Abstract
Because the diverse microbial communities on and in the body (microbiome) are tightly coevolved with human cells, it is vital to explore the evolutionary history of the human microbiome. With the advent of new methodologies and sequencing technologies, researchers can now explore different factors that influence the bacterial community structure and colonization of specific species in the human microbiome. Using distant out-groups, such as chimpanzees, and human populations with unique lifestyles, such as Amerindians, the history and formation of the modern human microbiome in Westernized societies can be elucidated, providing vital information into how to these microbial communities were impacted by past events. Large cultural and dietary revolutions, such as the Neolithic Revolution (~7500 years ago) and the Industrial Revolution (~200 years ago), largely impacted these microbial communities. Ancient events, such as interbreeding and admixture with our closest ancient relatives, such as Neanderthals or Denisovans, could also have impacted the microbiome that modern humans carry today. Reconstructing the evolutionary history of the human microbiome has proven to be an intricate tale, with impacts on modern health and disease, as well as the evolutionary fate of modern humans.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Abi-Rached L, Jobin MJ, Kulkarni S et al (2011) The shaping of modern human immune systems by multiregional admixture with archaic humans. Science 334:89–94. doi:10.1126/science.1209202
Adams JB, Johansen LJ, Powell LD et al (2011) Gastrointestinal flora and gastrointestinal status in children with autism—comparisons to typical children and correlation with autism severity. 22
Adler CJ, Dobney K, Weyrich LS et al (2013) Sequencing ancient calcified dental plaque shows changes in oral microbiota with dietary shifts of the Neolithic and Industrial revolutions. Nat Genet 45:450–455. doi:10.1038/ng.2536
Ajdić D, McShan WM, McLaughlin RE et al (2002) Genome sequence of Streptococcus mutans UA159, a cariogenic dental pathogen 99:14434–14439
Allentoft ME, Collins M, Harker D et al (2012) The half-life of DNA in bone: measuring decay kinetics in 158 dated fossils. Proc R Soc B Biol Sci 279:4724–4733. doi:10.1098/rspb.2012.1745
Arimatsu K, Yamada H, Miyazawa H et al (2014) Oral pathobiont induces systemic inflammation and metabolic changes associated with alteration of gut microbiota. Sci Rep. doi:10.1038/srep04828
Arumugam M, Raes J, Pelletier E et al (2011) Enterotypes of the human gut microbiome. Nature 473:174–180. doi:10.1038/nature09944
Aufderheide AC, Conrado R (1998) The cambridge encyclopedia of human paleopathology. Cambridge University Press, Cambridge
Behr MA (2013) Evolution of Mycobacterium tuberculosis. Adv Exp Med Biol 783:81–91. doi:10.1007/978-1-4614-6111-1_4
Berg M, Hudson P (1992) Rehabilitating the industrial revolution. Econ Hist Rev 45:24. doi:10.2307/2598327
Blaser MJ (2014) Missing microbes: how the overuse of antibiotics is fueling our modern plagues, 1st edn. Henry Holt and Co., New York
Blaser MJ, Dominguez-Bello MG, Contreras M et al (2012) Distinct cutaneous bacterial assemblages in a sampling of South American Amerindians and US residents
Blatt SH, Redmond BG, Cassman V, Sciulli PW (2011) Dirty teeth and ancient trade: evidence of cotton fibres in human dental calculus from late Woodland, Ohio. Int J Osteoarchaeol 21:669–678. doi:10.1002/oa.1173
Bocherens H, Billiou D, Mariotti A et al (2001) New isotopic evidence for dietary habits of Neandertals from Belgium. http://adelaideaus.library.ingentaconnect.com/content/ap/hu/2001/00000040/00000006/art00452. Accessed 12 Dec 2013
