AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 135:448–461 (2008)

Genetic Admixture, Relatedness, and Structure

Patterns Among Mexican Populations Revealed
by the Y-Chromosome
H. Rangel-Villalobos,1* J.F. Muñoz-Valle,2 A. González-Martı́n,3 A. Gorostiza,3,4 M.T. Magaña,5
and L.A. Páez-Riberos1
1
Centro de Investigación en Genética Molecular, Centro Universitario de la Ciénega, Universidad de Guadalajara
(CUCiénega-UdeG), CP 47810, Ocotlán, Jalisco, México
2
Instituto de Enfermedades Reumáticas y del Sistema Músculo-Esquelético, Centro Universitario de Ciencias de la
Salud (CUCS-UdeG), Universidad de Guadalajara, CP 44800, Jalisco, México
3
Departamento de Zoologı́a y Antropologı́a Fı́sica, Universidad Complutense de Madrid (UCM),
28040, Madrid, España
4
Laboratorio de Genética Molecular, Escuela Nacional de Antropologı́a e Historia (ENAH), CP 14030, México, DF
5
División de Genética, Centro de Investigación Biomédica de Occidente (CIBO-IMSS), CP 44800, Guadalajara,
Jalisco, México

KEY WORDS Y-STRs; Amerindians; Mestizos; Mexico; Mesoamerica; Hispanics; admixture

ABSTRACT Y-linked markers are suitable loci to an-
alyze genetic diversity of human populations, offering
knowledge of medical, forensic, and anthropological in-
terest. In a population sample of 206 Mestizo males
from western Mexico, we analyzed two binary loci (M3
and YAP) and six Y-STRs, adding to the analysis data of
Mexican Mestizos and Amerindians, and relevant world-
wide populations. The paternal ancestry estimated in
western Mexican-Mestizos was mainly European (60–
64%), followed by Amerindian (25–21%), and African
(15%). Significant genetic heterogeneity was estab-
lished between Mestizos from western (Jalisco State)
and northern Mexico (Chihuahua State) compared with
Mexicans from the center of the Mexican Republic
(Mexico City), this attributable to higher European
ancestry in western and northern than in central and
southeast populations, where higher Amerindian ances-
try was inferred. This genetic structure has important
different Pre-Hispanic evolutionary processes were evi-
dent. In Mesoamerican region, populations presented
higher migration rate (Nm 5 24.76), promoting genetic
homogeneity. Conversely, isolated groups from the
mountains and canyons of the Western and Northern Si-
erra Madre (Huichols and Tarahumaras, respectively)
presented a lower migration rate (Nm 5 10.27) and
stronger genetic differentiation processes (founder effect
and/or genetic drift), constituting a Pre-Hispanic popula-
tion substructure. Additionally, Tarahumaras presented
a higher frequency of Y-chromosomes without Q3 that
was explained by paternal European admixture (15%)
and, more interestingly, by a distinctive Native-Ameri-
can ancestry. In Purepechas, a special admixture pro-
cess involving preferential integration of non-Purepecha
women in their communities could explain contrary
genetic evidences (autosomal vs. Y-chromosome) for this
tribe. Am J Phys Anthropol 135:448–461, 2008. V 2007 C

implications for medical and forensic purposes. Two Wiley-Liss, Inc.

During the last few years, many markers have been
described at the nonpseudoautosomal region of the
human Y-chromosome for anthropological, genealogical,
and forensic purposes (Underhill et al., 2000; Hammer
et al., 2001; Butler, 2005). Among these, binary polymor-
phisms in the Y-chromosome are the result of unique (or
near-unique) mutation events, as base-pair substitutions
or insertion–deletions, which represent stable paternal-
lines known as haplogroups (Knijff, 2000); for instance,
the Y-chromosome Alu polymorphism, known as YAP or
DYS287, is an insertion that has been used to define the
paternal African component in human populations
(Hammer and Horai, 1995). In America, transition C?T
at the locus DYS199 defines M3, a Y-binary marker that
distinguishes Y-chromosomes predominant in Amerin-
dian males, which has been extensively used to charac-
terize native and Hispanic populations from America
(Lell et al., 1997; Batista-Dos-Santos et al., 1999; Mesa
et al., 2000; Carvajal-Carmona et al., 2000). On the other
hand, Y-linked STRs (Y-STRs) are multiallelic loci with a
higher mutation rate; they constitute the STR-haplo-
types used to analyze internal haplogroup diversity
(Kniff et al., 2000). The combined study of Y-STRs and
binary markers has demonstrated usefulness for recon-
This article contains supplementary material available via
the Internet at http://www.interscience.wiley.com/jpages/0002-9483/
suppmat.
Grant sponsor: Consejo Nacional de Ciencia y Tecnologı́a (CON-
ACyT); Grant number: 48710.
*Correspondence to: Dr. Héctor Rangel-Villalobos, Centro de
Investigación en Genética Molecular, Centro Universitario de la
Ciénega (CUCI-UdeG), Avenida Universidad No. 1115, Col. Paso
Blanco, CP 47810, Ocotlán, Jalisco, Mexico.
E-mail: hrangel@cuci.udg.mx
Received 19 February 2007; accepted 25 October 2007
DOI 10.1002/ajpa.20765
Published online 27 December 2007 in Wiley InterScience
(www.interscience.wiley.com).

