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"The Sahel, which extends from the Atlantic to the Red Sea coast of Sudan
and Eritrea and the Ethiopian highlands including fringes of the Sahara,
has witnessed human population demographic events that were pivotal in
prehistoric and historic periods of human history. Early occupation by *Homo
sapiens* of the Red Sea coast of Eritrea, and evidences of traces of
earlier urban settlements in much of Eritrea are some of the archaeological
and paleontological evidences that suggest a major contribution of this
area to prehistory and migration including the exodus of anatomically
modern humans to Eurasia"
http://www.nature.com/ejhg/journal/vaop/ncurrent/full/ejhg201441a.html#bib9
Article
European Journal of Human Genetics advance online publication 26 March
2014; doi: 10.1038/ejhg.2014.41
Y-chromosome E haplogroups: their distribution and implication to the
origin of Afro-Asiatic languages and pastoralism
EJHGOpen
Eyoab I Gebremeskel1,2 and Muntaser E Ibrahim1
1Department of Molecular Biology, Institute of Endemic Diseases, University
of Khartoum, Khartoum, Sudan
2Department of Biology, Eritrea Institute of Technology, Mai-Nefhi, Eritrea
Correspondence: Professor ME Ibrahim, Department of Molecular Biology,
Institute of Endemic Diseases, University of Khartoum, PO Box 102, Qasser
Street, Khartoum 11111, Sudan. Tel: +249 912576418; Fax: +249 9183793263;
E-mail: mibrahim_at_iend.org
Received 27 June 2013; Revised 11 February 2014; Accepted 13 February 2014
Advance online publication 26 March 2014
Most Y-chromosome haplogroup diversity in Africa, however, is present
within macrohaplogroup E that seem to have appeared 21 000–32 000 YBP
somewhere between the Red Sea and Lake Chad. The combined analysis of 17
bi-allelic markers in 1214 Y chromosomes together with cultural background
of 49 populations displayed in various metrics: network, multidimensional
scaling, principal component analysis and neighbor-joining plots, indicate
a major contribution of East African populations to the foundation of the
macrohaplogroup, suggesting a diversification that predates the appearance
of some cultural traits and the subsequent expansion that is more
associated with the cultural and linguistic diversity witnessed today. The
proto-Afro-Asiatic group carrying the E-P2 mutation may have appeared at
this point in time and subsequently gave rise to the different major
population groups including current speakers of the Afro-Asiatic languages
and pastoralist populations.Top of page
Introduction
Polymorphisms like bi-allelic mutations associated with the male-specific Y
(MSY) chromosome portion, are important tools that proved essential in
addressing aspects of human ancestry, migration episodes1 and testing
coalescence processes.2 Interestingly, some bi-allelic markers of the Y
chromosome not only have geographically defined distributions, but are also
associated with certain facets of human culture like languages3, 4 and
practice of pastoralism5 all of which contribute to the phenomenon of
genetic drift, probably the most single key element in shaping population
genetic structures.6 Intuitively, the high correlation between geographical
distribution of some of the major E haplogroups and distribution of
Afro-Asiatic languages, exemplary of established correlation between
languages and genes as proposed by Cavalli-Sforza7, 8 prompted us to
revisit such correlation in a multidisciplinary platform better suited to
unravel hitherto untold chapters of human history. No better venue to put
such approach into practice than the area of the Sahel and East Africa. The
Sahel, which extends from the Atlantic to the Red Sea coast of Sudan and
Eritrea and the Ethiopian highlands including fringes of the Sahara, has
witnessed human population demographic events that were pivotal in
prehistoric and historic periods of human history. Early occupation by Homo
sapiens of the Red Sea coast of Eritrea,9, 10, 11, 12, 13 and evidences of
traces of earlier urban settlements in much of Eritrea14, 15, 16 are some
of the archaeological and paleontological evidences that suggest a major
contribution of this area to prehistory and migration including the exodus
of anatomically modern humans to Eurasia. Furthermore, in addition to the
area being strikingly rich in genetic and linguistic diversity, it is one
of the few remaining enclaves of traditional pastoralism, a dying human
culture.17 Although suggestions has been made that East Africa is the
likely place of origin of Y-chromosome haplogroups including the major E
haplogroups, yet key questions on human origin and dispersal remain not
fully addressed. One query, however, is whether the major macrohaplogroup E
present almost in all continents and with particularly high frequency in
East and North Africa in plethora of ancestral lineages, because of gene
flow or an original early event of in situ evolution. Although a lot has
been done to refine the E macrohaplogroup tree, sampling representative
populations, like Eritreans, may still shed light on new dimensions of the
history of populations bearing these mutations. Despite a single attempt to
study Eritrean populations from the diaspora,18 no systematic analysis has
been done so far to address the genetic diversity of extant Eritrean
populations pertinent to questions like the origin of the Afro-Asiatic
languages and pastoralism in light of the distribution of E macrohaplogroup
as a case study.
