Insights from paleomicrobiology into the indigenous peoples of pre-colonial America - A Review
Identifieur interne : 000416 ( Pmc/Corpus ); précédent : 000415; suivant : 000417Insights from paleomicrobiology into the indigenous peoples of pre-colonial America - A Review
Auteurs : Millie I. Darling ; Helen D. DonoghueSource :
- Memórias do Instituto Oswaldo Cruz [ 0074-0276 ] ; 2014.
Abstract
This review investigates ancient infectious diseases in the Americas dated to the
pre-colonial period and considers what these findings can tell us about the history
of the indigenous peoples of the Americas. It gives an overview, but focuses on four
microbial pathogens from this period:
Url:
DOI: 10.1590/0074-0276140589
PubMed: 24714964
PubMed Central: 4015261
Links to Exploration step
PMC:4015261Le document en format XML
<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Insights from paleomicrobiology into the indigenous peoples
of pre-colonial America - A Review</title>
<author><name sortKey="Darling, Millie I" sort="Darling, Millie I" uniqKey="Darling M" first="Millie I" last="Darling">Millie I. Darling</name>
<affiliation><nlm:aff id="aff1">Division of Biosciences</nlm:aff>
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<author><name sortKey="Donoghue, Helen D" sort="Donoghue, Helen D" uniqKey="Donoghue H" first="Helen D" last="Donoghue">Helen D. Donoghue</name>
<affiliation><nlm:aff id="aff1">Division of Biosciences</nlm:aff>
</affiliation>
<affiliation><nlm:aff id="aff2">Division of Infection and Immunity, Centre for Clinical Microbiology, University College London, London,<country>UK</country>
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<sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Insights from paleomicrobiology into the indigenous peoples
of pre-colonial America - A Review</title>
<author><name sortKey="Darling, Millie I" sort="Darling, Millie I" uniqKey="Darling M" first="Millie I" last="Darling">Millie I. Darling</name>
<affiliation><nlm:aff id="aff1">Division of Biosciences</nlm:aff>
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</author>
<author><name sortKey="Donoghue, Helen D" sort="Donoghue, Helen D" uniqKey="Donoghue H" first="Helen D" last="Donoghue">Helen D. Donoghue</name>
<affiliation><nlm:aff id="aff1">Division of Biosciences</nlm:aff>
</affiliation>
<affiliation><nlm:aff id="aff2">Division of Infection and Immunity, Centre for Clinical Microbiology, University College London, London,<country>UK</country>
</nlm:aff>
</affiliation>
</author>
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<series><title level="j">Memórias do Instituto Oswaldo Cruz</title>
<idno type="ISSN">0074-0276</idno>
<idno type="eISSN">1678-8060</idno>
<imprint><date when="2014">2014</date>
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<front><div type="abstract" xml:lang="en"><p>This review investigates ancient infectious diseases in the Americas dated to the
pre-colonial period and considers what these findings can tell us about the history
of the indigenous peoples of the Americas. It gives an overview, but focuses on four
microbial pathogens from this period: <italic>Helicobacter pylori</italic>
,
<italic>Mycobacterium tuberculosis</italic>
, <italic>Trypanosoma cruzi</italic>
and <italic>Coccidioides immitis</italic>
, which cause stomach ulceration and gastric
cancer, tuberculosis, Chagas disease and valley fever, respectively. These pathogens
were selected as <italic>H. pylori</italic>
can give insight into ancient human
migrations into the Americas, <italic>M. tuberculosis </italic>
is associated with
population density and urban development, <italic>T. cruzi </italic>
can elucidate
human living conditions and <italic>C. immitis</italic>
can indicate agricultural
development. A range of methods are used to diagnose infectious disease in ancient
human remains, with DNA analysis by polymerase chain reaction one of the most
reliable, provided strict precautions are taken against cross contamination. The
review concludes with a brief summary of the changes that took place after European
exploration and colonisation.</p>
</div>
</front>
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<pmc article-type="review-article"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">Mem Inst Oswaldo Cruz</journal-id>
<journal-id journal-id-type="iso-abbrev">Mem. Inst. Oswaldo Cruz</journal-id>
<journal-title-group><journal-title>Memórias do Instituto Oswaldo Cruz</journal-title>
</journal-title-group>
<issn pub-type="ppub">0074-0276</issn>
<issn pub-type="epub">1678-8060</issn>
<publisher><publisher-name>Instituto Oswaldo Cruz, Ministério da Saúde</publisher-name>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">24714964</article-id>
<article-id pub-id-type="pmc">4015261</article-id>
<article-id pub-id-type="publisher-id">0074-0276140589</article-id>
<article-id pub-id-type="doi">10.1590/0074-0276140589</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Review</subject>
</subj-group>
</article-categories>
<title-group><article-title>Insights from paleomicrobiology into the indigenous peoples
of pre-colonial America - A Review</article-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Darling</surname>
<given-names>Millie I</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Donoghue</surname>
<given-names>Helen D</given-names>
</name>
<xref ref-type="aff" rid="aff1">1</xref>
<xref ref-type="aff" rid="aff2">2</xref>
<xref ref-type="corresp" rid="c01">+</xref>
</contrib>
</contrib-group>
<aff id="aff1"><label>1</label>
Division of Biosciences</aff>
<aff id="aff2"><label>2</label>
Division of Infection and Immunity, Centre for Clinical Microbiology, University College London, London,<country>UK</country>
</aff>
<author-notes><corresp id="c01"><label>+</label>
Corresponding author: <email>h.donoghue@ucl.ac.uk</email>
</corresp>
</author-notes>
<pub-date pub-type="epub"><day>04</day>
<month>4</month>
<year>2014</year>
</pub-date>
<pub-date pub-type="ppub"><month>4</month>
<year>2014</year>
</pub-date>
<volume>109</volume>
<issue>2</issue>
<fpage>131</fpage>
<lpage>139</lpage>
<history><date date-type="received"><day>19</day>
<month>12</month>
<year>2013</year>
</date>
<date date-type="received"><day>7</day>
<month>2</month>
<year>2014</year>
</date>
</history>
<permissions><license license-type="open-access" xlink:href="http://creativecommons.org/licenses/by-nc/3.0/"><license-p>This is an Open Access article distributed under the terms of the Creative
Commons Attribution Non-Commercial License, which permits unrestricted
non-commercial use, distribution, and reproduction in any medium, provided the
original work is properly cited.</license-p>
</license>
</permissions>
<abstract><p>This review investigates ancient infectious diseases in the Americas dated to the
pre-colonial period and considers what these findings can tell us about the history
of the indigenous peoples of the Americas. It gives an overview, but focuses on four
microbial pathogens from this period: <italic>Helicobacter pylori</italic>
,
<italic>Mycobacterium tuberculosis</italic>
, <italic>Trypanosoma cruzi</italic>
and <italic>Coccidioides immitis</italic>
, which cause stomach ulceration and gastric
cancer, tuberculosis, Chagas disease and valley fever, respectively. These pathogens
were selected as <italic>H. pylori</italic>
can give insight into ancient human
migrations into the Americas, <italic>M. tuberculosis </italic>
is associated with
population density and urban development, <italic>T. cruzi </italic>
can elucidate
human living conditions and <italic>C. immitis</italic>
can indicate agricultural
development. A range of methods are used to diagnose infectious disease in ancient
