The Impact of Selection, Gene Conversion, and Biased Sampling on the Assessment of Microbial Demography

Molecular Biology and Evolution

Volumn 33, Issue 7, 2016, Pages 1711-1725

  Lapierre, Marguerite ^a,b   Blin, Camille ^c,d,e   Lambert, Amaury ^b,c   Achaz, Guillaume ^a,b   Rocha, Eduardo P C ^d,e  

^a MUSÉUM NATIONAL D'HISTOIRE NATURELLE   (France)

^b Centre de Recherche Interdisciplinaire en Biologie   (France)

^c SORBONNE UNIVERSITÉ   (France)

^d INSTITUT PASTEUR   (France)

^e CNRS   (France)

Author keywords

Bacteria; Escherichia coli; Gene conversion; Natural selection; Population genomics; Population size

Indexed keywords

ARTICLE; DEMOGRAPHY; ESCHERICHIA COLI; GENE CONVERSION; GENEALOGY; HUMAN; NATURAL SELECTION; NONHUMAN; POPULATION GENOMICS; POPULATION SIZE; PURIFYING SELECTION; SAMPLING BIAS; SIMULATION; THEORETICAL STUDY; BACTERIAL GENOME; BACTERIUM; BIOLOGICAL MODEL; GENETIC SELECTION; GENETIC VARIATION; GENETICS; METAGENOMICS; MOLECULAR EVOLUTION; POPULATION GENETICS; PROCEDURES; SELECTION BIAS;

BACTERIA; EVOLUTION, MOLECULAR; GENE CONVERSION; GENETIC VARIATION; GENETICS, POPULATION; GENOME, BACTERIAL; METAGENOMICS; MODELS, GENETIC; SELECTION BIAS; SELECTION, GENETIC;

EID: 85018383851     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/MOLBEV/MSW048     Document Type: Article

References (110)