Bos KI, Schuenemann VJ, Golding GB et al (2011) A draft genome of Yersinia pestis from victims of the black death 478:506–510
Brandt G, Haak W, Adler CJ et al (2013) Ancient DNA reveals key stages in the formation of central European mitochondrial genetic diversity. Science 342:257–261. doi:10.1126/science.1241844
Bravo JA, Forsythe P, Chew MV et al (2011) Ingestion of Lactobacillus strain regulates emotional behavior and central GABA receptor expression in a mouse via the vagus nerve. Proc Natl Acad Sci 108:16050–16055. doi:10.1073/pnas.1102999108
Breton J, Massart S, Vandamme P et al (2013) Ecotoxicology inside the gut: impact of heavy metals on the mouse microbiome. BMC Pharmacol Toxicol 14:62. doi:10.1186/2050-6511-14-62
Brucker RM, Bordenstein SR (2013) The hologenomic basis of speciation: gut bacteria cause hybrid lethality in the genus nasonia. Science 341:667–669. doi:10.1126/science.1240659
Burger J, Kirchner M, Bramanti B et al (2007) Absence of the lactase-persistence-associated allele in early Neolithic Europeans. Proc Natl Acad Sci USA 104:3736–3741
Cabrera-Rubio R, Collado MC, Laitinen K et al (2012) The human milk microbiome changes over lactation and is shaped by maternal weight and mode of delivery. Am J Clin Nutr 96:544–551. doi:10.3945/ajcn.112.037382
Cameron AJ, Zimmet PZ, Dunstan DW et al (2003) Overweight and obesity in Australia: the 1999–2000 Australian diabetes, obesity and lifestyle study (AusDiab). Med J Aust 178:427–432
Cangemi de Gutierrez R, Santos V, Nader-Macías ME (2001) Protective effect of intranasally inoculated Lactobacillus fermentum against Streptococcus pneumoniae challenge on the mouse respiratory tract. FEMS Immunol Med Microbiol 31:187–195. doi:10.1111/j.1574-695X.2001.tb00519.x
Caporaso JG, Lauber CL, Walters WA et al (2012) Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J 6:1621–1624. doi:10.1038/ismej.2012.8
Caufield PW, Wannemuehler YM, Hansen JB (1982) Familial clustering of the Streptococcus mutans cryptic plasmid strain in a dental clinic population. Infect Immun 38:785–787
Chassard C, Delmas E, Robert C, Bernalier-Donadille A (2010) The cellulose-degrading microbial community of the human gut varies according to the presence or absence of methanogens. FEMS Microbiol Ecol 74:205–213. doi:10.1111/j.1574-6941.2010.00941.x
Cho I, Yamanishi S, Cox L et al (2012) Antibiotics in early life alter the murine colonic microbiome and adiposity. Nature 488:621–626. doi:10.1038/nature11400
Comas I, Coscolla M, Luo T et al (2013) Out-of-Africa migration and Neolithic coexpansion of Mycobacterium tuberculosis with modern humans. Nat Genet 45:1176–1182. doi:10.1038/ng.2744
Consortium THMP (2012) Structure, function and diversity of the healthy human microbiome. Nature 486:207–214
Contreras M, Costello EK, Hidalgo G et al (2010) The bacterial microbiota in the oral mucosa of rural Amerindians. Microbiol Read Engl 156:3282–3287. doi:10.1099/mic.0.043174-0
Cooper A, Poinar HN (2000) Ancient DNA: do it right or not at all. Science 289:1139–1139. doi: 10.1126/science.289.5482.1139b
Cooper A, Stringer CB (2013) Did the Denisovans cross wallace’s line? Science 342:321–323. doi:10.1126/science.1244869
Cornejo OE, Lefébure T, Pavinski Bitar PD et al (2013) Evolutionary and population genomics of the cavity causing bacteria streptococcus mutans. Mol Biol Evol. doi:10.1093/molbev/mss278
David LA, Maurice CF, Carmody RN et al (2013) Diet rapidly and reproducibly alters the human gut microbiome. Nature. doi:10.1038/nature12820
Davis R (1962) English Foreign trade, 1700–17741. Econ Hist Rev 15:285–303. doi:10.1111/j.1468-0289.1962.tb02239.x
