Section: Evolutionary Biology
Topic: Evolution, Genetics/Genomics, Population biology

How do monomorphic bacteria evolve? The Mycobacterium tuberculosis complex and the awkward population genetics of extreme clonality

Stritt, Christoph1, 2  ; Gagneux, Sebastien1, 2  
1 Swiss Tropical and Public Health Institute, Allschwil, Switzerland
2 University of Basel, Basel, Switzerland

Corresponding author(s): Stritt, Christoph (christoph.stritt@swisstph.ch); Gagneux, Sebastien (sebastien.gagneux@swisstph.ch)

10.24072/pcjournal.322 - Peer Community Journal, Volume 3 (2023), article no. e92.

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Exchange of genetic material through sexual reproduction or horizontal gene transfer is ubiquitous in nature. Among the few outliers that rarely recombine and mainly evolve by de novo mutation are a group of deadly bacterial pathogens, including the causative agents of leprosy, plague, typhoid, and tuberculosis. The interplay of evolutionary processes is poorly understood in these organisms. Population genetic methods allowing to infer mutation, recombination, genetic drift, and natural selection make strong assumptions that are difficult to reconcile with clonal reproduction and fully linked genomes consisting mainly of coding regions. In this review, we highlight the challenges of extreme clonality by discussing population genetic inference with the Mycobacterium tuberculosis complex, a group of closely related obligate bacterial pathogens of mammals. We show how uncertainties underlying quantitative models and verbal arguments affect previous conclusions about the way these organisms evolve. A question mark remains behind various quantities of applied and theoretical interest, including mutation rates, the interpretation of nonsynonymous polymorphisms, or the role of genetic bottlenecks. Looking ahead, we discuss how new tools for evolutionary simulations, going beyond the traditional Wright-Fisher framework, promise a more rigorous treatment of basic evolutionary processes in clonal bacteria.

Published online:
DOI: 10.24072/pcjournal.322
Type: Research article
Mots-clés : clonality, mutation, recombination, genetic drift, natural selection, simulation

Stritt, Christoph 1, 2; Gagneux, Sebastien 1, 2

1 Swiss Tropical and Public Health Institute, Allschwil, Switzerland
2 University of Basel, Basel, Switzerland
License: CC-BY 4.0
Copyrights: The authors retain unrestricted copyrights and publishing rights 
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Stritt, Christoph; Gagneux, Sebastien. How do monomorphic bacteria evolve? The Mycobacterium tuberculosis complex and the awkward population genetics of extreme clonality. Peer Community Journal, Volume 3 (2023), article  no. e92. doi : 10.24072/pcjournal.322. https://peercommunityjournal.org/articles/10.24072/pcjournal.322/

PCI peer reviews and recommendation, and links to data, scripts, code and supplementary information: 10.24072/pci.evolbiol.100644

Conflict of interest of the recommender and peer reviewers:
The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article.

[1] Achtman, M. Insights from genomic comparisons of genetically monomorphic bacterial pathogens, Philosophical Transactions of the Royal Society B: Biological Sciences, Volume 367 (2012) no. 1590, pp. 860-867 | DOI

[2] Achtman, M. Evolution, population structure, and phylogeography of genetically monomorphic bacterial pathogens, Annual Review of Microbiology, Volume 62 (2008), pp. 53-70 | DOI

[3] Allen, A. C.; Malaga, W.; Gaudin, C.; Volle, A.; Moreau, F.; Hassan, A.; Astarie-Dequeker, C.; Peixoto, A.; Antoine, R.; Pawlik, A.; Frigui, W.; Berrone, C.; Brosch, R.; Supply, P.; Guilhot, C. Parallel in vivo experimental evolution reveals that increased stress resistance was key for the emergence of persistent tuberculosis bacilli, Nature Microbiology, Volume 6 (2021) no. 8, pp. 1082-1093 | DOI

[4] Allen, J. M.; Light, J. E.; Perotti, M. A.; Braig, H. R.; Reed, D. L. Mutational Meltdown in Primary Endosymbionts: Selection Limits Muller's Ratchet, PLoS ONE, Volume 4 (2009) no. 3, p. e4969 | DOI

[5] Andersson, S. G.; Sharp, P. M. Codon usage in the Mycobacterium tuberculosis complex, Microbiology, Volume 142 (1996) no. 4, pp. 915-925 | DOI

[6] Balbi, K. J.; Rocha, E. P.; Feil, E. J. The temporal dynamics of slightly deleterious mutations in Escherichia coli and Shigella spp., Molecular Biology and Evolution, Volume 26 (2009) no. 2, pp. 345-355 | DOI

[7] Bobay, L. M.; Ochman, H. Impact of recombination on the base composition of bacteria and archaea, Molecular Biology and Evolution, Volume 34 (2017) no. 10, pp. 2627-2636 | DOI

[8] Bobay, L. M.; Traverse, C. C.; Ochman, H. Impermanence of bacterial clones, PNAS, Volume 112 (2015) no. 29, pp. 8893-8900 | DOI

[9] Bobay, L.-M.; Ochman, H. Factors driving effective population size and pan-genome evolution in bacteria, BMC Evolutionary Biology, Volume 18 (2018) no. 1, pp. 1-12 | DOI

[10] Boritsch, E. C.; Khanna, V.; Pawlik, A.; Honoré, N.; Navas, V. H.; Ma, L.; Bouchier, C.; Seemann, T.; Supply, P.; Stinear, T. P.; Brosch, R. Key experimental evidence of chromosomal DNA transfer among selected tuberculosis-causing mycobacteria, PNAS, Volume 113 (2016) no. 35, pp. 9876-9881 | DOI

[11] Bos, K. I.; Harkins, K. M.; Herbig, A.; Coscolla, M.; Weber, N.; Comas, I.; Forrest, S. A.; Bryant, J. M.; Harris, S. R.; Schuenemann, V. J.; Campbell, T. J.; Majander, K.; Wilbur, A. K.; Guichon, R. A.; Steadman, D. L.; Cook, D. C.; Niemann, S.; Behr, M. A.; Zumarraga, M.; Bastida, R.; Huson, D.; Nieselt, K.; Young, D.; Parkhill, J.; Buikstra, J. E.; Gagneux, S.; Stone, A. C.; Krause, J. Pre-Columbian mycobacterial genomes reveal seals as a source of New World human tuberculosis, Nature, Volume 514 (2014) no. 7253, pp. 494-497 | DOI

[12] Brites, D.; Gagneux, S. Co-evolution of Mycobacterium tuberculosis and Homo sapiens, Immunological Reviews, Volume 264 (2015) no. 1, pp. 6-24 | DOI

