Controlled fire use in early humans might have triggered the evolutionary emergence of tuberculosis

Edited by Marcus W. Feldman, Stanford University, Stanford, CA, and approved June 17, 2016 (received for review February 25, 2016)
July 25, 2016
113 (32) 9051-9056

Significance

Tuberculosis is an ancient human disease that continues to affect millions of people worldwide. A crucial component of the origins of the tuberculosis bacterium remains a mystery: What were the conditions that precipitated its emergence as an obligate transmissible human pathogen? Here, we identify a connection between the emergence of tuberculosis and another major event in human prehistory, namely the discovery of controlled fire use. Our results have serious and cautionary implications for the emergence of new infectious diseases—feedback between cultural innovation and alteration of living conditions can catalyze unexpected changes with potentially devastating consequences lasting thousands of years.

Abstract

Tuberculosis (TB) is caused by the Mycobacterium tuberculosis complex (MTBC), a wildly successful group of organisms and the leading cause of death resulting from a single bacterial pathogen worldwide. It is generally accepted that MTBC established itself in human populations in Africa and that animal-infecting strains diverged from human strains. However, the precise causal factors of TB emergence remain unknown. Here, we propose that the advent of controlled fire use in early humans created the ideal conditions for the emergence of TB as a transmissible disease. This hypothesis is supported by mathematical modeling together with a synthesis of evidence from epidemiology, evolutionary genetics, and paleoanthropology.

Continue Reading

Acknowledgments

This work was supported by the Australian Research Council through Grants FT140100398 (to M.M.T.) and FT12100168 (to D.C.).