Deer N (1949) The history of sugar, vol 1. Chapman and Hall Ltd., London
De La Fuente C, Flores S, Moraga M (2013) DNA from human ancient bacteria: a novel source of genetic evidence from archaeological dental calculus. Archaeometry 55:767–778. doi:10.1111/j.1475-4754.2012.00707.x
Dobney K, Brothwell D (1988) A scanning electron microscope study of archaeological dental calculus. In: Scanning electron microscopy in archaeology. Oxford, pp 372–385
Dominguez-Bello MG, Costello EK, Contreras M et al (2010) Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proc Natl Acad Sci 201002601. doi:10.1073/pnas.1002601107
Ennever J, Vogel JJ, Benson LA (1973) Lipid and calculus matrix calcification in vitro. J Dent Res 52:1056–1059
Filippo CD, Cavalieri D, Paola MD et al (2010) Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc Natl Acad Sci 107:14691–14696. doi:10.1073/pnas.1005963107
Flight MH (2014) Neurodevelopmental disorders: the gut-microbiome-brain connection. Nat Rev Neurosci 15:65–65. doi:10.1038/nrn3669
Fujimura KE, Demoor T, Rauch M et al (2014) House dust exposure mediates gut microbiome Lactobacillus enrichment and airway immune defense against allergens and virus infection. Proc Natl Acad Sci 111:805–810. doi:10.1073/pnas.1310750111
Gonzalez DJ, Haste NM, Hollands A et al (2011) Microbial competition between Bacillus subtilis and Staphylococcus aureus monitored by imaging mass spectrometry. Microbiology 157:2485–2492. doi:10.1099/mic.0.048736-0
Graham JC (1981) The French connection in the early history of canning. J R Soc Med 74:374–381. doi:10.1177/014107688107400511
Green RE, Krause J, Briggs AW et al (2010) A draft sequence of the Neandertal genome. Science 328:710–722. doi:10.1126/science.1188021
Haviland W, Walrath D, Prins H, McBride B (2010) Evolution and prehistory: the human challenge. Cengage Learning
Henry AG, Brooks AS, Piperno DR (2010) Microfossils in calculus demonstrate consumption of plants and cooked foods in Neanderthal diets (Shanidar III, Iraq. Proc Natl Acad Sci, Spy I and II, Belgium). doi:10.1073/pnas.1016868108
Henry AG, Piperno DR (2008) Using plant microfossils from dental calculus to recover human diet: a case study from Tell al-Raqā’i, Syria. J Archaeol Sci 35:1943–1950. doi:10.1016/j.jas.2007.12.005
Hermanussen M (2006) In: Fogel RW The escape from hunger and premature death, 1700–2100. Europe, America, and the third world. (Cambridge University Press, Cambridge, 2004), p 191. (£16.99, ISBN 0-521-00488-8, Paperback; £40.00, ISBN 0-521-80878-2, Hardback. J Biosoc Sci 38:571–572)
Hokama T, Hamamoto I, Takenaka S et al (1996) Throat microflora in breastfed and formula-fed infants. J Trop Pediatr 42:324–326
Hollox E, Hurles M, Kivisild T, Tyler-Smith C (2013) Human evolutionary genetics, 2nd edn. Garland Science, New York
Hooper LV, Gordon JI (2001) Commensal host-bacterial relationships in the gut. Science 292:1115–1118
Hu P, Brodie EL, Suzuki Y et al (2005) Whole-genome transcriptional analysis of heavy metal stresses in Caulobacter crescentus. J Bacteriol 187:8437–8449. doi:10.1128/JB.187.24.8437-8449.2005
Jhamnani K, Shivakumar V, Kalmady S et al (2013) Successful use of add-on minocycline for treatment of persistent negative symptoms in schizophrenia. J Neuropsychiatry Clin Neurosci 25:E06–07. doi:10.1176/appi.neuropsych.11120376
Jin L, Su B (2000) Natives or immigrants: modern human origin in east Asia. Nat Rev Genet 1:126–133. doi:10.1038/35038565
Jones PM (2009) Industrial enlightenment: science, technology and culture in Birmingham and the West Midlands, 1760–1820. Manchester University Press, Manchester
Kau AL, Ahern PP, Griffin NW et al (2011a) Human nutrition, the gut microbiome, and immune system: envisioning the future. Nature 474:327–336. doi:10.1038/nature10213