[13] Brites, D.; Loiseau, C.; Menardo, F.; Borrell, S.; Boniotti, M. B.; Warren, R.; Dippenaar, A.; Parsons, S. D. C.; Beisel, C.; Behr, M. A.; Fyfe, J. A.; Coscolla, M.; Gagneux, S. A new phylogenetic framework for the animal-adapted Mycobacterium tuberculosis complex, Frontiers in Microbiology, Volume 9 (2018), p. 2820 | DOI

[14] Casadevall, A. Evolution of intracellular pathogens, Annual Review of Microbiology, Volume 62 (2008), pp. 19-33 | DOI

[15] Charlesworth, B.; Morgan, M. T.; Charlesworth, D. The effect of deleterious mutations on neutral molecular variation, Genetics, Volume 134 (1993) no. 4, pp. 1289-1303 | DOI

[16] Charlesworth, B. Effective population size and patterns of molecular evolution and variation, Nature Reviews Genetics, Volume 10 (2009) no. 3, pp. 195-205 | DOI

[17] Charlesworth, B. The effects of deleterious mutations on evolution at linked sites, Genetics, Volume 190 (2012) no. 1, pp. 5-22 | DOI

[18] Chiner-Oms, Á.; López, M. G.; Moreno-Molina, M.; Furió, V.; Comas, I. Gene evolutionary trajectories in Mycobacterium tuberculosis reveal temporal signs of selection., PNAS, Volume 119 (2022) no. 17, p. e2113600119 | DOI

[19] Chiner-Oms, Á.; Sánchez-Busó, L.; Corander, J.; Gagneux, S.; Harris, S.; Young, D.; González-Candelas, F.; Comas, I. Genomic determinants of speciation and spread of the Mycobacterium tuberculosis complex, Science Advances, Volume 5 (2019) no. 6, p. eaaw3307 | DOI

[20] Clark, R. R.; Lapierre, P.; Lasek-Nesselquist, E.; Gray, T. A.; Derbyshire, K. M. A polymorphic gene within the Mycobacterium smegmatis esx1 locus determines mycobacterial self-identity and conjugal compatibility, mBio, Volume 13 (2022) no. 2, pp. e00213-22 | DOI

[21] Colangeli, R.; Gupta, A.; Vinhas, S. A.; Chippada Venkata, U. D.; Kim, S.; Grady, C.; Jones-López, E. C.; Soteropoulos, P.; Palaci, M.; Marques-Rodrigues, P.; Salgame, P.; Ellner, J. J.; Dietze, R.; Alland, D. Mycobacterium tuberculosis progresses through two phases of latent infection in humans, Nature Communications, Volume 11 (2020) no. 1, p. 4870 | DOI

[22] Cole, S.; Eiglmeier, K.; Parkhill, J.; James, K.; Thomson, N.; Wheeler, P.; Honore, N.; Garnier, T.; Churcher, C.; Harris, D.; others Massive gene decay in the leprosy bacillus, Nature, Volume 409 (2001) no. 6823, pp. 1007-1011 | DOI

[23] Cole, S. T.; Brosch, R.; Parkhill, J.; Garnier, T.; Churcher, C.; Harris, D.; Gordon, S. V.; Eiglmeier, K.; Gas, S.; Barry, C. E.; Tekaia, F.; Badcock, K.; Basham, D.; Brown, D.; Chillingworth, T.; Connor, R.; Davies, R.; Devlin, K.; Feltwell, T.; Gentles, S.; Hamlin, N.; Holroyd, S.; Hornsby, T.; Jagels, K.; Krogh, A.; McLean, J.; Moule, S.; Murphy, L.; Oliver, K.; Osborne, J.; Quail, M. A.; Rajandream, M.-A.; Rogers, J.; Rutter, S.; Seeger, K.; Skelton, J.; Squares, R.; Squares, S.; Sulston, J. E.; Taylor, K.; Whitehead, S.; Barrell, B. G. Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence, Nature, Volume 393 (1998) no. 6685, pp. 537-544 | DOI

[24] Comas, I.; Borrell, S.; Roetzer, A.; Rose, G.; Malla, B.; Kato-Maeda, M.; Galagan, J.; Niemann, S.; Gagneux, S. Whole-genome sequencing of rifampicin-resistant Mycobacterium tuberculosis strains identifies compensatory mutations in RNA polymerase genes, Nature Genetics, Volume 44 (2012) no. 1, pp. 106-110 | DOI

[25] Comas, I.; Coscolla, M.; Luo, T.; Borrell, S.; Holt, K. E.; Kato-Maeda, M.; Parkhill, J.; Malla, B.; Berg, S.; Thwaites, G.; Yeboah-Manu, D.; Bothamley, G.; Mei, J.; Wei, L.; Bentley, S.; Harris, S. R.; Niemann, S.; Diel, R.; Aseffa, A.; Gao, Q.; Young, D.; Gagneux, S. Out-of-Africa migration and Neolithic coexpansion of Mycobacterium tuberculosis with modern humans, Nature Genetics, Volume 45 (2013) no. 10, pp. 1176-1182 | DOI

[26] Comas, I.; Homolka, S.; Niemann, S.; Gagneux, S. Genotyping of genetically monomorphic bacteria: DNA sequencing in Mycobacterium tuberculosis highlights the limitations of current methodologies, PLoS ONE, Volume 4 (2009) no. 11 | DOI

[27] Copin, R.; Wang, X.; Louie, E.; Escuyer, V.; Coscolla, M.; Gagneux, S.; Palmer, G. H.; Ernst, J. D. Within-host evolution selects for a dominant genotype of Mycobacterium tuberculosis while T cells increase pathogen genetic diversity, PLoS Pathogens, Volume 12 (2016) no. 12, p. e1006111 | DOI

[28] Crook, D. W.; Rodrigues, C.; Ismail, N. A.; Mistry, N.; Iqbal, Z.; Merker, M.; Moore, D.; Walker, A. S.; Thwaites, G.; Niemann, S.; Wilson, J.; Cirillo, D. M.; Lachapelle, A. S.; Clifton, D. A.; Timothy, E.; Peto, A.; Hunt, M.; Knaggs, J.; Fowler, P. W.; Earle, S. G.; Grazian, C. Genome-wide association studies of global Mycobacterium tuberculosis resistance to 13 antimicrobials in 10,228 genomes identify new resistance mechanisms, PLoS Biology, Volume 20 (2022) no. 8, p. e3001755 | DOI

[29] Cury, J.; Haller, B. C.; Achaz, G.; Jay, F. Simulation of bacterial populations with SLiM, Peer Community Journal, Volume 2 (2022) | DOI