Top of page
Materials and methods
Y-chromosome genotyping of bi-allelic markers
A total of 1214 Y chromosomes, positive for E haplogroups, were considered
in the analysis. Out of an original sample of Eritrean males screened, 39 Y
chromosomes (49%) turned to be positive for E markers and were included in
the analysis. The language affiliation and present or past history of the
populations analyzed are given in Supplementary Table S1. The culture is
taken within the context of the current linguistic affiliation and
information of past and present subsistence practices. The history of
pastoralism is not restricted to cattle as it has been shown that livestock
may change according to environment as the case with Baggara Arabs who were
originally camel herders turned to cattle. Appropriate informed consent was
obtained from all participants. DNA samples were obtained from buccal
specimen using phosphate-buffered saline and DNA extraction was carried out
according to Miller et al,19 with minor modifications. The bi-allelic
variability at Y-chromosome-specific polymorphisms E-M107, E-M123, E-M148,
E-M191/P86, E-M200, E-M281, E-M329, E-M33, E-M34, E-M54, E-M81, E-P72,
E-U175, E-V19, E-V32, E-V6 (Y Chromosome Consortium (YCC), 2008),20 and E-M
7821 were used to generate MSY chromosome haplotypes. Primers for
genotyping were selected according to Karafet et al20 and Underhill et al22
and the references herewith. Most of the genotyping was done at BGI
Laboratory (Hong Kong, China). Published data of African, Asian and
European populations22, 23, 24, 25, 26, 27, 28, 29, 30, 31, 32, 33, 34 were
used alongside population data from this study for comparative analysis.
Y-chromosome haplogroup tree
The Y-chromosome haplogroup tree has been constructed manually following
YCC 2008 nomenclature20 with some modifications.35 The tree (Supplementary
Figure S1) contains the E haplogroups of Eritrean populations from this
study and those reported in the literature.22, 23, 24, 25, 26, 27, 28, 29,
30, 31, 32, 33, 34 Genotyping results for E-V13, E-V12, E-V22 and E-V32
reported for Eritrean samples and elsewhere23, 27 were retracted to E-M78
haplogroup level. All the analyses in this study were done at the same
resolution using the following 17 bi-allelic markers: E-M96, E-M33, E-P2,
E-M2, E-M58, E-M191, E-M154, E-M329, E-M215, E-M35, E-M78, E-M81, E-M123,
E-M34, E-V6, E-V16/E-M281 and E-M75.
Phylogenetic analysis
Median-joining network (Figure 1) was constructed using Network 4.6.1.1. (
http://www.fluxus-engineering.com) program.36 Effective mutation rate of
3.8–4.4 × 10−4 mutations/nucleotide/generation37 was used in estimating the
divergence time of the populations using Network program.
Figure 1.
Median-joining (MJ) network. Network manipulated to fit the geography of
the extant populations. MJ network was constructed using E haplogroup
frequencies. Group represented by ITAL contains all the Italian samples
pooled. Populations’ descriptions are given in Supplementary Table S1.
Full figure and legend (134K)
A neighbor-joining (NJ) tree (Figure 2) was constructed38 and evolutionary
analysis was conducted using MEGA5 (Tamura et al39).
Figure 2.
