Chapter 20 : The Evolutionary History, Demography, and Spread of the Complex

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Tuberculosis has plagued mankind over the centuries and probably accompanied modern out of Africa. The epidemiological agent of phthisis, also known as “consumption,” reached its epidemic apex during the 18th and 19th centuries. During the industrialization era, the disease was associated with the concentration of labor and poor socioeconomic settings that ultimately favored the spread of this “crowd” pathogen. This high-burden period was then followed by a progressive decline of the death and disease tolls that predated the antibiotic era and the BCG vaccination. The evolutionary histories of the host and its pathogen are intricately associated, implying that tuberculosis can only be fully understood in the light of origins, migrations, and demography ( ). Excluding these parameters from our analyses might lead us to false conclusions regarding evolution, epidemiology, and pathobiology. In the same line, there is also an urgent need to unravel the genomic features that can explain the contrasted infectivity and transmission observed between complex (MTBC) lineages ( ), without neglecting the genetic architecture of the host’s immune system ( ).

Citation: Barbier M, Wirth T. 2017. The Evolutionary History, Demography, and Spread of the Complex, p 453-473. In Jacobs, Jr. W, McShane H, Mizrahi V, Orme I (ed), Tuberculosis and the Tubercle Bacillus, Second Edition. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.TBTB2-0008-2016
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Figure 1

Diagram of the proposed evolutionary pathway of the tubercle bacilli illustrating successive losses of DNA in certain lineages (gray boxes). The diagram is based on the presence or absence of conserved deleted regions and on sequence polymorphisms in five selected genes. The distances between certain branches may not correspond to actual phylogenetic differences calculated by other methods. Blue arrows indicate that strains are characterized by 463. CTG (Leu), 95 ACC (Thr), typical for group 1 organisms. Green arrows indicate that strains belong to group 2 characterized by 463 CGG (Arg), 95 ACC (Thr). The red arrow indicates that strains belong to group 3, characterized by 463 CGG (Arg), 95 AGC (Ser), as defined by Sreevatsan et al. ( ). Adapted from Brosch et al. ( ).

Citation: Barbier M, Wirth T. 2017. The Evolutionary History, Demography, and Spread of the Complex, p 453-473. In Jacobs, Jr. W, McShane H, Mizrahi V, Orme I (ed), Tuberculosis and the Tubercle Bacillus, Second Edition. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.TBTB2-0008-2016
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Figure 2

The genome-based phylogeny of MTBC mirrors that of human mitochondrial genomes. Comparison of the MTBC phylogeny and a phylogeny derived from 4,955 mitochondrial genomes (mtDNA) representative of the main human haplogroups . Color-coding highlights the similarities in tree topology and geographic distribution between MTBC strains and the main human mitochondrial macrohaplogroups (black, African clades: MTBC lineages 5 and 6, human mitochondrial macrohaplogroups L0 to L3; pink, Southeast Asian and Oceanian clades: MTBC lineage 1, human mitochondrial macrohaplogroup M; blue, Eurasian clades: MTBC lineage 2 to 4, human mitochondrial macrohaplogroup N). Scale bars indicate substitutions per site. Adapted from Comas et al. ( ).

Citation: Barbier M, Wirth T. 2017. The Evolutionary History, Demography, and Spread of the Complex, p 453-473. In Jacobs, Jr. W, McShane H, Mizrahi V, Orme I (ed), Tuberculosis and the Tubercle Bacillus, Second Edition. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.TBTB2-0008-2016
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Figure 3

Whole-genome phylogeny of 261 strains belonging to the MTBC. Animal and specific deletions are indicated, as well as mutations affecting the PhoPR virulence regulator. Adapted from Bos et al. ( ) and Gonzalo-Asensio et al. ( ).

Citation: Barbier M, Wirth T. 2017. The Evolutionary History, Demography, and Spread of the Complex, p 453-473. In Jacobs, Jr. W, McShane H, Mizrahi V, Orme I (ed), Tuberculosis and the Tubercle Bacillus, Second Edition. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.TBTB2-0008-2016
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Figure 4

Biogeographical structure of the Beijing lineage. MStree based on 24 MIRU-VNTR markers delineating the clonal complexes (CCs) gathered from a worldwide collection (n = 4,987). Major nodes and associated multilocus variants were grouped into six CCs and a basal sublineage (BL). Genetic variability in the different Beijing lineage CCs and the BL calculated using a rarefaction procedure. Dots correspond to the mean allelic richness; boxes correspond to mean values ± standard error of the mean and error bars correspond to mean values ± standard deviation. Worldwide distribution of the Beijing CCs and BL. Each circle corresponds to a country, and circle sizes are proportional to the number of strains. Adapted from Merker et al. ( ).

Citation: Barbier M, Wirth T. 2017. The Evolutionary History, Demography, and Spread of the Complex, p 453-473. In Jacobs, Jr. W, McShane H, Mizrahi V, Orme I (ed), Tuberculosis and the Tubercle Bacillus, Second Edition. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.TBTB2-0008-2016
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Figure 5

Global phylogeny of 1,601 MTBC isolates inferred from a total of 91,648 SNPs spanning the whole genome. All seven main MTBC lineages are indicated in the inner area of the tree. The main sublineages are annotated at the outer arc along with lineage-specific RDs. Identified clades are color-coded. Adapted from Coll et al. ( ).

Citation: Barbier M, Wirth T. 2017. The Evolutionary History, Demography, and Spread of the Complex, p 453-473. In Jacobs, Jr. W, McShane H, Mizrahi V, Orme I (ed), Tuberculosis and the Tubercle Bacillus, Second Edition. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.TBTB2-0008-2016
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Figure 6

Consistent with a general pattern for measurably evolving populations, the evolutionary rates of microbial pathogens decrease as a function of the time span over which they are estimated. Data shown are selected representative examples, including one group of RNA viruses and several bacterial pathogens. Adapted from Biek et al. ( ).

Citation: Barbier M, Wirth T. 2017. The Evolutionary History, Demography, and Spread of the Complex, p 453-473. In Jacobs, Jr. W, McShane H, Mizrahi V, Orme I (ed), Tuberculosis and the Tubercle Bacillus, Second Edition. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.TBTB2-0008-2016
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Table 1

Correspondence table of the MTBC human-adapted strains identified by main typing methods and including the latest nomenclature

Citation: Barbier M, Wirth T. 2017. The Evolutionary History, Demography, and Spread of the Complex, p 453-473. In Jacobs, Jr. W, McShane H, Mizrahi V, Orme I (ed), Tuberculosis and the Tubercle Bacillus, Second Edition. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.TBTB2-0008-2016

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