human remains, with DNA analysis by polymerase chain reaction one of the most
reliable, provided strict precautions are taken against cross contamination. The
review concludes with a brief summary of the changes that took place after European
exploration and colonisation.</p>
</abstract>
<kwd-group><kwd>ancient DNA</kwd>
<kwd><italic>Helicobacter pylori</italic>
</kwd>
<kwd><italic>Mycobacterium tuberculosis</italic>
</kwd>
<kwd><italic>Trypanosoma cruzi</italic>
</kwd>
<kwd><italic>Coccidioides immitis</italic>
</kwd>
</kwd-group>
<counts><ref-count count="89"></ref-count>
<page-count count="189"></page-count>
</counts>
</article-meta>
</front>
<body><p>Infectious disease is the presence and growth of pathogenic biological agents within a
host, usually resulting in a clinically evident illness. Pathogenic biological agents
include bacteria, viruses, fungi and parasites. Many pathogens have a very long history
with the human species, with several having an association with primates long predating the
evolution of <italic>Homo sapiens</italic>
. Humans and pathogens have therefore evolved
together and had a great influence on each other. Because human and pathogen history is so
intertwined, much fascinating information can be learnt about ancient humans by studying
ancient pathogens.</p>
<p>For thousands of years North and South America have been home to different human
populations. Prior to European contact in 1492, these populations lived in the Americas
effectively isolated from the rest of the world. This resulted in very different societies
and human infectious diseases developing in the Eastern and Western Hemispheres. There are
written records of many of the past human infectious diseases of Eurasia, but due to the
destruction by European colonialists, it is not known if there were ever any local records
of past human infectious diseases of the Americas. To investigate these diseases we
therefore have to investigate ancient human remains through paleopathological and, more
recently, paleomicrobiological studies. Paleomicrobiology is an interdisciplinary subject
that necessarily overlaps with biology, archaeology, history and anthropology to
investigate past infectious diseases (<xref rid="B30" ref-type="bibr">Donoghue
2008</xref>
). Here, paleomicrobiological studies of the Americas are reviewed to determine
what they can tell us about the pre-colonial history of the indigenous peoples of the
Americas. Many earlier authors have explored this topic (<xref rid="B70" ref-type="bibr">Patrucco et al. 1983</xref>
, <xref rid="B86" ref-type="bibr">Verano 1997</xref>
, <xref rid="B73" ref-type="bibr">Ramenofsky et al. 2003</xref>
, <xref rid="B43" ref-type="bibr">Gerszten et al. 2012</xref>
, <xref rid="B4" ref-type="bibr">Anastasiou & Mitchell
2013</xref>
, <xref rid="B39" ref-type="bibr">Frías et al. 2013</xref>
, <xref rid="B47" ref-type="bibr">Harper & Armelagos 2013</xref>
) and have laid the
foundation for this review.</p>
<p>Infectious disease transmission occurs between humans in a variety of ways, ranging from
inhalation of infected moisture droplets, faecal-oral transmission, infection of wounds
from the environment, to transmission <italic>via</italic>
an insect vector. Population
density, association with animals, proximity of living areas to water sources and human
waste, trade links, genetic susceptibility and the use of agricultural methods such as
irrigation influence the infectious diseases that occur in the human population. For
example, a disease such as tuberculosis that is dependent on respiratory transmission needs
a large dense human population to be successfully maintained and transmitted.</p>
<p>It is generally believed that humans first migrated to the Americas approximately 13,000
years ago <italic>via</italic>
the Bering Land Bridge (Beringia) while sea levels were
significantly low. The humans who first arrived on the landmass that came to be known as
North and South America were battling against infectious diseases they brought with them
from Asia and those they acquired in the Americas. The aim is not to discuss in depth every
pathogen that plagued the pre-colonial Americas, so this review uses selected infectious
diseases as examples of the different relationships between humans and their environment.
The first of two sections discusses “heirloom” infectious diseases brought to the Americas
by the humans that first migrated there and focuses on two selected pathogens,
<italic>Helicobacter pylori</italic>
and <italic>Mycobacterium tuberculosis</italic>
.
The second section discusses diseases associated with the local environment, based on two
pathogens, <italic>Trypanosoma cruzi</italic>
and <italic>Coccidioides immitis</italic>
,
that began infecting humans after they settled in the Americas, causing “souvenir”
infectious diseases (<xref rid="B55" ref-type="bibr">Kliks 1990</xref>
).</p>
<p><italic>Paleomicrobiological methods</italic>
- An important method to investigate ancient
infectious diseases is the analysis of microbial ancient DNA (aDNA) by the polymerase chain
reaction (PCR). PCR revolutionised paleomicrobiological research because it enables trace
amounts of fragmented microbial aDNA to be identified and amplified. Thermal cycling is
used to amplify aDNA. DNA polymerase and primers - short oligonucleotides that flank a
specific target <italic>locus</italic>
in the DNA of the pathogen being investigated - are
the basis of the method. Microbial aDNA is only preserved under suitable environmental
conditions such as low temperatures, dryness and absence of sunlight (<xref rid="B30" ref-type="bibr">Donoghue 2008</xref>
).</p>
<p>Initially, bacterial pathogens were investigated using PCR targets present as multiple
copies in every cell. The same approach can be used for eukaryotic pathogens, such as
flagellated protozoa, where the kinetoplast provides an excellent target region (<xref rid="B15" ref-type="bibr">Aufderheide et al. 2004</xref>
). Other studies examine nuclear
or mitochondrial DNA. As PCR is such a sensitive technique there is great danger of
contamination by modern DNA either from the site or the laboratory. It is therefore
essential to use procedures to prevent contamination (<xref rid="B31" ref-type="bibr">Donoghue 2009</xref>
) including wearing protective clothing, physical isolation of the
work area, removal of the surface layer of samples, consideration of past studies that have
occurred in the laboratory and the use of negative control amplifications to detect
contamination. Results should be reproducible in other laboratories using the same
contamination control procedures.</p>
<p>Today, next generation sequencing, or whole genome sequencing, reduce the risk of
contamination, as there is no DNA amplification (<xref rid="B32" ref-type="bibr">Donoghue
2013</xref>
). Extracted DNA is fragmented, end-repaired and tagged, prior to analysis by
high throughput sequencers. When analysing aDNA, DNA fragment size gating can eliminate any
contaminating modern DNA. The use of magnetic beads or microarrays coated with
single-stranded DNA from a target genome can enrich aDNA recovery. The resulting sequences
are aligned and bioinformatics analysis used to identify all the genomes present in a
sample.</p>
<p>The samples for paleomicrobiological analyses can come from many different locations in
ancient human remains, mineralised or mummified. Microbial aDNA can occur in the dental
pulp of teeth, bone, mummified tissues (<xref rid="B33" ref-type="bibr">Drancourt &
Raoult 2005</xref>
) or coprolites. Bodies may be mummified naturally or by human
intervention. As mentioned by <xref rid="B83" ref-type="bibr">Swanston et al.