1. Achaz G. 2009. Frequency spectrum neutrality tests: one for all and all for one. Genetics 183:249–258.
2. Adams AM, Hudson RR. 2004. Maximum-likelihood estimation of demographic parameters using the frequency spectrum of unlinked single-nucleotide polymorphisms. Genetics 168:1699–1712.
3. Azarian T, Ali A, Johnson JA, Mohr D, Prosperi M, Veras NM, Jubair M, Strickland SL, Rashid MH, Alam MT, et al. 2014. Phylodynamic analysis of clinical and environmental Vibrio cholerae isolates from Haiti reveals diversification driven by positive selection. MBio 5:e01824–14.
4. Balbi KJ, Rocha EP, Feil EJ. 2009. The temporal dynamics of slightly deleterious mutations in Escherichia coli and Shigella spp. Mol Biol Evol. 26:345–355.
5. Barroso-Batista J, Sousa A, Lourenco M, Bergman ML, Sobral D, Demengeot J, Xavier KB, Gordo I. 2014. The first steps of adaptation of Escherichia coli to the gut are dominated by soft sweeps. PLoS Genet. 10:e1004182.
6. Bart MJ, Harris SR, Advani A, Arakawa Y, Bottero D, Bouchez V, Cassiday PK, Chiang CS, Dalby T, Fry NK, et al. 2014. Global population structure and evolution of Bordetella pertussis and their relationship with vaccination. MBio 5:e01074.
7. Baudry E, Depaulis F. 2003. Effect of misoriented sites on neutrality tests with outgroup. Genetics 165:1619–1622.
8. Beaumont MA, Zhang W, Balding DJ. 2002. Approximate Bayesian computation in population genetics. Genetics 162:2025–2035.
9. Bobay LM, Traverse CC, Ochman H. 2015. Impermanence of bacterial clones. Proc Natl Acad Sci U S A. 112:8893–8900.
10. Braverman JM, Hudson RR, Kaplan NL, Langley CH, Stephan W. 1995. The hitchhiking effect on the site frequency spectrum of DNA polymorphisms. Genetics 140:783–796.
11. Brenner DJ, Krieg NR, Staley JT. 2005. Bergey’s manual of systematic bacteriology. New York: Springer.
12. Charlesworth J, Eyre-Walker A. 2006. The rate of adaptive evolution in enteric bacteria. Mol Biol Evol. 23:1348–1356.
13. Cohen ML. 2000. Changing patterns of infectious disease. Nature 406:762–767.
14. Cohan FM, Perry EB. 2007. A systematics for discovering the fundamental units of bacterial diversity. Curr Biol. 17:R373–R386.
15. Comas I, Coscolla M, Luo T, Borrell S, Holt KE, Kato-Maeda M, Parkhill J, Malla B, Berg S, Thwaites G, et al. 2013. Out-of-Africa migration and Neolithic coexpansion of Mycobacterium tuberculosis with modern humans. Nat Genet. 45:1176–1182.
16. Cornejo OE, Lefebure T, Bitar PD, Lang P, Richards VP, Eilertson K, Do T, Beighton D, Zeng L, Ahn SJ, et al. 2013. Evolutionary and population genomics of the cavity causing bacteria Streptococcus mutans. Mol Biol Evol. 30:881–893.
17. Croucher NJ, Hanage WP, Harris SR, McGee L, van der Linden M, de Lencastre H, Sa-Leao R, Song JH, Ko KS, Beall B, et al. 2014. Variable recombination dynamics during the emergence, transmission and ‘disarming’ of a multidrug-resistant pneumococcal clone. BMC Biol. 12:49.
18. Davies MR, Holden MT, Coupland P, Chen JH, Venturini C, Barnett TC, Zakour NL, Tse H, Dougan G, Yuen KY, et al. 2015. Emergence of scarlet fever Streptococcus pyogenes emm12 clones in Hong Kong is associated with toxin acquisition and multidrug resistance. Nat Genet. 47:84–87.
19. Delaney NF, Balenger S, Bonneaud C, Marx CJ, Hill GE, Ferguson-Noel N, Tsai P, Rodrigo A, Edwards SV. 2012. Ultrafast evolution and loss of CRISPRs following a host shift in a novel wildlife pathogen, Mycoplasma gallisepticum. PLoS Genet. 8:e1002511.
20. Didelot X, Falush D. 2007. Inference of bacterial microevolution using multilocus sequence data. Genetics 175:1251–1266.