C 2007
V WILEY-LISS, INC.
 PATERNAL GENETIC STRUCTURE IN MEXICAN POPULATION
structing the demographic history of human populations
worldwide (Karafet et al., 1999; Lell et al., 2002; Zegura
et al., 2004).
In America, these studies are important because of
scarce knowledge concerning biological history and
relatedness among Native-American populations. Re-
garding these topics, Y-chromosome analysis provides us
with the opportunity to accept or discard hypotheses
proposed by other disciplines such as linguistics, ethnol-
ogy, and archeology. For example, geographic structure
of the Y-chromosome genetic variation has been used to
infer aspects of population history in South America,
demonstrating differential patterns of genetic drift and
gene flow (Tarazona-Santos et al., 2001). In Mexico,
there are [60 well-defined Amerindian tribes with their
own languages, customs, and religions (Scheffler, 1999).
They live throughout a large geographical extension of
Mexico, and can provide valuable information about de-
mographic events undergone by ancestral populations
living in Middle America, including important Prehis-
panic civilizations from Mesoamerica. In addition, the
entry of Europeans into the New World brought a num-
ber of significant changes in Native American popula-
tions. For instance, warfare and epidemiological dis-
eases caused a demographic decline that probably has
led to a reduction of the genetic diversity of these popu-
lations (Crawford, 1998). The increasing interactions
with peoples of European descendent, as well as the
introduction of African slaves, generated many Mestizo
populations in different parts of the Americas. As conse-
quence of these events, the indigenous American gene
pool has been substantially remodeled over the past 500
years (Schurr, 2004). For example, analysis of classic
markers in Mexican-Amerindians allowed suggesting
that there are no pure Indians groups in Mexico (Lisker
et al., 1996). In fact, analysis of the Y-chromosome and
mtDNA in the Mexican tribes Mixtecs, Zapotecs, and
Mixes, suggested differential gene flow, indicating that
European genes were introduced preferentially by males
(Torroni et al., 1994).
Despite the large number of Mexican-Ameridian
tribes, Mestizos represent the majority of the present-
day Mexican population that, using the Spanish lan-
guage as a selection criterion, constitutes about 90% of
the total population, whereas native communities pres-
ent a diminishing tendency because they are being
absorbed into the Mexican-Mestizo society (Fernández
and Serrano, 1996). Mexican-Mestizos are the result of
admixture, principally between Amerindians and Span-
iards, after the conquest of the New World; nevertheless,
when the number of natives decreased considerably in
some regions, Spaniards then brought African slaves
into Mexico. Over the next 250 years, new groups,
known as castes, were created (Aceves et al., 2006). The
National Institute of Anthropology defines a Mexican-
Mestizo as a person who was born in the country, who
has a Spanish-derived last name, and has a family of
Mexican ancestors back to the third generation. Despite
this well-established classification, the extent to which
several generations of intermarriage and interbreeding
between Mexican-Mestizos and ethnic groups have deter-
mined their actual genetic structure remains largely
unknown. Therefore, the possibility exists for signi-
ficant geographic structure within Mestizo populations
449
throughout the Mexican territory because of the differ-
ences in admixture among Spaniards, Amerindians, and
Africans (Bonilla et al., 2005).
Y-STRs haplotypes are ideal for investigating human-
population structure because they behave as (basically)
neutral markers, and their rapid evolution rate and
smaller effective population size means that they are
more sensitive indicators of genetic differentiation
between groups than are autosomal markers (Kayser
et al., 2003). Significant genetic differences among geo-
graphic Mexican populations would have important
implications for both forensic DNA and the medical com-
munity. Regarding the forensic DNA community, signifi-
cant geographic structure in genetic-pattern variation
would have to be taken into account when using or con-
structing databases for determining the probability that
unrelated individuals would match DNA profiles. Sepa-
rated databases would be required for each population/
geographic region. Conversely, the absence of significant
geographic structure would imply that the same data-
base could be utilized in populations from the same
region when one does not exist or is not available, which
is the situation for the majority of Mexican populations
at present (www.yhrd.org). With respect to the medical
community, the question of geographic structure within
Mexican populations influences the interpretation of geo-
graphic-pattern susceptibility to various diseases. The
existence of significant geographic structure in neutral
genetic markers would be consistent with a role for
underlying genetic differences in geographic variation
concerning disease susceptibility within Mexican popula-
tions. Conversely, the absence of significant geographic
structure would imply that geographic differences in dis-
ease susceptibility are instead due to variation in cul-
tural/environmental factors.
To address these questions, we studied eight Y-linked
markers (the binary loci M3 and YAP, and the following
six Y-STRs: DYS19, DYS389a DYS390, DYS391,
DYS392, and DYS393) in Mestizos from western Mexico,
adding the prior results of five Mexican Amerindian
groups (Páez-Riberos et al., 2006). This is, to our knowl-
edge, the first study of Y-linked markers analyzing dif-
ferent Mexican-Mestizo and Amerindian populations to
investigate geographic structure of the genetic variation
by AMOVA tests, paternal admixture, possible sceneries
of genetic differentiation between Mexican-Amerindian
tribes, and genetic relatedness analysis including rele-
vant worldwide population data.
MATERIALS AND METHODS
DNA samples
We analyzed a total sample of 314 unrelated Mexican
males. Mestizo samples consisted of 206 individuals with
a Spanish-derived surname and family history dating
back at least three generations. The majority of these
individuals were students from the Centro Universitario
de la Ciénega, Universidad de Guadalajara (CUCiénega-
UdeG) in Ocotlán, Jalisco State, Mexico, and had been
born in western Mexico, mainly including the states of
Jalisco, Nayarit, and Michoacán. Guadalajara City
located in western Mexico, is after Mexico City the sec-
ond largest metropolis in Mexico; the city was founded
by Spaniards in 1542 and has about 5 million inhabi-
tants at present. Western Mexican-Mestizos were origi-
nated by admixture occupying the surrounding areas of
large cities, such as Guadalajara City, whereas ethnic
American Journal of Physical Anthropology
450 H. RANGEL-VILLALOBOS ET AL.
groups remained far from cities in small isolated settle-
ments (Aceves et al., 2006).
The Amerindian sample was composed of 108 males,
including 34 Huichols from the Western Sierra Madre
in north of Jalisco and east of Nayarit, 16 Purépechas
from the lacustrine region of Michoacán, 20 Tarahuma-
ras from the mountains and canyons of Chihuahua, 34
Nahuas from the highlands in southern Puebla State,
and four Tzotzils from the state of Chiapas (see Fig. 1).
Detailed anthropological descriptions on the Huichol,
Purépecha, Tarahumara, Nahua, and Tzotzil sample
groups have been provided elsewhere (Rangel-Villalobos
et al., 2000; Páez-Riberos et al., 2006). Linguistically,
Nahuas, Huichols, and Tarahumaras are classified in
the same Nahua-Cuitlateco group, but Nahuas belong
to the Yutonahua family, whereas Huichols and Tarahu-
maras belong to the Yutoazteca family, while Tzotzils
belong to the Maya-Totonaco group, Mayense trunk,
Mayense family, and Yax sub-family (Sheffler, 1999).
Although a debate exists regarding the linguistic affilia-
tion of Purepéchas, they have been classified in the
Maya-Totonaco group, Purépecha trunk (Argueta-Villa-
mar, 1995). Prior to inclusion in our study, all volun-
teers signed an informed consent form, according to the
ethical guidelines of the Helsinki Declaration and
approved by the Ethical Research Committee at the
CUCiénega (UdeG). Differences in sample sizes for pur-
poses of analysis are properly indicated throughout the
text.
Laboratory analysis
DNA was extracted by standard phenol–chloroform
and salt-out methods. We analyzed six Y-STRs (DYS19,
DYS389a, DYS390, DYS391, DYS392, and DYS393)
with the primers and PCR conditions previously
detailed in Rangel-Villalobos et al. (2001). To analyze
the insertion/deletion YAP, we used the primers and
conditions suggested by Hammer and Horai (1995). The
marker M3 was analyzed according to the protocol
reported by Lell et al. (1997). We used the restriction
enzyme MunI (Life Technologies) to cut allele C of the
amplified product (181 and 30 pb), whereas allele T
American Journal of Physical Anthropology
Fig. 1. Geographical position and
sample size of the Mexican populations
used to estimate genetic distances
(Rst) and AMOVA tests using Y-STR
haplotypes (see Table 1). For discus-
sion purposes, limits of Mesoamerica
are indicated. [Color figure can be
viewed in the online issue, which is
available at www.interscience.wiley.
com.]
remained uncut (211 pb). In each case, we employed
positive controls to check correct digestion, as well as
negative controls to detect contamination. Amplified
products were run on vertical polyacrylamide gels with
1X TBE buffer prior to silver staining. We used the
term haplotypes and haplogroups for allele combina-
tions of Y-STRs and Y-binary loci, respectively. Hap-
logroups were named according to Y Chromosome
Consortium (2002) recommendations.
Data analysis
For each population, allele and haplotype frequencies
were estimated by counting method for Y-STRs and the
binary loci. Because of the small sample size (n 5 4),
Tzotzils were not analyzed individually, but rather were
included in pooled ethnic groups. Pairwise comparisons
of allele frequencies were carried out by exact tests. For
Mestizos and pooled ethnic groups, standard error (SE)
for allele frequencies was computed as the square root
of a binomial distribution: SE 5 Hf (1 2 f/n), where n
is sample size. The gene diversity (h) of each Y-STR was
P 2 as its theoretic heterozygosity as follows: h 5
calculated
1 2 f i , where f represents the frequency of the ith
allele. The following four haplotype-diversity parame-
ters were estimated for each population: number of dif-
ferent haplotypes; average of pairwise differences (p);
average of gene diversity, (h) and haplotype diversity
(D) with its variance. On the basis of binary Y-linked
markers M3 (C?T) and YAP (ins/del), we found three
different haplogroups: i) Q3 or Amerindian (T/del); ii)
xYAP or African (C/ins), and iii) the ancestral Y* (C/
del), without a well-defined geographical origin. Pater-
nal admixture components for each population were
established based on these haplogroups. In Mexican eth-
nic groups, the possible Amerindian/EuroAsian origin of
the ancestral Y* chromosomes was defined by their
Y-STR haplotype, analyzing their prevalence and/or low
frequency in populations on a worldwide database
(www.yhrd.org).
To improve global relationships of the analyzed Mexi-
can populations, additional population data from Mesti-
zos, Amerindians, Hispanics, and Spaniards were
 PATERNAL GENETIC STRUCTURE IN MEXICAN POPULATION 451
TABLE 1. Haplotype population data employed to estimate genetic distances (Rst values) and/or AMOVA
Population Origin of the sample n Reference
Hispanic
Mexican Western (Jalisco) 206 This study
Mexican Central (Mexico, City) 357 Luna-Vázquez et al., 2008a
Mexican North, Central (Chihuahua) 326 Gutiérrez-Alarcón et al., 2007a
Peruvian 24 different localities 79 Iannacone et al., 2005
Spanish Southwest, Spain 111 Gamero et al., 2002
Spanish Barcelona, Spain 239 Gené et al., 1999
Amerindian
Huichols Western, Mexico 34
Purépechas West-Central, Mexico 36 Páez-Riberos et al., 2006
Tarahumaras North Central, Mexico 20 This study
Nahuas South Central, Mexico 34
Tzotzil South East, Mexico 4
Otomı́ 1 16
Otomı́ 2 Hidalgo state 32 Barrot et al., 2007
Huastecos Central Region, Mexico 42
Tepehuas 13
Mayas Southeast, Mexico 6 Bianchi et al., 1998
Lengua-Ayoreo South, Paraguay 20 Bianchi et al., 1998
Chorote-Wichı́-Toba Salta, Argentina 25 Bianchi et al., 1998
Humahuaqueño and Susque Jujuy, Argentina 27 Bianchi et al., 1998
a
Published in www.ystr.org (release 20).