Kau AL, Ahern PP, Griffin NW et al (2011b) Human nutrition, the gut microbiome and the immune system. Nature 474:327–336
Lax S, Smith DP, Hampton-Marcell J et al (2014) Longitudinal analysis of microbial interaction between humans and the indoor environment. Science 345:1048–1052. doi:10.1126/science.1254529
Leff JW, Fierer N (2013) Bacterial communities associated with the surfaces of fresh fruits and vegetables. PLoS ONE 8:e59310. doi:10.1371/journal.pone.0059310
Ley RE, Bäckhed F, Turnbaugh P et al (2005) Obesity alters gut microbial ecology. Proc Natl Acad Sci USA 102:11070–11075. doi:10.1073/pnas.0504978102
Li J, Nasidze I, Quinque D et al (2013) The saliva microbiome of pan and homo. BMC Microbiol 13:204. doi:10.1186/1471-2180-13-204
Meyer M, Fu Q, Aximu-Petri A et al (2014) A mitochondrial genome sequence of a hominin from Sima de los Huesos. Nature 505:403–406. doi:10.1038/nature12788
Meyer M, Kircher M, Gansauge M-T et al (2012) A high-coverage genome sequence from an archaic denisovan individual. Science 338:222–226. doi:10.1126/science.1224344
Moeller AH, Degnan PH, Pusey AE et al (2012) Chimpanzees and humans harbour compositionally similar gut enterotypes. Nat Commun 3:1179. doi:10.1038/ncomms2159
Moeller AH, Peeters M, Ndjango J-B et al (2013) Sympatric chimpanzees and gorillas harbor convergent gut microbial communities. Genome Res 23:1715–1720. doi:10.1101/gr.154773.113
Muegge BD, Kuczynski J, Knights D et al (2011) Diet drives convergence in gut microbiome functions across mammalian phylogeny and within humans. Science 332:970–974. doi:10.1126/science.1198719
New Research Confirms “Out Of Africa” Theory of human evolution. In: ScienceDaily. http://www.sciencedaily.com/releases/2007/05/070509161829.htm. Accessed 10 Sep 2014
Okada H, Kuhn C, Feillet H, Bach J-F (2010) The “hygiene hypothesis” for autoimmune and allergic diseases: an update. Clin Exp Immunol 160:1–9. doi:10.1111/j.1365-2249.2010.04139.x
Payne AN, Chassard C, Lacroix C (2012) Gut microbial adaptation to dietary consumption of fructose, artificial sweeteners and sugar alcohols: implications for host–microbe interactions contributing to obesity. Obes Rev 13:799–809. doi:10.1111/j.1467-789X.2012.01009.x
Quigley L, McCarthy R, O’Sullivan O et al (2013) The microbial content of raw and pasteurized cow milk as determined by molecular approaches. J Dairy Sci 96:4928–4937. doi:10.3168/jds.2013-6688
Ramotar K, Conly JM, Chubb H, Louie TJ (1984) Production of menaquinones by intestinal anaerobes. J Infect Dis 150:213–218
Sajantila A (2013) Major historical dietary changes are reflected in the dental microbiome of ancient skeletons. Investig Genet 4:1–2. doi:10.1186/2041-2223-4-10
Sankararaman S, Patterson N, Li H et al (2012) The date of interbreeding between Neandertals and modern humans. PLoS Genet 8:e1002947. doi:10.1371/journal.pgen.1002947
Scarre C (2013) The human past: world prehistory and the development of human societies, 3rd edn edn. Thames & Hudson, New York
Schnorr SL, Candela M, Rampelli S et al (2014) Gut microbiome of the Hadza hunter-gatherers. Nat Commun. doi:10.1038/ncomms4654
Soares P, Ermini L, Thomson N et al (2009) Correcting for purifying selection: an improved human mitochondrial molecular clock. Am J Hum Genet 84:740–759. doi:10.1016/j.ajhg.2009.05.001
Song SJ, Lauber C, Costello EK et al (2013) Cohabiting family members share microbiota with one another and with their dogs. eLife 2:e00458. doi:10.7554/eLife.00458
Stecher B, Robbiani R, Walker AW et al (2007) Salmonella enterica Serovar Typhimurium exploits inflammation to compete with the intestinal microbiota. PLoS Biol 5:e244. doi:10.1371/journal.pbio.0050244