[30] Cvijović, I.; Good, B. H.; Desai, M. M. The effect of strong purifying selection on genetic diversity, Genetics, Volume 209 (2018) no. 4, pp. 1235-1278 | DOI

[31] Davies, J.; Davis, D. Origins and evolution of antibiotic resistance., Microbiology and Molecular Biology Reviews, Volume 74 (2010) no. 3, pp. 417-433 | DOI

[32] De Miranda, A. B.; Alvarez-Valin, F.; Jabbari, K.; Degrave, W. M.; Bernardi, G. Gene expression, amino acid conservation, and hydrophobicity are the main factors shaping codon preferences in Mycobacterium tuberculosis and Mycobacterium leprae, Journal of Molecular Evolution, Volume 50 (2000) no. 1, pp. 45-55 | DOI

[33] Denamur, E.; Clermont, O.; Bonacorsi, S.; Gordon, D. The population genetics of pathogenic Escherichia coli, Nature Reviews Microbiology, Volume 19 (2021) no. 1, pp. 37-54 | DOI

[34] Duchêne, S.; Holt, K. E.; Weill, F. X.; Le Hello, S.; Hawkey, J.; Edwards, D. J.; Fourment, M.; Holmes, E. C. Genome-scale rates of evolutionary change in bacteria, Microbial Genomics, Volume 2 (2016) no. 11, p. e000094 | DOI

[35] Duret, L.; Galtier, N. Biased gene conversion and the evolution of mammalian genomic landscapes, Annual Review of Genomics and Human Genetics, Volume 10 (2009), pp. 285-311 | DOI

[36] Dutta, N. K.; Karakousis, P. C. Latent tuberculosis infection: myths, models, and molecular mechanisms, Microbiology and Molecular Biology Reviews, Volume 78 (2014) no. 3, pp. 343-371 | DOI

[37] Emerson, B. C.; Hickerson, M. J. Lack of support for the time-dependent molecular evolution hypothesis, Molecular Ecology, Volume 24 (2015) no. 4, pp. 702-709 | DOI

[38] Eyre-Walker, A.; Keightley, P. D. The distribution of fitness effects of new mutations, Nature Reviews Genetics, Volume 8 (2007) no. 8, pp. 610-618 | DOI

[39] Farhat, M. R.; Shapiro, B. J.; Kieser, K. J.; Sultana, R.; Jacobson, K. R.; Victor, T. C.; Warren, R. M.; Streicher, E. M.; Calver, A.; Sloutsky, A.; Kaur, D.; Posey, J. E.; Plikaytis, B.; Oggioni, M. R.; Gardy, J. L.; Johnston, J. C.; Rodrigues, M.; Tang, P. K.; Kato-Maeda, M.; Borowsky, M. L.; Muddukrishna, B.; Kreiswirth, B. N.; Kurepina, N.; Galagan, J.; Gagneux, S.; Birren, B.; Rubin, E. J.; Lander, E. S.; Sabeti, P. C.; Murray, M. Genomic analysis identifies targets of convergent positive selection in drug-resistant Mycobacterium tuberculosis, Nature Genetics, Volume 45 (2013) no. 10, pp. 1183-1189 | DOI

[40] Felsenstein, J. The evolutionary advantage of recombination, Genetics, Volume 83 (1974) no. 4, pp. 845-859 | DOI

[41] Fishbein, S.; van Wyk, N.; Warren, R. M.; Sampson, S. L. Phylogeny to function: PE/PPE protein evolution and impact on Mycobacterium tuberculosis pathogenicity, Molecular Microbiology, Volume 96 (2015) no. 5, pp. 901-916 | DOI

[42] Fisher, R. A. The Genetical Theory of Natural Selection, Clarendon Press, 1930

[43] Fitzgerald, D. M.; Rosenberg, S. M. What is mutation? A chapter in the series: how microbes “jeopardize” the modern synthesis, PLoS Genetics, Volume 15 (2019) no. 4, p. e1007995 | DOI

[44] Ford, C. B.; Lin, P. L.; Chase, M. R.; Shah, R. R.; Iartchouk, O.; Galagan, J.; Mohaideen, N.; Ioerger, T. R.; Sacchettini, J. C.; Lipsitch, M.; Flynn, J. L.; Fortune, S. M. Use of whole genome sequencing to estimate the mutation rate of Mycobacterium tuberculosis during latent infection, Nature Genetics, Volume 43 (2011) no. 5, pp. 482-488 | DOI

[45] Ford, C. B.; Shah, R. R.; Maeda, M. K.; Gagneux, S.; Murray, M. B.; Cohen, T.; Johnston, J. C.; Gardy, J.; Lipsitch, M.; Fortune, S. M. Mycobacterium tuberculosis mutation rate estimates from different lineages predict substantial differences in the emergence of drug-resistant tuberculosis, Nature Genetics, Volume 45 (2013) no. 7, pp. 784-790 | DOI

[46] Gagneux, S. Ecology and evolution of Mycobacterium tuberculosis, Nature Reviews Microbiology, Volume 16 (2018) no. 4, pp. 202-213 | DOI

[47] Gagneux, S.; DeRiemer, K.; Van, T.; Kato-Maeda, M.; De Jong, B. C.; Narayanan, S.; Nicol, M.; Niemann, S.; Kremeri, K.; Gutierrez, M. C.; Hilty, M.; Hopewell, P. C.; Small, P. M. Variable host-pathogen compatibility in Mycobacterium tuberculosis, PNAS, Volume 103 (2006) no. 8, pp. 2869-2873 | DOI

[48] Galtier, N.; Enard, D.; Radondy, Y.; Bazin, E.; Belkhir, K. Mutation hot spots in mammalian mitochondrial DNA, Genome Research, Volume 16 (2006) no. 2, pp. 215-222 | DOI

[49] Gibson, B.; Wilson, D. J.; Feil, E.; Eyre-Walker, A. The distribution of bacterial doubling times in the wild, Proceedings of the Royal Society B: Biological Sciences, Volume 285 (2018) no. 1880 | DOI

[50] Gillespie, J. H. Population Genetics – A Concise Guide, The Johns Hopkins University Press, 2004

[51] Godfroid, M.; Dagan, T.; Kupczok, A. Recombination signal in Mycobacterium tuberculosis stems from reference-guided assemblies and alignment artefacts, Genome Biology and Evolution, Volume 10 (2018) no. 8, pp. 1920-1926 | DOI

[52] Gray, T. A.; Derbyshire, K. M. Blending genomes: distributive conjugal transfer in mycobacteria, a sexier form of HGT, Molecular Microbiology, Volume 108 (2018) no. 6, pp. 601-613 | DOI