Supporting Information

Appendix (PDF)
Supporting Information

References

1
MEJ Woolhouse, S Gowtage-Sequeria, Host range and emerging and reemerging pathogens. Emerg Infect Dis 11, 1842–1847 (2005).
2
KE Jones, et al., Global trends in emerging infectious diseases. Nature 451, 990–993 (2008).
3
MJ Blaser, D Kirschner, The equilibria that allow bacterial persistence in human hosts. Nature 449, 843–849 (2007).
4
AJ McMichael, Environmental and social influences on emerging infectious diseases: Past, present and future. Philos Trans R Soc Lond B Biol Sci 359, 1049–1058 (2004).
5
ND Wolfe, CP Dunavan, J Diamond, Origins of major human infectious diseases. Nature 447, 279–283 (2007).
6
M Woolhouse, E Gaunt, Ecological origins of novel human pathogens. Crit Rev Microbiol 33, 231–242 (2007).
7
RA Weiss, The Leeuwenhoek Lecture 2001. Animal origins of human infectious disease. Philos Trans R Soc Lond B Biol Sci 356, 957–977 (2001).
8
F Berna, et al., Microstratigraphic evidence of in situ fire in the Acheulean strata of Wonderwerk Cave, Northern Cape province, South Africa. Proc Natl Acad Sci USA 109, E1215–E1220 (2012).
9
W Roebroeks, P Villa, On the earliest evidence for habitual use of fire in Europe. Proc Natl Acad Sci USA 108, 5209–5214 (2011).
10
C Darwin The Descent of Man and Selection in Relation to Sex (John Murray, London, 1871).
11
L Attwell, K Kovarovic, J Kendal, Fire in the Plio-Pleistocene: The functions of hominin fire use, and the mechanistic, developmental and evolutionary consequences. J Anthropol Sci 93, 1–20 (2015).
12
RW Wrangham, JH Jones, G Laden, D Pilbeam, N Conklin-Brittain, The raw and the stolen. Cooking and the ecology of human origins. Curr Anthropol 40, 567–594 (1999).
13
R Wrangham, R Carmody, Human adaptation to the control of fire. Evol Anthropol 19, 187–199 (2010).
14
FW Marlowe, Hunter-gatherers and human evolution. Evol Anthropol 14, 54–67 (2005).
15
H Kaplan, K Hill, J Lancaster, AM Hurtado, A theory of human life history evolution: Diet, intelligence, and longevity. Evol Anthropol 9, 156–185 (2000).
16
PW Wiessner, Embers of society: Firelight talk among the Ju/′hoansi Bushmen. Proc Natl Acad Sci USA 111, 14027–14035 (2014).
17
CS Pepperell, et al., The role of selection in shaping diversity of natural M. tuberculosis populations. PLoS Pathog 9, e1003543 (2013).
18
KI Bos, et al., Pre-Columbian mycobacterial genomes reveal seals as a source of New World human tuberculosis. Nature 514, 494–497 (2014).
19
GL Kay, et al., Eighteenth-century genomes show that mixed infections were common at time of peak tuberculosis in Europe. Nat Commun 6, 6717 (2015).
20
S Gagneux, Host-pathogen coevolution in human tuberculosis. Philos Trans R Soc Lond B Biol Sci 367, 850–859 (2012).
21
I Comas, et al., Out-of-Africa migration and Neolithic coexpansion of Mycobacterium tuberculosis with modern humans. Nat Genet 45, 1176–1182 (2013).
22
JE Galagan, Genomic insights into tuberculosis. Nat Rev Genet 15, 307–320 (2014).
23
NH Smith, RG Hewinson, K Kremer, R Brosch, SV Gordon, Myths and misconceptions: The origin and evolution of Mycobacterium tuberculosis. Nat Rev Microbiol 7, 537–544 (2009).
24
M Coscolla, et al., Novel Mycobacterium tuberculosis complex isolate from a wild chimpanzee. Emerg Infect Dis 19, 969–976 (2013).
25
Y Blouin, et al., Significance of the identification in the Horn of Africa of an exceptionally deep branching Mycobacterium tuberculosis clade. PLoS One 7, e52841 (2012).
26
I Comas, et al., Population genomics of Mycobacterium tuberculosis in Ethiopia contradicts the virgin soil hypothesis for human tuberculosis in Sub-Saharan Africa. Curr Biol 25, 3260–3266 (2015).
27
WL Salo, AC Aufderheide, J Buikstra, TA Holcomb, Identification of Mycobacterium tuberculosis DNA in a pre-Columbian Peruvian mummy. Proc Natl Acad Sci USA 91, 2091–2094 (1994).
28
BT Arriaza, W Salo, AC Aufderheide, TA Holcomb, Pre-Columbian tuberculosis in northern Chile: Molecular and skeletal evidence. Am J Phys Anthropol 98, 37–45 (1995).
29
BM Rothschild, et al., Mycobacterium tuberculosis complex DNA from an extinct bison dated 17,000 years before the present. Clin Infect Dis 33, 305–311 (2001).
30
KAR Kennedy, SU Deraniyagala, Fossil remains of 28,000-year-old hominids from Sri Lanka. Curr Anthropol 30, 394–399 (1989).
31
I Hershkovitz, et al., Detection and molecular characterization of 9,000-year-old Mycobacterium tuberculosis from a Neolithic settlement in the Eastern Mediterranean. PLoS One 3, e3426 (2008).
32
3rd JO Falkinham, Surrounded by mycobacteria: Nontuberculous mycobacteria in the human environment. J Appl Microbiol 107, 356–367 (2009).
33
GL Simpson, TA Raffin, JS Remington, Association of prior nocardiosis and subsequent occurrence of nontuberculous mycobacteriosis in a defined, immunosuppressed population. J Infect Dis 146, 211–219 (1982).
34
JM Bryant, et al., Whole-genome sequencing to identify transmission of Mycobacterium abscessus between patients with cystic fibrosis: A retrospective cohort study. Lancet 381, 1551–1560 (2013).
35
JJ Smith, SM Travis, EP Greenberg, MJ Welsh, Cystic fibrosis airway epithelia fail to kill bacteria because of abnormal airway surface fluid. Cell 85, 229–236 (1996).
36
ML Aitken, et al., Respiratory outbreak of Mycobacterium abscessus subspecies massiliense in a lung transplant and cystic fibrosis center. Am J Respir Crit Care Med 185, 231–232 (2012).
37
MC Gutierrez, et al., Ancient origin and gene mosaicism of the progenitor of Mycobacterium tuberculosis. PLoS Pathog 1, e5 (2005).
38
J Wang, et al., Insights on the emergence of Mycobacterium tuberculosis from the analysis of Mycobacterium kansasii. Genome Biol Evol 7, 856–870 (2015).