included (Table 1). For purposes of comparison with
some previous reports, allele nomenclature for DYS389I
was adjusted (allele 9 corresponds to 12), DYS389II and
the binary loci M3 and YAP were excluded because they
were not analyzed in all cited populations. Genetic relat-
edness among populations was analyzed by different
approaches: a) haplotypes shared between populations,
b) Rst value, a molecular distance based on the sum of
the squared number of repeat differences between two
haplotypes, which is analogous to Fst but based on a
step-wise mutation model, c) statistical significance tests
of pair-wise Rst values, and d) Multidimensional Scaling
plot was created with Rst values to represent graphically
the genetic relationships among populations. In addition,
we estimated the correlation coefficient between genetic
and geographic distances, whose statistical significance
was evaluated by the Mantel test. Distances in km
between populations were computed using geographic
coordinates with the program Great Circle Calculator
(http://www.gb3pi.org.uk/great.html). Indices of popula-
tion genetic structure (molecular variance and F statis-
tics) were computed by the AMOVA test based on Rst
values. The AMOVA test based on Rst distance between
Y-STR haplotypes considers both frequency differences
among haplotypes, as well as haplotype relatedness. We
defined the variance of components due to the different
sources of variation (among groups, among populations
within groups, and within populations); their significan-
ces were tested by use of a nonparametric procedure
with 10,000 permutations. Different population grouping
for AMOVA tests were properly indicated in the text. We
quantified differences in gene flow between two Prehis-
panic regions: Amerindian populations from Mesoamer-
ica, and tribes from Mountains of the Sierra Madre. For
this purpose, Amerindian tribes were grouped to esti-
mate the effective number of migrants (Nm) on the basis
of Wright’s island-migration model, ignoring mutation
and assuming migration-drift equilibrium based on the
following formula for uniparental markers: Nm 5 (1/GST)
2 1 (Nei, 1987). For all these purposes, we used the soft-
ware’s ARLEQUIN 2000 (Scheneider et al., 2000), GDA
version 1.1 (Lewis and Zaykin, 2001), TREEVIEW pro-
gram (Page, 2001), and SPSS for Windows, release 10.01
(1999).
RESULTS
Allele frequencies and gene diversity
Allele frequencies for the six Y-STRs for five Mexican
populations and pooled ethnic groups are presented in
Table 2. Western Mestizos had similar Y-STR allele dis-
tribution to those from the state of Chihuahua (P [
0.05), but different to Mestizos from Mexico City and
pooled Mexican tribes for nearly all six Y-STRs (P \
0.05), except for DYS391 and DYS389I, respectively.
Regarding each Y-STR/population, a high frequency of
the allele 13 at DYS19 was observed in Amerindian
tribes (range, 70.6–81.3%), whereas allele 14 was the
mode at DYS19 in Mexican-Mestizos, similar to many
European populations (Kayser et al., 1997; Knijff et al.,
1997); in general, this resemblance was evident for all
six Y-STRs. For DYS389I, similarity among ethnic
groups was not as apparent due to differences in allele
distributions; in Huichols, allele DYS389I-12 was
detected, this is absent in the majority of worldwide pop-
ulations. Interestingly, only the Inuits, an Eskimo-Aleut
tribe from North America, presented a high frequency
for this allele (14%) (Kayser et al., 1997; Knijff et al.,
1997). This observation could imply an ancestral rela-
tionship between these Native-American groups,
whereas its presence in Mexican-Mestizos could be
explained by its ethnic component, probably deriving
from diffusion from their neighbors, the Huichols. For
DYS390, allele distribution in ethnic groups was also
heterogeneous; the Huichols were remarkable in their
high frequency of allele 24 (79.4%), and Tarahumaras in
their having only two alleles (23 and 24). For DYS391,
the Huichols once more were notable for a high allele
frequency (allele 10, 82.4%). For DYS392, we observed a
particular Gaussian distribution in pooled Mexican eth-
nic groups, attributable to the higher frequency of alleles

American Journal of Physical Anthropology

452 H. RANGEL-VILLALOBOS ET AL.
TABLE 2. Allele distribution (%) of six Y-linked STRs in five Mexican populations
Mestizo Huichol Tarahumara Purépecha Nahua Pooled-Amerindian
Allele n 5 206a n 5 34 n 5 20 n 5 16 n 5 34 tribes n 5 108b
DYS19
13 24.8 6 3.0 70.6 80 81.3 79.4 78 6 3.1
14 46.1 6 3.5 29.4 10 18.8 17.6 19.3 6 2.7
15 21.4 6 2.9 5 2.9 1.8 6 0.9
16 4.4 6 1.4 5 0.9 6 0.6
17 3.4 6 1.3
DYS389I
9 15.5 6 2.5 2.9 30 37.5 20.6 18.5 6 2.6
10 61.7 6 3.4 58.8 30 50.0 70.6 56.5 6 3.5
11 22.3 6 2.9 35.3 40 12.5 8.8 24.1 6 2.9
12 0.5 6 0.5 2.9 0.9 6 0.6
DYS390
21 2.9 6 1.2
22 8.7 6 2.0 2.9
23 27.7 6 3.1 8.8 40 12.5 11.8 17.6 6 2.6
24 50.5 6 3.5 79.4 60 37.5 64.7 63.9 6 3.4
25 8.3 6 1.9 11.8 37.5 17.6 15.9 6 2.5
26 1.9 6 1.0 12.5 2.9 2.8 6 1.1
DYS391
9 3.9 6 1.3 5.9 10 31.3 14.7 12.8 6 2.2
10 60.7 6 3.4 82.4 60 56.3 61.8 67 6 3.4
11 33.5 6 3.3 5.9 30 12.5 23.5 18.3 6 2.6
12 1.9 6 1.0 5.9 1.8 6 0.9
DYS392
10 2.9 0.9 6 0.6
11 35.0 6 3.3 5.9 1.8 6 0.9
12 2.4 6 1.1 11.8 15 31.3 17.6 6.4 6 1.6
13 43.7 6 3.5 38.2 45 43.8 29.4 20.2 6 2.7
14 10.2 6 2.1 44.1 35 18.8 14.7 33.9 6 3.2
15 2.9 6 1.2 5.9 5 6.3 14.7 27.5 6 3.0
16 4.4 6 1.4 8.8 7.3 6 1.7
17 1.5 6 0.8 5.9 1.8 6 0.9
DYS393
11 1 6 0.7
12 19.3 6 2.8 20 11.8 7.3 6 1.7
13 67.1 6 3.3 100 80 81.2 79.4 85.3 6 2.9
14 11.1 6 2.2 5.9 3.7 6 1.3
15 1.5 6 0.8 18.8 2.9 3.7 6 1.3
a
Differences in sample size is due to incomplete Y-haplotypes that were not included in Appendix 1 (Electronic supplementary material).
b
Four Tzotzil males were included at pooled Mexican ethnic groups.

TABLE 3. Gene diversity (h)a of six Y-linked STRs in five Mexican populations
Mestizo Huichol Tarahumara Purépecha Nahua Pooled-Amerindian tribes,
Y-linked STR n 5 206 n 5 34 n 5 20 n 5 16 n 5 34 n 5 108b
DYS19 67.7 41.5 34.5 30.4 33 35.4
DYS389I 54.6 52.8 66 59.4 44.8 58.8
DYS390 65.3 34.8 48 68.8 55.4 53.5
DYS391 51.7 31.1 54 56.2 53.1 50
DYS392 67.3 64.2 65 67.1 82.1 80.4
DYS393 50.0 0 32 30.5 34.3 26.43
a
Expected heterocigozity (Nei, 1987).
b
Four Tzotzil males were included at pooled Mexican ethnic groups.

