AMERICAN JOURNAL OF HUMAN BIOLOGY 00:00–00 (2014)

Original Research Article

Y-Chromosome Analysis in a Northwest Iberian Population: Unraveling the

Impact of Northern African Lineages
LUIS ALVAREZ,1,2* ESTELA CIRIA,1 SOFIA L. MARQUES,2 CRISTINA SANTOS,1 AND MARIA PILAR ALUJA1
1
Unitat Antropologia Biol
ogica, Universitat Aut
onoma de Barcelona, 08193, Bellaterra, Barcelona, Spain
2
IPATIMUP, Institute of Molecular Pathology and Immunology of the University of Porto, 4200-465 Porto, Portugal

Objectives: To provide new clues about the genetic origin, composition and structure of the population of the Span-
ish province of Zamora, with an emphasis on the genetic impact of the period of Islamic rule in the Iberian Peninsula.
Methods: Polymorphisms in the paternally inherited Y-chromosome, Single Nucleotide Polymorphisms and Short
Tandem Repeats, were analyzed in 235 unrelated males born in six different regions in the Zamora province.
Results: A relatively homogenous Y-chromosome haplogroup composition was observed in the Zamora province.
Haplogroups R1b1-P25 and I-M170, widespread in European populations, accounted for 64.9% of the total sample.
Moreover, all of the observed African lineages, accounting for 10.2% of the total variability, belonged to haplogroups
having Northwest African origin (E1b1b1b-M81, E1b1b1a-b-M78, and J1-M267).
Conclusions: No differences between regions or sub-structure due to geographical boundaries were detected. The
specific Northwest African male lineages observed contrast with the mitochondrial DNA data, where the majority of
African lineages were found to be sub-Saharan. This work made it possible to study the impact of recent historical
events in the male gene pool in the province of Zamora in Spain. Am. J. Hum. Biol. 00:000–000, 2014. C 2014 Wiley Peri-
V

odicals, Inc.

Research into the genetic diversity in European popula-
tions has mainly been focused on the interpretation of large-
scale variation patterns in light of prehistoric demographic
events [for a review, see Soares et al. (2010)]. Besides this
approach, the analysis of the impact of recent historical
events on the current genetic landscape of human popula-
tions, examined from a microgeographic perspective, has
gained relevance in the last decade [for a review, see Jobling
(2012)]. Genetic studies in Iberians have not been oblivious
to such perspectives, for example, the analysis of popula-
tions located in the northwestern quadrant of the Iberian
Peninsula, and have revealed interesting traits from an
anthropological and forensic point of view (Beleza et al.,
2006; Larruga et al., 2001; Mairal et al., 2013; Nogueiro
et al., 2010; Pardinas et al., 2012; Teixeira et al., 2011).
A study in this specific area of the Iberian Peninsula
(Alvarez et al., 2010) that centered on the analysis of the
mitochondrial DNA diversity pattern of the Spanish prov-
ince of Zamora (Fig. 1), found a high frequency of African
maternal lineages. Although the presence of African line-
ages in Iberia represent, per se, one of the peculiarities of
Iberians compared with other Europeans [for a review,
see Arroyo-Pardo et al. (2007)], those values reported for
the Zamora province population are one of the highest
reported so far in Iberia (Cerezo et al., 2012). Another
remarkable finding was the high frequency and diversity
of Middle Eastern lineages in this population.
The reconciliation of historical and genetic data to
explain such results points to a 300 year period, spanning
from the middle of the 8th century to the 11th century,
when there was Islamic rule in the area. The unstable
political/social situation of the Iberian Peninsula at that
time critically influenced the demography of the area.
Population movements, accompanied by the southern
expansion/consolidation of the Astur kingdom, affected
the heterogeneity of Zamora province territories, mainly
because of the course of the Duero River, which played an
important role as a defensive corridor (Lopez and San-
tonja, 1995). The lands situated in the northern area were
resettled at the end of the 8th century, but the southern
areas were only definitely part of the Astur kingdom in
the 11th century. In both locations, the origin of the set-
tlers is well known and involved Mozarabs from the
southern Muslim kingdoms, together with people from
Northwestern Iberia and Southern France, the latter only
being referred to in the southern areas of the Duero River
(Lopez and Santonja, 1995).
Populations involved in those resettlement events by
themselves do not explain, alone, the pattern of maternal
lineages found in the Zamora province. In view of wider
assumptions, the presence of Middle Eastern lineages in
Iberia has been commonly attributed to (i) the neolithiza-
tion process; and/or (ii) recent influences of Mediterra-
nean populations (Arroyo-Pardo et al., 2007), including
This article was published online on 14 August 2014. An error was sub-
sequently identified. This notice is included in the online version to indi-
cate that have been corrected 22 August 2014.
Contract grant sponsor: Ministerio Espa~ nol de Ciencia e Innovaci
on;
Contract grant number: CGL2006-07374; Contract grant sponsor: Gener-
alitat de Catalunya; Contract grant number: SGR 2014-1420.; Contract
grant sponsor: Fundaç~ao para a Ci^ encia e a Tecnologia; financed by the
European Social Funds (COMPETE-FEDER); Contract grant number:
PTDC/ATP-DEM/4545/2012 (to S.L.M.); Contract grant sponsor: FCT fel-
lowship, funded by POPH-QREN – Promotion of scientific employment,
supported by the European Social Fund and national funds of the Ministry
of Education and Science; Contract grant number: SFRH/BPD/65000/2009
(to L.A.).
*Correspondence to: Luis Alvarez, IPATIMUP, Institute of Molecular
Pathology and Immunology of the University of Porto, Rua Dr. Roberto
Frias s/n, 4200-465 Porto, Portugal. E-mail: lfernandez@ipatimup.pt
Additional Supporting Information may be found in the online version
of this article
Received 3 October 2013; Revision received 3 June 2014; Accepted 15
June 2014
DOI: 10.1002/ajhb.22602
Published online 00 Month 2014 in Wiley Online Library
(wileyonlinelibrary.com).