(2011)</xref>
, naturally mummified individuals are often more suitable for bacterial DNA
studies because the absence of any embalming processes leaves the local environment in the
tissues unchanged. Coprolites are fossilised faeces that are useful sources of pathogen
aDNA, especially for investigations of intestinal parasites (<xref rid="B9" ref-type="bibr">Araújo et al. 2011</xref>
).</p>
<p>The mycobacteria, including the <italic>M. tuberculosis</italic>
complex, have some unique
features that facilitate the persistence of their aDNA. These microbes have DNA with a high
proportion of guanine and cytosine that increases its stability and thick lipid-rich cell
walls. The bacterial cell walls protect the microbial DNA from the lytic enzymes of the
host cell when undergoing autolysis or necrosis. Both these features enable the direct
detection and characterisation of aDNA and lipid biomarkers of <italic>M.
tuberculosis</italic>
in ancient specimens. Indeed, the use of whole genome sequencing
has confirmed that <italic>M. tuberculosis</italic>
aDNA is better preserved than human
aDNA in the same specimens (<xref rid="B25" ref-type="bibr">Chan et al. 2013</xref>
).
Therefore, information can sometimes be gained from human remains based on the infecting
<italic>M. tuberculosis</italic>
aDNA rather than host aDNA.</p>
<p><xref rid="B85" ref-type="bibr">Tran et al. (2011)</xref>
described the variety of methods
to diagnose ancient disease using techniques other than the analysis of aDNA via PCR.
Biomolecules such as mycolic acids (of mycobacteria) and proteins can be detected in
ancient specimens using immunohistochemistry, immunochromatography and ELISA techniques.
Protein detection by mass spectroscopy and immuno-PCR are other potentially useful
techniques. As with DNA analysis by PCR, strict protocols must be followed to avoid
contamination and ensure authenticity of data.</p>
<p>The direct observation of ancient human material remains an important technique to diagnose
ancient infectious disease, but was especially so before the invention of molecular
methods. Observations include the direct detection of parasites in human remains or the
paleopathology caused by the presence of the pathogen. For example, a pre-Columbian mummy
of a young man in southern Peru had numerous granulomatous lesions and vesicles on his
skin. Giemsa staining and microscopy showed typical clumps of bacilli with morphology
similar to <italic>Bartonella bacilliformis</italic>
, the cause of Carrión’s disease,
spread by sandflies, that results in acute fatal anaemia or a condition known as verruga -
characterised by wart-like lesions (<xref rid="B2" ref-type="bibr">Allison et al.
1974a</xref>
). Many pathogens, including <italic>M. tuberculosis</italic>
, trigger
visible skeletal lesions in human remains and such material was used in the first study to
diagnose ancient tuberculosis by the detection of pathogenic bacterial aDNA (<xref rid="B81" ref-type="bibr">Spigelman & Lemma 1993</xref>
). Skeletal observations are
essential when DNA analysis and other biomolecular methods are inconclusive, but are often
problematic because different diseases can cause similar skeletal changes. Therefore
paleopathology alone may give insufficient evidence to diagnose a disease. Ideally,
morphological observation and biomolecular methods should be used to complement each other
and strengthen the evidence that a particular pathogen was present. Dating of ancient
specimens is a very important part of paleomicrobiological research. A variety of methods
are used, including the investigation of artefacts associated with the remains, the
archaeological and architectural features of the surrounding area, the stratigraphic
provenance of the remains and radiocarbon dating of the skeletons themselves and associated
organic matter.</p>
<p><italic>Heirloom human infectious diseases in the Americas</italic>
- This section
discusses human infectious diseases brought to the Americas with the humans that first
migrated there. Heirloom human infectious diseases are caused by bacteria, viruses or
parasites (<xref rid="B5" ref-type="bibr">Araújo & Ferreira 2000</xref>
), which have
evolved with humans in Africa, Europe and Asia. There are many studies and reviews of the
paleoparasitology of the Americas, including protozoa (<xref rid="B69" ref-type="bibr">Ortega & Bonavia 2003</xref>
, <xref rid="B27" ref-type="bibr">Costa et al.
2009</xref>
), roundworms (<xref rid="B7" ref-type="bibr">Araújo et al. 2008a</xref>
,
<xref rid="B59" ref-type="bibr">Leles et al. 2008</xref>
), pinworms (<xref rid="B52" ref-type="bibr">Iñiguez et al. 2006</xref>
), fleas and lice (<xref rid="B74" ref-type="bibr">Raoult et al. 2008</xref>
, <xref rid="B29" ref-type="bibr">Dittmar 2009</xref>
). However, there are far fewer reports of viral (<xref rid="B42" ref-type="bibr">Gentry et al. 1988</xref>
, <xref rid="B60" ref-type="bibr">Li
et al. 1999</xref>
) or bacterial infections. <xref rid="B11" ref-type="bibr">Arriaza et
al. (2013)</xref>
used the distribution of head lice (<italic>Pediculus humanus
capitis</italic>
) in archaic mummies from northern Chile as a bioindicator of cultural
behaviour, as the lice are associated with crowded living conditions. The human head louse
has also given insights into migration and the human colonisation of the New World (<xref rid="B13" ref-type="bibr">Ascunce et al. 2013</xref>
). <xref rid="B88" ref-type="bibr">Wirth et al. (2005)</xref>
reviewed the association of various microbes with their host
and examined the most appropriate candidates that can act as markers to enable human
migrations to be tracked. They concluded that the best example was <italic>H.