13, 14, and 15, which is in agreement with previous
reports on Amerindians (Bianchi et al., 1998). For
DYS393, Huichols had only allele 13, whereas Tarahu-
maras and Purépechas had only two alleles. Conversely,
the Nahua tribe was noteworthy in having a greater
number of alleles than the remaining Mexican tribes. As
consequence of these allele distributions, interesting dif-
ferences in gene diversity were noticeable between Mexi-
can-Mestizos and pooled Amerindian tribes (Table 3).
For instance, it was higher in Mestizos, particularly at
DYS19 and DYS393 (P \ 0.001); nevertheless, a higher
gene diversity was observed in pooled ethnic groups for
DYS389I and, mainly, DYS392 (P 5 0.0094). These pecu-
liar features can be used to identify Amerindian Y-chro-
mosomes when haplogroup is not available (transition
Q3), particularly the high prevalence of allele DYS19*13,
DYS393*13, and DYS392*14-17. Among Mexican Amer-
indian tribes, Huichols had the lowest gene diversity for
three Y-STRs and, conversely, Purépechas presented
higher gene diversity than Mexican-Mestizos at three

American Journal of Physical Anthropology

 PATERNAL GENETIC STRUCTURE IN MEXICAN POPULATION 453
TABLE 4. Distribution of Haplogroups Q3, xYAP, and *Y in Mexican populations
Haplogroup (%)
Geographical location at states
Mexican population Sample size (n) of Mexico Q3 Y* xYAP Reference
a
Western Mestizos 191 Jalisco, Nayarit, and Michoacán 17.3 68.1 14.7 This study
Huichol 34 Jalisco and Nayarit states 100 – – This study
Purépecha 16 Michoacán 93.8 6.3 – This study
Tarahumara 20 Chihuahua 55 45 – This study
Nahua 34 South of Puebla 79.4 17.6 2.9 This study
Tzotzil 4 San Cristobal, Chiapas 100 – – This study
Mixe 14 Highlands, Oaxaca 85.7 – 14.3 Lell et al., 1997
Mixtecs 10 Highlands, Oaxaca 70 30 – Lell et al., 1997
Zapotecs 6 Highlands, Oaxaca 50 50 – Lell et al., 1997
Mixtecsb 4 Tlapa, Guerrero 100 – – Bonilla et al., 2005
Nahuasb 22 Tlapa, Guerrero 59.1 40.9 – Bonilla et al., 2005
Tlapanecsb 6 Tlapa, Guerrero 83.3 16.7 – Bonilla et al., 2005
Total Tlapa region 48 Tlapa, Guerrero 60.4 39.6 – Bonilla et al., 2005
Total ethnic groups 186 76.4 22.0 1.6
a
Differences in sample size, is due to incomplete Y-haplotypes were not included in Appendix 1 (Electronic supplementary
material).
b
Data not considered for average estimation of total ethnic groups.

Y-STRs (DYS389I, DYS390, and DYS391), confirming a
previous observation with a small Mestizo sample (n 5
31) (Páez-Riberos et al., 2006).
Haplogroup distribution and paternal
genetic admixture
In the total Mexican population sample, 181 different
complete Y-STR haplotypes were observed in three hap-
logroups formed by M3 and YAP, including 75 Amerin-
dians (Q3), 88 undifferentiated (Y*), and 18 African
(xYAP) [Appendix 1; Electronic Supplementary Material
(ESM)]. Haplogroup frequencies in each population,
including data previously reported on Mexican ethnic
groups, are presented in Table 4.
In the cosmopolitan Mexican-Mestizo population,
Amerindian haplogroup Q3 was 17.3%. Although the ma-
jority of undifferentiated Y* haplogroups could represent
a European component, it must be considered that a pro-
portion of Y* also includes the second Amerindian line-
age Q-P36*, which gave rise to Q3. Both lineages consti-
tute the Q haplogroup, and these arrived together to the
New World through the Bering Strait (Ruı́z-Linares
et al., 1999; Lell et al., 2002). In two studies including
588 Native Americans (Zegura et al., 2004), and 478 His-
panic-Americans (Hammer et al., 2006), the frequency of
Q3 (52.6 and 7.9%) and Q-P36* (23.8 and 3.8%) were
determined; thus, considering that P* represented 45.3
and 48.1% of Q3, respectively, we made a roughly (but
similar) estimation of the Amerindian haplogroup Q in
this Mexican-Mestizo sample, which resulted in 25.1–
25.6%. Similarly, considering the average frequency of
Q3 in pooled Mexican tribes (76.4%) (Table 3), including
Mixes, Mixtecs, and Zapotecs from the Oaxaca State
highlands (Lell et al., 1997) and males from the Guer-
rero-State Tlapa region (Bonilla et al., 2005), the Amer-
indian component in Mestizos was again estimated
(21.4% 6 3.0). xYAP haplogroup frequency in Mestizos
was 14.7%, representing the African component of this
population. Taken together, these results indicated that
the paternal component in this Mestizo sample from
western Mexico would be principally European (60–
64%), followed by Amerindian (25–21%), and African
(15%), respectively.
In the Mexican ethnic groups studied herein, the pre-
dominant lineage was Q3 (84.3%), and nearly all the
remaining lineages were Y* (14.8%). Huichols had only
Amerindian haplogroups Q3, indicating null or low pa-
ternal admixture. Purépechas had a low frequency
(6.25%; 1/16) of the haplogroup Y* (Y*78) (Appendix 1;
ESM), which was inferred as ‘‘Amerindian’’ (see Method-
ology), presumably Q-P36*, supporting low paternal
admixture in Purépechas. Tarahumaras possessed the
highest frequency of haplogroups Y* (45%; 9/20); how-
ever, the majority of these (6/9) were inferred as Amer-
indians, indicating that the paternal nonnative admix-
ture in Tarahumaras would be nearly 15% (3/20).
Removing this admixture, Tarahumaras continued to
exhibit the highest Amerindian component without Q3
(35.3%; 6/17), suggesting a peculiar conformation pro-
cess with respect to the remaining Mexican ethnic
groups studied. This process in Tarahumaras could
involve a different prevalence of Native American line-
ages, as haplogroups P* and C, which would had arrived
to the Americas in a second migration event by a coastal
route (Schurr, 2004), helped by their geographical posi-
tion closer to Arid American tribes. Nahuas comprised
the unique tribe presenting the African haplogroup
xYAP (2.9%; 1/34), whereas five of the six Y* hap-
logroups were classified as non-Amerindians (14.7%; 5/
34). Consequently, Nahuas had the highest paternal
nonnative admixture (17.7%; 6/34), closely followed by
Tarahumaras (15%; 3/20). To describe the ancestral di-
versity of the Mexican ethnic groups, haplotype diver-
sity in Tarahumaras and Nahuas was estimated twice,
with and without the non Amerindian-inferred haplo-
types (Table 5). Omitting non-Amerindian haplotypes
(Y* and xY), the three Y-haplotype diversity parameters
were consistent confirming higher diversity of Mexican-
Mestizos, excepting for haplotype diversity (D) in Puré-
pechas. However, we must take into account that larger
Mestizo sample size results in smaller standard errors,
rendering their estimations more reliable. The higher
diversity in Mestizos is congruent to their admixed na-
ture (Gorodezky et al., 2001). Among Mexican-Amerin-
dian tribes, the highest and lowest genetic diversity
observed in Purépechas and Huichols, respectively, has
been reported with autosomal genetic systems (Rangel-
Villalobos et al., 2000).

American Journal of Physical Anthropology

454 H. RANGEL-VILLALOBOS ET AL.
TABLE 5. Haplotype diversity parameters at five Mexican populations
Population sample Different Average of pairwise Average gene Haplotype
size (n) haplotypes differences (p) diversity (%) diversity (D)
Mestizos (181) 121 4.1 6 2.1 51.7 6 28.6 98.8 6 0.32
Huichols (34) 15 2.3 6 1.3 28.7 6 17.9 89.8 6 3.2
Purépechas (16) 15 3.5 6 1.9 43.3 6 26.2 99.2 6 2.5
Tarahumaras (20/17) 17 3.7 6 1.9 45.9 6 27.1 98.4 6 2.1
14a 3.2 6 1.8 40.5 6 24.6 97.4 6 2.5
Nahuas (34/28)a 26 3.5 6 1.8 44.1 6 25.6 97.3 6 1.7
21a 2.9 6 1.6 36.3 6 21.9 96.3 6 2.4
a
Estimations omitting nonAmerindian Y* haplotypes from Tarahumaras (106, 139, 151) and Nahuas (99, 113, 114, 138, and xY
166).