[53] Guerrini, V.; Subbian, S.; Santucci, P.; Canaan, S.; Gennaro, M. L.; Pozzi, G. Experimental evolution of Mycobacterium tuberculosis in human macrophages results in low-frequency mutations not associated with selective advantage, PLoS ONE, Volume 11 (2016) no. 12, pp. 1-15 | DOI

[54] Gygli, S. M.; Borrell, S.; Trauner, A.; Gagneux, S. Antimicrobial resistance in Mycobacterium tuberculosis: mechanistic and evolutionary perspectives, FEMS Microbiology Reviews, Volume 41 (2017) no. 3, pp. 354-373 | DOI

[55] Haller, B. C.; Messer, P. W. SLiM 3: Forward Genetic Simulations Beyond the Wright-Fisher Model, Molecular Biology and Evolution, Volume 36 (2019) no. 3, pp. 632-637 | DOI

[56] Hanage, W. P. Not so simple after all: bacteria, their population genetics, and recombination, Cold Spring Harbor Perspectives in Biology, Volume 8 (2016) no. 7 | DOI

[57] Hedge, J.; Wilson, D. J. Bacterial phylogenetic reconstruction from whole genomes is robust to recombination but demographic inference is not, mBio, Volume 5 (2014) no. 6, pp. 5-8 | DOI

[58] Heller, R.; Chikhi, L.; Siegismund, H. R. The confounding effect of population structure on Bayesian skyline plot inferences of demographic history, PLoS ONE, Volume 8 (2013) no. 5, p. e62992 | DOI

[59] Hershberg, R.; Lipatov, M.; Small, P. M.; Sheffer, H.; Niemann, S.; Homolka, S.; Roach, J. C.; Kremer, K.; Petrov, D. A.; Feldman, M. W.; Gagneux, S. High functional diversity in Mycobacterium tuberculosis driven by genetic drift and human demography, PLoS Biology, Volume 6 (2008) no. 12, pp. 2658-2671 | DOI

[60] Hershberg, R.; Petrov, D. A. Selection on codon bias, Annual Review of Genetics, Volume 42 (2008), pp. 287-299 | DOI

[61] Hershberg, R.; Petrov, D. A. Evidence that mutation is universally biased towards AT in bacteria, PLoS Genetics, Volume 6 (2010) no. 9 | DOI

[62] Hildebrand, F.; Meyer, A.; Eyre-Walker, A. Evidence of selection upon genomic GC-content in bacteria, PLoS Genetics, Volume 6 (2010) no. 9 | DOI

[63] Ho, S. Y.; Duchêne, S.; Molak, M.; Shapiro, B. Time-dependent estimates of molecular evolutionary rates: evidence and causes, Molecular Ecology, Volume 24 (2015) no. 24, pp. 6007-6012 | DOI

[64] Ho, S. Y.; Lanfear, R.; Bromham, L.; Phillips, M. J.; Soubrier, J.; Rodrigo, A. G.; Cooper, A. Time-dependent rates of molecular evolution, Molecular Ecology, Volume 20 (2011) no. 15, pp. 3087-3101 | DOI

[65] Ho, S. Y. W.; Shapiro, B. Skyline-plot methods for estimating demographic history from nucleotide sequences, Molecular Ecology Resources, Volume 11 (2011) no. 3, pp. 423-434 | DOI

[66] Hoban, S.; Bertorelle, G.; Gaggiotti, O. E. Computer simulations: tools for population and evolutionary genetics, Nature Reviews Genetics, Volume 13 (2012) no. 2, pp. 110-122 | DOI

[67] Johri, P.; Aquadro, C. F.; Beaumont, M.; Charlesworth, B.; Excoffier, L.; Eyre-Walker, A.; Keightley, P. D.; Lynch, M.; McVean, G.; Payseur, B. A.; Pfeifer, S. P.; Stephan, W.; Jensen, J. D. Recommendations for improving statistical inference in population genomics, PLoS Biology, Volume 20 (2022) no. 5, p. e3001669 | DOI

[68] Kaiser, V. B.; Charlesworth, B. The effects of deleterious mutations on evolution in non-recombining genomes, Trends in Genetics, Volume 25 (2009) no. 1, pp. 9-12 | DOI

[69] Kapur, V.; Whittam, T. S.; Musser, J. M. Is Mycobacterium tuberculosis 15,000 years old?, Journal of Infectious Diseases, Volume 170 (1994) no. 5, pp. 1348-1349 | DOI

[70] Karboul, A.; Mazza, A.; Gey Van Pittius, N. C.; Ho, J. L.; Brousseau, R.; Mardassi, H. Frequent homologous recombination events in Mycobacterium tuberculosis PE/PPE multigene families: potential role in antigenic variability, Journal of Bacteriology, Volume 190 (2008) no. 23, pp. 7838-7846 | DOI

[71] Katju, V.; Bergthorsson, U. Old trade, new tricks: Insights into the spontaneous mutation process from the partnering of classical mutation accumulation experiments with high-throughput genomic approaches, Genome Biology and Evolution, Volume 11 (2019) no. 1, pp. 136-165 | DOI

[72] Katz, Y. Against storytelling of scientific results, Nature Methods, Volume 10 (2013) no. 11, p. 1045-1045 | DOI

[73] Kay, G. L.; Sergeant, M. J.; Zhou, Z.; Chan, J. Z.; Millard, A.; Quick, J.; Szikossy, I.; Pap, I.; Spigelman, M.; Loman, N. J.; Achtman, M.; Donoghue, H. D.; Pallen, M. J. Eighteenth-century genomes show that mixed infections were common at time of peak tuberculosis in Europe, Nature Communications, Volume 6 (2015) | DOI

[74] Kimura, M. The Neutral Theory of Molecular Evolution, Cambridge University Press, 1983

[75] Kuo, C. H.; Moran, N. A.; Ochman, H. The consequences of genetic drift for bacterial genome complexity, Genome Research, Volume 19 (2009) no. 8, pp. 1450-1454 | DOI

[76] Lanfear, R.; Kokko, H.; Eyre-Walker, A. Population size and the rate of evolution, Trends in Ecology & Evolution, Volume 29 (2014) no. 1, pp. 33-41 | DOI

[77] Lapierre, M.; Blin, C.; Lambert, A.; Achaz, G.; Rocha, E. P. The impact of selection, gene conversion, and biased sampling on the assessment of microbial demography, Molecular Biology and Evolution, Volume 33 (2016) no. 7, pp. 1711-1725 | DOI

[78] Lassalle, F.; Périan, S.; Bataillon, T.; Nesme, X.; Duret, L.; Daubin, V. GC-content evolution in bacterial genomes: the biased gene conversion hypothesis expands, PLoS Genetics, Volume 11 (2015) no. 2, p. e1004941 | DOI