39
SA Evans, A Colville, AJ Evans, AJ Crisp, ID Johnston, Pulmonary Mycobacterium kansasii infection: Comparison of the clinical features, treatment and outcome with pulmonary tuberculosis. Thorax 51, 1248–1252 (1996).
40
R Antia, RR Regoes, JC Koella, CT Bergstrom, The role of evolution in the emergence of infectious diseases. Nature 426, 658–661 (2003).
41
; World Health Organization Global Tuberculosis Report 2015 (WHO, Geneva, 2015).
42
RH Chisholm, MM Tanaka, The emergence of latent infection in the early evolution of Mycobacterium tuberculosis. Proc Biol Sci 283, 20160499 (2016).
43
FL Mendez, JC Watkins, MF Hammer, Neandertal origin of genetic variation at the cluster of OAS immunity genes. Mol Biol Evol 30, 798–801 (2013).
44
I McDougall, FH Brown, JG Fleagle, Stratigraphic placement and age of modern humans from Kibish, Ethiopia. Nature 433, 733–736 (2005).
45
C Stringer, Evolution: What makes a modern human. Nature 485, 33–35 (2012).
46
R Boyd, PJ Richerson Culture and the Evolutionary Process (Univ of Chicago Press, Chicago, 1988).
47
MC Stiner, A Gopher, R Barkai, Hearth-side socioeconomics, hunting and paleoecology during the late Lower Paleolithic at Qesem Cave, Israel. J Hum Evol 60, 213–233 (2011).
48
F Scherjon, C Bakels, K MacDonald, W Roebroeks, Burning the land. Curr Anthropol 56, 299–326 (2015).
49
K Hardy, et al., Dental calculus reveals potential respiratory irritants and ingestion of essential plant-based nutrients at Lower Palaeolithic Qesem Cave Israel. Quat Int 398, 129–135 (2015).
50
TV Larson, JQ Koenig, Wood smoke: Emissions and noncancer respiratory effects. Annu Rev Public Health 15, 133–156 (1994).
51
LP Naeher, et al., Woodsmoke health effects: A review. Inhal Toxicol 19, 67–106 (2007).
52
HH Lin, M Ezzati, M Murray, Tobacco smoke, indoor air pollution and tuberculosis: A systematic review and meta-analysis. PLoS Med 4, e20 (2007).
53
Jr RB Fick, ES Paul, WW Merrill, HY Reynolds, JS Loke, Alterations in the antibacterial properties of rabbit pulmonary macrophages exposed to wood smoke. Am Rev Respir Dis 129, 76–81 (1984).
54
JL Flynn, J Chan, Immunology of tuberculosis. Annu Rev Immunol 19, 93–129 (2001).
55
E Houtmeyers, R Gosselink, G Gayan-Ramirez, M Decramer, Regulation of mucociliary clearance in health and disease. Eur Respir J 13, 1177–1188 (1999).
56
M Inghammar, et al., COPD and the risk of tuberculosis--A population-based cohort study. PLoS One 5, e10138 (2010).
57
C Andréjak, et al., Chronic respiratory disease, inhaled corticosteroids and risk of non-tuberculous mycobacteriosis. Thorax 68, 256–262 (2013).
58
H Chu, L Zhao, H Xiao, Z Zhang, J Zhang, Prevalence of nontuberculosis mycobacterial in patients with bronchiectasis: A meta-analysis. Arch Med Sci 10, 661–668 (2014).
59
EL Corbett, et al., Risk factors for pulmonary mycobacterial disease in South African gold miners. A case-control study. Am J Respir Crit Care Med 159, 94–99 (1999).
60
P Sonnenberg, et al., Risk factors for pulmonary disease due to culture-positive M. tuberculosis or nontuberculous mycobacteria in South African gold miners. Eur Respir J 15, 291–296 (2000).
61
C Kolappan, R Subramani, Association between biomass fuel and pulmonary tuberculosis: A nested case-control study. Thorax 64, 705–708 (2009).
62
G Hu, et al., Risk of COPD from exposure to biomass smoke: A metaanalysis. Chest 138, 20–31 (2010).
63
M Arslan, I Akkurt, H Egilmez, M Atalar, I Salk, Biomass exposure and the high resolution computed tomographic and spirometric findings. Eur J Radiol 52, 192–199 (2004).
64
JJ Yeh, YC Wang, FC Sung, CYT Chou, CH Kao, Nontuberculosis mycobacterium disease is a risk factor for chronic obstructive pulmonary disease: A nationwide cohort study. Lung 192, 403–411 (2014).
65
D Rees, J Murray, Silica, silicosis and tuberculosis. Int J Tuberc Lung Dis 11, 474–484 (2007).
66
GJ Churchyard, et al., Silicosis prevalence and exposure-response relations in South African goldminers. Occup Environ Med 61, 811–816 (2004).
67
MP Cox, et al., Autosomal resequence data reveal Late Stone Age signals of population expansion in sub-Saharan African foraging and farming populations. PLoS One 4, e6366 (2009).
68
J Gonzalo-Asensio, et al., Evolutionary history of tuberculosis shaped by conserved mutations in the PhoPR virulence regulator. Proc Natl Acad Sci USA 111, 11491–11496 (2014).
69
EC Boritsch, et al., Pks5-recombination-mediated surface remodelling in Mycobacterium tuberculosis emergence. New Microbiol 1, 15019 (2016).
70
S Herfst, et al., Airborne transmission of influenza A/H5N1 virus between ferrets. Science 336, 1534–1541 (2012).
71
S Berg, et al., The burden of mycobacterial disease in ethiopian cattle: Implications for public health. PLoS One 4, e5068 (2009).
72
JP Cegielski, L Arab, J Cornoni-Huntley, Nutritional risk factors for tuberculosis among adults in the United States, 1971-1992. Am J Epidemiol 176, 409–422 (2012).
73
AP Starling, JT Stock, Dental indicators of health and stress in early Egyptian and Nubian agriculturalists: A difficult transition and gradual recovery. Am J Phys Anthropol 134, 520–528 (2007).
74
S Webb Palaeopathology of Aboriginal Australians: Health and Disease Across a Hunter-Gatherer Continent (Cambridge Univ Press, New York, 2009).
75
I Barnes, A Duda, OG Pybus, MG Thomas, Ancient urbanization predicts genetic resistance to tuberculosis. Evolution 65, 842–848 (2011).
76
SM Blower, H Dowlatabadi, Sensitivity and uncertainty analysis of complex models of disease transmission: An HIV model, as an example. Int Stat Rev 62, 229–243 (1994).