21. Didelot X, Meric G, Falush D, Darling AE. 2012. Impact of homologous and non-homologous recombination in the genomic evolution of Escherichia coli. BMC Genomics 13:256.
22. Drummond AJ, Rambaut A. 2007. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol. 7:214.
23. Drummond AJ, Nicholls GK, Rodrigo AG, Solomon W. 2002. Estimating mutation parameters, population history and genealogy simultaneously from temporally spaced sequence data. Genetics 161:1307–1320.
24. Drummond AJ, Rambaut A, Shapiro B, Pybus OG. 2005. Bayesian coalescent inference of past population dynamics from molecular sequences. Mol Biol Evol. 22:1185–1192.
25. Edgar RC. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32:1792–1797.
26. Eldholm V, Monteserin J, Rieux A, Lopez B, Sobkowiak B, Ritacco V, Balloux F. 2015. Four decades of transmission of a multidrug-resistant Mycobacterium tuberculosis outbreak strain. Nat Commun. 6:7119.
27. Frost SDW, Pybus OG, Gog JR, Viboud C, Bonhoeffer S, Bedford T. 2014. Eight challenges in phylodynamic inference. Epidemics 10:88–92.
28. Fu YX. 1997. Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925.
29. Fu R, Voordouw G. 1997. Targeted gene-replacement mutagenesis of dcrA, encoding an oxygen sensor of the sulfate-reducing bacterium Desulfovibrio vulgaris Hildenborough. Microbiology 143:1815–1826.
30. Gallet R, Cooper TF, Elena SF, Lenormand T. 2012. Measuring selection coefficients below 10(-3): method, questions, and prospects. Genetics 190:175–186.
31. Gascuel O. 1997. BIONJ: an improved version of the NJ algorithm based on a simple model of sequence data. Mol Biol Evol. 14:685–695.
32. Grad YH, Lipsitch M. 2014. Epidemiologic data and pathogen genome sequences: a powerful synergy for public health. Genome Biol. 15:538.
33. Grenfell BT, Pybus OG, Gog JR, Wood JL, Daly JM, Mumford JA, Holmes EC. 2004. Unifying the epidemiological and evolutionary dynamics of pathogens. Science 303:327–332.
34. Guttman DS, Morgan RL, Wang PW. 2008. The evolution of the pseudomonads. In: Fatmi M, Collmer A, Iacobellis MS, Mansfield JW, Murillo J, Schaad NW, Ullrich M, editors. Pseudomonas syringae pathovars and related pathogens—identification, epidemiology and genomics. Dordrecht: Springer. p. 307–319.
35. Hartl DL, Moriyama EN, Sawyer SA. 1994. Selection intensity for codon bias. Genetics 138:227–234.
36. Hasegawa M, Kishino H, Yano T, Stabler RA, Dawson LF, Martin MJ, Holt KE, Seth-Smith HM, Quail MA, Rance R, 1985. Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol. 22:160–174.
37. He M, Sebaihia M, Lawley TD, Stabler RA, Dawson LF, Martin MJ, Holt KE, Seth-Smith HM, Quail MA, Rance R, et al. 2010. Evolutionary dynamics of Clostridium difficile over short and long time scales. Proc Natl Acad Sci U S A. 107:7527–7532.
38. Hedge J, Wilson DJ. 2014. Bacterial phylogenetic reconstruction from whole genomes is robust to recombination but demographic inference is not. MBio 5:e02158.
39. Heller R, Chikhi L, Siegismund HR. 2013. The confounding effect of population structure on Bayesian skyline plot inferences of demographic history. PLoS One 8:e62992.
40. Hernandez RD. 2008. A flexible forward simulator for populations subject to selection and demography. Bioinformatics 24:2786–2787.
41. Hernandez RD, Williamson SH, Bustamante CD. 2007. Context dependence, ancestral misidentification, and spurious signatures of natural selection. Mol Biol Evol. 24:1792–1800.
42. Ho SY, Phillips MJ, Cooper A, Drummond AJ. 2005. Time dependency of molecular rate estimates and systematic overestimation of recent divergence times. Mol Biol Evol. 22:1561–1568.
43. Ho SY, Shapiro B. 2011. Skyline-plot methods for estimating demographic history from nucleotide sequences. Mol Ecol Resour. 11:423–434.