[79] Lawrence, J. G.; Hendrix, R. W.; Casjens, S. Where are the pseudogenes in bacterial genomes?, Trends in Microbiology, Volume 9 (2001) no. 11, pp. 535-540 | DOI

[80] Liu, Q.; Liu, H.; Shi, L.; Gan, M.; Zhao, X.; Lyu, L.-d.; Takiff, H. E. Local adaptation of Mycobacterium tuberculosis on the Tibetan Plateau, PNAS, Volume 118 (2021) no. 17, p. e2017831118 | DOI

[81] Liu, Q.; Wei, J.; Li, Y.; Wang, M.; Su, J.; Lu, Y.; López, M. G.; Qian, X.; Zhu, Z.; Wang, H.; Gan, M.; Jiang, Q.; Fu, Y.-X.; Takiff, H. E.; Comas, I.; Li, F.; Lu, X.; Fortune, S. M.; Gao, Q. Mycobacterium tuberculosis clinical isolates carry mutational signatures of host immune environments, Science Advances, Volume 6 (2020) no. 22, p. eaba4901 | DOI

[82] Liu, X.; Gutacker, M. M.; Musser, J. M.; Fu, Y. X. Evidence for recombination in Mycobacterium tuberculosis, Journal of Bacteriology, Volume 188 (2006) no. 23, pp. 8169-8177 | DOI

[83] Lynch, M. The Origins of Genome Architecture, Sinauer Associates Sunderland, MA, 2007

[84] Madacki, J.; Orgeur, M.; Mas Fiol, G.; Frigui, W.; Ma, L.; Brosch, R. ESX-1-Independent horizontal gene transfer by Mycobacterium tuberculosis complex strains, mBio, Volume 12 (2021) no. 3, pp. 1-19 | DOI

[85] Martin, C. J.; Cadena, A. M.; Leung, V. W.; Lin, P. L.; Maiello, P.; Hicks, N.; Chase, M. R.; Flynn, J. A. L.; Fortune, S. M. Digitally barcoding Mycobacterium tuberculosis reveals in vivo infection dynamics in the macaque model of tuberculosis, mBio, Volume 8 (2017) no. 3, pp. 1-12 | DOI

[86] Martin, D. P.; Lemey, P.; Posada, D. Analysing recombination in nucleotide sequences, Molecular Ecology Resources, Volume 11 (2011) no. 6, pp. 943-955 | DOI

[87] Maynard Smith, J. Do bacteria have population genetics?, Population genetics of bacteria: Symposium 52, Cambridge University Press, 1995, pp. 1-12

[88] Maynard Smith, J.; Smith, N. H.; O'Rourke, M.; Spratt, B. G. How clonal are bacteria?, PNAS, Volume 90 (1993) no. 10, pp. 4384-4388 | DOI

[89] McEvoy, C. R.; Falmer, A. A.; van Pittius, N. C.; Victor, T. C.; van Helden, P. D.; Warren, R. M. The role of IS6110 in the evolution of Mycobacterium tuberculosis, Tuberculosis, Volume 87 (2007) no. 5, pp. 393-404 | DOI

[90] Mcgrath, M.; Gey van Pittius, N. C.; Van Helden, P. D.; Warren, R. M.; Warner, D. F. Mutation rate and the emergence of drug resistance in Mycobacterium tuberculosis, Journal of Antimicrobial Chemotherapy, Volume 69 (2014) no. 2, pp. 292-302 | DOI

[91] Membrebe, J. V.; Suchard, M. A.; Rambaut, A.; Baele, G.; Lemey, P.; Thorne, J. Bayesian inference of evolutionary histories under time-dependent substitution rates, Molecular Biology and Evolution, Volume 36 (2019) no. 8, pp. 1793-1803 | DOI

[92] Menardo, F.; Gagneux, S.; Freund, F. Multiple merger genealogies in outbreaks of Mycobacterium tuberculosis, Molecular Biology and Evolution, Volume 38 (2021) no. 1, pp. 290-306 | DOI

[93] Menardo, F.; Duchêne, S.; Brites, D.; Gagneux, S. The molecular clock of Mycobacterium tuberculosis, PLoS Pathogens, Volume 15 (2019) no. 9, p. e1008067 | DOI

[94] Menardo, F.; Rutaihwa, L. K.; Zwyer, M.; Borrell, S.; Comas, I.; Conceição, E. C.; Coscolla, M.; Cox, H.; Joloba, M.; Dou, H. Y.; Feldmann, J.; Fenner, L.; Fyfe, J.; Gao, Q.; de Viedma, D. G.; Garcia-Basteiro, A. L.; Gygli, S. M.; Hella, J.; Hiza, H.; Jugheli, L.; Kamwela, L.; Kato-Maeda, M.; Liu, Q.; Ley, S. D.; Loiseau, C.; Mahasirimongkol, S.; Malla, B.; Palittapongarnpim, P.; Rakotosamimanana, N.; Rasolofo, V.; Reinhard, M.; Reither, K.; Sasamalo, M.; Duarte, R. S.; Sola, C.; Suffys, P.; Lima, K. V. B.; Yeboah-Manu, D.; Beisel, C.; Brites, D.; Gagneux, S. Local adaptation in populations of Mycobacterium tuberculosis endemic to the Indian Ocean Rim, F1000Research (2021) | DOI

[95] Merker, M.; Rasigade, J.-P.; Barbier, M.; Cox, H.; Feuerriegel, S.; Kohl, T. A.; Shitikov, E.; Klaos, K.; Gaudin, C.; Antoine, R.; Diel, R.; Borrell, S.; Gagneux, S.; Nikolayevskyy, V.; Andres, S.; Crudu, V.; Supply, P.; Niemann, S.; Wirth, T. Transcontinental spread and evolution of Mycobacterium tuberculosis W148 European/Russian clade toward extensively drug resistant tuberculosis, Nature Communications, Volume 13 (2022) no. 1, p. 5105 | DOI

[96] Merrikh, C. N.; Merrikh, H. Gene inversion potentiates bacterial evolvability and virulence, Nature Communications, Volume 9 (2018) no. 1 | DOI

[97] Molina, N.; Van Nimwegen, E. Universal patterns of purifying selection at noncoding positions in bacteria, Genome Research, Volume 18 (2008) no. 1, pp. 148-160 | DOI

[98] Möller, S.; du Plessis, L.; Stadler, T. Impact of the tree prior on estimating clock rates during epidemic outbreaks, PNAS, Volume 115 (2018) no. 16, pp. 4200-4205 | DOI