NJ tree based on FST values generated from Arlequin 3.11. Population names
are as given in Supplementary Table S1. Population life style: circle –
agriculturalists; square – pastoralists; triangle – nomads; inverted
triangle – nomadic pastoralists; diamond – agro-pastoralists. The
populations are colored according to their language family: red –
Afro-asiatic; blue – Nilo-Saharan; green – Niger-Kordofanian; yellow –
Khoisan; black – Italic and Basque.
Full figure and legend (83K)
Genetic structure and population differentiations
Multi-dimensional scaling (MDS) and principal component analysis (PCA) were
performed by using PAST (paleontological statistics) algorithms version
2.11 software (available online at
http://folk.uio.no/ohammer/past)40 based
on FST values generated from Arlequin ver3.11 program.41 Analysis of
molecular variance (AMOVA) was performed to verify statistical differences
between linguistic and geographic groups. Haplotype frequencies and
molecular differences of Y chromosome among haplogroups were taken into
account. FST values were calculated based on the number of pairwise
differences between Y-chromosome haplogroups. All calculations were
performed using Arlequin version 3.11 (Excoffier et al41) using the 17
bi-allelic data listed above. The correlation among genetic, linguistic and
geographic distances was assessed by the Mantel test using FST matrices
resulted from Arlequin analysis.
Top of page
Results
Y-chromosome haplogroup diversity
Bi-allelic frequencies of E haplogroups for the populations involved in the
analysis are given in Supplementary Figure S1 following the recent
nomenclature.20
Phylogenetic analysis
The network analysis on the chromosomes carrying E haplogroups was robust
enough with a main cluster near the root represented by Kunama (KUN)
encompassing most of Eritreans and Sudanese populations, including
Nilo-Saharan and Afro-Asiatic speakers suggesting that linguistic
divergence is either a subsequent event to population divergence, language
replacement or that the two linguistic families may have shared a common
origin. The Southern African populations, which include the Khoisan and
Bantu of South Africa populations, are shown to be divergent from the East
African larger cluster through its connection to the Somali population. The
network also suggests that dispersal of the haplogroup to Southern Africa
may reflect the spread of pastoralism from North East Africa.5 The Yemeni,
Saudi Arabia and Oman populations on the other hand form a Near Eastern
group. The link between the Yemeni and Omani populations with Afar and Saho
populations from Eritrea could be attributed to the geographical proximity
and possibly past genetic history. The Northern African populations tend to
separate into two distinct groups: one containing Moroccan Arabs and
Berbers and Saharawi, derived from the larger East African group and the
other includes the Northern African populations of Algeria, Egypt and
Tunisia, which forms a connection to both Europeans and Eritrean and
Ethiopians hinting to recent genetic relationship between North and East
African populations as is widely believed.30
The NJ tree, which was not rooted, on the other hand was quite robust in
showing similar grouping to that of the network, MDS and PCA plots to imply
a correlation with language and relevance to geography. With few
exceptions, all populations carrying the haplogroup were either
pastoralists or had recorded history of pastoralism. The populations that
made exceptions, includes Hausa, Fur and Masalit, have strong agricultural
practices, while the latter is thought to have recent history of mixed
farming or foraging. The other exceptions are Copts from Egypt and Tigrigna
from Eritrea, both with documented history of agricultural practices albeit
historically part of larger communities with established pastoralist
practices. The Nilo-Saharan speakers and Niger-Kordofanian were confined to
the cluster from Sudan and Eritrea.
Genetic structure and population differentiation
The MDS and the PCA plots (Figure 3 and Supplementary Figure S2,
respectively) generated from the E haplogroup frequency data portrayed
similar pattern that complement the network result. Generally four main
clusters can be identified from the MDS and PCA plots. In the MDS plot, one
of the main clusters (grey shaded) constitutes almost all Eastern Africans
including most Eritrean and Sudanese populations. The Saho and Afar
populations of Eritrea tend to cluster with the Near Eastern or Arabian
populations (brown shaded). The West and Southern African populations (blue
shaded) form the third cluster, while North African populations forming the
fourth cluster (green shaded). Interestingly, populations from Egypt,
Tunisia and Ethiopia (Ethiopian Jews) assumed an intermediate position
between the East African and Near Eastern clusters. The PCA (Supplementary
Figure S2) also gave the same result clustering the majority of East
Africans (grey shaded) in the first component and North Africans (brown
shaded) separated from Middle East populations (blue shaded) in the second
component. The first two components account 83% of the variations observed.