Relatedness among populations

Nahuas and Tarahumaras were the tribes sharing the
greatest number of haplotypes with Mestizos (seven and
two, respectively), whereas between Mexican ethnic
groups, Huichols and Purépechas shared the greatest
number of haplotypes with three (Appendix 1; ESM).
Most widely distributed haplotypes were Q19 (Huichols,
Purépechas, and Mestizos) and Q27 (Nahuas, Huichols,
and Tzotzils). Genetic relationships between populations
were estimated by means of Rst values (data not shown),
which were used to develop multidimensional scaling
analysis (MDS; stress 5 0.137, r 5 0.9512) (see Fig. 2).
The significance of pair-wise Rst values indicated that
Mexican-Mestizos present genetic differentiation from
the majority of populations (P \ 0.01), except between
those of western and northern-central Mestizos (P 5
0.4697), western Mestizos and southwestern Spaniards
(P 5 0.1494), Mexico City Mestizos and Otomı́ 1 (P 5
0.0967) and, in lower degree, between northern-central
Mestizos and southwestern Spaniards (P 5 0.0283). Fig. 2. Multidimensional Scaling plot of Rst values between
Genetic similarity was observed among Mexican ethnic Amerindian, Hispanic, and Spanish populations (see Table 1)
groups (P [ 0.05), including Nahuas, Huastecos, Otomı́- based on 6 Y-STRs. [Color figure can be viewed in the online
1, Otomı́-2, Purépechas, and Peruvian population, the issue, which is available at www.interscience.wiley.com.]
latter presenting the highest genetic differentiation with
Nahuas (P 5 0.0127).
To investigate possible scenarios of Prehispanic genetic Analysis molecular of variance
differentiation, Mantel test was performed solely utiliz-
ing data with a minimum sample size (n [ 15; Table 1) The first AMOVA test, employing the complete eight
to check correlation between geographic and genetic dis- Y-loci system, was carried out with Western Mexican-
tances. This correlation has been used to assess the rela- Mestizos (first group) and the Mexican-Amerindians
tive importance of genetic drift and natural selection in studied here, including Huichols, Purépechas, Tarahu-
determining the genetic variation of human populations. maras, Nahuas, and Tzotzils (second group) (Table 6).
The average contribution of drift by serial founder Results indicated that the main and significant supplier
effects has been estimated in 76–78% as minimum, of variability was at the intrapopulational level (71.11%;
whereas the remaining 22–24% could be explained by P 5 0.0000), which is lower than the observed among
specific population-selection, drift, and mutational his- Hispanic Americans (99.2%; nonsignificant) (Redd et al.,
tories (Ramachandran et al., 2005). Our results demon- 2006). Although this difference can be explained as a
strated a significant correlation between geography and result of the polymorphism of the Y-linked systems
Rst genetic distances (r 5 0.8359, z 5 0.17; P 5 0.002), employed in each study (11 Y-STRs vs. 6 Y-STRs/2
a little lower (r2 5 0.6987) than the cited global estima- Y-SNPs), the significant differentiation among the three
tion. Although the isolation-by-distance (IBD) model Mexican Mestizo populations, as will be discussed, can
(Wright, 1943) could be invoked in this context, this be attributable to the Mexico City sample. Conversely,
model assumes equal effective population sizes, which is the difference between Mexican Mestizos and Amerin-
probably violated in the Mexican-Amerindian sample. dian tribes supplied 20.56% of the total variability, but
Conversely, on removing the more geographically iso- this was nonsignificant. This nondifferentiation can be
lated ethnic groups from the Sierra Madre (Huichols and explained by the native genetic ancestry of the Mexican-
Tarahumaras; Fig. 1) the correlation was not significant Mestizos, who were generated by the admixture among
(r 5 20.3837, z 5 0.0396; P 5 0.803); therefore, in the Amerindians and Europeans, principally Spaniards.
remaining tribes from the Mesoamerican region, our Although differentiation among Amerindian tribes con-
results suggests a complex scenery, probably influenced stituted 8.3% of the total variation, it was significant
by elevated gene flow between prehispanic populations (P 5 0.0000), suggesting important genetic differentia-
influenced by particular demographic histories. tion processes between Mexican tribes.