[99] Monot, M.; Honoré, N.; Garnier, T.; Zidane, N.; Sherafi, D.; Paniz-Mondolfi, A.; Matsuoka, M.; Taylor, G. M.; Donoghue, H. D.; Bouwman, A.; Mays, S.; Watson, C.; Lockwood, D.; Khamesipour, A.; Dowlati, Y.; Jianping, S.; Rea, T. H.; Vera-Cabrera, L.; Stefani, M. M.; Banu, S.; MacDonald, M.; Sapkota, B. R.; Spencer, J. S.; Thomas, J.; Harshman, K.; Singh, P.; Busso, P.; Gattiker, A.; Rougemont, J.; Brennan, P. J.; Cole, S. T. Comparative genomic and phylogeographic analysis of Mycobacterium leprae, Nature Genetics, Volume 41 (2009) no. 12, pp. 1282-1289 | DOI

[100] Morales-Arce, A. Y.; Harris, R. B.; Stone, A. C.; Jensen, J. D. Evaluating the contributions of purifying selection and progeny-skew in dictating within-host Mycobacterium tuberculosis evolution, Evolution, Volume 74 (2020) no. 5, pp. 992-1001 | DOI

[101] Morales-Arce, A. Y.; Sabin, S. J.; Stone, A. C.; Jensen, J. D. The population genomics of within-host Mycobacterium tuberculosis, Heredity, Volume 126 (2021) no. 1, pp. 1-9 | DOI

[102] Moran, N. A. Accelerated evolution and Muller's rachet in endosymbiotic bacteria, PNAS, Volume 93 (1996) no. 7, pp. 2873-2878 | DOI

[103] Moreno-Molina, M.; Shubladze, N.; Khurtsilava, I.; Avaliani, Z.; Bablishvili, N.; Torres-Puente, M.; Villamayor, L.; Gabrielian, A.; Rosenthal, A.; Vilaplana, C.; Gagneux, S.; Kempker, R. R.; Vashakidze, S.; Comas, I. Genomic analyses of Mycobacterium tuberculosis from human lung resections reveal a high frequency of polyclonal infections, Nature Communications, Volume 12 (2021) no. 1, p. 2716 | DOI

[104] Mortimer, T. D.; Weber, A. M.; Pepperell, C. S. Signatures of selection at drug resistance loci in Mycobacterium tuberculosis, mSystems, Volume 8 (2017) no. 2, pp. 1-11 | DOI

[105] Mulholland, C. V.; Shockey, A. C.; Aung, H. L.; Cursons, R. T.; O’Toole, R. F.; Gautam, S. S.; Brites, D.; Gagneux, S.; Roberts, S. A.; Karalus, N.; Cook, G. M.; Pepperell, C. S.; Arcus, V. L. Dispersal of Mycobacterium tuberculosis driven by historical European trade in the South Pacific, Frontiers in Microbiology, Volume 10 (2019), pp. 1-13 | DOI

[106] Muller, H. J. The relation of recombination to mutational advance, Mutation Research - Fundamental and Molecular Mechanisms of Mutagenesis, Volume 1 (1964) no. 1, pp. 2-9 | DOI

[107] Naito, M.; Pawlowska, T. E. Defying Muller’s ratchet: ancient heritable endobacteria escape extinction through retention of recombination and genome plasticity, mBio, Volume 7 (2016) no. 3, pp. e02057-15 | DOI

[108] Namouchi, A.; Didelot, X.; Schöck, U.; Gicquel, B.; Rocha, E. P. After the bottleneck: genome-wide diversification of the Mycobacterium tuberculosis complex by mutation, recombination, and natural selection, Genome Research, Volume 22 (2012) no. 4, pp. 721-734 | DOI

[109] Neher, R. A. Genetic draft, selective interference, and population genetics of rapid adaptation, Annual Review of Ecology, Evolution, and Systematics, Volume 44 (2013), pp. 195-215 | DOI

[110] O'Neill, M. B.; Shockey, A.; Zarley, A.; Aylward, W.; Eldholm, V.; Kitchen, A.; Pepperell, C. S. Lineage specific histories of Mycobacterium tuberculosis dispersal in Africa and Eurasia, Molecular Ecology, Volume 28 (2019) no. 13, pp. 3241-3256 | DOI

[111] O’Neill, M. B.; Mortimer, T. D.; Pepperell, C. S. Diversity of Mycobacterium tuberculosis across Evolutionary Scales, PLOS Pathogens, Volume 11 (2015) no. 11 | DOI

[112] Orme, I. M. A new unifying theory of the pathogenesis of tuberculosis, Tuberculosis, Volume 94 (2014) no. 1, pp. 8-14 | DOI

[113] Outhred, A. C.; Gurjav, U.; Jelfs, P.; McCallum, N.; Wang, Q.; Hill-Cawthorne, G. A.; Marais, B. J.; Sintchenko, V. Extensive homoplasy but no evidence of convergent evolution of repeat numbers at MIRU loci in modern Mycobacterium tuberculosis lineages, Frontiers in Public Health, Volume 8 (2020), pp. 1-12 | DOI

[114] Pan, A.; Dutta, C.; Das, J. Codon usage in highly expressed genes of Haemophillus influenzae and Mycobacterium tuberculosis: translational selection versus mutational bias, Gene, Volume 215 (1998) no. 2, pp. 405-413 | DOI

[115] Payne, J. L.; Menardo, F.; Trauner, A.; Borrell, S.; Gygli, S. M.; Loiseau, C.; Gagneux, S.; Hall, A. R. Transition bias influences the evolution of antibiotic resistance in Mycobacterium tuberculosis, PLoS Biology, Volume 17 (2019) no. 5, pp. 1-23 | DOI

[116] Pepperell, C. S. Evolution of tuberculosis pathogenesis, Annual Review of Microbiology, Volume 76 (2022), pp. 661-680 | DOI

[117] Pepperell, C. S.; Casto, A. M.; Kitchen, A.; Granka, J. M.; Cornejo, O. E.; Holmes, E. C.; Birren, B.; Galagan, J.; Feldman, M. W. The role of selection in shaping diversity of natural M. tuberculosis populations, PLoS Pathogens, Volume 9 (2013) no. 8 | DOI

[118] Pepperell, C. S.; Hoeppner, V. H.; Lipatov, M.; Wobeser, W.; Schoolnik, G. K.; Feldman, M. W. Bacterial genetic signatures of human social phenomena among M. tuberculosis from an aboriginal canadian population, Molecular Biology and Evolution, Volume 27 (2010) no. 2, pp. 427-440 | DOI

