37. Good BH, Rouzine IM, Balick DJ, Hallatschek O, Desai MM (2011) Distribution of fixed beneficial mutations and the rate of adaptation in asexual populations. Proc Natl Acad Sci U S A 109: 4950–4955.

38. Perfeito L, Fernandes L, Mota C, Gordo I (2007) Adaptive mutations in bacteria: high rate and small effects. Science 317: 813–815. 17690297

39. Rouzine IM, Brunet E, Wilke CO (2008) The traveling-wave approach to asexual evolution: Muller's ratchet and speed of adaptation. Theor Popul Biol 73: 24–46. 18023832

40. Mueller LD, Joshi A, Santos M, Rose MR (2013) Effective population size and evolutionary dynamics in outbred laboratory populations of Drosophila. J Genet 92: 349–361. 24371158

41. Suzuki S, Ono N, Furusawa C, Ying BW, Yomo T (2011) Comparison of sequence reads obtained from three next-generation sequencing platforms. PLoS One 6: e19534. doi: 10.1371/journal.pone.0019534 21611185