44. Holmes EC. 2007. Viral evolution in the genomic age. PLoS Biol. 5:e278.
45. Holt KE, Baker S, Weill FX, Holmes EC, Kitchen A, Yu J, Sangal V, Brown DJ, Coia JE, Kim DW, et al. 2012. Shigella sonnei genome sequencing and phylogenetic analysis indicate recent global dissemination from Europe. Nat Genet. 44:1056–1059.
46. Hughes AL. 2005. Evidence for abundant slightly deleterious polymorphisms in bacterial populations. Genetics 169:533–538.
47. Jukes TH, Cantor CR: 1969. Evolution of protein molecules. Mammalian protein metabolism. New York: Academic Press. p. 21–132.
48. Kibota TT, Lynch M. 1996. Estimate of the genomic mutation rate deleterious to overall fitness in E. coli. Nature 381:694–696.
49. Kimura M. 1980. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol. 16:111–120.
50. Kimura M. 1983. The neutral theory of molecular evolution. Cambridge: Cambridge University Press.
51. Li LM, Grassly NC, Fraser C. 2014. Genomic analysis of emerging pathogens: methods, application and future trends. Genome Biol. 15:541.
52. Liao P-C, Huang S. 2012. Patterns of microbial genetic diversity and the correlation between bacterial demographic history and geohistory. In: Caliskan M, editor. Genetic diversity in microorganisms. Shangai: INTECH Open Access Publisher. p. 123–148.
53. Liu X, Fu YX. 2015. Exploring population size changes using SNP frequency spectra. Nat Genet. 47:555–559.
54. Lynch M. 2006. The origins of eukaryotic gene structure. Mol Biol Evol. 23:450–468.
55. Martiny JB, Bohannan BJ, Brown JH, Colwell RK, Fuhrman JA, Green JL, Horner-Devine MC, Kane M, Krumins JA, Kuske CR, et al. 2006. Microbial biogeography: putting microorganisms on the map. Nat Rev Microbiol. 4:102–112.
56. Mazet O, Rodriguez W, Chikhi L. 2015. Demographic inference using genetic data from a single individual: Separating population size variation from population structure. Theor Popul Biol. 104:46–58.
57. Merker M, Blin C, Mona S, Duforet-Frebourg N, Lecher S, Willery E, Blum MG, Rusch-Gerdes S, Mokrousov I, Aleksic E, et al. 2015. Evolutionary history and global spread of the Mycobacterium tuberculosis Beijing lineage. Nat Genet. 47:242–249.
58. Navarro A, Barton NH. 2002. The effects of multilocus balancing selection on neutral variability. Genetics 161:849–863.
59. Neuhauser C, Krone SM. 1997. The genealogy of samples in models with selection. Genetics 145:519–534.
60. Nguyen LT, Schmidt HA, von Haeseler A, Minh BQ. 2015. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol. 32:268–274.
61. Nielsen R, Beaumont MA. 2009. Statistical inferences in phylogeography. Mol Ecol. 18:1034–1047.
62. Nielsen R, Wakeley J. 2001. Distinguishing migration from isolation: a Markov chain Monte Carlo approach. Genetics 158:885–896.
63. Nubel U, Dordel J, Kurt K, Strommenger B, Westh H, Shukla SK, Zemlickova H, Leblois R, Wirth T, Jombart T, et al. 2010. A timescale for evolution, population expansion, and spatial spread of an emerging clone of methicillin-resistant Staphylococcus aureus. PLoS Pathog. 6:e1000855.
64. O’Fallon BD, Seger J, Adler FR. 2010. A continuous-state coalescent and the impact of weak selection on the structure of gene genealogies. Mol Biol Evol. 27:1162–1172.
65. Ochman H, Whittam TS, Caugant DA, Selander RK. 1983. Enzyme polymorphism and genetic population structure in Escherichia coli and Shigella. J Gen Microbiol. 129:2715–2726.
66. Pannell JR. 2003. Coalescence in a metapopulation with recurrent local extinction and recolonization. Evolution 57:949–961.
67. Paradis E, Claude J, Strimmer K. 2004. APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20:289–290.