[119] Pettersson, M. E.; Berg, O. G. Muller’s ratchet in symbiont populations, Genetica, Volume 130 (2007) no. 2, p. 199 | DOI

[120] Phelan, J. E.; Coll, F.; Bergval, I.; Anthony, R. M.; Warren, R.; Sampson, S. L.; Gey van Pittius, N. C.; Glynn, J. R.; Crampin, A. C.; Alves, A.; Bessa, T. B.; Campino, S.; Dheda, K.; Grandjean, L.; Hasan, R.; Hasan, Z.; Miranda, A.; Moore, D.; Panaiotov, S.; Perdigao, J.; Portugal, I.; Sheen, P.; de Oliveira Sousa, E.; Streicher, E. M.; van Helden, P. D.; Viveiros, M.; Hibberd, M. L.; Pain, A.; McNerney, R.; Clark, T. G. Recombination in pe/ppe genes contributes to genetic variation in Mycobacterium tuberculosis lineages, BMC Genomics, Volume 17 (2016) no. 1, pp. 1-12 | DOI

[121] Plutynski, A. Drift: a historical and conceptual overview, Biological Theory, Volume 2 (2007) no. 2, pp. 156-167 | DOI

[122] Price, M. N.; Arkin, A. P. Weakly deleterious mutations and low rates of recombination limit the impact of natural selection on bacterial genomes, mBio, Volume 6 (2015) no. 6 | DOI

[123] Rahman, S.; Kosakovsky Pond, S. L.; Webb, A.; Hey, J. Weak selection on synonymous codons substantially inflates dN/dS estimates in bacteria, PNAS, Volume 118 (2021) no. 20, p. e2023575118 | DOI

[124] Reichenberger, E. R.; Rosen, G.; Hershberg, U.; Hershberg, R. Prokaryotic nucleotide composition is shaped by both phylogeny and the environment, Genome Biology and Evolution, Volume 7 (2015) no. 5, pp. 1380-1389 | DOI

[125] Rocha, E. P. Neutral theory, microbial practice: challenges in bacterial population genetics, Molecular Biology and Evolution, Volume 35 (2018) no. 6, pp. 1338-1347 | DOI

[126] Rocha, E. P.; Danchin, A. Base composition bias might result from competition for metabolic resources, TRENDS in Genetics, Volume 18 (2002) no. 6, pp. 291-294

[127] Rocha, E. P.; Feil, E. J. Mutational patterns cannot explain genome composition: are there any neutral sites in the genomes of bacteria?, PLoS Genetics, Volume 6 (2010) no. 9, p. e1001104 | DOI

[128] Rocha, E. P.; Smith, J. M.; Hurst, L. D.; Holden, M. T.; Cooper, J. E.; Smith, N. H.; Feil, E. J. Comparisons of dN/dS are time dependent for closely related bacterial genomes, Journal of Theoretical Biology, Volume 239 (2006) no. 2, pp. 226-235 | DOI

[129] Ryndak, M. B.; Laal, S. Mycobacterium tuberculosis primary infection and dissemination: a critical role for alveolar epithelial cells, Frontiers in Cellular and Infection Microbiology, Volume 9 (2019) | DOI

[130] Sabin, S.; Herbig, A.; Vågene, Å. J.; Ahlström, T.; Bozovic, G.; Arcini, C.; Kühnert, D.; Bos, K. I. A seventeenth-century Mycobacterium tuberculosis genome supports a Neolithic emergence of the Mycobacterium tuberculosis complex, Genome Biology, Volume 21 (2020) no. 1, pp. 1-24 | DOI

[131] Sackman, A. M.; Harris, R. B.; Jensen, J. D. Inferring demography and selection in organisms characterized by skewed offspring distributions, Genetics, Volume 211 (2019) no. 3, pp. 1019-1028 | DOI

[132] Selander, R. K.; Musser, J. M.; Caugant, D. A.; Gilmour, M. N.; Whittam, T. S. Population genetics of pathogenic bacteria, Microbial Pathogenesis, Volume 3 (1987) no. 1, pp. 1-7 | DOI

[133] Shapiro, B. J. How the tubercle bacillus got its genome: modernising, modelling, and making sense of the stories we tell, Peer Community in Evolutionary Biology (2023) | DOI

[134] Shapiro, B. J.; David, L. A.; Friedman, J.; Alm, E. J. Looking for Darwin's footprints in the microbial world, Trends in Microbiology, Volume 17 (2009) no. 5, pp. 196-204 | DOI

[135] Smith, N. H.; Gordon, S. V.; de la Rua-Domenech, R.; Clifton-Hadley, R. S.; Hewinson, R. G. Bottlenecks and broomsticks: the molecular evolution of Mycobacterium bovis, Nature Reviews Microbiology, Volume 4 (2006) no. 9, pp. 670-681 | DOI

[136] Smith, T. M.; Youngblom, M. A.; Kernien, J. F.; Mohamed, M. A.; Bohr, L. L.; Mortimer, T. D.; O'neill, M. B.; Pepperell, C. S. Rapid adaptation of a complex trait during experimental evolution of Mycobacterium tuberculosis, Elife, Volume 11 (2022), p. e78454 | DOI

[137] Stern, D. L. The genetic causes of convergent evolution, Nature Reviews Genetics, Volume 14 (2013) no. 11, pp. 751-764 | DOI

[138] Stritt, C.; Gagneux, S. How do monomorphic bacteria evolve? The Mycobacterium tuberculosis complex and the awkward population genetics of extreme clonality, Zenodo, 2023 | DOI

[139] Supply, P.; Marceau, M.; Mangenot, S.; Roche, D.; Rouanet, C.; Khanna, V.; Majlessi, L.; Criscuolo, A.; Tap, J.; Pawlik, A.; Fiette, L.; Orgeur, M.; Fabre, M.; Parmentier, C.; Frigui, W.; Simeone, R.; Boritsch, E. C.; Debrie, A. S.; Willery, E.; Walker, D.; Quail, M. A.; Ma, L.; Bouchier, C.; Salvignol, G.; Sayes, F.; Cascioferro, A.; Seemann, T.; Barbe, V.; Locht, C.; Gutierrez, M. C.; Leclerc, C.; Bentley, S. D.; Stinear, T. P.; Brisse, S.; Médigue, C.; Parkhill, J.; Cruveiller, S.; Brosch, R. Genomic analysis of smooth tubercle bacilli provides insights into ancestry and pathoadaptation of Mycobacterium tuberculosis, Nature Genetics, Volume 45 (2013) no. 2, pp. 172-179 | DOI