pylori</italic>
. Recent advances in understanding the genomics and genetic lineages of
<italic>H. pylori</italic>
and another pathogen with close links to human lineages,
<italic>M. tuberculosis</italic>
, are highlighted below.</p>
<p><italic>H. pylori</italic>
- <italic>Human migration into the Americas</italic>
-
<italic>H. pylori</italic>
is a Gram-negative bacterium. It can be used as a marker of
prehistoric human migrations because it has been associated with humans throughout human
evolution. Indeed, bacteria related to <italic>H. pylori</italic>
are found in non-human
primates and other mammals, indicating the long history of co-evolution with mammalian
species. Due to this long association with <italic>H. pylori</italic>
, human gastric
physiology has evolved so that the presence of the bacterium is advantageous in some ways
and may protect the human stomach from other bacterial infections (<xref rid="B14" ref-type="bibr">Atherton 2006</xref>
). Human transmission of the bacterium is not well
understood, but is believed to most often occur between humans via the oral-oral or the
faecal-oral route.</p>
<p>A study by <xref rid="B62" ref-type="bibr">Linz et al. (2007)</xref>
using a large dataset
of modern <italic>H. pylori</italic>
DNA sequences has revealed that, as with humans, the
genetic diversity of <italic>H. pylori</italic>
decreases with geographical distance from
East Africa. This indicates that the first humans, who evolved in East Africa, were
infected with <italic>H. pylori</italic>
prior to their migrations out of this area 58,000
years ago. The findings of <xref rid="B34" ref-type="bibr">Falush et al. (2003)</xref>
support this research, as they showed that bacterial sequences of one virulence-associated
gene (<italic>vacA</italic>
) and fragments of seven housekeeping genes differ according to
the continent in which they are found and the human population with which they are
associated.</p>
<p>Ancient strains of <italic>H. pylori</italic>
have been identified in human remains
discovered in the Americas. The first discovery, in a mummified individual from the funeral
cave of La Ventana in Chihuahua State desert in Mexico, dated to approximately 1350 AD
(<xref rid="B24" ref-type="bibr">Castillo-Rojas et al. 2008</xref>
). Pre-Columbian
<italic>H. pylori</italic>
was confirmed by 16S <italic>rRNA</italic>
DNA sequences. The
second discovery, by <xref rid="B83" ref-type="bibr">Swanston et al. (2011)</xref>
, was
based on a Kwäday Dän Ts’ìnchi individual found in the Samuel Glacier in Tatshenshini-Alsek
Park in British Columbia in Canada, from the late XVII and mid-XIX centuries. The
<italic>H. pylori</italic>
DNA amplified from the stomach of the Kwäday Dän Ts’ìnchi
individual contained a <italic>vacA</italic>
m2a/m1d allele associated with indigenous
American strains, but also a <italic>vacA</italic>
s2 allele, rare in Asian strains, but
commonly associated with European strains. The Kwäday Dän Ts’ìnchi individual was
radiocarbon dated to approximately 1670-1850 AD, a time after European contact with the
Americas. Therefore the most likely reason that the European and indigenous American
regions are present in bacteria amplified from this individual is because there were
Europeans present in Canada during the individual’s lifetime and the <italic>H.
pylori</italic>
bacteria in the Kwäday Dän Ts’ìnchi individual are therefore hybrids.
Both these <italic>H. pylori</italic>
findings in these historical individuals therefore
support the theory that humans first migrated to the Americas from Asia. The Mexican mummy
was dated to approximately 1350 AD, a time prior to European contact with the Americas, so
the evidence that humans first migrated to the Americas from Asia is especially strong from
this source.</p>
<p><xref rid="B89" ref-type="bibr">Yamaoka et al. (2002)</xref>
analysed modern strains of
<italic>H. pylori</italic>
associated with indigenous peoples of the Americas, based on
variations in the alleles <italic>vacA</italic>
, <italic>cagA</italic>
- part of the
<italic>cag</italic>
pathogenicity island in the <italic>H. pylori </italic>
genome and
the right end of the <italic>cag</italic>
pathogenicity island. They found that some native
Colombian and Alaskan strains possessed novel <italic>vacA</italic>
and/or
<italic>cagA</italic>
gene structures and were more closely related to East Asian than
to non-Asian <italic>H. pylori</italic>
. Also, some native Alaskan strains appear to have
originated in Central Asia and to have arrived after strains found in South America
suggesting that <italic>H. pylori</italic>
crossed the Bering Strait from Asia to the New
World at different times.</p>
<p>In a study of another modern population, a group of Amerindian subjects from Amazonia, East
Asian <italic>H. pylori </italic>
genotypes were present for each of the
<italic>loci</italic>
examined, but were absent in a mestizo population from Caracas.
These findings provide evidence that <italic>H. pylori </italic>
has been present in humans
at least since ancestors of Amerindians migrated from Asia more than 11,000 years ago
(<xref rid="B44" ref-type="bibr">Ghose et al. 2002</xref>
). A more recent study of
modern strains from Mexico (<xref rid="B23" ref-type="bibr">Camorlinga-Ponce et al.
2011</xref>
) showed that Mexican indigenous people with Amerindian markers are colonised
with <italic>H. pylori</italic>
showing an admixture of Asian, European and African strains
in genes known to interact with the gastric mucosa. In addition, evidence was found of
novel Amerindian <italic>cagA</italic>
and <italic>vacA</italic>
alleles in indigenous
groups of North and South America.</p>
<p>The most obvious route for human migration to the Americas from Asia was via Beringia - the
Bering Land Bridge that existed for hundreds of years while sea levels were low,
approximately 13,000 years ago. However, <xref rid="B8" ref-type="bibr">Araújo et al.
(2008b)</xref>
suggest that this cannot have been the only way that humans first entered
the pre-Columbian Americas. Abundant evidence of parasites such as hookworm
(<italic>Ancylostoma duodenale</italic>
, <italic>Necator americanus</italic>
), whipworm
(<italic>Trichuris trichiura</italic>
) and threadworm (<italic>Strongyloides
stercoralis</italic>
) has been identified across the Americas (<xref rid="B3" ref-type="bibr">Allison et al. 1974b</xref>
, <xref rid="B70" ref-type="bibr">Patrucco et al.
1983</xref>
, <xref rid="B9" ref-type="bibr">Araújo et al. 2011</xref>
, <xref rid="B53" ref-type="bibr">Jiménez et al. 2012</xref>
). These parasites are host specific
so must have entered the Americas with migrating humans. However, their spread into the New
World cannot be explained easily by a migration through Beringia. These parasites need warm
moist soils to develop in and to this day do not occur in traditional populations in the
Arctic region (<xref rid="B9" ref-type="bibr">Araújo et al. 2011</xref>
). None of these
parasites could have survived the freezing conditions of the Siberia-Alaska region that
humans would have had to pass through if reaching the Americas via the Bering Land Bridge.