68. Pepperell CS, Casto AM, Kitchen A, Granka JM, Cornejo OE, Holmes EC, Birren B, Galagan J, Feldman MW. 2013. The role of selection in shaping diversity of natural M. tuberculosis populations. PLoS Pathog. 9:e1003543.
69. Perez-Losada M, Crandall KA, Zenilman J, Viscidi RP. 2007. Temporal trends in gonococcal population genetics in a high prevalence urban community. Infect Genet Evol. 7:271–278.
70. Perfeito L, Fernandes L, Mota C, Gordo I. 2007. Adaptive mutations in bacteria: high rate and small effects. Science 317:813–815.
71. Price MN, Dehal PS, Arkin AP. 2009. FastTree: computing large minimum evolution trees with profiles instead of a distance matrix. Mol Biol Evol. 26:1641–1650.
72. Prosperi M, Veras N, Azarian T, Rathore M, Nolan D, Rand K, Cook RL, Johnson J, Morris JG Jr, Salemi M. 2013. Molecular epidemiology of community-associated methicillin-resistant Staphylococcus aureus in the genomic era: a cross-sectional study. Sci Rep. 3:1902.
73. Przeworski M, Charlesworth B, Wall JD. 1999. Genealogies and weak purifying selection. Mol Biol Evol. 16:246–252.
74. Pybus OG, Rambaut A, Harvey PH. 2000. An integrated framework for the inference of viral population history from reconstructed genealogies. Genetics 155:1429–1437.
75. Ramos-Onsins SE, Rozas J. 2002. Statistical properties of new neutrality tests against population growth. Mol Biol Evol. 19:2092–2100.
76. Reynolds AP, Richards G, de la Iglesia B, Rayward-Smith VJ. 2006. Clustering rules: a comparison of partitioning and hierarchical clustering algorithms. J Math Model Algorithms. 5:475–504.
77. Rocha E, Danchin A. 2004. An analysis of determinants of amino acids substitution rates in bacterial proteins. Mol Biol Evol. 21:108–116.
78. Rocha E, Smith J, Hurst L, Holden M, Cooper J, Smith N, Feil E. 2006. Comparisons of dN/dS are time dependent for closely related bacterial genomes. J Theor Biol. 239:226–235.
79. Rocha EPC, Feil EJ. 2010. Mutational patterns cannot explain genome composition: are there any neutral sites in the genomes of bacteria? Plos Genetics 6:e1001104.
80. Roumagnac P, Weill FX, Dolecek C, Baker S, Brisse S, Chinh NT, Le TA, Acosta CJ, Farrar J, Dougan G, et al. 2006. Evolutionary history of Salmonella typhi. Science 314:1301–1304.
81. Sanchez-Buso L, Comas I, Jorques G, Gonzalez-Candelas F. 2014. Recombination drives genome evolution in outbreak-related Legionella pneumophila isolates. Nat Genet. 46:1205–1211.
82. Sarkar SF, Guttman DS. 2004. Evolution of the core genome of Pseudomonas syringae, a highly clonal, endemic plant pathogen. Appl Environ Microbiol. 70:1999–2012.
83. Schierup MH, Hein J. 2000. Consequences of recombination on traditional phylogenetic analysis. Genetics 156:879–891.
84. Schliep KP. 2011. phangorn: phylogenetic analysis in R. Bioinformatics 27:592–593.
85. Schmidt HA, Strimmer K, Vingron M, von Haeseler A. 2002. TREE-PUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics 18:502–504.
86. Sharp PM, Emery LR, Zeng K. 2010. Forces that influence the evolution of codon bias. Philos Trans R Soc Lond B Biol. 365:1203–1212.
87. Stegger M, Wirth T, Andersen PS, Skov RL, De Grassi A, Simoes PM, Tristan A, Petersen A, Aziz M, Kiil K, et al. 2014. Origin and evolution of European community-acquired methicillin-resistant Staphylococcus aureus. MBio 5:e01044–e01014.
88. Tajima F. 1989a. The effect of change in population size on DNA polymorphism. Genetics 123:597–601.
89. Tajima F. 1989b. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595.
90. Takeuchi N, Cordero OX, Koonin EV, Kaneko K. 2015. Gene-specific selective sweeps in bacteria and archaea caused by negative frequency-dependent selection. BMC Biol. 13:20.