Tattersall I (2009) Human origins: out of Africa. Proc Natl Acad Sci 106:16018–16021. doi:10.1073/pnas.0903207106
Tito RY, Knights D, Metcalf J et al (2012) Insights from characterizing extinct human gut microbiomes. PLoS ONE 7:e51146. doi:10.1371/journal.pone.0051146
Wade WG (2013) The oral microbiome in health and disease. Pharmacol Res 69:137–143. doi:10.1016/j.phrs.2012.11.006
Weyrich LS, Feaga HA, Park J et al (2013) Resident microbiota affect Bordetella pertussis infectious dose and host specificity. J Infect Dis jit597. doi:10.1093/infdis/jit597
Willing BP, Vacharaksa A, Croxen M et al (2011) Altering host resistance to infections through microbial transplantation. PLoS ONE 6:e26988. doi:10.1371/journal.pone.0026988
Wolpoff MH, Hawks J, Caspari R (2000) Multiregional, not multiple origins. Am J Phys Anthropol 112:129–136. doi:10.1002/(SICI)1096-8644(200005)112:1<129:AID-AJPA11>3.0.CO;2-K
Wood B, Richmond BG (2000) Human evolution: taxonomy and paleobiology. J Anat 197:19–60. doi:10.1046/j.1469-7580.2000.19710019.x
Yatsunenko T, Rey FE, Manary MJ et al (2012) Human gut microbiome viewed across age and geography. Nature 486:222–227. doi:10.1038/nature11053
Yildirim S, Yeoman CJ, Sipos M et al (2010) Characterization of the fecal microbiome from non-human wild primates reveals species specific microbial communities. PLoS ONE 5:e13963. doi:10.1371/journal.pone.0013963
Yong E (2012) Gut microbial “enterotypes” become less clear-cut. Nature. doi:10.1038/nature.2012.10276
WHO (2004) | The world health report 2004—changing history. http://www.who.int/whr/2004/en/. Accessed 12 Jan 2012
Acknowledgments
Many thanks for the photographs of calculus and a coprolite that were provided by Dr. Julien Soubrier and Alexander Boast at the University of Adelaide.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Glossary
- Allopatric
-
A descriptive term of processes, such as evolution, that happen to two different populations of organisms separated into different geographical locations
- Amerindians
-
Indigenous populations that are currently living in North or South America, which are typically living without contact with Westernized civilizations
- Anatomically modern humans
-
Hominids that are morphologically similar to modern Homo sapiens sapiens, i.e. modern humans, and likely originated from Africa around 200,000 years ago
- Archaic humans
-
Hominids that share a lineage with Homo sapiens after the evolutionary split from chimpanzees, including Neandertals and Denisovans
- Bacterial ‘fingerprints’ or fingerprinting
-
This is a technique that sequences a single gene conserved across all bacterial species, typically the gene encoding the 16S ribosomal RNA subunit, which provides a picture of all the bacterial species present and their abundances. These sequences can be highly specific to an individual, acting the same way a fingerprint does in forensics
- Biofilm
-
This is a diverse bacterial community that forms works together as a single organism and can form on surfaces of hot springs, pipes, or even human teeth
- Convergent evolution
-
An evolutionary process that results in similar outcomes, i.e. function, even though the species that are evolving are in different locations or are unrelated
- Enterotypes
-
A simple way of classifying gut microbiomes based on the largest proportions of dominant bacterial phyla present in a sample
- Hygiene hypothesis
-
The theory that a lack of exposure to microbes (or an increased exposure to sterile environments) increases one’s susceptibility to disease by failing to stimulate the immune system during development