C 2014 Wiley Periodicals, Inc.

V
2 L. ALVAREZ ET AL.
Fig. 1. Provincial administrative level in Spain highlighting the geographical location of the Zamora Province (white color); miniature show-
ing regional subdivision of the Zamora Province, codes as follows: Aliste (AL), Bajo Duero (BD), Benavente (BV), Campos-Pan (CP), Sanabria
(SN), and Sayago (SY).
Sephardic Jews (Teixeira et al., 2011). In parallel, several
arguments have been used to explain the presence of Afri-
can lineages in this region. These include (i) prehistoric
links (Cerezo et al., 2012; Izagirre et al., 2005); (ii) inter-
breeding between Christians and Muslims (females) in
Iberia during the 7th–15th century (Pereira et al., 2005);
(iii) the relocation of moriscos (converted Muslims) at the
end of the 16th century (Adams et al., 2008); and/or iv)
the African slave trade during the 16th–19th centuries
(Comissao Nacional para as Comemoraçoes dos Descobri-
mentos Portugueses, 1999).
To test these scenarios, we use paternally inherited Y-
chromosome polymorphisms (Single Nucleotide
Polymorphisms-SNPs and Sort Tandem Repeats-STRs) to
provide new clues of the genetic origin, composition, and
structure of the Zamora province in the Western Euro-
pean context. Moreover, the same strategy adopted by
Alvarez et al. (2010) dividing the territory into six regions
(see miniature in Fig. 1), is followed to determine the
genetic microdifferentiation.
MATERIAL AND METHODS
Sampling strategy and DNA isolation
Blood samples were taken from 235 unrelated males
born in the Zamora province after obtaining their
informed consent. In all cases, a confidentiality question-
American Journal of Human Biology
naire was completed to obtain, whenever possible, perso-
nal data up to the third ancestral generation. The ethics
committees of the Universitat Autonoma de Barcelona
(UAB) and the Specialized Attention Board at the Health-
care Complex of Zamora, authorized by its Medical Direc-
tor, approved this study and the written informed
consent. The regional distribution of each sample was
defined taking into account the birthplace of the grandfa-
ther, resulting in: 36 samples from Aliste (AL), 31 from
Bajo Duero (BD), 43 from Benavente (BV), 50 from
Campos-Pan (CP), 47 from Sanabria (SN), and 28 from
Sayago (SY).
Total DNA isolation from whole blood was performed
using Jetquick Blood DNA Spin Kit (Genomed) according
to the manufacturersrecommendations.
Y-SNP genotyping
Thirty-three previously published SNP of the Male-
Specific portion of the Y-chromosome (MSY) were analyzed
in order to define major lineages. Twenty-two markers
(12f2a, LLy22g, M2, M9, M20, M52, M74, M78, M81, M94,
M123, M170, M173, M201, M207, M213, M215, M223,
M253, 12f2a, SYR4064, and YAP) were typed as previously
described by Alvarez et al. (2009). The remaining eleven
markers (M92, M102, M166, M172, M267, P15, P16, M153,
P25, SRY10831.2, and SRY2627) were typed in a multiplex
 Y-CHROMOSOME VARIATION IN NORTHWEST IBERIA 3