Information & Authors

Information

Published in

Go to Proceedings of the National Academy of Sciences
Proceedings of the National Academy of Sciences
Vol. 113 | No. 32
August 9, 2016
PubMed: 27457933

Classifications

Submission history

Published online: July 25, 2016
Published in issue: August 9, 2016

Keywords

  1. tuberculosis
  2. pathogen evolution
  3. cultural evolution
  4. epidemiology
  5. mathematical modeling

Acknowledgments

This work was supported by the Australian Research Council through Grants FT140100398 (to M.M.T.) and FT12100168 (to D.C.).

Notes

This article is a PNAS Direct Submission.

Authors

Affiliations

Rebecca H. Chisholm
School of Biotechnology and Biomolecular Sciences, University of New South Wales, Sydney 2052, Australia;
Evolution & Ecology Research Centre, University of New South Wales, Sydney 2052, Australia;
James M. Trauer
School of Public Health and Preventive Medicine, Monash University, Melbourne 3004, Australia;
Darren Curnoe
Palaeontology, Geobiology and Earth Archives Research Centre, University of New South Wales, Sydney 2052, Australia
Mark M. Tanaka1 [email protected]
School of Biotechnology and Biomolecular Sciences, University of New South Wales, Sydney 2052, Australia;
Evolution & Ecology Research Centre, University of New South Wales, Sydney 2052, Australia;

Notes

1
To whom correspondence should be addressed. Email: [email protected].
Author contributions: R.H.C. and M.M.T. formulated the model; M.M.T. coordinated the study; R.H.C. analyzed data; and R.H.C., J.M.T., D.C., and M.M.T. wrote the paper.

Competing Interests

The authors declare no conflict of interest.

Metrics & Citations

Metrics

Note: The article usage is presented with a three- to four-day delay and will update daily once available. Due to ths delay, usage data will not appear immediately following publication. Citation information is sourced from Crossref Cited-by service.


Citation statements

Altmetrics

Citations

If you have the appropriate software installed, you can download article citation data to the citation manager of your choice. Simply select your manager software from the list below and click Download.

Cited by

    Loading...

    View Options

    View options

    PDF format

    Download this article as a PDF file

    DOWNLOAD PDF

    Get Access

    Login options

    Check if you have access through your login credentials or your institution to get full access on this article.

    Personal login Institutional Login

    Recommend to a librarian

    Recommend PNAS to a Librarian

    Purchase options

    Purchase this article to access the full text.

    Single Article Purchase

    Controlled fire use in early humans might have triggered the evolutionary emergence of tuberculosis
    Proceedings of the National Academy of Sciences
    • Vol. 113
    • No. 32
    • pp. 8873-E4756

    Media

    Figures

    Tables

    Other

    Share

    Share

    Share article link

    Share on social media