[140] Tantivitayakul, P.; Ruangchai, W.; Juthayothin, T.; Smittipat, N.; Disratthakit, A.; Mahasirimongkol, S.; Viratyosin, W.; Tokunaga, K.; Palittapongarnpim, P. Homoplastic single nucleotide polymorphisms contributed to phenotypic diversity in Mycobacterium tuberculosis, Scientific Reports, Volume 10 (2020) no. 1, pp. 1-10 | DOI

[141] Tarashi, S.; Fateh, A.; Mirsaeidi, M.; Siadat, S. D.; Vaziri, F. Mixed infections in tuberculosis: the missing part in a puzzle, Tuberculosis, Volume 107 (2017), pp. 168-174 | DOI

[142] Tellier, A.; Lemaire, C. Coalescence 2.0: a multiple branching of recent theoretical developments and their applications, Molecular Ecology, Volume 23 (2014) no. 11, pp. 2637-2652 | DOI

[143] Templeton, A. R. Population Genetics and Microevolutionary Theory, John Wiley & Sons, 2021 | DOI

[144] Thorpe, H. A.; Bayliss, S. C.; Hurst, L. D.; Feil, E. J. Comparative analyses of selection operating on nontranslated intergenic regions of diverse bacterial species, Genetics, Volume 206 (2017) no. 1, pp. 363-376 | DOI

[145] Tibayrenc, M.; Ayala, F. J. Is predominant clonal evolution a common evolutionary adaptation to parasitism in pathogenic parasitic protozoa, fungi, bacteria, and viruses?, Advances in Parasitology, Volume 97 (2017), pp. 243-325 | DOI

[146] Trauner, A.; Liu, Q.; Via, L. E.; Liu, X.; Ruan, X.; Liang, L.; Shi, H.; Chen, Y.; Wang, Z.; Liang, R.; Zhang, W.; Wei, W.; Gao, J.; Sun, G.; Brites, D.; England, K.; Zhang, G.; Gagneux, S.; Barry, C. E.; Gao, Q. The within-host population dynamics of Mycobacterium tuberculosis vary with treatment efficacy, Genome Biology, Volume 18 (2017) no. 1, pp. 1-17 | DOI

[147] Uplekar, S.; Heym, B.; Friocourt, V.; Rougemont, J.; Cole, S. T. Comparative genomics of ESX genes from clinical isolates of Mycobacterium tuberculosis provides evidence for gene conversion and epitope variation, Infection and Immunity, Volume 79 (2011) no. 10, pp. 4042-4049 | DOI

[148] Vos, M.; Didelot, X. A comparison of homologous recombination rates in bacteria and archaea, ISME Journal, Volume 3 (2009) no. 2, pp. 199-208 | DOI

[149] Wang, L.; Asare, E.; Shetty, A. C.; Sanchez-Tumbaco, F.; Edwards, M. R.; Saranathan, R.; Weinrick, B.; Xu, J.; Chen, B.; Bénard, A.; Dougan, G.; Leung, D. W.; Amarasinghe, G. K.; Chan, J.; Basler, C. F.; Jacobs, W. R.; Tufariello, J. M. Multiple genetic paths including massive gene amplification allow Mycobacterium tuberculosis to overcome loss of ESX-3 secretion system substrates, PNAS, Volume 119 (2022) no. 8 | DOI

[150] Wang, T. C.; Chen, F. C. The evolutionary landscape of the Mycobacterium tuberculosis genome, Gene, Volume 518 (2013) no. 1, pp. 187-193 | DOI

[151] Weissman, J. L.; Fagan, W. F.; Johnson, P. L. Linking high GC content to the repair of double strand breaks in prokaryotic genomes, PLoS Genetics, Volume 15 (2019) no. 11, pp. 1-19 | DOI

[152] Weller, C.; Wu, M. A generation-time effect on the rate of molecular evolution in bacteria, Evolution, Volume 69 (2015) no. 3, pp. 643-652 | DOI

[153] Williams, M. J.; Zapata, L.; Werner, B.; Barnes, C. P.; Sottoriva, A.; Graham, T. A. Measuring the distribution of fitness effects in somatic evolution by combining clonal dynamics with dN/dS ratios, eLife, Volume 9 (2020), pp. 1-19 | DOI

[154] Wilson, D. J.; The CRyPTIC Consortium GenomegaMap: within-species genome-wide dN/dS estimation from over 10,000 genomes, Molecular Biology and Evolution, Volume 37 (2020) no. 8, pp. 2450-2460 | DOI

[155] Windels, E. M.; Fox, R.; Yerramsetty, K.; Krouse, K.; Wenseleers, T.; Swinnen, J.; Matthay, P.; Verstraete, L.; Wilmaerts, D.; Van Den Bergh, B.; Michiels, J. Population bottlenecks strongly affect the evolutionary dynamics of antibiotic persistence, Molecular Biology and Evolution, Volume 38 (2021) no. 8, pp. 3345-3357 | DOI

[156] Woese, C. R.; Goldenfeld, N. How the microbial world saved evolution from the Scylla of molecular biology and the charybdis of the Modern Synthesis, Microbiology and Molecular Biology Reviews, Volume 73 (2009) no. 1, pp. 14-21 | DOI

[157] World Health Organization Global tuberculosis report 2022, 2022 (https://www.who.int/teams/global-tuberculosis-programme/tb-reports/global-tuberculosis-report-2022)

[158] Wright, S. Evolution in mendelian populations, Genetics, Volume 16 (1931) no. 97 | DOI

[159] Yang, Z. Likelihood ratio tests for detecting positive selection and application to primate lysozyme evolution, Molecular Biology and Evolution, Volume 15 (1998) no. 5, pp. 568-573 | DOI

[160] Yang, Z. PAML 4: phylogenetic analysis by maximum likelihood, Molecular Biology and Evolution, Volume 24 (2007) no. 8, pp. 1586-1591 | DOI

[161] Yang, Z. Molecular Evolution – A Statistical Approach, Oxford University Press, 2014

[162] Yang, Z.; Bielawski, J. R. Statistical methods for detecting molecular adaptation, Trends in Ecology and Evolution, Volume 15 (2000) no. 12, pp. 496-503 | DOI

[163] Young, D.; Robertson, B. Genomics: leprosy—a degenerative disease of the genome, Current Biology, Volume 11 (2001) no. 10, p. R381-R383 | DOI

[164] Zwyer, M.; Cengiz, C.; Ghielmetti, G.; Pacciarini, M. L.; Scaltriti, E.; Van Soolingen, D.; Dötsch, A.; Reinhard, M.; Gagneux, S.; Brites, D. A new nomenclature for the livestock-associated Mycobacterium tuberculosis complex based on phylogenomics, Open Research Europe, Volume 1 (2021) | DOI

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