assay by MassARRAYTM (Sequenom) technology at the

46.4 (29.4-64.3)
frequencies, with the Bayesian 0.95 credible region, for the Zamora province (ZA) and the considered regions (codes as in Fig. 1), are showed. Abbreviations: N, sample size; Ĥ, Neis diversity
TABLE 1. Phylogenetic tree based on 33 Y-SNPs (LLY22g, M2, M20, M52, M92, M166, M281, P15 and P16 polymorphisms were found in ancestral state in all samples) Relative haplogroup

10.7 (3.9-27.4)

17.9 (8.0-35.8)

10.7 (3.9-27.4)

0.749 6 0.070
7.1 (2.2-22.8)

3.6 (0.8-17.8)

3.6 (0.8-17.8)
0.0 (0.1-11.9)
0.0 (0.1-11.9)

0.0 (0.1-11.9)
0.0 (0.1-11.9)

0.0 (0.1-11.9)

0.0 (0.1-11.9)
0.0 (0.1-11.9)

0.0 (0.1-11.9)
0.0 (0.1-11.9)
0.0 (0.1-11.9)

0.0 (0.1-11.9)
0.0 (0.1-11.9)
SY (N 5 28) Spanish National Genotyping Centre (CeGen).
The classification of samples into haplogroups was
made using the phylogeny proposed by Karafet et al.
(2008).

Y-STR genotyping
Sixteen Y-STR markers (DYS456, DYS389I, DYS390,

51.1 (37.2-64.8)

0.724 6 0.066
8.5 (3.5-20.0)
6.4 (2.3-17.2)
4.3 (1.3-14.3)
6.4 (2.3-17.2)
4.3 (1.3-14.3)

4.3 (1.3-14.3)

4.3 (1.3-14.3)
8.5 (3.5-20.0)

2.1 (0.5-11.1)
SN (N 5 47)

0.0 (0.1-7.4)

0.0 (0.1-7.4)

0.0 (0.1-7.4)
0.0 (0.1-7.4)
0.0 (0.1-7.4)
0.0 (0.1-7.4)
0.0 (0.1-7.4)

0.0 (0.1-7.4)
0.0 (0.1-7.4)
DYS389II, DYS458, DYS19, DYS385, DYS393, DYS391,
DYS439, DYS635, DYS392, Y GATA H4, DYS437,
DYS438, and DYS448) corresponding to 17 loci, as
DYS385 includes two locus, were coamplified with the
AmpFlSTRVY-filerTM kit (AB Applied Biosystems, Foster
R

City, CA) using the manufacturers’ recommendations.

The STR profiles were obtained on an ABI 3130XL
60.0 (46.1-72.4)

0.635 6 0.077
8.0 (3.3-18.9)
6.0 (2.2-16.2)

4.0 (1.2-13.5)

4.0 (1.2-13.5)
4.0 (1.2-13.5)
2.0 (0.5-10.4)
2.0 (0.5-10.4)

2.0 (0.5-10.4)
2.0 (0.5-10.4)
2.0 (0.5-10.4)

2.0 (0.5-10.4)
2.0 (0.5-10.4)
Genetic Analyzer using GeneMapperV R Software (Applied
CP (N 5 50)

0.0 (0.0-7.0)

0.0 (0.0-7.0)

0.0 (0.0-7.0)

0.0 (0.0-7.0)
0.0 (0.0-7.0)

0.0 (0.0-7.0)