Figure 3.
MDS plot based on the FST values generated from Arlequin 3.11 and using Rho
similarity measures and with stress value of 0.07101. Populations’
descriptions are given in Supplementary Table S1.
Full figure and legend (212K)
As indicated in the AMOVA summary (Table 1), when Eritrean populations were
grouped according to geographic location, most of the genetic variance
(82.11%) was found within populations; a value that is similar to that
obtained (82.44%) when the populations were grouped according to their
linguistic affiliation. Variance among populations within the linguistic
groups was 14.71%, which is slightly higher than the variance among the
geographic groups (13.17%). The genetic variance among the linguistic and
geographical groups was 2.85% and 4.71%, respectively. AMOVA analysis was
also carried out to see the variation of populations from this study and
from published works in relation to their linguistic and geographic
affiliation. For this purpose, populations were grouped as Afro-Asiatic,
Nilo-Saharan and Niger-Kordofanian with the exclusion of Middle East and
Europeans populations in both cases. Most of the genetic variance (52.66%)
was found to be within populations. The genetic variance among groups and
populations within groups were 18.73% and 28.66%, respectively. The AMOVA
result after grouping the population into North, South, West and East
Africans was different from grouping the populations according to their
linguistic affiliation. The results were 25.89% variance among groups,
19.63% among populations within groups and 54.48% within populations.
Mantel test showed no correlation between geographical isolation and
linguistic affiliation of the populations and their genetic distance.
Table 1 - Summary of AMOVA analysis.
Full table
Top of page
Discussion
The Sahel, which extends between the Atlantic coast of Africa and the Red
Sea plateau, represents one of the least sampled areas and populations in
the domain of human genetics. The position of Eritrea adjacent to the Red
Sea coast provides opportunities for insights regarding human migrations
within and beyond the African landscape.
Worth noting in the current data set is the absence of differentiation of
Eritrean populations along their geographical and linguistic affiliation,
which may be a reflection of their admixture42 or a common founding
population with subsequent drift. Sharing of derived alleles for E and
other more deep Y-chromosome lineages (unpublished data) of Eritreans with
other populations from the region renders this part of East Africa a likely
scene for some of the earliest demographic episodes within as well as
subsequent expansion off the continent; a scenario that seems to
corroborate paleontological, archeological and genetic evidences.9, 43, 44,
45
The network cluster associated with the Eritrean Nilo-Saharan Kunama
(Figure 1) may represent an expansion event following the out-of-Africa
migration,31, 46 possibly close to the origin of the ancestral Y-chromosome
clades.47, 48, 49 The expansion, carrying the diversified E-P2 mutation,
may be responsible for the migration of male populations to different parts
of the continent and henceforth the rise and spread of the bearers of the
macrohaplogroup.50 These type of population movements, or demic expansions,
driven by climatic change and/or spread of pastoralism and to some extent
agriculture,51, 52, 53, 54 are not uncommon in human history. This scenario
is more substantiated by the refining of the E-P2 (Trombetta et al35) and
its two basal clades E-M2 and E-M329, which are believed to be prevalent
exclusively in Western Africa and Eastern Africa, respectively.
Interestingly, this ancestral cluster includes populations like Fulani who
has previously shown to display Eastern African ancestry, common history
with the Hausa who are the furthest Afro-Asiatic speakers to the west in
the Sahel, with a large effective size and complex genetic background.23
The Fulani who currently speak a language classified as Niger-Kordofanian
may have lost their original tongue to associated sedentary group similar
to other cattle herders in Africa a common tendency among pastoralists.
Clearly cultural trends exemplified by populations, like Hausa or Massalit,
the latter who have neither strong tradition in agriculture nor animal
husbandry, were established subsequent to the initial differentiation of
haplogroup E. For example, the early clusters within the network also
include Nilo-Saharan speakers like Kunama of Eritrea and Nilotic of Sudan
who are ardent nomadic pastoralists but speak a language of
non-Afro-Asiatic background the predominant linguistic family within the
macrohaplogroup.
