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Polymorphie Alu Insertions and the Asian Origin of Native
American Populations
1 Department of Biological Sciences, Florida International University, University Park Campus, Mi-
ami, FL 33199.
2 Instituto de Gentica, Universidad Nacional de Colombia, Santa F de Bogot, Colombia.
3 Department of Pathology, Stanley S. Scott Cancer Center, Louisiana State University Medicai
Center, 1901 Perdido Street, New Orleans, LA 70112.
4 Department of Biochemistry and Molecular Biology and Center for Molecular and Human Genetics,
Louisiana State University Medical Center, 1901 Perdido Street, New Orleans, LA 70112; and Laboratory
of Molecular Genetics, Alton Ochsner Medical Foundation, New Orleans, LA 70121.
5 Department of Anthropology, Pennsylvania State University, University Park, PA 16802.
6 Department of Natural and Health Sciences, Barry University, 1 1300 N.E. 2d Avenue, Miami, FL
33161.
Address correspondence to R.J. Herrera.
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24 / NO VICK ET AL.
walking over the Bering land bridge that was exposed during the last glaci-
ation, some 20,000 years ago (Fladmark 1983).
Several hypotheses have been formulated to explain the origins of hu-
mans in the New World. The tripartite hypothesis proposes three waves of
migration that originated in northern Asia and gave rise to the three main
genetic and linguistic clusters: Eskaleut, Nadene, and Amerind (Greenberg
1987). Under this hypothesis there were three distinct migrations. The first
one, sometime before 15,000 years ago, originated the Amerind cluster, which
spread over most of the New World. The second migration, 15,000-10,000
years ago, gave rise to the Nadene group. The third wave, 10,000 years ago,
founded the Eskaleut cluster. This hypothesis has been corroborated by dental
data (Greenberg et al. 1986) and by nuclear and mitochondrial DNA genetic
data (Wallace and Torroni 1992; Cavalli-Sforza et al. 1994).
Multiple migrations also have been proposed (Cavalli-Sforza et al.
1994), as have single-migration models (Rogers et al. 1991). One possibility,
according to the single-migration model, portrays a mostly ice-covered North
America during the last glacial maximum with some ice areas suitable for
habitation (Rogers et al. 1991). The isolation that may have occurred in this
ice-free refugium may have encouraged differentiation, genetic drift, and in-
dependent differentiation (Rogers et al. 1991). This differentiation may have
yielded the profile of multiple migrations postulated by other researchers.
Several polymorphic genetic systems have been used to study native
American phylogeny. These include mitochondrial DNA, variable number of
tandem repeats (VNTRs), restriction fragment length polymorphisms
(RFLPs), and point mutations in Alu sequences (O'Rourke et al. 1992; Schan-
field 1992; Kidd, Pakstis et al. 1993; Torroni et al. 1994; Kidd and Kidd
1996; Knight et al. 1996). Alu sequences are the largest family of short in-
terspersed repetitive elements (SINEs) in humans, with an excess of 500,000
copies per haploid genome [for reviews see Deininger and Batzer (1993) and
Novick et al. (1996)]. Alu elements are ancestrally derived from the endo-
plasmic reticulum signal recognition particle 7SL RNA gene (Ullu and
Tschudi 1984), with which they share about 90% sequence similarity through-
out most of their sequences (Ullu and Tschudi 1984). Alu elements are distrib-
uted throughout the genomes of primates. Recently, one Alu subfamily was
found to be largely human specific (HS) (Batzer 1990; Batzer and Deininger
1991). Members of this subfamily have been inserted recently into the human
lineage genome, within the last 200,000 to 6 million years (Batzer 1991 ; Batzer
and Deininger 1991). A limited number of Alu elements are transcriptionally
active (Matera et al. 1990) and undergo amplification into other genomic lo-
cations (Wallace et al. 1991) in a process termed retroposition.
In addition to the polymorphic nature of many Alu insertions, several
features make Alu elements exceptional genetic markers: the stability of the
Alu insertion event, the lack of a known mechanism for the precise removal
of Alu elements from their specific chromosomal site of insertion, and the
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Polymorphie Alu Insertions / 25
low rate of de novo insertions that reach polymorphic levels ( atzer and
Deininger 1991). These characteristics make it highly unlikely that the same
Alu insertion could occur more than once independently at the same locus or
that once inserted, an element could be removed without leaving vestiges of
its existence behind. Furthermore, the ancestral state of an Alu insertion in-
variably is the absence (complete and exact) of the element at a particular
locus and the presence of an insertion at that site, the forward mutational
change. This is an invaluable attribute not present in other polymorphic sys-
tems (e.g., RFLPs) where the ancestral state is ambiguous.