Biosystems) in the Servei de Genomica, Universitat

Autonoma de Barcelona. Genotyping of samples was per-
formed by comparisons with sequenced ladders included
in the kit and GeneScanTM 500 LIZTM Size Standard
(Applied Biosystems).
The locus nomenclature and allele designation were
performed according to the ISFG guidelines (Gusmao
65.1 (50.1-77.6)

0.574 6 0.089
2.3 (0.6-12.0)
4.7 (1.4-15.5)

4.7 (1.4-15.5)
4.7 (1.4-15.5)

4.7 (1.4-15.5)
7.0 (2.5-18.7)

2.3 (0.6-12.0)
2.3 (0.6-12.0)

2.3 (0.6-12.0)
BV (N 5 43)

0.0 (0.1-8.0)
0.0 (0.1-8.0)
0.0 (0.1-8.0)

0.0 (0.1-8.0)

0.0 (0.1-8.0)
0.0 (0.1-8.0)
0.0 (0.1-8.0)
0.0 (0.1-8.0)

0.0 (0.1-8.0)

et al., 2006; Mulero et al., 2006).

Comparative dataset
The comparative analysis was performed using avail-
able data of 1212 North Africans [238 from Libya (Ottoni
et al., 2011); 102 from Algeria (Robino et al., 2008); 225
from Tunisia (Fadhlaoui-Zid et al., 2011; Frigi et al.,
61.3 (43.7-76.3)
12.9 (5.3-29.0)

0.615 6 0.096
3.2 (0.8-16.2)

3.2 (0.8-16.2)
6.5 (0.2-20.8)
6.5 (0.2-20.8)

3.2 (0.8-16.2)

3.2 (0.8-16.2)
BD (N 5 31)

0.0 (0.1-8.9)
0.0 (0.1-8.9)
0.0 (0.1-8.9)
0.0 (0.1-8.9)

0.0 (0.1-8.9)

0.0 (0.1-8.9)
0.0 (0.1-8.9)
0.0 (0.1-8.9)

0.0 (0.1-8.9)

0.0 (0.1-8.9)
0.0 (0.1-8.9)

2006); and 647 from Morocco (Aboukhalid et al., 2010;

estimator

Alvarez et al., 2009; Gaibar et al., 2011; Laouina et al.,

2011; Palet et al., 2010)], summarized in Supporting Infor-
mation Table 1.

Data analysis
The haplogroup and haplotype frequencies were esti-
41.7 (27.1-57.9)
11.1 (4.5-25.4)

0.811 6 0.060
2.8 (0.7-14.2)
2.8 (0.7-14.2)
8.3 (3.0-21.9)
2.8 (0.7-14.2)
8.3 (3.0-21.9)
2.8 (0.7-14.2)

5.6 (1.7-18.2)

5.6 (1.7-18.2)
2.8 (0.7-14.2)

2.8 (0.7-14.2)

2.8 (0.7-14.2)
AL (N 5 36)

0.0 (0.1-9.5)
0.0 (0.1-9.5)

0.0 (0.1-9.5)

0.0 (0.1-9.5)

0.0 (0.1-9.5)

0.0 (0.1-9.5)

mated by direct counting, and the Bayesian 0.95 credible

regions (95% CR) for the haplogroup distribution were cal-
culated, using a Bayesian approach for binomial sam-
pling, by means of SAMPLING software (Macaulay,
personal communication).
The complete haplogroup composition was used to esti-
mate (i) Nei’s gene diversity (Nei, 1987); (ii) possible dif-
54.9 (48.5-61.1)

0.684 6 0.033

ferences at a regional level using the exact test of

ZA (N 5 235)

4.7 (2.7-8.2)
5.5 (3.3-9.2)
2.6 (1.2-5.5)
1.7 (0.7-4.3)
5.1 (3.0-8.7)
1.3 (0.5-3.7)
4.3 (2.3-7.7)
2.6 (1.2-5.5)
4.7 (2.7-8.2)
5.5 (3.3-9.2)
0.4 (0.1-2.3)
0.9 (0.3-3.0)
1.3 (0.5-3.7)
0.4 (0.1-2.3)
1.7 (0.7-4.3)
0.9 (0.3-3.0)