The subclades of the network some of which are associated with the practice
of pastoralism are most likely to have taken place in the Sahara, among an
early population that spoke ancestral language common to both Nilo-Saharan
and Afro-Asiatic speakers, although it is yet to be determined whether
pastoralism was an original culture to Nilo-Saharan speakers, a cultural
acquisition or vice versa; and an interesting notion to entertain in the
light of the proposition that pastoralism may be quite an antiquated event
in human history.17 Pushing the dates of the event associated with the
origin and spread of pastoralism to a proposed 12 000–22 000 YBP, as
suggested by the network dating, will solve the matter spontaneously as the
language differences would not have appeared by then and an original
pastoralist ancestral group with a common culture and language50 is a
plausible scenario to entertain. Such dates will accommodate both the
Semitic/pastoralism-associated expansion and the introduction of Bos taurus
to Europe from North East Africa or Middle East.55 The network result put
North African populations like the Saharawi, Morocco Berbers and Arabs in a
separate cluster. Given the proposed origin of Maghreb ancestors56, 57, 58,
59 in North Africa, our network dating suggested a divergence of North
Western African populations from Eastern African as early as 32 000 YBP,
which is close to the estimated dates to the origin of E-P2
macrohaplogroup.30, 60 It can be further inferred that the high frequency
of E-M81 in North Africa and its association to the Berber-speaking
populations25, 30, 32, 60, 61 may have occurred after the splitting of that
early group, leading to local differentiation and flow of some markers as
far as Southern Europe.30, 60, 62
A branching in the network may once again represent an episode of human
migration that carried the haplogroup E-M35 and its subhaplogroups farther
to the western coast of the Red Sea to Yemen, Oman and Saudi Arabia and
concurrently down to Southern Africa as part of a more recent Y chromosome
motivated out of Africa migration episode.
The PCA and MDS display similar interesting grouping of the Afar and Saho
populations of Eritrea with their Near Eastern Arabian populations to
conjure up on the genetic relationship of the two sides of the Red Sea. The
arrival of the E-M35 and derived subclades, for example, E-M123/E-M34, to
Arabia appears to be strongly linked to expansion into East Africa, North
Africa, Europe, Southern Africa, an event that is likely related to
pastoralism, hastened by its advent and amenable for analysis and dating
using approaches similar to what was proposed for the co-migration of Y
chromosome and disease traits.63
The presence of archeological10, 11, 12, 13 and agro-pastoral9, 14, 16
evidences from this side of the Red Sea and the history of migration of
animals across the Red Sea,64 however, calls for more molecular dissection
of common haplogroups shared by these coastal populations. As suggested by
others, this may give clues not only to the origin of E-M123, J-M267,
K-M70, but also to the origin of Semitic languages.65, 66 Indeed the trail
of such historical movements are detectable by molecular signatures of
markers like Y chromosome giving insights into episodes of even more
regional nature, for example, the high frequency of E-V32 in Eritrea, in
concordance to oral history, supports the historical ties between North
East Africa (Egypt) and East Africa including Eritrea, Sudan, Ethiopia and
Somalia.
Top of page
Conclusion and future work
Although most of the data sets in our study define the deep ancestry of the
phylogeny, they still shed some information to our interpretations of
recent phenomena such as the current genetic diversity of the E haplogroup
in an implication to the origin and spread of Afro-Asiatic languages and to
the history of pastoralism.67 Such perspectives, however, should be tested
by using more recently derived markers5, 47 within the major haplogroups to
explain the archeological findings and the historical and current
demography of the region. Moreover, more comparative genetic analysis
between the two sides of the Red Sea, specially emphasizing on E-M123/E-M34
or E-M78 haplogroups, will not only refine the route of exit of H. sapiens
sapiens from East Africa but also the genealogies of Afro-Asiatic languages
in the region.
Top of page
Conflict of interest
The authors declare no conflict of interest.
Top of page
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Acknowledgements
We thank all the people who participated in donating buccal samples. We
remain deeply indebted to Professor Fulvio Cruciani for reviewing the first
draft of the manuscript and to the anonymous reviewers for their invaluable
comments and guidance.
Supplementary Information accompanies this paper on European Journal of
Human Genetics website
Received on Wed Mar 26 2014 - 19:58:18 EDT