<xref rid="B8" ref-type="bibr">Araújo et al. (2008b)</xref>
therefore infer that these
findings suggest alternative migration routes into the Americas and suggest that some
humans (and their parasitic stowaways) arrived via transpacific migration in boats or by
coastal migration, possibly through the sub-Arctic region. This area requires further
research to understand how this may have happened.</p>
<p><italic>M. tuberculosis - Dense human populations</italic>
- <italic>M.
tuberculosis</italic>
is a bacterium found across the world. There are a group of
closely related pathogenic bacteria known collectively as the <italic>M.
tuberculosis</italic>
complex. The principle cause of human tuberculosis is <italic>M.
tuberculosis sensu stricto</italic>
, whereas <italic>Mycobacterium bovis</italic>
is the
principle cause of tuberculosis in bovids and other animals. <italic>M.
tuberculosis</italic>
and <italic>M. bovis </italic>
evolved from a common ancestor
(<xref rid="B46" ref-type="bibr">Gutierrez et al. 2005</xref>
) and genomics indicate
that ancestral mycobacteria probably began infecting early hominids in East Africa
approximately three million years ago. Modern analyses of <italic>M. tuberculosis</italic>
reveal that it is an extremely diverse bacterium and appears to have co-evolved with its
human hosts (<xref rid="B41" ref-type="bibr">Gagneux et al. 2006</xref>
, <xref rid="B49" ref-type="bibr">Hershberg et al. 2008</xref>
). Therefore, <italic>M.
tuberculosis</italic>
, like <italic>H. pylori</italic>
, has been associated with humans
for so long its diversity is linked to human migratory history and different strains of the
bacterium are associated with different regions of the world.</p>
<p>Tuberculosis was first identified in humans in the pre-colonial Americas, using
morphological evidence in a mummified child, dated to approximately 700 AD, from the Nazca
culture of Southern Peru (<xref rid="B1" ref-type="bibr">Allison et al. 1973</xref>
, <xref rid="B43" ref-type="bibr">Gerszten et al. 2012</xref>
). This mummy had bone pathology
suggestive of tuberculosis and microscopic evidence of acid-alcohol resistant bacilli.
Subsequent PCR studies have identified ancient <italic>M. tuberculosis</italic>
complex DNA
in pre-colonial human remains, thereby confirming its presence prior to European contact.
<xref rid="B78" ref-type="bibr">Salo et al. (1994)</xref>
were the first to do so using
PCR to demonstrate <italic>M. tuberculosis</italic>
complex DNA from a hilar lymph node
lesion in a 1,000 year-old naturally mummified body from southern Peru. <xref rid="B10" ref-type="bibr">Arriaza et al. (1995)</xref>
successfully used PCR to diagnose
tuberculosis in ancient human remains in Chile dated to approximately 1040 AD. The
<italic>M. tuberculosis</italic>
complex was also detected in North American material
from early XI century Mississippi and XV century Canada (<xref rid="B20" ref-type="bibr">Braun et al. 1998</xref>
). These and other studies (i Prat & de Souza 2003) confirm
that the <italic>M. tuberculosis</italic>
complex was present in the Americas prior to
1492. An early suggestion that these infections were caused by <italic>M. bovis</italic>
(<xref rid="B28" ref-type="bibr">Daniel 2000</xref>
) was thrown into doubt by the
findings of <xref rid="B77" ref-type="bibr">Rothschild et al. (2001)</xref>
, who used PCR
to detect <italic>M. tuberculosis</italic>
complex aDNA from a 17,000 year-old Pleistocene
bison metacarpal from Natural Trap Cave, Wyoming. Attempts at typing the aDNA fragments led
to the conclusion that the bison tuberculosis was clearly distinct from modern <italic>M.
bovis</italic>
, but resembled human <italic>M. tuberculosis</italic>
or
<italic>Mycobacterium africanum</italic>
.</p>
<p>The doubts about the existence of tuberculosis in the pre-colonial Americas arose largely
because of the great tuberculosis epidemics that raged among indigenous peoples of the
Americas after European contact (<xref rid="B87" ref-type="bibr">Wilbur & Buikstra
2006</xref>
). Such epidemics suggested that these populations had not been exposed to
the disease before. It is now suggested that the tuberculosis epidemics that raged among
indigenous populations after European contact occurred because of exposure to more virulent
European strains of the disease. There is accumulating evidence that ancestral <italic>M.
tuberculosis</italic>
lineages are less virulent (<xref rid="B40" ref-type="bibr">Gagneux 2012</xref>
) and it is intriguing to speculate that this also applied to the
indigenous tuberculosis in the Americas. However, its genetic characterisation is only now
about to be published (<xref rid="B19" ref-type="bibr">Bos et al. 2014</xref>
).</p>
<p>It is interesting to discuss the social structure of the ancient human populations in which
<italic>M. tuberculosis</italic>
complex DNA has been discovered. The oldest known cases
of <italic>M. tuberculosis sensu stricto</italic>
were identified by aDNA and skeletal
evidence in human remains recovered from a 9,000 year-old Neolithic settlement in the
Eastern Mediterranean (<xref rid="B50" ref-type="bibr">Hershkovitz et al. 2008</xref>
).
This settlement is one of the earliest known human villages with evidence of animal
domestication and agriculture. The shift from gatherer-hunters to settled farming
communities in the Neolithic period meant that infectious diseases such as tuberculosis
that are associated with denser human populations became endemic in agricultural
populations from this period onwards. Across the world, the presence of tuberculosis often
correlates with the existence of animal domestication because domesticated animals are
needed to maintain large human populations and these large populations thereby maintain the
tuberculosis. It was previously believed that this correlation existed because humans
caught the disease from their animals, but this cannot be the case as <italic>M.
tuberculosis</italic>
is genetically more ancestral than <italic>M. bovis</italic>
(<xref rid="B21" ref-type="bibr">Brosch et al. 2002</xref>
).</p>
<p>The Chiribaya population, in which <xref rid="B78" ref-type="bibr">Salo et al.
(1994)</xref>
found tuberculosis, was agricultural and occupied the Osmore Valley of
Peru between approximately 1000-1300 AD. A tuberculosis-like disease was present in
prehistoric populations from Northwest Argentina in the XIV-XV centuries. Six of 70
excavated individuals provided evidence of the existence of the disease in the Santa María
Valley between the end of the Late Ceramic Period and the onset of the expansion of the
Inca Empire (<xref rid="B12" ref-type="bibr">Arrieta et al. 2011</xref>
). A further study
described a case from the Nasca culture from southern Peru dating to about 900 AD (<xref rid="B64" ref-type="bibr">Lombardi & Cáceres 2000</xref>
). The authors concluded
that there was a pandemic level of tuberculosis in the Southern Peruvian coast at this
time. The population in Chile, studied by <xref rid="B10" ref-type="bibr">Arriaza et al.