0.9 (0.3-3.0)
0.9 (0.3-3.0)

population differentiation (Raymond and Rousset, 1995);

and (iii) the effect of geographical boundaries on regional
populations (eastern vs. western; north vs. south; and
regions divided by the main rivers) using AMOVA analy-
sis (Excoffier et al., 1992), with ARLEQUIN 3.5.1.2 soft-
ware (Excoffier and Lischer, 2010). Complementarily, the
AMOVA analysis, using Slatkin’s linearized FST pairwise
genetic distance (Slatkin, 1995), was further applied to
detect possible geographical substructure based on
regional Y-STRs haplotype information
Haplogroups E1b1b1b-M81, E1b1b1a-b-M78 (showing
allele 10 in DYS439 locus) and a subset of J1-M267, that
account for the majority of the variation present in North-
western African populations, have been considered
markers of the contribution of the Islamic rule period to
the Southern European populations (Cruciani et al., 2004;
Francalacci and Sanna, 2008; Semino et al., 2004). Fol-
lowing the criteria adopted by Capelli et al. (2009), the
posterior distribution of the Time to the Most Recent

American Journal of Human Biology

4 L. ALVAREZ ET AL.

TABLE 2. Estimated probabilities for the each country, ethnic/linguistic group and population considered in the matching analysis and the cor-
responding standard deviations (SD)

Country Ethnic/Language Population Sample Size E1b1b (%) Probability (SD)

Libya
Cosmopolitan 238 64 (26.9) 9.0 (8.3)
Benghazi ” ” 4.8 (6.2)
Tunisia
Berbers 160 125 (78.1) 14.7 (10.2)
Sejenane 47 24 (51.1) 3.8 (5.5)
Takrouna 19 19(100) 9.7 (8.5)
Chenini-Douiret 27 27 (100) 1.3 (3.3)
Jradou 32 32 (100) 10.2 (8.7)
Sened 35 23 (65.7) 5.7 (6.7)
Adalusians 32 14 (43.8) 10.5 (8.8)
Zaghouan ” ” 5.8 (6.7)
Arabs 33 22 (66.7) 13.6 (9.9)
Tunis ” ” 7.3 (7.5)
Algeria
Arabs 102 52 (51.0) 11.2 (9.1)
Oran ” ” 5.7 (6.7)
Marocco
Berbers 190 108 (56.8) 11.6 (9.2)
Rabat 69 34 (49.3) 6.2 (7.0)
Figuig Oasis 52 17 (32.7) 4.2 (5.8)
Khenifra 36 26 (72.2) 5.1 (6.4)
Azgour Valley 33 31 (93.9) 6.0 (6.9)
Arabs 223 105 (47.1) 10.3 (8.8)
Rabat 130 61 (46.9) 6.5 (7.1)
Figuig Oasis 44 8 (18.2) 6.2 (7.0)
El Jadida 49 36 (73.5) 1.2 (3.1)
Sahrawi 68 37 (54.4) 10.8 (9.0)
Rabat ” ” 6.1 (6.9)
Cosmopolitan 166 91 (54.8) 8.4 (8.0)
Casablanca ” ” 4.2 (5.8)