American Journal of Physical Anthropology

 PATERNAL GENETIC STRUCTURE IN MEXICAN POPULATION
TABLE 6. AMOVA tests in Mexican populations
Eight Y-linked locia
Comparison Variation (%) P-value
Between groups (FCT) 20.56 0.1544
Among populations into groups (FSC) 8.3 0.0000
Into populations (FST) 71.11 0.0000
a
Including M3 and YAP in the six Mexican populations here studied. Groups: (1) Western Mestizos and (2) Amerindians.
b
Including 3 Mexican-Mestizos and 10 Mexican-Amerindian populations, representing two groups (Table 1).
c
Including 10 Mexican Amerindians in two groups: (1) Huichols and Tarahumaras and (2) the remaining tribes.
To obtain a broad perspective of the genetic structure
in Mexican populations, we performed additional
AMOVA tests using haplotype data for the six Y-STRs
and for all 13 Mexican samples described in Table 1. In
the second AMOVA test, one group included three Mexi-
can-Mestizo populations (Western, Northern-Central and
Mexico City), while the second group included all the
remaining 10 Mexican-Amerindian populations (Table 6).
Again, the majority of variability occurred at intrapopu-
lational level (84.28%; P 5 0.0000), whereas the lowest
and significant variability was attributed to differences
among populations into groups (3.47%; P 5 0.0000). Sim-
ilar to the first AMOVA test, the variability attributable
to genetic structure between Mexican-Mestizo and Amer-
indian groups was not significant (12.25%; P 5 0.0527)
due to the shared genetic background reducing the
genetic differentiation between them.
To investigate the genetic structure of Mexican-Mesti-
zos and Amerindians independently, additional AMOVA
tests were conducted. Among the three Mexican-Mestizo
populations (those of Chihuahua State, Jalisco State,
and Mexico City), interpopulational variability was low
but significant (FST 5 3.14%; P 5 0.0000). Subsequently,
AMOVA tests were repeated, excluding each Mestizo
population sample. The lowest interpopulational vari-
ability was obtained when the Mexico-City sample was
excluded (Chihuahua vs. Jalisco; FST 5 20.00058), ren-
dering the difference between Mestizos from Chihuahua
(northern-central) and Jalisco (western) nonsignificant
(P 5 0.4482). The other two combinations (Jalisco vs.
Mexico City, and Chihuahua vs. Mexico City) provided
significant P-values (P 5 0.0000), demonstrating genetic
heterogeneity among Mexican-Mestizos attributable to
the differentiation of Mexico City.
Among the 10 Mexican-Amerindian tribes (Table 1),
AMOVA tests displayed a significant interpopulational
variability (FST 5 9.29%; P 5 0.0000) that was about
three times larger than among Mexican-Mestizos. To es-
tablish the role of the geographically more isolated and
differentiated tribes to the heterogeneity of Mexican
Amerindians, we repeated the AMOVA test separating
tribes from the Sierra Madre in one group (Tarahumaras
and Huichols), and remaining tribes representing to
Mesoamerica in the second group (Purépechas, Nahuas,
Tepehuas, Mayas, Otomı́1, Otomı́2, Tzotzils, and Huaste-
cos) (Table 6). As previously noted, intrapopulational
variability attributable to the genetic Y-linked system
was predominant (82.71%; P 5 0.0000), followed by the
variability between groups (FCT 5 15.46%; P 5 0.03519),
both of these significant; only the variability among pop-
ulations into groups was the smallest and not significant
(FSC 5 1.83%; P 5 0.14663). Together, these results indi-
cated that the genetic structure among Mexican-Amerin-
dian tribes is attributable to these two geographical
regions: one representing isolated populations from
455
Six Y-STRsb Six Y-STRsc
Variation (%) P-value Variation (%) P-value
12.25 0.0527 15.46 0.03519
3.47 0.0000 1.83 0.14663
84.28 0.0000 82.71 0.0000
mountains and canyons of the Sierra Madre, and the
second to Mesoamerican tribes (see Fig. 1), demonstrat-
ing homogeneity among populations into these geograph-
ical regions. Once defined these two Amerindian regions,
we checked for differences in gene flow between them.
We quantified the effective number of migrants (Nm),
indicating that among Amerindians from Mesoamerica
the migration rate is nearly double that among those
from the Sierra Madre (Nm 5 24.76 vs. 10.27).
DISCUSSION
In Mexico at present, two main populations are clearly
defined: Spanish-speaking Mestizos, who commonly rep-
resent Mexicans to the world, and Mexican ethnic
groups, also described herein as Amerindian tribes. After
500 years of biological admixture among mainly Span-
ish, Amerindian, and African ancestries, it is not sur-
prising to find a complex pattern of genetic variation
throughout the country. This is, to our knowledge, the
first study of genetic heterogeneity, admixture estimates,
and genetic relatedness using Y-linked haplotypes in
Mexican populations, including both Mestizo and Amer-
indian populations. We must state that, because of the
limited sample sizes, principally for most of the Mexican
Amerindian tribes here described, and the limited num-
ber of Y-linked loci analyzed, some observations could
reflect different levels of sampling error; accordingly,
some of them should be considered preliminary.
Allele distribution
Y-STR allele distributions of pooled Mexican Amerin-
dian tribes were similar to previous reports of Native
Americans (Rodrı́guez-Delfı́n et al., 1997; Bianchi et al.,
1998); however, these distributions were different from
Mexican-Mestizos from western Mexico (this study) and
distributions published to date from Chihuahua State
and Mexico City (www.yhrd.org). Heterogeneous modal
alleles, extreme allele frequencies (mode closer to 1), and
reduced genetic diversity in the majority of Y-STRs/Mex-
ican Amerindian tribes (excepting DYS392 and Purépe-
chas, respectively) appear to be the consequence of
different factors acting individually or in conjunction,
namely as follows: i) the smaller diversification time
since the peopling of the New World by ancestral Asian
groups, ii) higher geographical isolation levels, iii) foun-
der effects, and iv) low effective population size, propiti-
ating genetic drift (Crawford et al., 1998; Bortolini et al.,
2002). Among Mexican tribes, these characteristics were
noteworthy in Huichols, as previously observed with
autosomal DNA markers (Rangel-Villalobos et al., 2000),
and as could be expected by their cultural and geograph-
ical isolation level (Diguet, 1992).
American Journal of Physical Anthropology
456 H. RANGEL-VILLALOBOS ET AL.
Admixture estimates in Mexican-Mestizos
Admixture estimates in western Mexican-Mestizos
underscored the predominance of the European male
contribution (60–64%), followed by Amerindian (25–
21%) and African (15%) ancestry. Although prelimi-
nary, this result represented a high Amerindian paternal
component in Mexican-Mestizos compared with other
Latin American populations; for instance, this has been
established at 12.1% in Hispanic-Americans (Hammer
et al., 2006), 10% in La Plata, Argentina (Bianchi et al.,
1997), 0–5% in Brazil (Batista-Dos-Santos et al., 1999;
Carvalho-Silva et al., 2001), and 1% in Antioquia,
Colombia (Carvajal-Carmona et al., 2000). Conversely,
Amerindian ancestry appears to be low in western Mes-
tizos with regard to haplogroup Q3 frequency in Mexico
City (17.3 vs. 26.9%; P 5 0.0353) (Martı́nez-Mariagnac
et al., 2007), and in previous estimates ranging from
27.6 to 94.5% in 19 Mexican-Mestizos by means of ABO
blood systems, serum enzymes, and/or autosomal DNA
markers (Bonilla et al., 2005). Although a previous esti-
mate of European ancestry obtained with autosomal
markers in western Mexican-Mestizos was very close to
our results (56.1 vs. 60%), Native-American and African
ancestry estimates were different (43 and 0.9%, respec-
tively) (Cerda-Flores et al., 2002).
With respect to African ancestry in Mexican-Mestizos,
there are records indicating that this came principally
from the western coast of the African continent (between
the Senegal River and the Portuguese Angola) (Godor-
ezky et al., 2001). Nonetheless, it must be considered
that Spaniards, in themselves, also contributed to this
paternal African ancestry because they possess this as a
trace of the Neolithic-diffusion process in Europe (E3b*;
defined by M35), and as a consequence of Islamic rule on
the Iberian Peninsula for three centuries, increasing
from central to the southern Iberian peninsula (Pereira
et al., 2000). This multiethnic diversity is well docu-
mented in the genetic background of Spaniards, includ-
ing Phoenicians, Greeks, Romans, Visigoths, Arabs, and
Jews, this probably more evidently in the lower social
classes, who comprised the principal immigrants to
America (Godorezky et al., 2001). Moreover, the differ-
ences between Y-linked and autosomal admixture esti-
mates of the same Mexican Mestizo population (Cerda-
Flores et al., 2002) could be explained by two reasons: 1)
the inherent African component of Spaniards that,
because the limited number of Y-SNPs here analyzed,
was not exactly discriminated and 2) principally, by the
intrinsic differences between genetic systems that influ-
ence dynamics of admixture. For instance, the analysis
of both systems (in addition to the X-chromosome) in Anti-
oquia, Colombia, has suggested that after foundation, con-
tinuing admixture with Spanish men (but not with native
women) has increased the European nuclear ancestry of
this Latin American population (Bedoya et al., 2006).
From the maternal point of view, two reports on Mexi-
can-Mestizos demonstrated a greater extent of Amerin-
dian mtDNA haplogroups (89.1 and 90%) regarding the
native Y-chromosomes estimated herein (25%) (Green
et al., 2000; Martı́nez-Mariagnac et al., 2007). This effect
has been described as asymmetric gene flow, representa-
tive of unions between indigenous women and European
men, and has been observed in different Latin-American
populations (Torroni et al., 1994; Batista-Dos-Santos
et al., 1999; Carvajal-Carmona et al., 2000; Mesa et al.,
2000; Seielstad, 2000; Rodriguez-Delfı́n et al., 2001;
American Journal of Physical Anthropology
Campos-Sánchez et al., 2006). However, similar Native-
American contributions from the paternal (85–91%) and
maternal (98%) lineages were found in a southeastern
population (Tlapa, Guerrero State), suggesting that in
isolated and inbred Mexican populations (such as ethnic
groups), similar Amerindian ancestry could be found
from both maternal and paternal inheritance (Bonilla
et al., 2005).
Analyzing Mexican-Mestizos with a broader viewpoint