(1995)</xref>
, was also agricultural. All the skeletons analysed in their paper were
dated to 500-1000 AD, which correlates with fully agricultural societies in this region.
Agricultural societies are likely places to find tuberculosis because they generally have
large populations of people living in close contact. Tuberculosis is a density-dependent
disease (<xref rid="B16" ref-type="bibr">Barnes et al. 2011</xref>
) that is generally only
present in populations such as these.</p>
<p>High population density enables the transmission and maintenance of tuberculosis because it
is transmitted between people via the inhalation of infected droplets coughed or sneezed
from the lungs of an infected individual. Likelihood of infection therefore increases when
people are living in close contact and the chance of the disease being maintained within
the population is higher in larger populations (<xref rid="B31" ref-type="bibr">Donoghue
2009</xref>
). Thus the discovery of tuberculosis in indigenous populations in the
Americas provides us with interesting information about the size of these populations. They
must have been sufficiently large for the disease to be maintained and the people must have
been living in close contact to each other, in order for the disease to be transmitted.</p>
<p><italic>M. tuberculosis</italic>
has been found in North and South America, but strangely,
concrete evidence of tuberculosis appears lacking in the ancient Mayan cultures of
Mesoamerica. It is probable that the ancient Maya were infected with tuberculosis as their
population size was sufficient, they had well established trade routes across the Americas
that would have enabled the disease to spread and Mayan art displays individuals that have
features characteristic of tuberculosis (<xref rid="B65" ref-type="bibr">Mackowiak et al.
2005</xref>
). Possible reasons for this lack of evidence of tuberculosis have been
discussed (<xref rid="B65" ref-type="bibr">Mackowiak et al. 2005</xref>
, <xref rid="B87" ref-type="bibr">Wilbur & Buikstra 2006</xref>
). One explanation may be
that persons suffering from tuberculosis were disposed of in a specific way after death
that has not yet been discovered by modern archaeologists. <xref rid="B87" ref-type="bibr">Wilbur and Buikstra (2006)</xref>
commented, however, on the very poor state of bone
preservation in these remains that may have led to the lack of aDNA data. They also
suggested that the particular <italic>M. tuberculosis</italic>
genetic lineage in this
population was less likely to disseminate from the lung into the bones. It should be noted
that in any event, skeletal tuberculosis was extremely rare even in the pre-antibiotic era,
with only around 3-5% of infections resulting in visible lesions (<xref rid="B76" ref-type="bibr">Resnick & Niwayama 1995</xref>
).</p>
<p><italic>Souvenir human infectious diseases in the Americas</italic>
- When humans first
migrated to the Americas they found a landmass already inhabited by wildlife and their
pathogens. Many microorganisms that originally infected American wildlife jumped the
species barrier and adapted to enable them to cause zoonotic infections in humans. Examples
based on historical material or modern genomic studies include bartonellosis or Carrión’s
disease (<xref rid="B2" ref-type="bibr">Allison et al. 1974a</xref>
), mucocutaneous
leishmaniasis (<xref rid="B27" ref-type="bibr">Costa et al. 2009</xref>
), Lyme borreliosis
(<xref rid="B67" ref-type="bibr">Margos et al. 2008</xref>
), salmonellosis (<xref rid="B79" ref-type="bibr">Sawicki et al. 1976</xref>
), toxoplasmosis (<xref rid="B58" ref-type="bibr">Lehmann et al. 2006</xref>
) and treponematosis (<xref rid="B66" ref-type="bibr">Marden & Ortner 2011</xref>
). Two souvenir diseases are
discussed below in more depth, as each gives insight into the environment where pathogens
and indigenous peoples interacted.</p>
<p><italic>T. cruzi - Human living conditions</italic>
- Chagas disease exists in the Americas
today from southern North America to southern Argentina and causes much human suffering. It
is caused by the <italic>T. cruzi</italic>
parasite. <italic>T. cruzi</italic>
is one of
the three major pathogens in the trypanosomatid group. The other pathogens of the group are
<italic>Trypanosoma brucei</italic>
that causes African sleeping sickness and
<italic>Leishmania </italic>
spp. The trypanosomatid group consists of very ancient
eukaryotic flagellate protozoa of the Kinetoplastida order that have a single flagellum.
<xref rid="B82" ref-type="bibr">Stevens et al. (1999)</xref>
dated the divergence of
<italic>T. cruzi</italic>
and <italic>T. brucei</italic>
to approximately one hundred
million years ago, following the separation of the landmasses of Africa, South America and
Euroamerica. <italic>T. cruzi</italic>
and <italic>T. brucei</italic>
have since evolved to
become quite different pathogens.</p>
<p>Kinetoplastida are characterised by the presence of kinetoplast DNA near the flagellate’s
basal body. Kinetoplast DNA is an extra nuclear DNA network of circular molecules that
corresponds to the parasite mitochondrial genome (<xref rid="B6" ref-type="bibr">Araújo et
al. 2009</xref>
). This kinetoplast DNA is extremely useful in the identification of
<italic>T. cruzi</italic>
in ancient remains. Detection of the kinetoplast DNA is very
sensitive due to the high copy number/cell (several thousand) and can readily be achieved
by PCR amplification and detection via hybridisation with a probe (<xref rid="B45" ref-type="bibr">Guhl et al. 1999</xref>
, <xref rid="B15" ref-type="bibr">Aufderheide et al.
2004</xref>
). Evidence for <italic>T. cruzi</italic>
can also come from the observation
of ancient remains, as the disease can often result in morphological changes such as
megacolon - enlargement of the colon (<xref rid="B45" ref-type="bibr">Guhl et al.
1999</xref>
, <xref rid="B75" ref-type="bibr">Reinhard et al. 2003</xref>
). Therefore,
mummies have been essential to the diagnosis of <italic>T. cruzi</italic>
via such
morphological observations. Using such methods, ancient <italic>T. cruzi </italic>
has been
found in ancient human remains across the Americas from Northern Chile (<xref rid="B45" ref-type="bibr">Guhl et al. 1999</xref>
) to central Brazil (<xref rid="B35" ref-type="bibr">Fernandes et al. 2008</xref>
) to North America (<xref rid="B75" ref-type="bibr">Reinhard et al. 2003</xref>
).</p>
<p><italic>T. cruzi</italic>
is transmitted between its vertebrate hosts via a triatomine
insect vector. <italic>T. cruzi</italic>
is a very heterogeneous parasite with many
different genetic and phenotypic markers, indicating its great diversity. It infects many
triatomine insects that act as a vector for parasite transmission between mammals.