Common Ancestor (TMRCA) for any pair of haplotypes
differing at k loci, was calculated for these specific hap-
logroups, using the Infinite Alleles Model (IAM) approach
implemented by Walsh (2001). This model is considered a
reasonable approximation of when individuals match at
most markers, and therefore, few mutations are expected
to occur as in the short temporal framework considered
here (1.3ky) (Capelli et al., 2009; Walsh, 2001). Consider-
ing 16 Y-STR markers (17 loci) with an overall mutation
rate of 2.458 3 1023 estimated over 192,000 meiosis,
data available in the YHRD database (Willuweit et al.,
2007), in a temporal framework of 1300 years (the year
711 marks the beginning of the Islamic rule period in Ibe-
ria), encompassing 42 generations [31-year generation
length according to Helgason et al. (2003)].
In this scenario, 0, 1, 2 or 3 mutational differences are
the most likely consequence (Supporting Information
Fig. 1 and Supporting Information Table 2). Therefore,
the Zamora province Y-chromosomes belonging to the con-
sidered haplogroups (E1b1b1b-M81, E1b1b1a-b-M78, and
J1-M267) identical, with one, two or three mutational dif-
ferences from the Northwest African STR haplotypes,
were considered compatible with an Islamic rule period
ancestry.
Several Northwest African populations were evaluated
as the possible source of the Islamic rule period ancestry
of the Zamora province. A dataset combining geographical
and cultural information was compiled for this purpose.
The probability of origin at each population and its stand-
ard deviation was calculated as defined by Mendizabal
et al. (2008). Match haplotypes considered in the analysis
were defined in a two-step process: (1) haplotypes of the
dataset with 0, 1, 2, or 3 mutational differences to the
Zamora province ones; and (2) haplotypes inside each
dataset subpopulation with 0, 1, 2, or 3 mutational differ-
ences to the ones selected in the first-step. Therefore, the
profiles selected in the first step were considered as the
central/ancestral population from which, in the temporal
framework analyzed, both the Zamora and the remaining
dataset subpopulation have equal probability to be their
descendants.
The dataset included 1212 North African samples (Sup-
porting Information Table 1) for which the same 17 STRs
loci analyzed in this study were genotyped. Within the
selected North African populations, the haplogroup classi-
fication, if not available, was inferred from the Y-STR hap-
lotypes using the web-accessible program Whit Atheys’
Haplogroup Predictor (www.hprg.com/hapest5/), based on
a Bayesian allele frequency approach. Complementarily
the DYS458.2 allele was used to determine the J1 chromo-
somes (Myres et al., 2007). With the aim of confirming the
efficiency of the method, a prediction test was performed
using all the samples for which both STRs and SNPs were
available. As a result, a total of 93.2% of correct assign-
ments were obtained for the general data, and 94.8% for
data regarding the E1b1b haplogroup (Supporting Infor-
mation Table 1).
RESULTS AND DISCUSSION
The analysis of the 17 Y-STR loci discriminated 219
haplotypes (Supporting Information Table 3) in the 235
analyzed Y-chromosomes. Moreover, according to the 33
genotyped SNPs, samples were classified into 19 different
haplogroups and subhaplogroups, amongst the possible
34 (Table 1). The four main branches, E*-M215, I*-M170,
J*-12f2a, and R1*-M173, had higher frequencies (8%),
accounting together for up to 91.8% of the detected

