Global expansion of Mycobacterium tuberculosis lineage 4 shaped by colonial migration and local adaptation

Ola B. Brynildsrud; Caitlin S. Pepperell; Philip Suffys; Louis Grandjean; Johana Monteserin; Nadia Debech; Jon Bohlin; Kristian Alfsnes; John O.H. Pettersson; Ingerid Kirkeleite; Fatima Fandinho; Marcia Aparecida Da Silva; Joao Perdigao; Isabel Portugal; Miguel Viveiros; Taane Clark; Maxine Caws; Sarah Dunstan; Phan Vuong Khac Thai; Beatriz Lopez; Viviana Ritacco; Andrew Kitchen; Tyler S. Brown; Dick Van Soolingen; Mary B. O'Neill; Kathryn E. Holt; Edward J. Feil; Barun Mathema; Francois Balloux; Vegard Eldholm

doi:10.1126/sciadv.aat5869

Global expansion of Mycobacterium tuberculosis lineage 4 shaped by colonial migration and local adaptation

Ola B. Brynildsrud, Caitlin S. Pepperell, Philip Suffys, Louis Grandjean, Johana Monteserin, Nadia Debech, Jon Bohlin, Kristian Alfsnes, John O.H. Pettersson, Ingerid Kirkeleite, Fatima Fandinho, Marcia Aparecida Da Silva, Joao Perdigao, Isabel Portugal, Miguel Viveiros, Taane Clark, Maxine Caws, Sarah Dunstan, Phan Vuong Khac Thai, Beatriz LopezViviana Ritacco, Andrew Kitchen, Tyler S. Brown, Dick Van Soolingen, Mary B. O'Neill, Kathryn E. Holt, Edward J. Feil, Barun Mathema, Francois Balloux, Vegard Eldholm

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Abstract

On the basis of population genomic and phylogeographic analyses of 1669 Mycobacterium tuberculosis lineage 4 (L4) genomes, we find that dispersal of L4 has been completely dominated by historical migrations out of Europe. We demonstrate an intimate temporal relationship between European colonial expansion into Africa and the Americas and the spread of L4 tuberculosis (TB). Markedly, in the age of antibiotics, mutations conferring antimicrobial resistance overwhelmingly emerged locally (at the level of nations), with minimal cross-border transmission of resistance. The latter finding was found to reflect the relatively recent emergence of these mutations, as a similar degree of local restriction was observed for susceptible variants emerging on comparable time scales. The restricted international transmission of drug-resistant TB suggests that containment efforts at the level of individual countries could be successful.

Original language	English
Article number	eaat5869
Journal	Science Advances
Volume	4
Issue number	10
DOIs	https://doi.org/10.1126/sciadv.aat5869
Publication status	Published - 17 Oct 2018

ASJC Scopus subject areas

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UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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Brynildsrud, O. B., Pepperell, C. S., Suffys, P., Grandjean, L., Monteserin, J., Debech, N., Bohlin, J., Alfsnes, K., Pettersson, J. O. H., Kirkeleite, I., Fandinho, F., Da Silva, M. A., Perdigao, J., Portugal, I., Viveiros, M., Clark, T., Caws, M., Dunstan, S., Thai, P. V. K., ... Eldholm, V. (2018). Global expansion of Mycobacterium tuberculosis lineage 4 shaped by colonial migration and local adaptation. Science Advances, 4(10), [eaat5869]. https://doi.org/10.1126/sciadv.aat5869

Brynildsrud, OB, Pepperell, CS, Suffys, P, Grandjean, L, Monteserin, J, Debech, N, Bohlin, J, Alfsnes, K, Pettersson, JOH, Kirkeleite, I, Fandinho, F, Da Silva, MA, Perdigao, J, Portugal, I, Viveiros, M, Clark, T, Caws, M, Dunstan, S, Thai, PVK, Lopez, B, Ritacco, V, Kitchen, A, Brown, TS, Van Soolingen, D, O'Neill, MB, Holt, KE, Feil, EJ, Mathema, B, Balloux, F & Eldholm, V 2018, 'Global expansion of Mycobacterium tuberculosis lineage 4 shaped by colonial migration and local adaptation', Science Advances, vol. 4, no. 10, eaat5869. https://doi.org/10.1126/sciadv.aat5869