We recently reported the application of a polymerase chain reaction
(PCR) based Alu insertion polymorphism assay to the analysis of population
relationships in a worldwide survey (Batzer et al. 1994; Novick et al. 1995).
In the present study we analyzed a group of 24 native American populations
using 5 polymorphic Alu insertion sites with regard to their genetic structure,
interpopulation affinities, and relationships with respect to 6 non-American
groups. The results presented here corroborate the Asian origin of native
American populations but do not support the multiple-migration hypothesis
for the establishment of the tripartite Eskaleut, Nadene, and Amerind lin-
guistic groups. Instead, the phylogenetic relationships among the native
American groups reflect their geographic distribution. The presented data also
demonstrate close phylogenetic relationships between mainland Chinese and
native Americans, particularly Mayan groups. This may indicate recent gene
flow from Asia to the New World.
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26 / NOVICK ET AL.
Population Localization
1 Alaska native Aleut Islands
2 Greenland native Greenland
Amplified DNA fragments were visualized using ultraviolet light and a Cy-
bertech CSI Imaging System.
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Polymorphie Alu Insertions / 27
Figure 1. Geographie distribution of the native American populations examined in this study. See
Table 1 for the names of the numbered populations.
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28 / NO VICK ET AL.
Results
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Polymorphie Alu Insertions / 29
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30 / NOVICK ET AL.
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32 / NOVICK ET AL.
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Polymorphie Alu Insertions / 33
less gene flow than average. Our analysis indicates that the non-American
populations are outliers in terms of having higher than predicted heterozy-
gosity. The exception to this is the Chinese, which group within the native
American populations (Figure 3). Within the native American groups both
the Inca and the Moskoke have heterozygosity values beyond the theoretical
expectation. This finding is consistent with the high average heterozygosity
observed in both groups and the clustering pattern observed for the Inca in
the maximum-likelihood tree.
Discussion
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34 / NOVICK ET AL.
Figure 3. Centroid analysis of gene flow. The heterozygosity of each population (_y axis) is plotted
against the distance of the population from the centroid (the overall mean allele fre-
quencies of the populations) (x axis). The upper plot includes all 30 populations, and
the lower plot illustrates the centroid analysis of only the native American populations.
Filled circles represent native American populations; open circles indicate non- American
groups.
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Polymorphie Alu Insertions / 35
values are smaller than what we observed for a set of worldwide populations
(Batzer et al. 1994), as would be expected from a more closely related set of
populations in the native American group. Aborigines in the New World are
thought to derive from a limited number of individuals. Under these condi-
tions genetic diversity is expected to be reduced because of a bottleneck
effect. In addition, as humans migrated south from Alaska to Tierra del Fuego,
genetic drift would be expected to increasingly limit variability. When the
levels of heterozygosity are examined, we observe that, although the average
heterozygosity among North American groups is 51% higher than the com-
bined Central and South American average heterozygosity, the South Ameri-
can population exhibits an 18% higher average heterozygosity than the Cen-
tral American groups. Although admixture may be responsible for high levels
of heterozygosity in some North and South American populations, the higher
level of heterozygosity in South American groups compared with Central
American populations does not support only north to south migrations of
people from northern Asia to the southernmost regions of South America.
The relationship between populations can be deduced from the topology
of the maximum-likelihood tree (Figure 2). In the tree and consistent with
previous reports (Batzer et al. 1994; Novick et al. 1995), the African groups
are closer to the hypothetical ancestor. This is compatible with a probable
placement of the origin of the polymorphic Alu insertions and of the ancestors
of modern human populations in Africa.
The Inca are found at a distance from the other native American pop-
ulations. In addition, the Inca and Moskoke groups show the highest average
heterozygosity (0.45 and 0.42, respectively) and the highest gene flow (cen-
troid analysis, Figure 3). These results lead us to conclude that these two
populations have experienced a significant degree of admixture with non-
American native groups (i.e., Europeans and/or Africans). It is possible that
at the sites where our samples were collected, these two populations are rela-
tively admixed.
In two cases, the Buctzotz Maya/Campeche Maya and the Alaska/
Greenland natives, closely related populations collected from different
regions cluster together in the maximum-likelihood tree (Figure 2). This also
reflects the specificity and resolving power of polymorphic Alu insertions. It
is significant that the related Alaskan native (Eskaleut) and Greenland Eskimo
populations, located approximately 3000 miles apart, group so closely in the
maximum-likelihood analysis.