American Journal of Human Biology

 Y-CHROMOSOME VARIATION IN NORTHWEST IBERIA
variability (15 of the 19 detected clusters), with R1*-M173
being the most frequent (59.3%) by far. The haplogroup
frequency values obtained for the different regions
showed a relative homogeneity with overlapping Bayesian
0.95 credible regions (Table 1).
Diversity values and substructure analysis
Diversity values based on haplogroup frequencies (Ĥ) in
the analyzed chromosomes are listed in Table 1. The
Zamora province population (0.684) is in the same range
as other populations of the same geographic area, for
example, 0.638 and 0.620 in the Spanish regions of Galicia
and Northwest Castile, respectively (Adams et al., 2008),
and 0.642 in North Portugal (Beleza et al., 2006). In gen-
eral, lower values correspond to those populations located
in the northeastern quadrant, whereas those located in
the north to southwestern portion had higher values.
The observed pattern in the Iberian Peninsula was also
observed at the Zamora regional level (Table 1). Higher
diversity (Ĥ) values are present in the western regions
(highest in AL: 0.811 6 0.060) and lower values in the
eastern ones (lowest in BV: 0.574 6 0.089), the latter
being in the same range as the populations located in the
northeastern quadrant of Iberia.
The haplogroup distribution of the different regions
was tested to further investigate the underlying substruc-
ture of the province. First, the exact test of population dif-
ferentiation (Raymond and Rousset, 1995) only showed
statistically significant differences between SY and the
eastern regions of BD and BV (P 5 0.029 and P 5 0.024),
but no differences were observed when the Bonferroni cor-
rection for multiple testing was applied. On the contrary,
the AMOVA analysis (Excoffier et al., 1992) at both hap-
logroup and haplotypes (Y-STRs) levels showed no signifi-
cance when taking the Province as a whole (FST 5 0.015,
P 5 0.127 and FST 5 0.011, P 5 0.056, respectively) or
when any possible geographical boundaries were tested,
for example, eastern vs. western (FCT 5 0.017, P 5 0.097
and FCT 5 0.029, P 5 0.096, respectively).
Phylogeographic analysis
Almost all the Y-chromosomes classified into the wide-
spread R haplogroup in European populations belong to
the R1*-M173 subclade, being more frequently found for
the Western European populations (Capelli et al., 2006;
Cruciani et al., 2002; Rosser et al., 2000; Semino et al.,
2000), as well as in the Iberian populations (Adams et al.,
2008; Alonso et al., 2005; Alvarez et al., 2009; Beleza
et al., 2006; Bosch et al., 2001; Brion et al., 2004; Flores
et al., 2004; Goncalves et al., 2005; Pardinas et al., 2012),
analyzed so far.
The R1*-M173 frequency detected in the Zamora prov-
ince (59.3%) is in accordance with values previously
observed in populations from adjacent geographical areas:
Portuguese districts of Bragança (64%), Guarda (59.9%),
and Vila Real (64.1%) (Beleza et al., 2006); and the Span-
ish areas of Galicia (57%), Northwest Castile (62%)
(Adams et al., 2008), and Asturias (61.9%) (Pardinas
et al., 2012).
The I*-M170 haplogroup is also widespread in Euro-
pean populations, and its distribution and posterior
expansion and spread reflects its origin before the last gla-
ciation (Rootsi et al., 2004; Semino et al., 2000). In the
analyzed Y-chromosomes of the Zamora province popula-
5
tion, the observed overall value of 8.2% is in the same
range as those values previously described in several Ibe-
rian populations, for example, 6% (Adams et al., 2008),
and 7.5% (Alonso et al., 2005).
Haplogroups J, G, and K
The J-12f2 haplogroup distribution over the European
continent points out a Middle East origin associated with
the Neolithization process (Semino et al., 2004), with its
higher frequencies found in the Jewish and non-Jewish
population from Turkey (Behar et al., 2004; Hammer
et al., 2000). Its presence in Iberia can be also assigned to
the presence of Jews and Arab introgressions in historical
times (as the J1-M267 subclade, previously described).
In the analyzed Y-chromosomes, this haplogroup
accounts for up to the 11.5% of the variability detected in
the Zamora province, a value similar to that previously
reported for the Iberian populations (10%) (Adams et al.,
2008; Alonso et al., 2005).
The J-12f2 haplogroup together with the G-M201 and
K*-M9(xP*-M74) have been detected in high frequencies
(69%) in Sephardic Jewish populations (Adams et al.,
2008) and in a Northeastern Portuguese Crypto-Jewish
community (30.3%) (Nogueiro et al., 2010), with hap-
logroup J-12f2 being the most prevalent (47.0% and
36.8%, respectively). However, the value observed in the
Zamora province population (17.9%) is in the same range
as the values previously detected for the neighboring pop-
ulations of Northwest Castile (16%) in Spain (Adams
et al., 2008) and Tras-os-Montes (18%) in Portugal (Beleza
et al., 2006).
African lineages
The presence of African lineages in the Zamora prov-
ince population was described by Alvarez et al. (2010),
where mtDNA haplogroups L1b, L2b, L3b, M1, and
U6a1a accounted for 5.7% of the total haplogroup compo-
sition. The majority of these African lineages (80.2%) cor-
responded to specific sub-Saharan haplogroups (L1b, L2b,
and L3b). In this sense, the high sub-Saharan hap-
logroups frequency in the southern regions of the Zamora