<italic>T. cruzi</italic>
can infect nearly all the tissues of more than one hundred
species of mammals. Indeed <xref rid="B63" ref-type="bibr">Llewellyn et al. (2011)</xref>
revealed that even within a single mammalian reservoir, great diversity could often be
present. Triatomine insects hide inside animal nests/human homes and extract blood from the
host while it is sleeping. <italic>T. cruzi</italic>
is present in the triatomine faeces,
so when the insect bite causes itching the faeces are pushed into the bite wound and the
parasite enters the bloodstream and causes infection. The parasite has very little effect
on most feral American animals that it infects, suggesting that it has infected these
animals for such a long time that they have evolved and adapted to live normally with it.
The disease does however often cause premature death in humans, most often as a result of
cardiac complications (<xref rid="B15" ref-type="bibr">Aufderheide et al. 2004</xref>
).
This indicates the more recent association of humans with this parasite and shorter time to
adapt to living with the parasite, as compared to feral animals of the Americas.</p>
<p>Initially it was believed that humans first entered the <italic>T. cruzi</italic>
life
cycle in the Andean region when triatomine insects became domiciled after the development
of urban populations, a sedentary lifestyle and animal domestication (<xref rid="B26" ref-type="bibr">Coimbra Jr 1988</xref>
). However, it is now thought more likely that humans
entered into the zoonotic cycle of <italic>T. cruzi</italic>
very soon after entering the
Americas (<xref rid="B36" ref-type="bibr">Ferreira et al. 2011</xref>
) as research
indicates that <italic>T. cruzi</italic>
was infecting prehistoric indigenous populations
long before the development of urban centres in the Andean region. The work of <xref rid="B15" ref-type="bibr">Aufderheide et al. (2004)</xref>
revealed that <italic>T.
cruzi</italic>
has been infecting peoples of the Andean coast for at least 9,000 years
and before the development of urban centres in the Andean region. Triatomine insects
require some sort of nest to live in, so it may have been the straw bedding of indigenous
nomadic populations that first led to humans coming into contact with this parasite.
Indigenous urban populations often had houses of wattle and thatch that would again have
been ideal nests for triatomine insects. Humans would have been a great new source of food
for the triatomine insects and their living conditions, a great new place for protection
from climatic changes and predators.</p>
<p><xref rid="B61" ref-type="bibr">Lima et al. (2008)</xref>
used aDNA analyses to show that
<italic>T. cruzi</italic>
infected both ancient nomadic and urban indigenous peoples of
the Americas. They detected <italic>T. cruzi </italic>
human infection in Brazil dating back
at least 4,500 years, in an individual from a hunter-gatherer population that preceded
<italic>T. infestans </italic>
domiciliation. The <italic>T. cruzi </italic>
I genotype
was demonstrated 4,500-7,000 years ago in the state of Minas Gerais, where this genotype is
currently absent, suggesting that the distribution pattern of <italic>T. cruzi
</italic>
genotypes in humans has changed in time and place. <italic>T. cruzi </italic>
I is
widespread among wild mammals and sylvatic vectors of all biomes. This genotype is commonly
isolated from humans and wild mammals in the Amazon Basin today. In contrast, <italic>T.
cruzi </italic>
II has a focal distribution in nature, but is the main agent of human
infection in other Brazilian regions. Further understanding of the exact nesting conditions
triatomine insects require may help us learn more about the living conditions of indigenous
peoples of the Americas that first put them in contact with this insect.</p>
<p><italic>Coccidioidomycosis - Human agricultural development</italic>
- Coccidioidomycosis,
also known as valley fever, is a non-communicable ascomycete fungal disease associated with
desert-like areas. The disease is acquired <italic>via</italic>
the inhalation of the
spores of the fungus, which is found approximately 20 cm beneath the surface of the soil.
Today <italic>C. immitis </italic>
is found in the San Joaquin Valley, California. The
closely related <italic>Coccidioides posadasii</italic>
, also known as non-California
<italic>C. immitis</italic>
, has a wider distribution, being recovered from across the
southwestern United States of America, southern California, northern, central and southern
Mexico and South America (<xref rid="B38" ref-type="bibr">Fisher et al. 2002</xref>
).</p>
<p><italic>C. immitis</italic>
goes through a saprophytic stage and a parasitic stage in its
life cycle. The saprophytic stage is a very hardy mould phase that leads to the maturation
of the hyphal cells into arthroconidia (rectangular spores). The parasitic phase begins
when a human or animal inhales the arthroconidia. Once inside the host lungs the
arthroconidia then enlarge to become spherules (spherical double-walled cells). Upon
spherule rupture endospores are released that can disseminate in the host and re-initiate
the spherulation cycle. This causes a disseminated form of the disease, in which the
spherules enter the bloodstream and spread beyond the lungs. Disseminated
coccidioidomycosis occurs particularly during pregnancy and is frequently fatal. However,
in most cases of infection there are either no symptoms or only minor cold-like symptoms
(<xref rid="B56" ref-type="bibr">Kolivras et al. 2001</xref>
). Strict precautions have
to be taken by individuals, such as archaeologists, who are at risk of becoming infected
(<xref rid="B72" ref-type="bibr">Poirier & Feder 2001</xref>
).</p>
<p><italic>C. immitis</italic>
and <italic>C. posadasii</italic>
are the only members of this
genus capable of causing life-threatening disease in humans and other mammals. Other
members of this family live predominantly as plant pathogens, so it is most parsimonious to
assume that mammalian virulence was recently and uniquely acquired in
<italic>Coccidioides</italic>
(<xref rid="B80" ref-type="bibr">Sharpton et al.
2009</xref>
). It is believed that the common ancestor of <italic>Coccidioides</italic>
and non-pathogenic species likely grew on dead or decaying animal matter or on external
surfaces of an animal host, such as hair. However, once this association with animals was
established, the shift from plant-based to animal-based nutrition ultimately led to
disease. The two <italic>Coccidioides </italic>
species diverged 5.1 million years ago, well
before humans arrived in the New World (<xref rid="B71" ref-type="bibr">Pitulko et al.
2004</xref>
), so this evolutionary transition to a pathogenic phenotype probably
involved mainly rodent hosts and not humans. Some animals, such as mice, now have genes
that make them resistant to the disease, which has led to the suggestion that this reflects
the prolonged period of time over which <italic>Coccidioides</italic>
spp have infected
feral American animals (<xref rid="B54" ref-type="bibr">Kirkland & Fierer
1996</xref>
).</p>
<p><xref rid="B48" ref-type="bibr">Harrison et al. (1991)</xref>
presented the first
microscopic evidence of prehistoric human infection with <italic>Cocci- dioides</italic>
.