Although the three linguistic clusters are not equally represented in our
population set, the maximum-likelihood analysis does not show a distribution
compatible with the Eskaleut (Alaskan and Greenland natives), Nadene (Nav-
ajo), and Amerind (the rest of the native American populations in this study)
linguistic clusters. Rather, the phylogenetic tree exhibits three major identi-
fiable groups reflecting geographic distribution. One group (going from north
to south) includes populations from North America (Sioux, Moskoke, Alas-
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36 / NOVICK ET AL.
kan natives, Greenland natives, Buctzotz Maya, and Campeche Maya). This
cluster also incorporates the Wayuu from Colombia. This tribe has kept a
centuries-old commercial relationship with the populations from the Dutch
Antilles, with which they show a strong degree of admixture (Yunis et al.
1994). This may explain their location in the North American paraphyletic
group, closer to European Americans. The second paraphyletic group includes
populations from Central America (Ngobe and Waunana). The third group
contains most of the populations from South America: Guambiano, Kogui,
Quechua, Ingano, Paez, Guayabero, Chimila, and Kantiana. It is significant
that the Asian (Chinese) population is phylogenetically closer to most of the
North American groups than to the Central and South American groups. Also,
the phylogenetic affinities among native American populations parallel the
north to south geographic distribution of the groups, with most of the South
American populations and North American populations being more related
to the Central American groups than to each other. It is possible that a single
migration to the New World followed by partial isolation and genetic drift
gave rise to this geographic distribution and the observed differences in allele
frequencies between the native American populations.
As previously reported for 42 populations worldwide with 120 allele
frequencies from classical genetic markers (Cavalli-Sforza et al. 1994), Asian
populations, including native American groups, and European populations
cluster on the same branch when analyzed using the 5 polymorphic Alu
insertion loci. Also, as with the classical markers studied by Cavalli-Sforza
et al. (1994), the African populations group by themselves (Figure 2). The
close correspondence between the results from these two types of DNA
marker systems adds support to the significance of /-derived phylogenetic
analysis.
Our analyses also show that the Chinese consistently cluster within the
North American group. This parallels previously published data on mito-
chondrial DNA that establish native American mitochondrial DNA as derived
from a few mitochondrial haplotypes found in Asian populations of south-
eastern China (Shurr et al. 1990; Ballinger et al. 1992; Torroni et al. 1992;
Wallace and Torroni 1992). Yet it contrasts with the position of the Chinese
in phylogenetic trees derived from 120 allele frequencies (Cavalli-Sforza et
al. 1994). Using classical genetic markers, Cavalli-Sforza et al. (1994) found
that the Chinese are located on a different branch from the native Americans,
off the second bifurcation. Eurasian populations, including native Americans,
northeastern Asians, and Caucasoids, group on another branch off the second
bifurcation. Because of their attributes as genetic markers, the polymorphic
Alu insertions may provide a level of phylogenetic sensitivity that allows for
the detection of some evolutionary relationships (Chinese-native American).
Modern humans are assumed to have migrated from Africa to Europe
and Asia and from there to the Americas through the Bering Strait. In this
scenario it should be expected that the Chinese would be located somewhere
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Polymorphie Alu Insertions / 37
in between the African groups and the native American populations. There-
fore it is interesting that the Chinese group closer to the Amerinds, such as
the Mayan populations, than to Alaskan and Greenland natives, who represent
a more recent and continuing wave of migrants from Asia.
Under conditions where genetic differences are not generated by new
alleles, as in the case of the Alu insertions of this study (all five insertions
took place before humans migrated out of Africa), all genetic differences at
these loci must be the result of genetic drift and possibly selection. Under
these conditions native Americans would be expected to be more different
from each other and from their Asian ancestors. Although genetic drift was
supposedly a prominent phenomenon as humans migrated south in limited
numbers, humans were subjected to ever decreasing diversity, as opposed to
the more open and interactive migrations such as the ones from Africa to Asia
or Europe. In other words, because variations between all human populations,
as far as these five Alu insertions are concerned, are due to bottleneck events
and genetic drift, situations that favor these two phenomena would act to
make populations differ more from each other and from groups less influenced
by these forces. Therefore, why are native Americans so similar to each other
and the Chinese? One possibility is that instead of a single migration wave,
several migration waves from the same source population took place. Also,
recent and generalized migrations from Asia may have helped to keep the
homogeneity of the native American genetic stock and its close genetic af-
finity to the Chinese.
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