- Indigenous
-
A modern human population that is native to a specific place over a long time span, usually prior to European colonization during the colonial period
- Industrial Revolution
-
A cultural change that occurred the eighteenth and nineteenth centuries, following the invention of the machine, and lead to numerous social and economic changes
- Isotope analysis
-
The identification of chemical elements within compounds that are present in material to determine differences in composition, variation, or change, i.e. using carbon isotopes to track the diet of humans
- Linear Pottery culture (LBK)
-
Linearbandkermik (LBK) is a culture existing about ~7500 years before present, which were Europe’s first farmers and are demarcated by a distinct banding pattern on the pottery
- Microbiome
-
Any microbial community that exists in one space, i.e. the human body
- Metagenome
-
The defining term of all of the genomes that exist in the human body, which includes the human genome and the bacterial or microbial genomes present
- Metabarcoding
-
A technique that sequences one ‘barcoding’ or identifying gene conserved across a wide array of species as a means of surveying biodiversity
- Next-generation DNA sequencing techniques
-
DNA sequencing by any diverse means to sequencing full genomes or millions of different sequencings in one experiment
- Neolithic Revolution
-
A cultural and revolutionary process in which humans adopt farming techniques, leading to a whole host of social and economic changes
- Oral caries (cavities)
-
An oral disease caused primarily by S. mutans, which deteriorates the enamel on the tooth surface and exposes nervous tissue
- Post-depositional bias
-
Alterations to microbial communities after the sample is deposited or collected that occur due to environmental or decompositional factors
- Periodontal disease
-
An oral disease of the gingiva or gums, in which diverse bacterial communities stimulate inflammation and destroy gingival tissue
- Sanger DNA sequencing techniques
-
Chain termination DNA sequencing invented by Peter Sanger in 1977, which was a common method to determine the sequencing of deoxynucleotides in a single strand of only one DNA molecule
- Scanning electron microscopy
-
A form of visualization that identifies the shapes of objects via a focused beam of electrons, illuminating the size and shape of many microorganisms
- Sedentary lifestyles
-
Modern human habits that revolve around activities that do not involve physical movement (walking or running), resulting in the majority of a person’s time spent sitting or not moving
- Sympatric
-
A descriptive term of processes, such as evolution, that happen to organisms located in the same location
- Taphonomy
-
A process of degradation that ancient samples undergo, where DNA is enzymatically broken down and degraded, limiting the genetic information that can be obtained from a material. The process is highly dynamic and is dependent upon a vast array of variables, including temperature, water content, and soil chemistry
Rights and permissions
Copyright information
© 2015 Springer International Publishing Switzerland
About this chapter
Cite this chapter
Weyrich, L.S. (2015). Evolution of the Human Microbiome and Impacts on Human Health, Infectious Disease, and Hominid Evolution. In: Gontier, N. (eds) Reticulate Evolution. Interdisciplinary Evolution Research, vol 3. Springer, Cham. https://doi.org/10.1007/978-3-319-16345-1_9
Download citation
DOI: https://doi.org/10.1007/978-3-319-16345-1_9
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-16344-4
Online ISBN: 978-3-319-16345-1
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)