91. Tatusova T, Ciufo S, Federhen S, Fedorov B, McVeigh R, O’Neill K, Tolstoy I, Zaslavsky L. 2015. Update on RefSeq microbial genomes resources. Nucleic Acids Res. 43:D599–D605.
92. Tazi L, Perez-Losada M, Gu W, Yang Y, Xue L, Crandall KA, Viscidi RP. 2010. Population dynamics of Neisseria gonorrhoeae in Shanghai, China: a comparative study. BMC Infect. Dis. 10:13.
93. Tellier A, Lemaire C. 2014. Coalescence 2.0: a multiple branching of recent theoretical developments and their applications. Mol Ecol. 23:2637–2652.
94. Tenaillon O, Skurnik D, Picard B, Denamur E. 2010. The population genetics of commensal Escherichia coli. Nat Rev Microbiol. 8:207–217.
95. Thornton K. 2005. Recombination and the properties of Tajima’s D in the context of approximate-likelihood calculation. Genetics 171:2143–2148.
96. Touchon M, Cury J, Yoon E-J, Krizova L, Cerqueira GC, Murphy C, Feldgarden M, Wortman J, Clermont D, Lambert T, et al. 2014. The genomic diversification of the whole acinetobacter genus: origins, mechanisms, and consequences. Genome Biol Evol. 6:2866–2882.
97. Touchon M, Hoede C, Tenaillon O, Barbe V, Baeriswyl S, Bidet P, Bingen E, Bonacorsi S, Bouchier C, Bouvet O, et al. 2009. Organised genome dynamics in the Escherichia coli species results in highly diverse adaptive paths. PLoS Genet. 5:e1000344.
98. Treangen TJ, Ambur OH, Tonjum T, Rocha EPC. 2008. The impact of the neisserial DNA uptake sequences on genome evolution and stability. Genome Biol. 9:R60.
99. Volz EM, Koelle K, Bedford T. 2013. Viral phylodynamics. PLoS Comput Biol. 9:e1002947.
100. Vos M, Didelot X. 2009. A comparison of homologous recombination rates in bacteria and archaea. ISME J. 3:199–208.
101. Wall JD. 1999. Recombination and the power of statistical tests of neutrality. Genet Res. 74:65–79.
102. Weinert LA, Chaudhuri RR, Wang J, Peters SE, Corander J, Jombart T, Baig A, Howell KJ, Vehkala M, Valimaki N, et al. 2015. Genomic signatures of human and animal disease in the zoonotic pathogen Streptococcus suis. Nat Commun. 6:6740.
103. Wielgoss S, Barrick JE, Tenaillon O, Cruveiller S, Chane-Woon-Ming B, Medigue C, Lenski RE, Schneider D. 2011. Mutation rate inferred from synonymous substitutions in a long-term evolution experiment with Escherichia coli. G3 1:183–186.
104. Williamson S, Orive ME. 2002. The genealogy of a sequence subject to purifying selection at multiple sites. Mol Biol Evol. 19:1376–1384.
105. Wirth T, Falush D, Lan R, Colles F, Mensa P, Wieler LH, Karch H, Reeves PR, Maiden MC, Ochman H, et al. 2006. Sex and virulence in Escherichia coli: an evolutionary perspective. Mol Microbiol. 60:1136–1151.
106. Wirth T, Morelli G, Kusecek B, van Belkum A, van der Schee C, Meyer A, Achtman M. 2007. The rise and spread of a new pathogen: seroresistant Moraxella catarrhalis. Genome Res. 17:1647–1656.
107. Wong VK, Baker S, Pickard DJ, Parkhill J, Page AJ, Feasey NA, Kingsley RA, Thomson NR, Keane JA, Weill FX, et al. 2015. Phylogeographical analysis of the dominant multidrug-resistant H58 clade of Salmonella Typhi identifies inter- and intracontinental transmission events. Nat Genet. 47:632–639.
108. Yang Z. 2007. PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol. 24:1586–1591.
109. Young LJ, Young J: 2013. Statistical ecology. New York: Springer Science & Business Media.
110. Zhou Z, McCann A, Weill FX, Blin C, Nair S, Wain J, Dougan G, Achtman M. 2014. Transient Darwinian selection in Salmonella enterica serovar Paratyphi A during 450 years of global spread of enteric fever. Proc Natl Acad Sci U S A. 111:12199–12204.