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abstract = "On the basis of population genomic and phylogeographic analyses of 1669 Mycobacterium tuberculosis lineage 4 (L4) genomes, we find that dispersal of L4 has been completely dominated by historical migrations out of Europe. We demonstrate an intimate temporal relationship between European colonial expansion into Africa and the Americas and the spread of L4 tuberculosis (TB). Markedly, in the age of antibiotics, mutations conferring antimicrobial resistance overwhelmingly emerged locally (at the level of nations), with minimal cross-border transmission of resistance. The latter finding was found to reflect the relatively recent emergence of these mutations, as a similar degree of local restriction was observed for susceptible variants emerging on comparable time scales. The restricted international transmission of drug-resistant TB suggests that containment efforts at the level of individual countries could be successful.",

author = "Brynildsrud, {Ola B.} and Pepperell, {Caitlin S.} and Philip Suffys and Louis Grandjean and Johana Monteserin and Nadia Debech and Jon Bohlin and Kristian Alfsnes and Pettersson, {John O.H.} and Ingerid Kirkeleite and Fatima Fandinho and {Da Silva}, {Marcia Aparecida} and Joao Perdigao and Isabel Portugal and Miguel Viveiros and Taane Clark and Maxine Caws and Sarah Dunstan and Thai, {Phan Vuong Khac} and Beatriz Lopez and Viviana Ritacco and Andrew Kitchen and Brown, {Tyler S.} and {Van Soolingen}, Dick and O'Neill, {Mary B.} and Holt, {Kathryn E.} and Feil, {Edward J.} and Barun Mathema and Francois Balloux and Vegard Eldholm",

note = "Funding Information: C.S.P. was supported by the NIH grant number 1R01AI113287-01A1. K.E.H. is funded by a Viertel Foundation of Australia Senior Medical Research Fellowship. F.B. acknowledges support from the BBSRC GCRF scheme and the National Institute for Health Research University College London Hospitals Biomedical Research Centre. Publisher Copyright: Copyright {\textcopyright} 2018 The Authors, some rights reserved. Copyright: Copyright 2018 Elsevier B.V., All rights reserved.",

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AU - Monteserin, Johana

AU - Debech, Nadia

AU - Bohlin, Jon

AU - Alfsnes, Kristian

AU - Pettersson, John O.H.

AU - Kirkeleite, Ingerid

AU - Fandinho, Fatima

AU - Da Silva, Marcia Aparecida

AU - Perdigao, Joao

AU - Portugal, Isabel

AU - Viveiros, Miguel

AU - Clark, Taane

AU - Caws, Maxine

AU - Dunstan, Sarah

AU - Thai, Phan Vuong Khac

AU - Lopez, Beatriz

AU - Ritacco, Viviana

AU - Kitchen, Andrew

AU - Brown, Tyler S.

AU - Van Soolingen, Dick

AU - O'Neill, Mary B.

AU - Holt, Kathryn E.

AU - Feil, Edward J.

AU - Mathema, Barun

AU - Balloux, Francois

AU - Eldholm, Vegard

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N2 - On the basis of population genomic and phylogeographic analyses of 1669 Mycobacterium tuberculosis lineage 4 (L4) genomes, we find that dispersal of L4 has been completely dominated by historical migrations out of Europe. We demonstrate an intimate temporal relationship between European colonial expansion into Africa and the Americas and the spread of L4 tuberculosis (TB). Markedly, in the age of antibiotics, mutations conferring antimicrobial resistance overwhelmingly emerged locally (at the level of nations), with minimal cross-border transmission of resistance. The latter finding was found to reflect the relatively recent emergence of these mutations, as a similar degree of local restriction was observed for susceptible variants emerging on comparable time scales. The restricted international transmission of drug-resistant TB suggests that containment efforts at the level of individual countries could be successful.

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Global expansion of Mycobacterium tuberculosis lineage 4 shaped by colonial migration and local adaptation

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