They identified human remains in Arizona dated to approximately 1000-1400 AD and therefore
belonging to the Sinagua culture. Evidence that the individual had suffered from
coccidioidomycosis included the presence of spherules (in the parasitic stage) preserved
within the skeleton and the presence of massive widespread lesions suggestive of the
disease. Contamination by the fungus after death was ruled out because of the presence of
the lesions and the fact that all the fungi present were identified as being in the
parasitic stage. This research was carried out before PCR was a widespread technique used
in paleomicrobiology, so there were no DNA analyses carried out to confirm the diagnosis.
Evidence of ancient cocci- dioidomycosis infection has also been reported by <xref rid="B84" ref-type="bibr">Temple (2006)</xref>
in the Los Muertos site in Arizona, which
is still an endemic region for coccidioidomycosis today. An ancient adult male of the
Hohokum population was found in this region dated to approximately 1150 AD, with lesions
suggestive of the disease. Again, the diagnosis is entirely based on the paleopathology of
the skeletal lesions.</p>
<p>There was frequent soil contact in prehistoric Hohokum populations in this region because
the region contained many irrigation canals that were used to support agriculture (<xref rid="B17" ref-type="bibr">Bayman 2001</xref>
, <xref rid="B84" ref-type="bibr">Temple
2006</xref>
). Significant construction efforts on the canals took place around the time
that this human individual is approximately dated. Digging and maintaining these canals
would have placed workers in direct contact with the soil that is the habitat of
<italic>Coccidioides</italic>
and therefore put workers at risk of infection. Given
these circumstances, the fact that people still suffer from coccidioidomycosis in this area
today and the skeletal lesions present on the individual, it appears likely that
pre-colonial peoples of this region were infected with this fungus. In future, molecular
evidence from aDNA analyses should be able to confirm this.</p>
<p>Analysis of microsatellite <italic>loci</italic>
from <italic>C. immitis </italic>
showed
that genetic diversity in this fungus is geographically partitioned throughout North
America (<xref rid="B37" ref-type="bibr">Fisher et al. 2001</xref>
). In contrast, the South
American <italic>C. immitis </italic>
population appears to have originated from a single
North American population centred in Texas. Genetic analyses show that South American
<italic>C. immitis </italic>
strains have undergone rapid population growth, consistent
with an epidemic increase in post-colonisation population size. <xref rid="B37" ref-type="bibr">Fisher et al. (2001)</xref>
estimated that the introduction into South America
occurred within the last 9,000-140,000 years and noted that this increase in range
parallels that of <italic>H. sapiens</italic>
. They cited <xref rid="B57" ref-type="bibr">Lacy and Swatek (1974)</xref>
who had noted that viable <italic>C. immitis</italic>
was
strongly associated with Amerindian middens in California and this appeared to be due to
the soil alkalinity and past accumulation of domestic contaminants. Because of this, <xref rid="B37" ref-type="bibr">Fisher et al. (2001)</xref>
suggest that the colonisation of
South America by <italic>C. immitis </italic>
represents a relatively recent and rapid
co-dispersal of a host and its pathogen.</p>
<p><italic>European contact with the Americas</italic>
- What happened subsequent to European
discovery of the Americas completely shifted the global distribution of human infectious
diseases. Human infectious diseases had evolved independently in the Eastern and Western
Hemispheres for thousands of years. Both Hemispheres were home to human populations in
which hunting and gathering and the development of agriculture and urban centres were
present, yet the geography, climate and native organisms in the hemispheres were different.
For these reasons and because of simple chance, there were very different human infectious
diseases present in the Eastern and Western Hemispheres (<xref rid="B68" ref-type="bibr">Merbs 1992</xref>
, <xref rid="B22" ref-type="bibr">Camargo 1994</xref>
). Europeans
brought many fatal infectious diseases, including smallpox, measles and malaria, to the
Americas that had not existed there before, so indigenous peoples of the Americas had no
genetic resistance to them. In contrast, Europeans had developed high degrees of immunity
to these diseases over the centuries they had been exposed.</p>
<p>The work of <xref rid="B16" ref-type="bibr">Barnes et al. (2011)</xref>
shows that
populations with a long history of urban settlement have greater genetic resistance to
tuberculosis. However, another consequence of long-term urbanisation is the development of
more virulent strains of pathogens, as transmission is more likely and a large population
enables virulent pathogens to persist. This population effect is clearly demonstrated by
examining the historical distribution of measles virus in insular communities, where the
virus died out once all susceptible individuals had been infected only to recur after the
virus was re-introduced (<xref rid="B18" ref-type="bibr">Black 1966</xref>
). Such findings
may explain why the Eastern Hemisphere, that has a longer history of urban settlement,
contained more human infectious diseases and more virulent strains of some indigenous
pathogens.</p>
<p>During the “period of exploration”, a greater number of human infectious diseases were
taken to the Americas from Europe than <italic>vice versa</italic>
. In addition,
considering post-colonial disease epidemiology, the indigenous peoples of the Americas
represented a naïve population. The combination of infectious disease, displacement and
warfare, brought to America by European colonialism, caused widespread devastation.</p>
<p>Paleomicrobiology is a fast developing area of research that can give us much interesting
and useful biological, anthropological, historical and archaeological information. The
microbial pathogens described in this review can illuminate the pre-colonial history of the
indigenous peoples of the Americas, but raise more questions.</p>
<p>The work on <italic>H. pylori</italic>
has provided information about human migrations into
the Americas, but highlights the need for much more research. Further investigations should
be carried out to consider how ancient human populations could have reached the Americas by
sea. Investigating other heirloom infectious diseases in ancient human remains may also
facilitate our understanding of migration into the Americas. Further research on <italic>M.
tuberculosis</italic>
, using hybridisation and DNA capture techniques, for example, may
detect tuberculosis in cultures and sites, such as Mesoamerica, where evidence is currently
lacking. Investigating which strains of <italic>M. tuberculosis</italic>
are present in
ancient human remains may tell us about ancient human migrations, but also help answer the
question of whether indigenous American strains were significantly different from European
strains. If European strains were more virulent this could explain why there was such
devastation from tuberculosis post-contact. Research into <italic>T. cruzi</italic>
and its
insect vector should lead to greater understanding of the living conditions of the
indigenous peoples of the Americas that first put them in contact with this insect and
parasite. Molecular evidence is required to confirm the existing diagnoses of <italic>C.
immitis</italic>
and/or <italic>C. posadasii </italic>
in the pre-Columbian Americas.
Distinction between these two closely related fungi may yield interesting data on their
ancient distribution in the environment.</p>
<p>The study of paleomicrobiology enables us to confirm paleopathological diagnoses and to
answer historical questions about the extent and impact of human infectious diseases. As
has been illustrated above, paleomicrobiology can provide evidence of ancient and
historical migrations and indicate the living conditions of past populations. Paleogenomics
also can provide real time calibration of genetic changes within pathogens and to link such
changes with the society of their human hosts.</p>
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