throughout the country, the previous admixture esti-
mates showed geographic area-associated ancestral-com-
ponent variation (Bonilla et al., 2005), which has been
represented in a tripolar diagram representing Amerin-
dian, European, and African ancestries (Godorezky
et al., 2001). In terms of this viewpoint, although the
number of genetically pure individuals of any of the
three racial components would be insignificant, higher
Amerindian, European, and African ancestry would be
greater in southeastern, northern, and coastal regions of
Mexico, respectively. All together, the pairwise compari-
son of allele frequencies, MDS, significance test of Rst
values and AMOVA tests indicated a higher and signifi-
cant paternal similarity between Mexican-Mestizos from
northern-central and western Mexico, but significant
genetic differentiation from Mestizos from Mexico City,
who had a closer genetic relationship with the Otomı́-1
ethnic group. Thus, we could state that there is a higher
European ancestry in Mestizos from northern-central
and western Mexico in comparison with Mestizos from
Mexico City, who presumably would have higher Amer-
indian ancestry, partially supporting the tripolar dia-
gram from the paternal side. Concurrently, the same
pattern has been observed in a population data report of
autosomal STRs in Mestizos from of Veracruz, a state in
central region along the Gulf of Mexico (Licea-Cadena
et al., 2006); the authors reported similarity between the
cities of Chihuahua and Monterrey (northern group) and
between Mexico City and the city of Veracruz (central-
eastern group), but significant differentiation for some
STRs between these northern and southern-central
groups. The same conclusion, adding western Mestizos
from Jalisco State to the northern region, has been
obtained with nine autosomal STRs (Rangel-Villalobos,
unpublished data). Supporting a higher Amerindian
component in the southeastern region, analysis of ances-
try-informative markers (AIMs) in the city of Tlapa,
Guerrero, has displayed elevated Amerindian ancestry
in this population (94.5%) (Bonilla et al., 2005). Addition-
ally, in a preliminary study analyzing M3 and YAP Y-bi-
nary loci we observed a higher frequency of the Amerin-
dian haplogroup Q3 in the Costa Chica-area of Oaxaca
and Guerrero on the south coast (59.1%; n 5 22) than on
the western coast including the states of Jalisco and
Michoacán (22%; n 5 59) (see Fig. 1). On the other
hand, despite having a well-documented African ances-
try in the Costa Chica (Aguirre, 1989), the estimated fre-
quency of African haplogroup xYAP did not increase in
this region (9%; n 5 22), nor did it on the western coast
(3.4%; n 5 59). Although our sample size limits the con-
clusions of these results, they undermine the suggested
increment of African ancestry along the Mexican Coast,
at least for the paternal side. Conversely, some studies
with classical genetic markers (Bonilla et al., 2005) and
autosomal DNA markers support higher African ances-
try at specific coastal locations in Mexico. For instance,
in the Costa Chica of Oaxaca and Guerrero two African
haplotypes in the b-globin gene (Bantu and Benin) capa-
 PATERNAL GENETIC STRUCTURE IN MEXICAN POPULATION
ble of causing sickle cell anemia (Hb S) have been
detected at high frequencies (52.4 and 19%, respectively)
(Magaña et al., 2002). Another example is the Yanga
population from Veracruz State in Mexico’s central
region along the Gulf of Mexico, where autosomal STRs
also have suggested a higher African ancestry in this
population (Gorostiza and González-Martı́n, 2004).
Population genetic structure in Mexican-Mestizos
AMOVA tests in Mexican-Mestizos demonstrated sig-
nificant population heterogeneity, this attributable to the
differentiation of Mexico City; presumably, because a
higher Amerindian ancestry. This paternal genetic struc-
ture, but no maternal (mtDNA), has been observed
among Hispanic populations from Costa Rica, Mexico,
and the southwestern United States (Campos-Sánchez
et al., 2006). Although we have estimated a similar het-
erogeneity with autosomal STRs (unpublished data), a
previuos study with autosomal DNA markers have con-
cluded that homogeneity exists among Mexican-Mestizo
populations. For instance, Cerda-Flores et al. (2002)
reported similar ancestral contributions in Mestizos from
the same regions analyzed in this work: Mexico City
(central), Jalisco (western), and Nuevo León (northern).
In addition to the use of different genetic systems (previ-
ously discussed, autosomal vs. Y-linked loci), these oppo-
site conclusions could be explained as the result of addi-
tional genetic intrapopulation structure. This fact has
been demonstrated in Mexico City by means of classical
blood markers with individuals classified according to
their socioeconomic status, showing higher Amerindian
ancestry in the low (48%) as compared with the high
(27.6%) socioeconomic status (Lisker et al., 2004). Simi-
larly, a recent analysis of AIMs in Mexico City demon-
strated a significant association between European
admixture proportion and higher educational status
(odds ratio [OR] 5 9.4) (Martı́nez-Mariagnac et al.,
2007). This result is not surprising, considering the low
educational status and poorly qualified work of the in-
digenous people, rending it difficult for these individuals
to be incorporated into the economical and social devel-
opment of the large cities to which they arrive from ru-
ral communities (Valencia-Rojas, 2000). This intrapopu-
lational structure could be responsible for the differences
previously observed in admixture estimates from the
same Mexican-Mestizo populations, in which sampling
bias could be invoked (Bonilla et al., 2005). Regarding
the western Mestizo population sample, is important to
note that the majority of University of Guadalajara stu-
dents (here studied) can be classified into a low or mid-
dle socioeconomic status; thus, the potential sample bias
would get homogeneous to Mestizos from the West
(Jalisco) and Mexico City, which did not happened, rein-
forcing the results of heterogeneity between these Mexi-
can-Mestizo populations. In Hispanics from the US, this
genetic heterogeneity has also been established by
means of autosomal DNA markers (Bertoni et al., 2003).
In the western US, Hispanics are mainly of Mexican ori-
gin, with an elevated Native-American contribution
(35.6–57.9%), while in the eastern US, Hispanics are
predominantly of Cuban and Puerto-Rican origin, with a
low Native-American component (0–21.3%).
In general, the tripolar diagram is suitable for describ-
ing the genetic composition of Mexican populations;
nevertheless, further comments derive from data already
discussed. First, based on significant genetic differentia-
457
tion we can define two groups of Mexican-Mestizos: the
northern-western and central—the latter represented by
Mexico City—and probably southeastern neighbors. Sec-
ond, preliminary results of paternal African ancestry on
the coasts in three different Mexican states imply seri-
ous limitations concerning the description of a higher
African ancestry along the coastlines, suggesting that
this can only be applied with certainty to particular loca-
tions of the coastal region. Third, the tripolar diagram
displays an insignificant number of genetically pure indi-
viduals in any of the three ancestral components. This
would not be true on considering individuals from rural
communities with high levels of isolation and/or inbreed-
ing, from both well-established Amerindian groups and
indigenous communities, in which Spanish-speaking
individuals could formally be classified as Mestizos. The
results of Bonilla et al. (2005) suggest that this could be
frequent in rural populations from the southeastern
region. Consequently, Native-American ancestry in the
tripolar diagram should be broader, considering that it
would have a higher proportion of genetically pure
Amerindian individuals as compared with Africans and
Europeans. Fourth, socioeconomic-related genetic-intra-
population structure should be clarified for the majority
of Mexican cities for it to be included in final considera-
tion in future models. Fifth, at least for Mexican-Mesti-
zos is well-known a high gene flow by migration
throughout the country; therefore, instead of geographi-
cal limits, genetic differentiation by clines would be
expected among Mexican populations. Finally, to eluci-
date these genetic structures throughout Mexican popu-
lations, a deeper genetic analysis (including AIMs,
mtDNA, and Y-linked markers) is required of other Mex-
ican-Mestizo populations, especially of those from large
urban cities from the Mexican Southeast, as well as
from Amerindian groups, analyzing larger sample sizes.
Paternal nondifferentiation between northern and
western Mexican-Mestizo populations has important and
immediate consequences within the forensic context. To
our knowledge, in Mexico only there are two Y-STR data-
bases including the complete minimum haplotype sug-
gested for male-identification purposes: from Chihuahua
and Mexico City (www.yhrd.org). Our results allow using
the Chihuahua database for forensic casework analysis
in Jalisco, where Guadalajara, the second most impor-
tant Mexican city, is located. Considering that geneti-
cally these comprised a geographical group, this data-
base could be used in nearby states where this informa-
tion does not exist. One problem in applying Y-STR
databases in forensic casework is because of the great
polymorphism of the Y-STRs; thus, in the majority of
cases haplotype frequency estimation is limited by the
database sample size (Butler et al., 2005). Male Y-STR
homogeneity among cited Mexican-Mestizo populations
permits us to put together databases from the same
region, thus improving their haplotype estimates. Simi-
lar homogeneity for Y-STRs and mtDNA has been dem-
onstrated in Hispanic-American populations (excluding
those from Texas, US) (Kayser et al., 2003), concluding
that disease susceptibility within US populations is more
likely to reflect cultural/environmental factors than
underlying genetic heterogeneity. Although in this study
mtDNA was not analyzed, a similar quantity of this
Amerindian ancestry has been reported in western and
northern-central Mexican-Mestizos (82 and 89%, respec-
tively) (Green et al., 2000; Sandoval et al., 2006), alto-
gether this observation and our results suggest a rela-
American Journal of Physical Anthropology
458 H. RANGEL-VILLALOBOS ET AL.