province, 18.2% in Sayago, and 8.1% in Bajo Duero
reported therein, have no parallels with any other ana-
lyzed areas in Iberia, with the exception of Southern Por-
tugal, where two municipalities showed particular high
values, 22% in Alcacer do Sal and 8.7% in Coruche (Cer-
ezo et al., 2012; Pereira et al., 2005; Pereira et al., 2010).
In contrast to the mtDNA results, no specific sub-
Saharan haplogroups were found in the analyzed
Y-chromosomes of the Zamora province population.
Regarding the North African ancestry, a specific set of
Northwest African haplogroups have been described as
markers of the Islamic rule period contribution to South-
ern European populations, E1b1b1b-M81, E1b1b1a-b-
M78 (showing allele 10 in DYS439 locus), and a subset of
J1-M267 (Capelli et al., 2009; Cruciani et al., 2004; Fran-
calacci and Sanna, 2008; Semino et al., 2004). In the
Zamora province, these haplogroups altogether account
for 10.2% of the variation (5.5% for E1b1b1b-M81; 0% for
E1b1b1a-b-M78—showing allele 10 in DYS439 locus—
and 4.7% for J1-M267).
All 12 haplotypes corresponding to 13 individuals inside
the E1b1b1b-M81 haplogroup and none of the nine J1-
M267 match the criteria for an ancestry compatible with
American Journal of Human Biology
6 L. ALVAREZ ET AL.
the Islamic rule period in Iberia (Supporting Information
Table 4). The values obtained for the three markers (5.5%
for E1b1b1b-M81; 0% for E1b1b1a-b-M78, and 0% for J1-
M267) are in the same range as those reported by Capelli
et al. (2009) for 717 individuals in Spain (5.2%, 1.0%, and
1.5%, respectively) using nine STR loci.
In an attempt to assign the origin of the selected Islamic
rule period ancestry haplotypes found in the Zamora prov-
ince to a specific country, ethnic/linguistic group, and popu-
lation in North-West Africa, we focused on the haplogroup
E1b1b1b-M81 inferred probabilities listed in Table 2. This
haplogroup is common in the Northern African popula-
tions, associated with the Imazighen ethnic group, with
frequencies of around 80% (Alvarez et al., 2009; Bosch
et al., 2001; Cruciani et al., 2004; Cruciani et al., 2002).
The country/ethnic group showing a higher probability of
being the source of Northwestern African haplotypes found
in the Zamora province population were Tunisian Berbers
(14.7%), followed by Tunisian Arabs (13.6%), and Moroccan
Berbers (11.6%), while the rest of the countries/ethnic
groups considered, taken together, accounted for 60.1% of
the probability. When the analysis was performed at popu-
lation level, probabilities were scattered among several Ber-
ber populations from Tunis and Morocco. The results
indicated the Tunisian Berbers from Jradou (10.2%) and
the Tunisian Berbers from Takrouna (9.7%) as the most
probable candidates to be the source of the Northwestern
African haplotypes compatible with an Islamic rule period
ancestry found in the Zamora province population.
Overall, this work has made it possible to study of the
impact of recent historical events on the male gene pool of
Zamora province, with an emphasis on the contribution
resulting from the Islamic rule period in the Iberian Pen-
insula that altered the genetic composition of the region.
Considering the markers of such contribution, both
E1b1b1b-M81 and J1-M267 chromosomes were identified,
although only the first ones were found with an ancestry
compatible with the Islamic rule period in Iberia. The dif-
ferent behavior of E1b1b1b-M81 and J1-M267 chromo-
somes can be explain by the complex history of the former
clade showing different genetic backgrounds in Eurasian
and Arabic populations, according to Tofanelli et al.
(2009). In contrast, the E1b1b1b-M81 clade, as previously
stated, is almost restricted to Northern African popula-
tions matching the present area of distribution of the Ima-
zighen ethnic group. These results support the entrance
of Northern African Y-chromosomes in recent times, in
contrast with pre-historical events.
The interbreeding between Christians and Muslims in
this period occurred in an imbalanced way, involving mainly
Christian males, due to cultural constrictions (Pereira et al.,
2005). Therefore, the relocation of moriscos in the northern
and western parts of Spain, at the end of the 16th century,
after the Revolt of Las Alpujarra, had been hypothesized to
be the explanation for the irregular distribution of the North
African ancestry proportions in Iberia, based on the pres-
ence of the E1b1b1b-M81 haplogroup (Adams et al., 2008).
In this context, the presence of three different groups of
moriscos, settled in the Zamora province territory preceding
their final expulsion in the beginning of the 17th century,
has been described: (i) descendants of those mudejares bap-
tized in 1502; (ii) moriscos from Granada, deported in 1570;
and (iii) moriscos linked to domestic service (Martin, 2003).
Clearly, these groups have left a mark on the current gene
pool of the Province. It may have been that the expulsion,
American Journal of Human Biology
unlike in other parts of the Peninsula, was not carried out
as forcefully.
ACKNOWLEDGMENT
The authors are very grateful to sample donors and all
the workers of regional health centers of the Zamora prov-
ince for their selfless support in the sampling process.
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