tive homogeneity of both maternal and paternal Native-
American ancestry in Mestizos from Chihuahua and
Jalisco that allow inferring the same conclusion about
disease susceptibility for these Mexican populations. On
the other hand, the genetic heterogeneity attributable to
the Mexican City sample needs further research, includ-
ing different genetic systems (mtDNA, Y-chromosome
and autosomal markers), and additional central and
southeastern Mexican-Mestizo populations, to confirm
and/or precisely define the genetic structure throughout
this country (geographical limits and heterogeneity
levels).
Admixture and genetic relatedness between
Mexican ethnic groups
Previous estimates of European admixture in Mexican
ethnic groups with blood groups and serum protein
markers ranged from 8.8% in Huichols to 37.3% in
Huastecos, whereas in Nahuas the European ancestry
estimate was 29.6% (Lisker et al., 1996). The position of
the Huichols in the lowest admixture range is in agree-
ment with our results because all of these presented
haplogroup Q3. Paternal admixture estimates in Amer-
indians from Mexico revealed nonnative ancestry in
Nahuas and Tarahumaras; the former was the more
admixed group with European (17.6%) and African
ancestry (2.9%), sharing the largest number of haplo-
types with Mestizos (both Q3 and Y*), which represent
gene flow effects with Mestizos. The wide geographic dis-
tribution of Nahuas in 13 of the 31 Mexican states
explains their high admixture, although there may be
differences in admixture proportions among them related
with the respective degree of isolation and acculturation
(Lisker et al., 1996).
In Tarahumaras, detected European admixture (15%;
3/20) was striking considering their geographical and
cultural isolation in the Sierra of Chihuahua (northern
region; Fig. 1), along with a previous report with autoso-
mal DNA markers presenting highest differentiation
with Mexican-Mestizos (Rangel-Villalobos et al., 2000);
thus, we expected a high frequency of Amerindian hap-
logroup Q3. Contrariwise, this group had the lowest fre-
quency of Q3 among Mexican tribes (55%). Nonetheless,
they were clearly differentiated from Mestizos and their
close relationship with Huichols was confirmed, in
agreement with their linguistic affiliation and ethno-
graphic records (Scheffler, 1999). Therefore, the genetic
differentiation of Tarahumaras, as showed by their posi-
tion in the multidimensional scaling (see Fig. 2), could
be explained by their high frequency (29.4%; 5/17) of
Native-American haplotypes Y*, namely Q-P36*, M242,
or RPS4Y (Seieslstad et al., 2003; Zegura et al., 2004).
This peculiarity could be a consequence of their geo-
graphical position at the north-central region of Mexico
in Arid American, and closer to South Na-Dene groups,
regarding Meso-American groups from central and
southeast Mexico. In addition, genetic drift-associated
differentiation could be acting in Tarahumaras, as sug-
gested by their extreme allele frequencies and AMOVA
results indicating Huichols and Tarahumaras as respon-
sible for the significant differentiation among Mexican-
Amerindians. Concurrently, these groups entertain a
similar amount of cultural and geographic isolation in
small communities of the Sierra Madre (but in different
regions), although historical records exist of relation-
American Journal of Physical Anthropology
ships with Mexican-Mestizos, this favoring admixture,
as detected in this study in Tarahumaras (Heras, 1995).
In Purépechas, a previous report with autosomal
markers suggested European admixture based on the
following observations (Rangel-Villalobos et al., 2000): 1)
high gene diversity with regard to other ethnic groups,
2) nonsignificant differentiation and geographic proxim-
ity to western Mexican-Mestizos, facilitating gene flow
between these, 3) Spanish cultural, linguistic, and reli-
gious influence, 4) less geographic isolation, and 5) the
well-described migration of Purépecha males to the US
and large cities in Mexico to work as employees (Schef-
fler, 1999). Accordingly, we anticipated finding nonnative
Y-chromosomes in Purépechas; notwithstanding this and
conversely, all Y-chromosomes were Amerindian. This
paternal evidence of no admixture in Purépechas, in
addition to their high gene diversity (Table 4) and haplo-
type diversity (Table 5; omitting non-Amerindian haplo-
types), could be explained as a result of their political
and cultural predominance in Mesoamerica, especially in
western Mexico, in addition to their Pre-Hispanic multi-
ethnic nature when this was shaped 1,500 years ago
(Argueta-Villamar, 1995; Páez-Riberos et al., 2006).
Respect to the differences between conclusions obtained
with autosomal and Y-linked loci, one possible explana-
tion for reconciling this contrary genetic evidence would
imply a particular admixture process involving mar-
riages between Purépecha males and non-Purépecha
females; thus, Purépecha males leaving their commun-
ities to work in urban cities would mate with non-Puré-
pecha women (presumably Hispanic and Mestizo
women), who later would be incorporated into this com-
munity. This interpretation would be in agreement with
the lesser male migration rate claimed for the Y-chromo-
some, indicating the major female tendency for relocat-
ing at the husband’s place of residence, which has been
documented in two-thirds of human populations (Seies-
tald et al., 1998).
Conversely, in the admixture process of one Latin
American population (Antioquia, Colombia), it has been
claimed that admixture with Spanish men (but not with
native women) has increased the European nuclear
ancestry (Bedoya et al., 2006). These results suggest im-
portant differences in the admixture process of Hispanic
populations and Amerindian tribes. On the other hand,
mtDNA analysis in Purépechas failed to detect European
admixture because their haplogroups were mainly Amer-
indian (98%) (Sandoval et al., 2006). However, although
maternal inheritance did not show admixture in Purépe-
chas, this proposal should not be discarded, given that
Amerindian mtDNA haplogroups are predominant in
Mexican-Mestizos (Green et al., 2000; Sandoval et al.,
2006). The limited Purépecha sample size in both studies
compels a deeper analysis for reconciling this opposite
genetic evidence (autosomal vs. mtDNA/Y-chromosome).
Genetic structure between Mexican
Amerindian tribes
Agricultural development in Mesoamerica had impor-
tant consequences in the cultural and demographical
history of America. At the time of Spanish contact, de-
mographic estimates indicate that Mesoamerica was the
most densely populated area from America with perhaps
25 million people (Cavalli-Sforza et al., 1994). For that
time, important Meso-American civilizations had been
formed and/or destroyed, for instance, the Olmec, Teoti-
 PATERNAL GENETIC STRUCTURE IN MEXICAN POPULATION
huacán, Toltec, Maya, and Aztec civilizations, among
many others, in which complex systems of Chiefdoms
and states were developed, with several and complex
socioeconomic relationships among these (Fiedel, 1992).
On the other hand, populations living in mountains and
canyons, such as the Huichols and Tarahumaras, car-
ried out hunter-gathering activities and seasonal agri-
culture reaching limited population sizes and scarce
relationships with other populations due to their geo-
graphical isolation (Diguet, 1992). Concurrently,
AMOVA tests demonstrated that paternal genetic struc-
ture in Mexican native populations was attributable to
the more isolated Amerindian groups, in this case from
the Western Sierra Madre in northern (Tarahumaras)
and western (Huichols) Mexico. This genetic homogene-
ity among Mexican ethnic groups from Mesoamerica
also inferred in seven populations with five autosomal
markers (Buentello-Malo et al., 2003), probably is the
consequence of their elevated migration rate (Nm),
which was nearly three times greater than previous
estimates from North America (Mexico and US) using Y-
binary loci (Nm 5 8.1) (Bortolini et al., 2002). Together,
these results demonstrate a high gene flow in Mesoa-
merica prior to the Spanish Conquest, creating a trend
toward homogenization of the gene pool among Amerin-
dian populations from this region. Similar results of geo-
graphic structure have been reported in South Amerin-
dians, in which Andean populations (analogous to Meso-
america) presented greater homogeneity than non-
Andean populations located in the eastern part of the
continent, with different genetic-drift and gene-flow pat-
terns (Tarazona-Santos et al., 2001). Within this con-
text, our results support a complex scenario of genetic
differentiation among Amerindians from Mesoamerica,
which does not agree with the IBD model.
CONCLUSIONS
The Y-linked markers analyzed allowed us to estimate
the paternal ancestral components in western Mexican-
Mestizos. A significant genetic heterogeneity was estab-
lished between northern and western Mestizos with
respect to those from Mexico City. These results were
compatible with the tripolar diagram that explains the
genetic composition of the Mexican population, in which
higher European ancestry is suggested in northern and
western Mexican populations in comparison with central
and southeastern populations. However, Y-linked prelim-
inary results have failed to detect higher African ances-
try in coastal regions. On the other hand, genetic homo-
geneity was demonstrated among Mexican ethnic groups
from Mesoamerica, suggesting a high Pre-Hispanic
migration rate in this region. Conversely, genetic hetero-
geneity was attributable to isolated ethnic mountain-
and canyon-dwelling groups of the Sierra Madre, where
genetic differentiation processes were appreciated as
founder effect and/or genetic drift. Although small sam-
ple sizes limit conclusions concerning individual Mexican
ethnic groups, results pointed to Nahuas and Huichols
as the most and the least admixed groups, respectively.
Tarahumaras were distinctive because of their high
frequency of Amerindian Y-chromosomes without Q3.
Finally, in Purépechas we suggest a special admixture
process for explaining contrary genetic evidences prefer-
entially involving the integration of non-Purepécha
women into their communities.
459
ACKNOWLEDGMENTS
We thank all volunteers, especially indigenous males,
who participated in this study. We thank to QFB stu-
dents of the Molecular Genetics Laboratory (CUCienega-
UdeG) for technical assistance.
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